Graphene Oxide Nanoparticles and Organoids: A Prospective Advanced Model for Pancreatic Cancer Research
Abstract
:1. Introduction
2. Organoid Models for Studying Cancer
2.1. Origin of Organoids
2.1.1. Organoids Generation from Resected Tissues
2.1.2. Organoids Generation from Biopsy
2.1.3. Organoid Generation from Pluripotent Stem Cells
2.1.4. Organoids Generation from Organ-Specific Adult Stem Cells
2.1.5. Organoid Generation from 3D Printing
2.2. Extracellular Matrix of Organoids
2.2.1. Animal-Derived Matrix
2.2.2. Engineered Matrix
2.3. Tumor Microenvironment of Organoids
2.3.1. Culture Medium
2.3.2. Non-Neoplastic Cells
2.3.3. Angiogenesis
3. A Graphene Oxide Platform for Cancer Research
3.1. Properties of Graphene Oxide
3.1.1. Mechanical Properties
3.1.2. Water Dispersibility
3.1.3. Thermal Properties
3.1.4. Electrical Properties
3.1.5. Chemical Properties
3.1.6. Optical Properties
3.1.7. PH-Sensitivity
3.2. Graphene Oxide in Cancer Diagnosis
3.2.1. Magnetic Resonance Imaging
3.2.2. Fluorescence Imaging
3.2.3. Photoacoustic Imaging
3.2.4. Raman Imaging
3.2.5. Computed Tomograph
3.3. Graphene Oxide in Cancer Treatment
3.3.1. Delivery System
Drug Delivery
Gene Delivery
Antibody Delivery
Type of Nanomaterials | Advantages | Limitations | Carriers (Drugs/Gene/Antibody) | Reference |
---|---|---|---|---|
GO-CS-(FA) | smaller size, positive surface charge, increased compatibility, high loading capacity | thermally unstable | drug: Chitosan/Folic acid | [176] |
GO–PEG–FA/GNPs–DOX | high drug loading capacity, acceptable biocompatibility, pH-responsive drug release profile | slow drug release | drug: Doxorubicin hydrochloride | [182] |
HA-GO-Met | selectively targeting CD44+ triple-negative breast cancer (TNBC) cells, anti-cancer efficacy in vitro and in vivo | complex synthetic method | drug: Metformin | [185] |
PVA-SA/3D-GO | lower swelling and higher release | complex synthetic method, percentages of GO influence delivery | drug: Curcumin | [189] |
(DTX/PTX)-MgFe2O4-GO-PVA | sustained and controlled release | complex synthetic method without an in vivo test | drug: Paclitaxel, Docetaxel | [190] |
FU-GO/NHs | FU-GO/NHs more cytotoxic than free FU, fast uptake, and temperature and pH-responsive | no normal cells for comparison | drug: 5-fluorouracil | [195] |
GO/PEI/DS-DOX-MTX | dual drug loading, good selectivity, prolonged drug existence in the blood circulation system, and pH-dependent controlled and sustained release | complex synthetic method | drug: Doxorubicin, Methotrexate | [199] |
PEG-GO-PEI-FA/siRNA | siRNA condensation and stable | complex synthetic method without an in vivo test | gene: siRNA | [203] |
GO-LCO+(-FAM-DNA) | co-delivery of anti-tumor drugs and genes with low cytotoxicity | complex synthetic method | drug: Doxorubicin chloride gene: DNA | [204] |
GA-PEG-NGO-Dendrimer/anti-VEGFa siRNA | stability, low toxicity, negligible hemolytic activity, high transfection efficiency, and targeted | complex synthetic method | gene: anti-VEGFa siRNA | [205] |
APTES-GO-(pEFGP-p53) | Ninety percent of the cells were transfected | unstable during the heating process, complex synthetic method, and no in vivo test | gene: EFGP-p53 plasmid | [207] |
GOCL/DNA | high transfection, low toxicity, a library of 9 cationic lipids screening | no biological milieu test | gene: DNA | [208] |
GO-Abs/PEI/PAH-Cit/DOX | targeted cancer cells, release by mild acidic pH stimulation | complex synthetic method | antibody: integrin αⅤβ3 drug: Doxorubicin | [143] |
GO-MNps-EDC-MAb | targeted drug delivery, enhanced biocompatibility | potential cytotoxicity, stability, and uniformity of the composites | antibody: CA IX cDNA | [209] |
MSNs-CPT@A-F@PDA@GO | MSNs exhibited stimuli (pH, NIR irradiation)-responsive controlled release, a higher specificity, and efficient cytotoxicity toward cancer cells | complex synthetic method, without an in vivo test | antibody: anti-human EGFR drug: Cisplatin | [210] |
GO-CS-anti-EpCAM-siRNA | antitumor effect, accumulates siRNA in tumor tissues, and biosafety carrier | complex synthetic method, no significant differences between GCE/siRNA and Lipo/siRNA for downregulation rates of survivin-mRNA | antibody: anti-EpCAM gene: survivin-siRNA | [211] |
CMC/PVP GO-FA-Curcumin | enhanced antiangiogenesis, apoptosis, and tumor growth inhibition | complex synthetic method | antibody: folic acid antibody drug: curcumin | [214] |
NOTA-GO-FSHR-mAb | stability and high specificity for FSHR, use for early metastasis detection, and targeted delivery of therapeutics | complex synthetic method | antibody: anti-follicle-stimulating hormone receptor drug: Doxorubicin | [215] |
3.3.2. Phototherapy
Photothermal Therapy
Photodynamic Therapy
3.3.3. Angiogenesis and Anti-Angiogenesis Therapy
4. Frontiers in Pancreatic Cancer Organoids and Graphene Oxide Platform
4.1. Current Research of Graphene Oxide in 3D Culture Tumor
Type of Graphene-Based Nanoparticle | Categories of Origin | Function and Highlights | Ref. |
---|---|---|---|
Graphene oxide (GO) | liver (HepG2), breast (MCF-7) and colon (HT-29) cancer cells | Microfluidic Lab-on-a-Chip systems | [240] |
GO | human brain | used multi-omics techniques to investigate the mechanisms of GO on lipid homeostasis in a 3D brain organoid model. Transcriptomics and lipidomics indicated that direct contact with GO altered lipid homeostasis through ER stress in 3D human brain organoids | [246] |
GO | Inner ear organoids (IEOs) | promote cell–extracellular matrix interactions and cell–cell gap junctions, potential applications for drug testing | [247] |
GO | U87, U251 GSCs and primary GSCs | GO could promote differentiation and reduce malignancy in GSCs via an unanticipated epigenetic mechanism | [244] |
Graphene oxide (GO) flakes | Human Glioblastoma | GO flakes translocated deeply into the spheroids | [243] |
Gold-graphene hybrid nanomaterial (Au@GO) | co-culture spheroids of HeLa/Ovarian cancer and HeLa/human umbilical vein endothelial cell (HUVEC) | Au@GO nanoparticles displayed selectivity towards the fast-dividing HeLa cells, which could not be observed to this extent in 2D cultures. | [248] |
Graphene oxide (GO)-based nanocarrier for siRNA | lung cancer(A549) | high potential of unmodified GO to carry siRNA | [242] |
Fluorescent chitosan/graphene oxide hybrid microspheres (GCS/GO) | human umbilical cord mesenchymal stem cells | The hybrid microspheres can support long-time stem cell expansion, autofluorescence also makes observing and tracking the stem cells’ behavior on the surface of microsphere scaffolds | [249] |
HA-EDA-PHEA-DVS/GO composite nano gel | human colon cancer cells (HCT 116) | conduct thermal ablation of solid tumors | [250] |
graphene oxide (GO) loaded with PEGylated superparamagnetic iron oxide nanoparticles and grafted with methotrexate and stimuli-responsive linkers (GO-SPION-MTX) | breast cancer cell | GO-SPION-MTX was internalized by the folate-receptor-positive cancer cells and induced high cytotoxicity on exposure to NIR laser rays | [245] |
Herceptin-stabilized graphene | breast cancer cells (SKBR-3) | ultrasonic-assisted method in one-step synthesis, long-term stability in aqueous solutions | [251] |
Graphene nanoplates | human endothelial cells, human brain perivascular pericytes, primary neurons, human astroglia cells, and primary microglia | spheroid bulk is formed by neural cells and microglia and the surface by endothelial cells and they upregulate key structural and functional proteins of the blood-brain barrier. These cellular constructs are utilized to preliminary screen the permeability of polymeric, metallic, and ceramic nanoparticles | [252] |
Graphene quantum dots (GQDs) | human hepatoma cell line (HepG2 cells) | The chirality of GQDs (L/D-GQDs) was modification with L/D-cysteines. L-GQDs are more effective as nanocarriers for Doxorubicin delivery | [253] |
Hydroxylated GQDs (OH-GQDs) | mice intestinal crypts | OH-GQD treatment significantly reduced the size of the surviving intestinal organoids. | [254] |
reduced graphene oxide-branched polyethyleneimine-polyethylene glycol (rGO-BPEI-PEG) | uniformly sized neural stem cell (NSC)-derived neurospheres | Photothermal therapy (PTT) application of brain tumor spheroids generated by the microfluidic device using rGO-BPEI-PEG nanocomposite as the PTT agent | [255] |
Magnetic nanoparticle-decorated reduced graphene oxide (m-rGO) | neuroblastoma cells (SH-SY5Y) | encapsulating SH-SY5Y to promote cell differentiation and induce oriented cell growth owing to its excellent biocompatibility and electrical conductivity | [256] |
Reduced graphene oxide (rGO) was the carrier for the loading of doxorubicin (DOX) and chlorin e6 (Ce6) (rGO-PEG/Ce6 and rGO-PEG/DOX) | glioma cells (U87) | PTT showed great treatment efficacy in the 3D tumor spheroid mode than CT and PDT | [257] |
Reduced graphene oxide-MXene (rGO-Mxene) hydrogel | epithelial adenocarcinoma, neuroblastoma, and fibroblasts | strong affinity of cellular protrusions (neurites, lamellipodia, and filopodia) to grow and connect along architectural network paths within the rGO-Mxene hydrogel, leading to control over macroscopic formations of cellular networks for technologically relevant bioengineering applications | [258] |
Gelatin with methacryloyl groups (GeIMA) and reduced graphene oxide (rGO) | colon carcinoma cells (RKO) | GelMA with higher crosslink densities and promote proliferation | [259] |
Vertically coated GO micropatterns (vGO-MPs) | human liver cancer cells (HepG2) | Cytophilic GO is selectively coated on the sidewalls of micro-wells fabricated from a cell-adhesion-resistive polymer to efficiently initiate distinct donut-like formation of cancer cell spheroids. Highly stable, the anticancer effects improved | [241] |
Engineered carbon nanotubes (CNTs) | intestinal organoids | promoted the development of intestinal organoids over time, CNTs reduced the hardness of the extracellular matrix by decreasing the elasticity and increasing the viscosity | [260] |
Nanowire (NW)-templated 3D fuzzy graphene (NT-3DFG) | primary E18 rat cortical tissues | a hybrid nanomaterial for remote, nongenetic, photothermal stimulation of 2D and 3D neural cellular systems. | [261] |
3D interconnected graphene–carbon nanotube web (3D GCNT web) | glioma and healthy cortical cells | 3D trajectories and velocity distribution of individual infiltrating glioma to be reconstructed with unprecedented precision | [262] |
Three-dimensional graphene foam (3D-GFs) | neural stem cell (NSC) | 3D-GFs can enhance the NSC differentiation towards astrocytes and especially neurons. | [263] |
3D-SR-Bas with active biosensors: graphene field-effect transistor (GFET) | human cardiac spheroids (HUES9 hESCs) | provided continuous and stable multiplexed recordings of field potentials with high sensitivity and spatiotemporal resolution, | [264] |
4.2. Current Research of Graphene Oxide in Pancreatic Cancer
Nanocarrier | Function | Model of Pancreatic Cancer | Type of Study | Reference |
---|---|---|---|---|
GO | selectively targets cancer stem cells (CSCs) of multiple cancer cell types | MIA PaCa-2 | in vitro | [239] |
GO | a multiplexed Maglev-based nanotechnology as a screening tool for PDAC in populations with hyperglycemia | plasma of patients | in vitro | [270] |
GO | enhance the combined effect of hyperthermia and radiation treatment | - | in vitro | [272] |
GO | investigate toxicity | BxPC-3, AsPC-1 | in vitro | [273] |
GO nanoflakes | cancer identification at early stages via analysis of the personalized biomolecular corona (BC) | plasma of patients | in vitro | [267] |
GO nanosheets | nanoparticle-enabled blood test and serum levels of acute-phase protein detection | human blood | in vitro | [274] |
GO sheets | synergistic analysis of protein corona and hemoglobin levels | plasma of patients | in vitro | [275] |
GO-Au nanosheets | circulating tumor cells (CTCs) were captured with high sensitivity at a low concentration of target cells | blood of patient | in vitro | [269] |
GO–Protein Corona Complexes | protein cornona detection, in vitro diagnostic (IVD) testing | plasma samples of PDAC patients | in vitro | [276] |
GOQDs | facile pulsed-laser ablation in liquid (PLAL) technique for preparing GOQDs exhibited excellent optoelectronic properties | PANC-1 | in vitro | [277] |
GQD-HSA-Gem | drug delivery and bioimaging | PANC-1 | in vitro | [278] |
MWCNT-COOH/GO | use as two- and three-dimensional scaffolds to tissue engineer tumor models | PANC-1, BxPC-3, AsPC-1 | in vitro | [279] |
Nitrogen-doped graphene quantum dots (NGQDs) | pre-miR-132 detection for diagnosis | - | in vitro | [280] |
PAH/FA/PEG/GO siRNA (HDAC1/K-Ras) complex | siRNA delivery, photothermal (808 nm), and gene therapy | MIA PaCa-2/Athymic nude mice (BALB/cASlac-nu) | in vitro, in vivo | [265] |
Polymer-GO | Efficient capture and release of viable circulating tumor cells | PANC-1 | in vitro | [281] |
Reduced GO-gold-palladium (rGO-Au-Pd) | detect carbohydrate antigen 24-2 (CA242) marker | human serum | in vitro | [282] |
rGO | Photothermal (980 nm) | mice Panc02-H7/C57BL/6 mice | in vitro, in vivo | [283] |
RGO | S. spinosa leaf extract reduced the GO into RGO, photothermal (808 nm) | mice Panc02-H7 | in vitro | [224] |
RGO FET | identify early diagnostic biomarker miRNA10b | plasma samples | in vitro | [284] |
rGO@AuNS-lipid (DODAB/DOPE-FA) | imaging: photoacoustic/photothermal; therapy: PTT/gene | Capan-1/Capan-1 tumor-bearing nude mice | in vitro, in vivo | [271] |
ss-DNA@GoQdot@miR-141 | GoQdot modified and thiolated single-stranded DNA detection probes (thiol-ss-DNA) on screen-printed electrodes (SPEs) interacted with the miR-141 marker, electrochemical biosensor | - | in vitro | [285] |
Au-GO@ZC-DOX | high intracellular uptake, chemo-phototherapy | MIA PaCa-2, PANC-1 | in vitro | [266] |
Anti-PEAK1-GO-PPE | a low-cost electrochemical immunosensor on paper for the quantitative analysis of biomarker PEAK1 | - | in vitro | [268] |
AuNCs/GO | GO improved the sensitivity of AuNCs-based PEC immunosensors, Glypican-1 (GPC1), antigen (CEA), and glutathione (GSH) for early diagnosis | PANC-1/Balb/c-nu mice | in vitro, in vivo | [286] |
carboxyl-GO | ultra-sensitive carboxyl-functionalized graphene oxide (GO-COOH)-based surface plasmon resonance (SPR) immunosensors using a carbohydrate antigen (CA) 199 (CA199) biomarker | blood of the patient | in vitro | [287] |
4.3. Limitation of Current Organoids for Pancreatic Cancer Research
4.4. The Barriers of Graphene Oxide for Pancreatic Cancer Research
4.5. Future of Pancreatic Cancer Organoids and Graphene Oxide Model Systems
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Siegel, R.L.; Miller, K.D.; Fuchs, H.E.; Jemal, A. Cancer statistics, 2021. Ca Cancer J. Clin. 2021, 71, 7–33. [Google Scholar] [CrossRef] [PubMed]
- World Health Organization. Who Report on Cancer: Setting Priorities, Investing Wisely and Providing Care for All; World Health Organization: Geneva, Switzerland, 2020. [Google Scholar]
- Luo, W.; Wang, J.; Chen, H.; Ye, L.; Qiu, J.; Liu, Y.; Wang, R.; Weng, G.; Liu, T.; Su, D.; et al. Epidemiology of pancreatic cancer: New version, new vision. Clin. J Cancer Res. 2023, 35, 438–450. [Google Scholar] [CrossRef]
- Kubota, K. Recent advances and limitations of surgical treatment for pancreatic cancer. World J. Clin. Oncol. 2011, 2, 225–228. [Google Scholar] [CrossRef] [PubMed]
- Yang, G.; Guan, W.; Cao, Z.; Guo, W.; Xiong, G.; Zhao, F.; Feng, M.; Qiu, J.; Liu, Y.; Zhang, M.Q.; et al. Integrative Genomic Analysis of Gemcitabine Resistance in Pancreatic Cancer by Patient-derived Xenograft Models. Clin. Cancer Res. 2021, 27, 3383–3396. [Google Scholar] [CrossRef] [PubMed]
- Zhang, B.; Zhou, F.; Hong, J.; Ng, D.M.; Yang, T.; Zhou, X.; Jin, J.; Zhou, F.; Chen, P.; Xu, Y. The role of FOLFIRINOX in metastatic pancreatic cancer: A meta-analysis. World J. Surg. Oncol. 2021, 19, 182. [Google Scholar] [CrossRef] [PubMed]
- Hammel, P.; Huguet, F.; van Laethem, J.-L.; Goldstein, D.; Glimelius, B.; Artru, P.; Borbath, I.; Bouché, O.; Shannon, J.; André, T.; et al. Effect of Chemoradiotherapy vs. Chemotherapy on Survival in Patients with Locally Advanced Pancreatic Cancer Controlled after 4 Months of Gemcitabine with or without Erlotinib: The LAP07 Randomized Clinical Trial. JAMA 2016, 315, 1844–1853. [Google Scholar] [CrossRef]
- Garcia, P.L.; Miller, A.L.; Yoon, K.J. Patient-Derived Xenograft Models of Pancreatic Cancer: Overview and Comparison with Other Types of Models. Cancers 2020, 12, 1327. [Google Scholar] [CrossRef]
- Huang, W.; Navarro-Serer, B.; Jeong, Y.J.; Chianchiano, P.; Xia, L.; Luchini, C.; Veronese, N.; Dowiak, C.; Ng, T.; Trujillo, M.A.; et al. Pattern of Invasion in Human Pancreatic Cancer Organoids Is Associated with Loss of SMAD4 and Clinical Outcome. Cancer Res. 2020, 80, 2804–2817. [Google Scholar] [CrossRef]
- Miyabayashi, K.; Baker, L.A.; Deschênes, A.; Traub, B.; Caligiuri, G.; Plenker, D.; Alagesan, B.; Belleau, P.; Li, S.; Kendall, J.; et al. Intraductal Transplantation Models of Human Pancreatic Ductal Adenocarcinoma Reveal Progressive Transition of Molecular Subtypes. Cancer Discov. 2020, 10, 1566–1589. [Google Scholar] [CrossRef]
- Zhang, X.; Wang, Y.; Luo, G.; Xing, M. Two-dimensional graphene family material: Assembly, biocompatibility and sensors applications. Sensors 2019, 19, 2966. [Google Scholar] [CrossRef]
- Aliyev, E.; Filiz, V.; Khan, M.M.; Lee, Y.J.; Abetz, C.; Abetz, V. Structural Characterization of Graphene Oxide: Surface Functional Groups and Fractionated Oxidative Debris. Nanomaterials 2019, 9, 1180. [Google Scholar] [CrossRef]
- Han, X.M.; Zheng, K.W.; Wang, R.L.; Yue, S.F.; Chen, J.; Zhao, Z.W.; Song, F.; Su, Y.; Ma, Q. Functionalization and optimization-strategy of graphene oxide-based nanomaterials for gene and drug delivery. Am. J. Transl. Res. 2020, 12, 1515–1534. [Google Scholar]
- Ma, X.; Tao, H.; Yang, K.; Feng, L.; Cheng, L.; Shi, X.; Li, Y.; Guo, L.; Liu, Z. A functionalized graphene oxide-iron oxide nanocomposite for magnetically targeted drug delivery, photothermal therapy, and magnetic resonance imaging. Nano Res. 2012, 5, 199–212. [Google Scholar] [CrossRef]
- Xiao, X.; Zhang, Y.; Zhou, L.; Li, B.; Gu, L. Photoluminescence and Fluorescence Quenching of Graphene Oxide: A Review. Nanomaterials 2022, 12, 2444. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.; Yang, Y.; Li, K.; Li, J. Application of graphene oxide in tumor targeting and tumor therapy. J. Biomater. Sci. Polym. Ed. 2023, 34, 2551–2576. [Google Scholar] [CrossRef]
- Pourjavadi, A.; Asgari, S.; Hosseini, S.H. Graphene oxide functionalized with oxygen-rich polymers as a pH-sensitive carrier for co-delivery of hydrophobic and hydrophilic drugs. J. Drug Deliv. Sci. Technol. 2020, 56, 101542. [Google Scholar] [CrossRef]
- Campbell, E.; Hasan, M.T.; Pho, C.; Callaghan, K.; Akkaraju, G.R.; Naumov, A.V. Graphene Oxide as a Multifunctional Platform for Intracellular Delivery, Imaging, and Cancer Sensing. Sci. Rep. 2019, 9, 416. [Google Scholar] [CrossRef]
- Lin, B.; Chen, H.; Liang, D.; Lin, W.; Qi, X.; Liu, H.; Deng, X. Acidic pH and High-H2O2 Dual Tumor Microenvironment-Responsive Nanocatalytic Graphene Oxide for Cancer Selective Therapy and Recognition. ACS Appl. Mater. Interfaces 2019, 11, 11157–11166. [Google Scholar] [CrossRef] [PubMed]
- Feng, L.; Li, K.; Shi, X.; Gao, M.; Liu, J.; Liu, Z. Smart pH-responsive nanocarriers based on nano-graphene oxide for combined chemo-and photothermal therapy overcoming drug resistance. Adv. Healthc. Mater. 2014, 3, 1261–1271. [Google Scholar] [CrossRef] [PubMed]
- Zhao, X.; Yang, L.; Li, X.; Jia, X.; Liu, L.; Zeng, J.; Guo, J.; Liu, P. Functionalized Graphene Oxide Nanoparticles for Cancer Cell-Specific Delivery of Antitumor Drug. Bioconjugate Chem. 2015, 26, 128–136. [Google Scholar] [CrossRef]
- Deb, A.; Andrews, N.G.; Raghavan, V. Natural polymer functionalized graphene oxide for co-delivery of anticancer drugs: In-vitro and in-vivo. Int. J. Biol. Macromol. 2018, 113, 515–525. [Google Scholar] [CrossRef]
- Sato, T.; Stange, D.E.; Ferrante, M.; Vries, R.G.; Van Es, J.H.; Van den Brink, S.; Van Houdt, W.J.; Pronk, A.; Van Gorp, J.; Siersema, P.D.; et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett’s epithelium. Gastroenterology 2011, 141, 1762–1772. [Google Scholar] [CrossRef]
- Boj, S.F.; Hwang, C.I.; Baker, L.A.; Chio, I.I.C.; Engle, D.D.; Corbo, V.; Jager, M.; Ponz-Sarvise, M.; Tiriac, H.; Spector, M.S.; et al. Organoid models of human and mouse ductal pancreatic cancer. Cell 2015, 160, 324–338. [Google Scholar] [CrossRef] [PubMed]
- Kim, M.; Mun, H.; Sung, C.O.; Cho, E.J.; Jeon, H.-J.; Chun, S.-M.; Jung, D.J.; Shin, T.H.; Jeong, G.S.; Kim, D.K.; et al. Patient-derived lung cancer organoids as in vitro cancer models for therapeutic screening. Nat. Commun. 2019, 10, 3991. [Google Scholar] [CrossRef] [PubMed]
- Fujii, M.; Shimokawa, M.; Date, S.; Takano, A.; Matano, M.; Nanki, K.; Ohta, Y.; Toshimitsu, K.; Nakazato, Y.; Kawasaki, K.; et al. A Colorectal Tumor Organoid Library Demonstrates Progressive Loss of Niche Factor Requirements during Tumorigenesis. Cell Stem Cell 2016, 18, 827–838. [Google Scholar] [CrossRef]
- van de Wetering, M.; Francies, H.E.; Francis, J.M.; Bounova, G.; Iorio, F.; Pronk, A.; van Houdt, W.; van Gorp, J.; Taylor-Weiner, A.; Kester, L.; et al. Prospective Derivation of a Living Organoid Biobank of Colorectal Cancer Patients. Cell 2015, 161, 933–945. [Google Scholar] [CrossRef]
- Hill, S.J.; Decker, B.; Roberts, E.A.; Horowitz, N.S.; Muto, M.G.; Worley, M.J.; Feltmate, C.M.; Nucci, M.R.; Swisher, E.M.; Nguyen, H.; et al. Prediction of DNA Repair Inhibitor Response in Short-Term Patient-Derived Ovarian Cancer Organoids. Cancer Discov. 2018, 8, 1404–1421. [Google Scholar] [CrossRef]
- Kopper, O.; De Witte, C.J.; Lõhmussaar, K.; Valle-Inclan, J.E.; Hami, N.; Kester, L.; Balgobind, A.V.; Korving, J.; Proost, N.; Begthel, H.; et al. An organoid platform for ovarian cancer captures intra- and interpatient heterogeneity. Nat. Med. 2019, 25, 838–849. [Google Scholar] [CrossRef] [PubMed]
- Nanki, Y.; Chiyoda, T.; Hirasawa, A.; Ookubo, A.; Itoh, M.; Ueno, M.; Akahane, T.; Kameyama, K.; Yamagami, W.; Kataoka, F.; et al. Patient-derived ovarian cancer organoids capture the genomic profiles of primary tumours applicable for drug sensitivity and resistance testing. Sci. Rep. 2020, 10, 12581. [Google Scholar] [CrossRef]
- Drost, J.; Karthaus, W.R.; Gao, D.; Driehuis, E.; Sawyers, C.L.; Chen, Y.; Clevers, H. Organoid culture systems for prostate epithelial and cancer tissue. Nat. Protoc. 2016, 11, 347–358. [Google Scholar] [CrossRef] [PubMed]
- Servant, R.; Garioni, M.; Vlajnic, T.; Blind, M.; Pueschel, H.; Müller, D.C.; Zellweger, T.; Templeton, A.J.; Garofoli, A.; Maletti, S.; et al. Prostate cancer patient-derived organoids: Detailed outcome from a prospective cohort of 81 clinical specimens. J. Pathol. 2021, 254, 543–555. [Google Scholar] [CrossRef]
- Driehuis, E.; Gracanin, A.; Vries, R.G.J.; Clevers, H.; Boj, S.F. Establishment of Pancreatic Organoids from Normal Tissue and Tumors. STAR Protoc. 2020, 1, 100192. [Google Scholar] [CrossRef] [PubMed]
- Gendoo, D.M.A.; Denroche, R.E.; Zhang, A.; Radulovich, N.; Jang, G.H.; Lemire, M.; Fischer, S.; Chadwick, D.; Lungu, I.M.; Ibrahimov, E.; et al. Whole genomes define concordance of matched primary, xenograft, and organoid models of pancreas cancer. PLoS Comput. Biol. 2019, 15, e1006596. [Google Scholar] [CrossRef]
- Broutier, L.; Mastrogiovanni, G.; Verstegen, M.M.; Francies, H.E.; Gavarró, L.M.; Bradshaw, C.R.; Allen, G.E.; Arnes-Benito, R.; Sidorova, O.; Gaspersz, M.P.; et al. Human primary liver cancer-derived organoid cultures for disease modeling and drug screening. Nat. Med. 2017, 23, 1424–1435. [Google Scholar] [CrossRef]
- Li, L.; Knutsdottir, H.; Hui, K.; Weiss, M.J.; He, J.; Philosophe, B.; Cameron, A.M.; Wolfgang, C.L.; Pawlik, T.M.; Ghiaur, G.; et al. Human primary liver cancer organoids reveal intratumor and interpatient drug response heterogeneity. JCI Insight 2019, 4, e121490. [Google Scholar] [CrossRef] [PubMed]
- Thomas, P.B.; Perera, M.P.J.; Alinezhad, S.; Joshi, A.; Saadat, P.; Nicholls, C.; Devonport, C.P.; Calabrese, A.R.; Templeton, A.R.; Wood, J.R.; et al. Culture of Bladder Cancer Organoids as Precision Medicine Tools. J. Vis. Exp. 2021, 178, e63192. [Google Scholar] [CrossRef]
- Yu, L.; Li, Z.; Mei, H.; Li, W.; Chen, D.; Liu, L.; Zhang, Z.; Sun, Y.; Song, F.; Chen, W.; et al. Patient-derived organoids of bladder cancer recapitulate antigen expression profiles and serve as a personal evaluation model for CAR-T cells in vitro. Clin. Transl. Immunol. 2021, 10, e1248. [Google Scholar] [CrossRef]
- Choi, S.Y.; Cho, Y.-H.; Kim, D.-S.; Ji, W.; Choi, C.-M.; Lee, J.C.; Rho, J.K.; Jeong, G.S. Establishment and Long-Term Expansion of Small Cell Lung Cancer Patient-Derived Tumor Organoids. Int. J. Mol. Sci. 2021, 22, 1349. [Google Scholar] [CrossRef]
- Hu, Y.; Sui, X.; Song, F.; Li, Y.; Li, K.; Chen, Z.; Yang, F.; Chen, X.; Zhang, Y.; Wang, X.; et al. Lung cancer organoids analyzed on microwell arrays predict drug responses of patients within a week. Nat. Commun. 2021, 12, 2581. [Google Scholar] [CrossRef]
- Lee, D.; Kim, Y.; Chung, C. Scientific Validation and Clinical Application of Lung Cancer Organoids. Cells 2021, 10, 3012. [Google Scholar] [CrossRef]
- Nanki, K.; Toshimitsu, K.; Takano, A.; Fujii, M.; Shimokawa, M.; Ohta, Y.; Matano, M.; Seino, T.; Nishikori, S.; Ishikawa, K.; et al. Divergent Routes toward Wnt and R-spondin Niche Independency during Human Gastric Carcinogenesis. Cell 2018, 174, 856–869. [Google Scholar] [CrossRef]
- Seidlitz, T.; Merker, S.R.; Rothe, A.; Zakrzewski, F.; Von Neubeck, C.; Grützmann, K.; Sommer, U.; Schweitzer, C.; Schölch, S.; Uhlemann, H.; et al. Human gastric cancer modelling using organoids. Gut 2019, 68, 207–217. [Google Scholar] [CrossRef] [PubMed]
- Jacob, F.; Salinas, R.D.; Zhang, D.Y.; Nguyen, P.T.T.; Schnoll, J.G.; Wong, S.Z.H.; Thokala, R.; Sheikh, S.; Saxena, D.; Prokop, S.; et al. A Patient-Derived Glioblastoma Organoid Model and Biobank Recapitulates Inter- and Intra-tumoral Heterogeneity. Cell 2020, 180, 188–204. [Google Scholar] [CrossRef] [PubMed]
- Krieger, T.G.; Tirier, S.M.; Park, J.; Jechow, K.; Eisemann, T.; Peterziel, H.; Angel, P.; Eils, R.; Conrad, C. Modeling glioblastoma invasion using human brain organoids and single-cell transcriptomics. Neuro-Oncology 2020, 22, 1138–1149. [Google Scholar] [CrossRef]
- Karakasheva, T.A.; Kijima, T.; Shimonosono, M.; Maekawa, H.; Sahu, V.; Gabre, J.T.; Cruz-Acuña, R.; Giroux, V.; Sangwan, V.; Whelan, K.A.; et al. Generation and Characterization of Patient-Derived Head and Neck, Oral, and Esophageal Cancer Organoids. Curr. Protoc. Stem Cell Biol. 2020, 53, e109. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Francies, H.E.; Secrier, M.; Perner, J.; Miremadi, A.; Galeano-Dalmau, N.; Barendt, W.J.; Letchford, L.; Leyden, G.M.; Goffin, E.K.; et al. Organoid cultures recapitulate esophageal adenocarcinoma heterogeneity providing a model for clonality studies and precision therapeutics. Nat. Commun. 2018, 9, 2983. [Google Scholar] [CrossRef]
- Berg, H.F.; Hjelmeland, M.E.; Lien, H.; Espedal, H.; Fonnes, T.; Srivastava, A.; Stokowy, T.; Strand, E.; Bozickovic, O.; Stefansson, I.M.; et al. Patient-derived organoids reflect the genetic profile of endometrial tumors and predict patient prognosis. Commun. Med. 2021, 1, 20. [Google Scholar] [CrossRef]
- Bi, J.; Newtson, A.M.; Zhang, Y.; Devor, E.J.; Samuelson, M.I.; Thiel, K.W.; Leslie, K.K. Successful Patient-Derived Organoid Culture of Gynecologic Cancers for Disease Modeling and Drug Sensitivity Testing. Cancers 2021, 13, 2901. [Google Scholar] [CrossRef] [PubMed]
- Boretto, M.; Maenhoudt, N.; Luo, X.; Hennes, A.; Boeckx, B.; Bui, B.; Heremans, R.; Perneel, L.; Kobayashi, H.; Van Zundert, I.; et al. Patient-derived organoids from endometrial disease capture clinical heterogeneity and are amenable to drug screening. Nat. Cell Biol. 2019, 21, 1041–1051. [Google Scholar] [CrossRef]
- Collins, A.; Miles, G.J.; Wood, J.; Macfarlane, M.; Pritchard, C.; Moss, E. Patient-derived explants, xenografts and organoids: 3-dimensional patient-relevant pre-clinical models in endometrial cancer. Gynecol. Oncol. 2020, 156, 251–259. [Google Scholar] [CrossRef]
- Lee, S.H.; Hu, W.; Matulay, J.T.; Silva, M.V.; Owczarek, T.B.; Kim, K.; Chua, C.W.; Barlow, L.J.; Kandoth, C.; Williams, A.B.; et al. Tumor Evolution and Drug Response in Patient-Derived Organoid Models of Bladder Cancer. Cell 2018, 173, 515–528. [Google Scholar] [CrossRef] [PubMed]
- Gao, D.; Vela, I.; Sboner, A.; Iaquinta, P.J.; Karthaus, W.R.; Gopalan, A.; Dowling, C.; Wanjala, J.N.; Undvall, E.A.; Arora, V.K.; et al. Organoid cultures derived from patients with advanced prostate cancer. Cell 2014, 159, 176–187. [Google Scholar] [CrossRef]
- Maenhoudt, N.; Defraye, C.; Boretto, M.; Jan, Z.; Heremans, R.; Boeckx, B.; Hermans, F.; Arijs, I.; Cox, B.; Van Nieuwenhuysen, E.; et al. Developing Organoids from Ovarian Cancer as Experimental and Preclinical Models. Stem Cell Rep. 2020, 14, 717–729. [Google Scholar] [CrossRef]
- Maenhoudt, N.; Vankelecom, H. Protocol for establishing organoids from human ovarian cancer biopsies. STAR Protoc. 2021, 2, 100429. [Google Scholar] [CrossRef] [PubMed]
- Weeber, F.; Van De Wetering, M.; Hoogstraat, M.; Dijkstra, K.K.; Krijgsman, O.; Kuilman, T.; Gadellaa-Van Hooijdonk, C.G.M.; Van Der Velden, D.L.; Peeper, D.S.; Cuppen, E.P.J.G.; et al. Preserved genetic diversity in organoids cultured from biopsies of human colorectal cancer metastases. Proc. Natl. Acad. Sci. USA 2015, 112, 13308–13311. [Google Scholar] [CrossRef] [PubMed]
- Yang, C.; Xia, B.-R.; Jin, W.-L.; Lou, G. Circulating tumor cells in precision oncology: Clinical applications in liquid biopsy and 3D organoid model. Cancer Cell Int. 2019, 19, 341. [Google Scholar] [CrossRef] [PubMed]
- Jo, J.; Xiao, Y.; Sun, A.X.; Cukuroglu, E.; Tran, H.D.; Göke, J.; Tan, Z.Y.; Saw, T.Y.; Tan, C.P.; Lokman, H.; et al. Midbrain-like Organoids from Human Pluripotent Stem Cells Contain Functional Dopaminergic and Neuromelanin-Producing Neurons. Cell Stem Cell 2016, 19, 248–257. [Google Scholar] [CrossRef]
- Norrie, J.L.; Nityanandam, A.; Lai, K.; Chen, X.; Wilson, M.; Stewart, E.; Griffiths, L.; Jin, H.; Wu, G.; Orr, B.; et al. Retinoblastoma from human stem cell-derived retinal organoids. Nat. Commun. 2021, 12, 4535. [Google Scholar] [CrossRef]
- McCauley, H.A.; Wells, J.M. Pluripotent stem cell-derived organoids: Using principles of developmental biology to grow human tissues in a dish. Development 2017, 144, 958–962. [Google Scholar] [CrossRef]
- Crespo, M.; Vilar, E.; Tsai, S.-Y.; Chang, K.; Amin, S.; Srinivasan, T.; Zhang, T.; Pipalia, N.H.; Chen, H.J.; Witherspoon, M.; et al. Colonic organoids derived from human induced pluripotent stem cells for modeling colorectal cancer and drug testing. Nat. Med. 2017, 23, 878–884. [Google Scholar] [CrossRef]
- Lee, D.F.; Su, J.; Kim, H.S.; Chang, B.; Papatsenko, D.; Zhao, R.; Yuan, Y.; Gingold, J.; Xia, W.; Darr, H.; et al. Modeling Familial Cancer with Induced Pluripotent Stem Cells. Cell 2015, 161, 240–254. [Google Scholar] [CrossRef]
- Hwang, J.W.; Desterke, C.; Féraud, O.; Richard, S.; Ferlicot, S.; Verkarre, V.; Patard, J.J.; Loisel-Duwattez, J.; Foudi, A.; Griscelli, F.; et al. iPSC-Derived Embryoid Bodies as Models of c-Met-Mutated Hereditary Papillary Renal Cell Carcinoma. Int. J. Mol. Sci. 2019, 20, 4867. [Google Scholar] [CrossRef] [PubMed]
- Huang, L.; Desai, R.; Conrad, D.N.; Leite, N.C.; Akshinthala, D.; Lim, C.M.; Gonzalez, R.; Muthuswamy, L.B.; Gartner, Z.; Muthuswamy, S.K. Commitment and oncogene-induced plasticity of human stem cell-derived pancreatic acinar and ductal organoids. Cell Stem Cell 2021, 28, 1090–1104. [Google Scholar] [CrossRef] [PubMed]
- Hepburn, A.C.; Sims, C.H.C.; Buskin, A.; Heer, R. Engineering Prostate Cancer from Induced Pluripotent Stem Cells—New Opportunities to Develop Preclinical Tools in Prostate and Prostate Cancer Studies. Int. J. Mol. Sci. 2020, 21, 905. [Google Scholar] [CrossRef] [PubMed]
- Drost, J.; Clevers, H. Translational applications of adult stem cell-derived organoids. Development 2017, 144, 968–975. [Google Scholar] [CrossRef] [PubMed]
- Broutier, L.; Andersson-Rolf, A.; Hindley, C.J.; Boj, S.F.; Clevers, H.; Koo, B.K.; Huch, M. Culture and establishment of self-renewing human and mouse adult liver and pancreas 3D organoids and their genetic manipulation. Nat. Protoc. 2016, 11, 1724–1743. [Google Scholar] [CrossRef] [PubMed]
- Drost, J.; van Jaarsveld, R.H.; Ponsioen, B.; Zimberlin, C.; van Boxtel, R.; Buijs, A.; Sachs, N.; Overmeer, R.M.; Offerhaus, G.J.; Begthel, H.; et al. Sequential cancer mutations in cultured human intestinal stem cells. Nature 2015, 521, 43–47. [Google Scholar] [CrossRef] [PubMed]
- Sachs, N.; De Ligt, J.; Kopper, O.; Gogola, E.; Bounova, G.; Weeber, F.; Balgobind, A.V.; Wind, K.; Gracanin, A.; Begthel, H.; et al. A Living Biobank of Breast Cancer Organoids Captures Disease Heterogeneity. Cell 2018, 172, 373–386. [Google Scholar] [CrossRef] [PubMed]
- Turco, M.Y.; Gardner, L.; Hughes, J.; Cindrova-Davies, T.; Gomez, M.J.; Farrell, L.; Hollinshead, M.; Marsh, S.G.E.; Brosens, J.J.; Critchley, H.O.; et al. Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium. Nat. Cell Biol. 2017, 19, 568–577. [Google Scholar] [CrossRef]
- Gu, Q.; Tomaskovic-Crook, E.; Wallace, G.G.; Crook, J.M. 3D Bioprinting Human Induced Pluripotent Stem Cell Constructs for In Situ Cell Proliferation and Successive Multilineage Differentiation. Adv. Healthc. Mater. 2017, 6, 1700175. [Google Scholar] [CrossRef]
- Hiller, T.; Berg, J.; Elomaa, L.; Röhrs, V.; Ullah, I.; Schaar, K.; Dietrich, A.-C.; Al-Zeer, M.; Kurtz, A.; Hocke, A.; et al. Generation of a 3D Liver Model Comprising Human Extracellular Matrix in an Alginate/Gelatin-Based Bioink by Extrusion Bioprinting for Infection and Transduction Studies. Int. J. Mol. Sci. 2018, 19, 3129. [Google Scholar] [CrossRef]
- Lee, A.; Hudson, A.R.; Shiwarski, D.J.; Tashman, J.W.; Hinton, T.J.; Yerneni, S.; Bliley, J.M.; Campbell, P.G.; Feinberg, A.W. 3D bioprinting of collagen to rebuild components of the human heart. Science 2019, 365, 482–487. [Google Scholar] [CrossRef]
- Park, J.Y.; Shim, J.-H.; Choi, S.-A.; Jang, J.; Kim, M.; Lee, S.H.; Cho, D.-W. 3D printing technology to control BMP-2 and VEGF delivery spatially and temporally to promote large-volume bone regeneration. J. Mater. Chem. B 2015, 3, 5415–5425. [Google Scholar] [CrossRef] [PubMed]
- Tytgat, L.; Van Damme, L.; Ortega Arevalo, M.D.P.; Declercq, H.; Thienpont, H.; Otteveare, H.; Blondeel, P.; Dubruel, P.; Van Vlierberghe, S. Extrusion-based 3D printing of photo-crosslinkable gelatin and κ-carrageenan hydrogel blends for adipose tissue regeneration. Int. J. Biol. Macromol. 2019, 140, 929–938. [Google Scholar] [CrossRef]
- Yi, H.G.; Jeong, Y.H.; Kim, Y.; Choi, Y.J.; Moon, H.E.; Park, S.H.; Kang, K.S.; Bae, M.; Jang, J.; Youn, H.; et al. A bioprinted human-glioblastoma-on-a-chip for the identification of patient-specific responses to chemoradiotherapy. Nat. Biomed. Eng. 2019, 3, 509–519. [Google Scholar] [CrossRef] [PubMed]
- Reid, J.A.; Palmer, X.-L.; Mollica, P.A.; Northam, N.; Sachs, P.C.; Bruno, R.D. A 3D bioprinter platform for mechanistic analysis of tumoroids and chimeric mammary organoids. Sci. Rep. 2019, 9, 7466. [Google Scholar] [CrossRef]
- Langer, E.M.; Allen-Petersen, B.L.; King, S.M.; Kendsersky, N.D.; Turnidge, M.A.; Kuziel, G.M.; Riggers, R.; Samatham, R.; Amery, T.S.; Jacques, S.L.; et al. Modeling Tumor Phenotypes In Vitro with Three-Dimensional Bioprinting. Cell Rep. 2019, 26, 608–623. [Google Scholar] [CrossRef] [PubMed]
- Xu, F.; Celli, J.; Rizvi, I.; Moon, S.; Hasan, T.; Demirci, U. A three-dimensional in vitro ovarian cancer coculture model using a high-throughput cell patterning platform. Biotechnol. J. 2011, 6, 204–212. [Google Scholar] [CrossRef]
- Zhao, Y.; Yao, R.; Ouyang, L.; Ding, H.; Zhang, T.; Zhang, K.; Cheng, S.; Sun, W. Three-dimensional printing of Hela cells for cervical tumor model in vitro. Biofabrication 2014, 6, 035001. [Google Scholar] [CrossRef]
- Ma, X.; Qu, X.; Zhu, W.; Li, Y.-S.; Yuan, S.; Zhang, H.; Liu, J.; Wang, P.; Lai, C.S.E.; Zanella, F.; et al. Deterministically patterned biomimetic human iPSC-derived hepatic model via rapid 3D bioprinting. Proc. Natl. Acad. Sci. USA 2016, 113, 2206–2211. [Google Scholar] [CrossRef]
- Aisenbrey, E.A.; Murphy, W.L. Synthetic alternatives to Matrigel. Nat. Rev. Mater. 2020, 5, 539–551. [Google Scholar] [CrossRef] [PubMed]
- Kleinman, H.K.; Martin, G.R. Matrigel: Basement membrane matrix with biological activity. Semin. Cancer Biol. 2005, 15, 378–386. [Google Scholar] [CrossRef] [PubMed]
- Acerbi, I.; Cassereau, L.; Dean, I.; Shi, Q.; Au, A.; Park, C.; Chen, Y.Y.; Liphardt, J.; Hwang, E.S.; Weaver, V.M. Human breast cancer invasion and aggression correlates with ECM stiffening and immune cell infiltration. Integr. Biol. 2015, 7, 1120–1134. [Google Scholar] [CrossRef]
- Broguiere, N.; Lüchtefeld, I.; Trachsel, L.; Mazunin, D.; Rizzo, R.; Bode, J.W.; Lutolf, M.P.; Zenobi-Wong, M. Morphogenesis Guided by 3D Patterning of Growth Factors in Biological Matrices. Adv. Mater. 2020, 32, 1908299. [Google Scholar] [CrossRef]
- Hapach, L.A.; VanderBurgh, J.A.; Miller, J.P.; Reinhart-King, C.A. Manipulation of in vitro collagen matrix architecture for scaffolds of improved physiological relevance. Phys. Biol. 2015, 12, 061002. [Google Scholar] [CrossRef] [PubMed]
- Jabaji, Z.; Brinkley, G.J.; Khalil, H.A.; Sears, C.M.; Lei, N.Y.; Lewis, M.; Stelzner, M.; Martín, M.G.; Dunn, J.C.Y. Type I Collagen as an Extracellular Matrix for the In Vitro Growth of Human Small Intestinal Epithelium. PLoS ONE 2014, 9, e107814. [Google Scholar] [CrossRef] [PubMed]
- Xiao, W.; Zhang, R.; Sohrabi, A.; Ehsanipour, A.; Sun, S.; Liang, J.; Walthers, C.M.; Ta, L.; Nathanson, D.A.; Seidlits, S.K. Brain-Mimetic 3D Culture Platforms Allow Investigation of Cooperative Effects of Extracellular Matrix Features on Therapeutic Resistance in Glioblastoma. Cancer Res. 2018, 78, 1358–1370. [Google Scholar] [CrossRef]
- Gjorevski, N.; Sachs, N.; Manfrin, A.; Giger, S.; Bragina, M.E.; Ordóñez-Morán, P.; Clevers, H.; Lutolf, M.P. Designer matrices for intestinal stem cell and organoid culture. Nature 2016, 539, 560–564. [Google Scholar] [CrossRef]
- Capeling, M.M.; Czerwinski, M.; Huang, S.; Tsai, Y.-H.; Wu, A.; Nagy, M.S.; Juliar, B.; Sundaram, N.; Song, Y.; Han, W.M.; et al. Nonadhesive Alginate Hydrogels Support Growth of Pluripotent Stem Cell-Derived Intestinal Organoids. Stem Cell Rep. 2019, 12, 381–394. [Google Scholar] [CrossRef]
- Gupta, A.K.; Coburn, J.M.; Davis-Knowlton, J.; Kimmerling, E.; Kaplan, D.L.; Oxburgh, L. Scaffolding kidney organoids on silk. J. Tissue Eng. Regen. Med. 2019, 13, 812–822. [Google Scholar] [CrossRef]
- Broguiere, N.; Isenmann, L.; Hirt, C.; Ringel, T.; Placzek, S.; Cavalli, E.; Ringnalda, F.; Villiger, L.; Züllig, R.; Lehmann, R.; et al. Growth of Epithelial Organoids in a Defined Hydrogel. Adv. Mater. 2018, 30, 1801621. [Google Scholar] [CrossRef] [PubMed]
- Hunt, D.R.; Klett, K.C.; Mascharak, S.; Wang, H.; Gong, D.; Lou, J.; Li, X.; Cai, P.C.; Suhar, R.A.; Co, J.Y.; et al. Engineered Matrices Enable the Culture of Human Patient-Derived Intestinal Organoids. Adv. Sci. 2021, 8, 2004705. [Google Scholar] [CrossRef]
- Below, C.R.; Kelly, J.; Brown, A.; Humphries, J.D.; Hutton, C.; Xu, J.; Lee, B.Y.; Cintas, C.; Zhang, X.; Hernandez-Gordillo, V.; et al. A microenvironment-inspired synthetic three-dimensional model for pancreatic ductal adenocarcinoma organoids. Nat. Mater. 2022, 21, 110–119. [Google Scholar] [CrossRef] [PubMed]
- Merenda, A.; Fenderico, N.; Maurice, M.M. Wnt Signaling in 3D: Recent Advances in the Applications of Intestinal Organoids. Trends Cell Biol. 2020, 30, 60–73. [Google Scholar] [CrossRef] [PubMed]
- Urbischek, M.; Rannikmae, H.; Foets, T.; Ravn, K.; Hyvönen, M.; De La Roche, M. Organoid culture media formulated with growth factors of defined cellular activity. Sci. Rep. 2019, 9, 6193. [Google Scholar] [CrossRef] [PubMed]
- Gu, Y.; Fu, J.; Lo, P.-K.; Wang, S.; Wang, Q.; Chen, H. The effect of B27 supplement on promoting in vitro propagation of Her2/neu-transformed mammary tumorspheres. J. Biotech. Res. 2011, 3, 7. [Google Scholar]
- Merker, S.R.; Weitz, J.; Stange, D.E. Gastrointestinal organoids: How they gut it out. Dev. Biol. 2016, 420, 239–250. [Google Scholar] [CrossRef]
- Rabata, A.; Fedr, R.; Soucek, K.; Hampl, A.; Koledova, Z. 3D Cell Culture Models Demonstrate a Role for FGF and WNT Signaling in Regulation of Lung Epithelial Cell Fate and Morphogenesis. Front. Cell Dev. Biol. 2020, 8, 574. [Google Scholar] [CrossRef] [PubMed]
- Ma, H.-c.; Zhu, Y.-j.; Zhou, R.; Yu, Y.-y.; Xiao, Z.-z.; Zhang, H.-b. Lung cancer organoids, a promising model still with long way to go. Crit. Rev. Oncol./Hematol. 2022, 171, 103610. [Google Scholar] [CrossRef]
- Neal, J.T.; Li, X.; Zhu, J.; Giangarra, V.; Grzeskowiak, C.L.; Ju, J.; Liu, I.H.; Chiou, S.-H.; Salahudeen, A.A.; Smith, A.R.; et al. Organoid Modeling of the Tumor Immune Microenvironment. Cell 2018, 175, 1972–1988. [Google Scholar] [CrossRef]
- Zhao, H.; Jiang, E.; Shang, Z. 3D Co-culture of Cancer-Associated Fibroblast with Oral Cancer Organoids. J. Dent. Res. 2021, 100, 201–208. [Google Scholar] [CrossRef]
- Tsai, S.; McOlash, L.; Palen, K.; Johnson, B.; Duris, C.; Yang, Q.; Dwinell, M.B.; Hunt, B.; Evans, D.B.; Gershan, J.; et al. Development of primary human pancreatic cancer organoids, matched stromal and immune cells and 3D tumor microenvironment models. BMC Cancer 2018, 18, 335. [Google Scholar] [CrossRef]
- Courau, T.; Bonnereau, J.; Chicoteau, J.; Bottois, H.; Remark, R.; Assante Miranda, L.; Toubert, A.; Blery, M.; Aparicio, T.; Allez, M.; et al. Cocultures of human colorectal tumor spheroids with immune cells reveal the therapeutic potential of MICA/B and NKG2A targeting for cancer treatment. J. Immunother. Cancer 2019, 7, 74. [Google Scholar] [CrossRef] [PubMed]
- Dijkstra, K.K.; Cattaneo, C.M.; Weeber, F.; Chalabi, M.; Van De Haar, J.; Fanchi, L.F.; Slagter, M.; Van Der Velden, D.L.; Kaing, S.; Kelderman, S.; et al. Generation of Tumor-Reactive T Cells by Co-culture of Peripheral Blood Lymphocytes and Tumor Organoids. Cell 2018, 174, 1586–1598. [Google Scholar] [CrossRef]
- Truelsen, S.L.B.; Mousavi, N.; Wei, H.; Harvey, L.; Stausholm, R.; Spillum, E.; Hagel, G.; Qvortrup, K.; Thastrup, O.; Harling, H.; et al. The cancer angiogenesis co-culture assay: In vitro quantification of the angiogenic potential of tumoroids. PLoS ONE 2021, 16, e0253258. [Google Scholar] [CrossRef] [PubMed]
- Lim, J.T.C.; Kwang, L.G.; Ho, N.C.W.; Toh, C.C.M.; Too, N.S.H.; Hooi, L.; Benoukraf, T.; Chow, P.K.; Dan, Y.Y.; Chow, E.K.; et al. Hepatocellular carcinoma organoid co-cultures mimic angiocrine crosstalk to generate inflammatory tumor microenvironment. Biomaterials 2022, 284, 121527. [Google Scholar] [CrossRef]
- Bonanini, F.; Kurek, D.; Previdi, S.; Nicolas, A.; Hendriks, D.; De Ruiter, S.; Meyer, M.; Clapés Cabrer, M.; Dinkelberg, R.; García, S.B.; et al. In vitro grafting of hepatic spheroids and organoids on a microfluidic vascular bed. Angiogenesis 2022, 25, 455–470. [Google Scholar] [CrossRef] [PubMed]
- Kook, M.G.; Lee, S.-E.; Shin, N.; Kong, D.; Kim, D.-H.; Kim, M.-S.; Kang, H.K.; Choi, S.W.; Kang, K.-S. Generation of Cortical Brain Organoid with Vascularization by Assembling with Vascular Spheroid. Int. J. Stem Cells 2022, 15, 85–94. [Google Scholar] [CrossRef]
- Lim, J.; Ching, H.; Yoon, J.-K.; Jeon, N.L.; Kim, Y. Microvascularized tumor organoids-on-chips: Advancing preclinical drug screening with pathophysiological relevance. Nano Converg. 2021, 8, 12. [Google Scholar] [CrossRef]
- Chen, Z.; Wei, X.; Dong, S.; Han, F.; He, R.; Zhou, W. Challenges and Opportunities Associated with Platelets in Pancreatic Cancer. Front Oncol. 2022, 12, 850485. [Google Scholar] [CrossRef]
- Mai, S.; Inkielewicz-Stepniak, I. Pancreatic cancer and platelets crosstalk: A potential biomarker and target. Front. Cell Dev. Biol. 2021, 9, 749689. [Google Scholar] [CrossRef]
- Whitener, K.E.; Sheehan, P.E. Graphene synthesis. Diam. Relat. Mater. 2014, 46, 25–34. [Google Scholar] [CrossRef]
- Marcano, D.C.; Kosynkin, D.V.; Berlin, J.M.; Sinitskii, A.; Sun, Z.; Slesarev, A.; Alemany, L.B.; Lu, W.; Tour, J.M. Improved Synthesis of Graphene Oxide. ACS Nano 2010, 4, 4806–4814. [Google Scholar] [CrossRef] [PubMed]
- Zhu, Y.; Murali, S.; Cai, W.; Li, X.; Suk, J.W.; Potts, J.R.; Ruoff, R.S. Graphene and Graphene Oxide: Synthesis, Properties, and Applications. Adv. Mater. 2010, 22, 3906–3924. [Google Scholar] [CrossRef]
- Alam, S.N.; Sharma, N.; Kumar, L. Synthesis of Graphene Oxide (GO) by Modified Hummers Method and Its Thermal Reduction to Obtain Reduced Graphene Oxide (rGO). Graphene 2017, 6, 1–18. [Google Scholar] [CrossRef]
- Naik, J.P.; Sutradhar, P.; Saha, M. Molecular scale rapid synthesis of graphene quantum dots (GQDs). J. Nanostructure Chem. 2017, 7, 85–89. [Google Scholar] [CrossRef]
- Jiříčková, A.; Jankovský, O.; Sofer, Z.; Sedmidubský, D. Synthesis and Applications of Graphene Oxide. Materials 2022, 15, 920. [Google Scholar] [CrossRef] [PubMed]
- Sharma, N.; Sharma, V.; Jain, Y.; Kumari, M.; Gupta, R.; Sharma, S.K.; Sachdev, K. Synthesis and Characterization of Graphene Oxide (GO) and Reduced Graphene Oxide (rGO) for Gas Sensing Application. Macromol. Symp. 2017, 376, 1700006. [Google Scholar] [CrossRef]
- Sharma, H.; Mondal, S. Functionalized Graphene Oxide for Chemotherapeutic Drug Delivery and Cancer Treatment: A Promising Material in Nanomedicine. Int. J. Mol. Sci. 2020, 21, 6280. [Google Scholar] [CrossRef] [PubMed]
- Dreyer, D.R.; Park, S.; Bielawski, C.W.; Ruoff, R.S. The chemistry of graphene oxide. Chem. Soc. Rev. 2010, 39, 228–240. [Google Scholar] [CrossRef]
- Sun, L. Structure and synthesis of graphene oxide. Chin. J. Chem. Eng. 2019, 27, 2251–2260. [Google Scholar] [CrossRef]
- Lee, C.; Wei, X.; Kysar, J.W.; Hone, J. Measurement of the elastic properties and intrinsic strength of monolayer graphene. Science 2008, 321, 385–388. [Google Scholar] [CrossRef] [PubMed]
- Mouhat, F.; Coudert, F.-X.; Bocquet, M.-L. Structure and chemistry of graphene oxide in liquid water from first principles. Nat. Commun. 2020, 11, 1566. [Google Scholar] [CrossRef] [PubMed]
- Hu, X.; Yu, Y.; Hou, W.; Zhou, J.; Song, L. Effects of particle size and pH value on the hydrophilicity of graphene oxide. Appl. Surf. Sci. 2013, 273, 118–121. [Google Scholar] [CrossRef]
- Balandin, A.A.; Ghosh, S.; Bao, W.; Calizo, I.; Teweldebrhan, D.; Miao, F.; Lau, C.N. Superior thermal conductivity of single-layer graphene. Nano Lett. 2008, 8, 902–907. [Google Scholar] [CrossRef] [PubMed]
- Baek, S.J.; Hong, W.G.; Park, M.; Kaiser, A.B.; Kim, H.J.; Kim, B.H.; Park, Y.W. The effect of oxygen functional groups on the electrical transport behavior of a single piece multi-layered graphene oxide. Synth. Met. 2014, 191, 1–5. [Google Scholar] [CrossRef]
- Yang, Y.; Cao, J.; Wei, N.; Meng, D.; Wang, L.; Ren, G.; Yan, R.; Zhang, N. Thermal Conductivity of Defective Graphene Oxide: A Molecular Dynamic Study. Molecules 2019, 24, 1103. [Google Scholar] [CrossRef]
- Chaudhary, K.; Kumar, K.; Venkatesu, P.; Masram, D.T. Protein immobilization on graphene oxide or reduced graphene oxide surface and their applications: Influence over activity, structural and thermal stability of protein. Adv. Colloid Interface Sci. 2021, 289, 102367. [Google Scholar] [CrossRef] [PubMed]
- Park, O.-K.; Kim, S.-G.; You, N.-H.; Ku, B.-C.; Hui, D.; Lee, J.H. Synthesis and properties of iodo functionalized graphene oxide/polyimide nanocomposites. Compos. Part B Eng. 2014, 56, 365–371. [Google Scholar] [CrossRef]
- Yao, Y.; Chen, X.; Zhu, J.; Zeng, B.; Wu, Z.; Li, X. The effect of ambient humidity on the electrical properties of graphene oxide films. Nanoscale Res. Lett. 2012, 7, 363. [Google Scholar] [CrossRef]
- Amadei, C.A.; Stein, I.Y.; Silverberg, G.J.; Wardle, B.L.; Vecitis, C.D. Fabrication and morphology tuning of graphene oxide nanoscrolls. Nanoscale 2016, 8, 6783–6791. [Google Scholar] [CrossRef] [PubMed]
- Ghanbari, S.; Ahour, F.; Keshipour, S. An optical and electrochemical sensor based on l-arginine functionalized reduced graphene oxide. Sci. Rep. 2022, 12, 19398. [Google Scholar] [CrossRef]
- Ngqalakwezi, A.; Nkazi, D.; Seifert, G.; Ntho, T. Effects of reduction of graphene oxide on the hydrogen storage capacities of metal graphene nanocomposite. Catal. Today 2020, 358, 338–344. [Google Scholar] [CrossRef]
- Jia, X.; Zhang, E.; Yu, X.; Lu, B. Facile Synthesis of Copper Sulfide Nanosheet@Graphene Oxide for the Anode of Potassium-Ion Batteries. Energy Technol. 2020, 8, 1900987. [Google Scholar] [CrossRef]
- Pereira, G.F.L.; Fileti, E.E.; Siqueira, L.J.A. Performance of supercapacitors containing graphene oxide and ionic liquids by molecular dynamics simulations. Carbon 2023, 208, 102–110. [Google Scholar] [CrossRef]
- Xu, B.; Yue, S.; Sui, Z.; Zhang, X.; Hou, S.; Cao, G.; Yang, Y. What is the choice for supercapacitors: Graphene or graphene oxide? Energy Environ. Sci. 2011, 4, 2826–2830. [Google Scholar] [CrossRef]
- Yao, K.; Manjare, M.; Barrett, C.A.; Yang, B.; Salguero, T.T.; Zhao, Y. Nanostructured Scrolls from Graphene Oxide for Microjet Engines. J. Phys. Chem. Lett. 2012, 3, 2204–2208. [Google Scholar] [CrossRef] [PubMed]
- Naumov, A.V. Optical Properties of Graphene Oxide. In Graphene Oxide; John Wiley and Sons: Hoboken, NJ, USA, 2016; pp. 147–174. [Google Scholar]
- Wu, J.; Jia, L.; Zhang, Y.; Qu, Y.; Jia, B.; Moss, D.J. Graphene Oxide for Integrated Photonics and Flat Optics. Adv. Mater. 2021, 33, 2006415. [Google Scholar] [CrossRef]
- Esmaeili, Y.; Bidram, E.; Zarrabi, A.; Amini, A.; Cheng, C. Graphene oxide and its derivatives as promising In-vitro bio-imaging platforms. Sci. Rep. 2020, 10, 18052. [Google Scholar] [CrossRef]
- Boedtkjer, E.; Pedersen, S.F. The Acidic Tumor Microenvironment as a Driver of Cancer. Annu. Rev. Physiol. 2020, 82, 103–126. [Google Scholar] [CrossRef]
- Zhou, T.; Zhou, X.; Xing, D. Controlled release of doxorubicin from graphene oxide based charge-reversal nanocarrier. Biomaterials 2014, 35, 4185–4194. [Google Scholar] [CrossRef]
- Yang, X.; Wang, Y.; Huang, X.; Ma, Y.; Huang, Y.; Yang, R.; Duan, H.; Chen, Y. Multi-functionalized graphene oxide based anticancer drug-carrier with dual-targeting function and pH-sensitivity. J. Mater. Chem. 2011, 21, 3448–3454. [Google Scholar] [CrossRef]
- Borandeh, S.; Abdolmaleki, A.; Abolmaali, S.S.; Tamaddon, A.M. Synthesis, structural and in-vitro characterization of β-cyclodextrin grafted L-phenylalanine functionalized graphene oxide nanocomposite: A versatile nanocarrier for pH-sensitive doxorubicin delivery. Carbohydr. Polym. 2018, 201, 151–161. [Google Scholar] [CrossRef]
- Kavitha, T.; Abdi, S.I.; Park, S.Y. pH-sensitive nanocargo based on smart polymer functionalized graphene oxide for site-specific drug delivery. Phys. Chem. Chem. Phys. 2013, 15, 5176–5185. [Google Scholar] [CrossRef]
- Wang, P.; Huang, C.; Xing, Y.; Fang, W.; Ren, J.; Yu, H.; Wang, G. NIR-Light- and pH-Responsive Graphene Oxide Hybrid Cyclodextrin-Based Supramolecular Hydrogels. Langmuir 2019, 35, 1021–1031. [Google Scholar] [CrossRef] [PubMed]
- Guo, L.; Shi, H.; Wu, H.; Zhang, Y.; Wang, X.; Wu, D.; An, L.; Yang, S. Prostate cancer targeted multifunctionalized graphene oxide for magnetic resonance imaging and drug delivery. Carbon 2016, 107, 87–99. [Google Scholar] [CrossRef]
- Gonzalez-Rodriguez, R.; Campbell, E.; Naumov, A. Multifunctional graphene oxide/iron oxide nanoparticles for magnetic targeted drug delivery dual magnetic resonance/fluorescence imaging and cancer sensing. PLoS ONE 2019, 14, e0217072. [Google Scholar] [CrossRef]
- Ali, R.; Aziz, M.H.; Gao, S.; Khan, M.I.; Li, F.; Batool, T.; Shaheen, F.; Qiu, B. Graphene oxide/zinc ferrite nanocomposite loaded with doxorubicin as a potential theranostic mediu in cancer therapy and magnetic resonance imaging. Ceram. Int. 2022, 48, 10741–10750. [Google Scholar] [CrossRef]
- Chaudhari, N.S.; Pandey, A.P.; Patil, P.O.; Tekade, A.R.; Bari, S.B.; Deshmukh, P.K. Graphene oxide based magnetic nanocomposites for efficient treatment of breast cancer. Mater. Sci. Eng. C 2014, 37, 278–285. [Google Scholar] [CrossRef]
- Molaei, M.J. Magnetic graphene, synthesis, and applications: A review. Mater. Sci. Eng. B 2021, 272, 115325. [Google Scholar] [CrossRef]
- Guo, Y.; Zhang, X.; Wu, F.-G. A graphene oxide-based switch-on fluorescent probe for glutathione detection and cancer diagnosis. J. Colloid Interface Sci. 2018, 530, 511–520. [Google Scholar] [CrossRef] [PubMed]
- Li, R.; Gao, R.; Wang, Y.; Liu, Z.; Xu, H.; Duan, A.; Zhang, F.; Ma, L. Gastrin releasing peptide receptor targeted nano-graphene oxide for near-infrared fluorescence imaging of oral squamous cell carcinoma. Sci. Rep. 2020, 10, 11434. [Google Scholar] [CrossRef]
- Ma, K.; Xie, W.; Liu, W.; Wang, L.; Wang, D.; Tang, B.Z. Graphene Oxide Based Fluorescent DNA Aptasensor for Liver Cancer Diagnosis and Therapy. Adv. Funct. Mater. 2021, 31, 2102645. [Google Scholar] [CrossRef]
- Liu, L.; Ma, Q.; Cao, J.; Gao, Y.; Han, S.; Liang, Y.; Zhang, T.; Song, Y.; Sun, Y. Recent progress of graphene oxide-based multifunctional nanomaterials for cancer treatment. Cancer Nanotechnol. 2021, 12, 18. [Google Scholar] [CrossRef]
- Fu, Q.; Zhu, R.; Song, J.; Yang, H.; Chen, X. Photoacoustic Imaging: Contrast Agents and Their Biomedical Applications. Adv. Mater 2019, 31, e1805875. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Zhang, H.; Wang, Y.; Wu, H.; Zeng, B.; Zhang, Y.; Tian, Q.; Yang, S. Hydrophilic graphene oxide/bismuth selenide nanocomposites for CT imaging, photoacoustic imaging, and photothermal therapy. J. Mater Chem. B 2017, 5, 1846–1855. [Google Scholar] [CrossRef] [PubMed]
- Moon, H.; Kumar, D.; Kim, H.; Sim, C.; Chang, J.-H.; Kim, J.-M.; Kim, H.; Lim, D.-K. Amplified Photoacoustic Performance and Enhanced Photothermal Stability of Reduced Graphene Oxide Coated Gold Nanorods for Sensitive Photoacoustic Imaging. ACS Nano 2015, 9, 2711–2719. [Google Scholar] [CrossRef]
- Wang, Z.; Sun, X.; Huang, T.; Song, J.; Wang, Y. A Sandwich Nanostructure of Gold Nanoparticle Coated Reduced Graphene Oxide for Photoacoustic Imaging-Guided Photothermal Therapy in the Second NIR Window. Front. Bioeng. Biotechnol. 2020, 8, 655. [Google Scholar] [CrossRef]
- Zhang, Y.; Guo, Z.; Zhu, H.; Xing, W.; Tao, P.; Shang, W.; Fu, B.; Song, C.; Hong, Y.; Dickey, M.D.; et al. Synthesis of Liquid Gallium@Reduced Graphene Oxide Core–Shell Nanoparticles with Enhanced Photoacoustic and Photothermal Performance. J. Am. Chem. Soc. 2022, 144, 6779–6790. [Google Scholar] [CrossRef]
- Chen, J.; Liu, C.; Zeng, G.; You, Y.; Wang, H.; Gong, X.; Zheng, R.; Kim, J.; Kim, C.; Song, L. Indocyanine Green Loaded Reduced Graphene Oxide for In Vivo Photoacoustic/Fluorescence Dual-Modality Tumor Imaging. Nanoscale Res. Lett 2016, 11, 85. [Google Scholar] [CrossRef]
- Okada, M.; Smith, N.I.; Palonpon, A.F.; Endo, H.; Kawata, S.; Sodeoka, M.; Fujita, K. Label-free Raman observation of cytochrome c dynamics during apoptosis. Proc. Natl. Acad. Sci. USA 2012, 109, 28–32. [Google Scholar] [CrossRef] [PubMed]
- Liu, Q.; Wei, L.; Wang, J.; Peng, F.; Luo, D.; Cui, R.; Niu, Y.; Qin, X.; Liu, Y.; Sun, H.; et al. Cell imaging by graphene oxide based on surface enhanced Raman scattering. Nanoscale 2012, 4, 7084–7089. [Google Scholar] [CrossRef]
- Zhang, Z.; Wang, M.; Gao, D.; Luo, D.; Liu, Q.; Yang, J.; Li, Y. Targeted Raman Imaging of Cells Using Graphene Oxide-Based Hybrids. Langmuir 2016, 32, 10253–10258. [Google Scholar] [CrossRef] [PubMed]
- Seo, S.H.; Joe, A.; Han, H.W.; Manivasagan, P.; Jang, E.S. Methylene Blue-Loaded Mesoporous Silica-Coated Gold Nanorods on Graphene Oxide for Synergistic Photothermal and Photodynamic Therapy. Pharmaceutics 2022, 14, 2242. [Google Scholar] [CrossRef]
- Antwi-Boasiako, A.A.; Dunn, D.; Dasary, S.S.R.; Jones, Y.K.; Barnes, S.L.; Singh, A.K. Bioconjugated graphene oxide-based Raman probe for selective identification of SKBR3 breast cancer cells. J. Raman Spectrosc. 2017, 48, 1056–1064. [Google Scholar] [CrossRef]
- Yang, L.; Zhen, S.J.; Li, Y.F.; Huang, C.Z. Silver nanoparticles deposited on graphene oxide for ultrasensitive surface-enhanced Raman scattering immunoassay of cancer biomarker. Nanoscale 2018, 10, 11942–11947. [Google Scholar] [CrossRef] [PubMed]
- Sun, B.; Wu, J.; Cui, S.; Zhu, H.; An, W.; Fu, Q.; Shao, C.; Yao, A.; Chen, B.; Shi, D. In situ synthesis of graphene oxide/gold nanorods theranostic hybrids for efficient tumor computed tomography imaging and photothermal therapy. Nano Res. 2017, 10, 37–48. [Google Scholar] [CrossRef]
- Li, Z.; Tian, L.; Liu, J.; Qi, W.; Wu, Q.; Wang, H.; Ali, M.C.; Wu, W.; Qiu, H. Graphene Oxide/Ag Nanoparticles Cooperated with Simvastatin as a High Sensitive X-Ray Computed Tomography Imaging Agent for Diagnosis of Renal Dysfunctions. Adv. Healthc. Mater. 2017, 6, 1700413. [Google Scholar] [CrossRef]
- Suslova, E.V.; Kozlov, A.P.; Shashurin, D.A.; Rozhkov, V.A.; Sotenskii, R.V.; Maximov, S.V.; Savilov, S.V.; Medvedev, O.S.; Chelkov, G.A. New Composite Contrast Agents Based on Ln and Graphene Matrix for Multi-Energy Computed Tomography. Nanomaterials 2022, 12, 4110. [Google Scholar] [CrossRef]
- Lalwani, G.; Sundararaj, J.L.; Schaefer, K.; Button, T.; Sitharaman, B. Synthesis, characterization, in vitro phantom imaging, and cytotoxicity of a novel graphene-based multimodal magnetic resonance imaging-X-ray computed tomography contrast agent. J. Mater. Chem. B 2014, 2, 3519–3530. [Google Scholar] [CrossRef]
- Dou, R.; Du, Z.; Bao, T.; Dong, X.; Zheng, X.; Yu, M.; Yin, W.; Dong, B.; Yan, L.; Gu, Z. The polyvinylpyrrolidone functionalized rGO/Bi2S3 nanocomposite as a near-infrared light-responsive nanovehicle for chemo-photothermal therapy of cancer. Nanoscale 2016, 8, 11531–11542. [Google Scholar] [CrossRef]
- Zhang, H.; Wu, H.; Wang, J.; Yang, Y.; Wu, D.; Zhang, Y.; Zhang, Y.; Zhou, Z.; Yang, S. Graphene oxide-BaGdF5 nanocomposites for multi-modal imaging and photothermal therapy. Biomaterials 2015, 42, 66–77. [Google Scholar] [CrossRef]
- Divya, K.; Jisha, M.S. Chitosan nanoparticles preparation and applications. Environ. Chem. Lett. 2018, 16, 101–112. [Google Scholar] [CrossRef]
- Hosseini, S.M.; Mazinani, S.; Abdouss, M.; Kalhor, H.; Kalantari, K.; Amiri, I.S.; Ramezani, Z. Designing chitosan nanoparticles embedded into graphene oxide as a drug delivery system. Polym. Bull. 2022, 79, 541–554. [Google Scholar] [CrossRef]
- Li, J.; Cai, C.; Li, J.; Li, J.; Li, J.; Sun, T.; Wang, L.; Wu, H.; Yu, G. Chitosan-Based Nanomaterials for Drug Delivery. Molecules 2018, 23, 2661. [Google Scholar] [CrossRef] [PubMed]
- Yan, T.; Zhang, H.; Huang, D.; Feng, S.; Fujita, M.; Gao, X.-D. Chitosan-Functionalized Graphene Oxide as a Potential Immunoadjuvant. Nanomaterials 2017, 7, 59. [Google Scholar] [CrossRef] [PubMed]
- Zalba, S.; ten Hagen, T.L.M.; Burgui, C.; Garrido, M.J. Stealth nanoparticles in oncology: Facing the PEG dilemma. J. Control. Release 2022, 351, 22–36. [Google Scholar] [CrossRef]
- Sun, X.; Liu, Z.; Welsher, K.; Robinson, J.T.; Goodwin, A.; Zaric, S.; Dai, H. Nano-graphene oxide for cellular imaging and drug delivery. Nano Res. 2008, 1, 203–212. [Google Scholar] [CrossRef]
- Zhou, T.; Zhang, B.; Wei, P.; Du, Y.; Zhou, H.; Yu, M.; Yan, L.; Zhang, W.; Nie, G.; Chen, C.; et al. Energy metabolism analysis reveals the mechanism of inhibition of breast cancer cell metastasis by PEG-modified graphene oxide nanosheets. Biomaterials 2014, 35, 9833–9843. [Google Scholar] [CrossRef]
- Samadian, H.; Mohammad-Rezaei, R.; Jahanban-Esfahlan, R.; Massoumi, B.; Abbasian, M.; Jafarizad, A.; Jaymand, M. A de novo theranostic nanomedicine composed of PEGylated graphene oxide and gold nanoparticles for cancer therapy. J. Mater. Res. 2020, 35, 430–441. [Google Scholar] [CrossRef]
- Lee, S.Y.; Kang, M.S.; Jeong, W.Y.; Han, D.-W.; Kim, K.S. Hyaluronic Acid-Based Theranostic Nanomedicines for Targeted Cancer Therapy. Cancers 2020, 12, 940. [Google Scholar] [CrossRef]
- Vahedi, N.; Tabandeh, F.; Mahmoudifard, M. Hyaluronic acid–graphene quantum dot nanocomposite: Potential target drug delivery and cancer cell imaging. Biotechnol. Appl. Biochem. 2022, 69, 1068–1079. [Google Scholar] [CrossRef]
- Basu, A.; Upadhyay, P.; Ghosh, A.; Bose, A.; Gupta, P.; Chattopadhyay, S.; Chattopadhyay, D.; Adhikary, A. Hyaluronic acid engrafted metformin loaded graphene oxide nanoparticle as CD44 targeted anti-cancer therapy for triple negative breast cancer. Biochim. Biophys. Acta BBA—Gen. Subj. 2021, 1865, 129841. [Google Scholar] [CrossRef] [PubMed]
- Pramanik, N.; Ranganathan, S.; Rao, S.; Suneet, K.; Jain, S.; Rangarajan, A.; Jhunjhunwala, S. A Composite of Hyaluronic Acid-Modified Graphene Oxide and Iron Oxide Nanoparticles for Targeted Drug Delivery and Magnetothermal Therapy. ACS Omega 2019, 4, 9284–9293. [Google Scholar] [CrossRef] [PubMed]
- Aslam, M.; Kalyar, M.A.; Raza, Z.A. Polyvinyl alcohol: A review of research status and use of polyvinyl alcohol based nanocomposites. Polym. Eng. Sci. 2018, 58, 2119–2132. [Google Scholar] [CrossRef]
- Muppalaneni, S.; Omidian, H. Polyvinyl Alcohol in Medicine and Pharmacy: A Perspective. J. Dev. Drugs 2013, 2, 000112. [Google Scholar] [CrossRef]
- Mirzaie, Z.; Reisi-Vanani, A.; Barati, M. Polyvinyl alcohol-sodium alginate blend, composited with 3D-graphene oxide as a controlled release system for curcumin. J. Drug Deliv. Sci. Technol. 2019, 50, 380–387. [Google Scholar] [CrossRef]
- Gholami, A.; Habibi, B.; Hosseini, S.A.; Matin, A.A.; Samadi, N. Controlled release of anticancer drugs via the magnetic magnesium iron nanoparticles modified by graphene oxide and polyvinyl alcohol: Paclitaxel and docetaxel. Nanomed. J. 2021, 8, 200–210. [Google Scholar] [CrossRef]
- Arkaban, H.; Barani, M.; Akbarizadeh, M.R.; Pal Singh Chauhan, N.; Jadoun, S.; Dehghani Soltani, M.; Zarrintaj, P. Polyacrylic Acid Nanoplatforms: Antimicrobial, Tissue Engineering, and Cancer Theranostic Applications. Polymers 2022, 14, 1259. [Google Scholar] [CrossRef]
- Torabi, M.; Yaghoobi, F.; Karimi Shervedani, R.; Kefayat, A.; Ghahremani, F.; Rashidiyan Harsini, P. Mn(II) & Gd(III) deferrioxamine complex contrast agents & temozolomide cancer prodrug immobilized on folic acid targeted graphene/polyacrylic acid nanocarrier: MRI efficiency, drug stability & interactions with cancer cells. Colloids Surf. A Physicochem. Eng. Asp. 2022, 652, 129797. [Google Scholar] [CrossRef]
- Sgarlata, C.; D’Urso, L.; Consiglio, G.; Grasso, G.; Satriano, C.; Forte, G. pH sensitive functionalized graphene oxide as a carrier for delivering gemcitabine: A computational approach. Comput. Theor. Chem. 2016, 1096, 1–6. [Google Scholar] [CrossRef]
- Bharali, D.J.; Sahoo, S.K.; Mozumdar, S.; Maitra, A. Cross-linked polyvinylpyrrolidone nanoparticles: A potential carrier for hydrophilic drugs. J. Colloid Interface Sci. 2003, 258, 415–423. [Google Scholar] [CrossRef] [PubMed]
- Ashjaran, M.; Babazadeh, M.; Akbarzadeh, A.; Davaran, S.; Salehi, R. Stimuli-responsive polyvinylpyrrolidone-NIPPAm-lysine graphene oxide nano-hybrid as an anticancer drug delivery on MCF7 cell line. Artif. Cells Nanomed. Biotechnol. 2019, 47, 443–454. [Google Scholar] [CrossRef]
- Najafabadi, A.P.; Pourmadadi, M.; Yazdian, F.; Rashedi, H.; Rahdar, A.; Díez-Pascual, A.M. pH-sensitive ameliorated quercetin delivery using graphene oxide nanocarriers coated with potential anticancer gelatin-polyvinylpyrrolidone nanoemulsion with bitter almond oil. J. Drug Deliv. Sci. Technol. 2023, 82, 104339. [Google Scholar] [CrossRef]
- Zhang, S.; Yang, K.; Feng, L.; Liu, Z. In vitro and in vivo behaviors of dextran functionalized graphene. Carbon 2011, 49, 4040–4049. [Google Scholar] [CrossRef]
- Xie, M.; Lei, H.; Zhang, Y.; Xu, Y.; Shen, S.; Ge, Y.; Li, H.; Xie, J. Non-covalent modification of graphene oxide nanocomposites with chitosan/dextran and its application in drug delivery. RSC Adv. 2016, 6, 9328–9337. [Google Scholar] [CrossRef]
- Rajeev, M.R.; Manjusha, V.; Anirudhan, T.S. Transdermal delivery of doxorubicin and methotrexate from polyelectrolyte three layer nanoparticle of graphene oxide/polyethyleneimine/dextran sulphate for chemotherapy: In vitro and in vivo studies. Chem. Eng. J. 2023, 466, 143244. [Google Scholar] [CrossRef]
- Ou, L.; Sun, T.; Liu, M.; Zhang, Y.; Zhou, Z.; Zhan, X.; Lu, L.; Zhao, Q.; Lai, R.; Shao, L. Efficient miRNA Inhibitor Delivery with Graphene Oxide-Polyethylenimine to Inhibit Oral Squamous Cell Carcinoma. Int. J. Nanomed. 2020, 15, 1569–1583. [Google Scholar] [CrossRef]
- Hoseini-Ghahfarokhi, M.; Mirkiani, S.; Mozaffari, N.; Abdolahi Sadatlu, M.A.; Ghasemi, A.; Abbaspour, S.; Akbarian, M.; Farjadain, F.; Karimi, M. Applications of Graphene and Graphene Oxide in Smart Drug/Gene Delivery: Is the World Still Flat? Int. J. Nanomed. 2020, 15, 9469–9496. [Google Scholar] [CrossRef]
- Du, S.; Wang, Y.; Ao, J.; Wang, K.; Zhang, Z.; Yang, L.; Liang, X. Targeted Delivery of siRNA to Ovarian Cancer Cells Using Functionalized Graphene Oxide. Nano LIFE 2018, 8, 1850001. [Google Scholar] [CrossRef]
- Wang, Y.; Sun, G.; Gong, Y.; Zhang, Y.; Liang, X.; Yang, L. Functionalized Folate-Modified Graphene Oxide/PEI siRNA Nanocomplexes for Targeted Ovarian Cancer Gene Therapy. Nanoscale Res. Lett. 2020, 15, 57. [Google Scholar] [CrossRef] [PubMed]
- Cao, X.; Zheng, S.; Zhang, S.; Wang, Y.; Yang, X.; Duan, H.; Huang, Y.; Chen, Y. Functionalized Graphene Oxide with Hepatocyte Targeting as Anti-Tumor Drug and Gene Intracellular Transporters. J. Nanosci. Nanotechnol. 2015, 15, 2052–2059. [Google Scholar] [CrossRef] [PubMed]
- Qu, Y.; Sun, F.; He, F.; Yu, C.; Lv, J.; Zhang, Q.; Liang, D.; Yu, C.; Wang, J.; Zhang, X.; et al. Glycyrrhetinic acid-modified graphene oxide mediated siRNA delivery for enhanced liver-cancer targeting therapy. Eur. J. Pharm. Sci. 2019, 139, 105036. [Google Scholar] [CrossRef] [PubMed]
- Sun, Q.; Wang, X.; Cui, C.; Li, J.; Wang, Y. Doxorubicin and anti-VEGF siRNA co-delivery via nano-graphene oxide for enhanced cancer therapy in vitro and in vivo. Int. J. Nanomed. 2018, 13, 3713–3728. [Google Scholar] [CrossRef] [PubMed]
- Mirzaie, V.; Ansari, M.; Nematollahi-Mahani, S.N.; Moballegh Nasery, M.; Karimi, B.; Eslaminejad, T.; Pourshojaei, Y. Nano-Graphene Oxide-supported APTES-Spermine, as Gene Delivery System, for Transfection of pEGFP-p53 into Breast Cancer Cell Lines. Drug Des. Dev. Ther. 2020, 14, 3087–3097. [Google Scholar] [CrossRef] [PubMed]
- Di Santo, R.; Quagliarini, E.; Palchetti, S.; Pozzi, D.; Palmieri, V.; Perini, G.; Papi, M.; Capriotti, A.L.; Laganà, A.; Caracciolo, G. Microfluidic-generated lipid-graphene oxide nanoparticles for gene delivery. Appl. Phys. Lett. 2019, 114, 2733–2741. [Google Scholar] [CrossRef]
- Bugárová, N.; Špitálsky, Z.; Mičušík, M.; Bodík, M.; Šiffalovič, P.; Koneracká, M.; Závišová, V.; Kubovčíková, M.; Kajanová, I.; Zaťovičová, M.; et al. A Multifunctional Graphene Oxide Platform for Targeting Cancer. Cancers 2019, 11, 753. [Google Scholar] [CrossRef]
- Tran, A.V.; Shim, K.; Vo Thi, T.T.; Kook, J.K.; An, S.S.A.; Lee, S.W. Targeted and controlled drug delivery by multifunctional mesoporous silica nanoparticles with internal fluorescent conjugates and external polydopamine and graphene oxide layers. Acta Biomater. 2018, 74, 397–413. [Google Scholar] [CrossRef]
- Chen, S.; Zhang, S.; Wang, Y.; Yang, X.; Yang, H.; Cui, C. Anti-EpCAM functionalized graphene oxide vector for tumor targeted siRNA delivery and cancer therapy. Asian J. Pharm. Sci. 2021, 16, 598–611. [Google Scholar] [CrossRef]
- Li, Y.; Lu, Q.; Liu, H.; Wang, J.; Zhang, P.; Liang, H.; Jiang, L.; Wang, S. Antibody-Modified Reduced Graphene Oxide Films with Extreme Sensitivity to Circulating Tumor Cells. Adv. Mater. 2015, 27, 6848–6854. [Google Scholar] [CrossRef]
- Xiao, H.; Jensen, P.E.; Chen, X. Elimination of Osteosarcoma by Necroptosis with Graphene Oxide-Associated Anti-HER2 Antibodies. Int. J. Mol. Sci. 2019, 20, 4360. [Google Scholar] [CrossRef]
- Sahne, F.; Mohammadi, M.; Najafpour, G.D. Single-Layer Assembly of Multifunctional Carboxymethylcellulose on Graphene Oxide Nanoparticles for Improving in Vivo Curcumin Delivery into Tumor Cells. ACS Biomater. Sci. Eng. 2019, 5, 2595–2609. [Google Scholar] [CrossRef]
- Yang, D.; Feng, L.; Dougherty, C.A.; Luker, K.E.; Chen, D.; Cauble, M.A.; Banaszak Holl, M.M.; Luker, G.D.; Ross, B.D.; Liu, Z.; et al. In vivo targeting of metastatic breast cancer via tumor vasculature-specific nano-graphene oxide. Biomaterials 2016, 104, 361–371. [Google Scholar] [CrossRef] [PubMed]
- Zou, L.; Wang, H.; He, B.; Zeng, L.; Tan, T.; Cao, H.; He, X.; Zhang, Z.; Guo, S.; Li, Y. Current Approaches of Photothermal Therapy in Treating Cancer Metastasis with Nanotherapeutics. Theranostics 2016, 6, 762–772. [Google Scholar] [CrossRef] [PubMed]
- Feng, L.; Wu, L.; Qu, X. New horizons for diagnostics and therapeutic applications of graphene and graphene oxide. Adv. Mater. 2013, 25, 168–186. [Google Scholar] [CrossRef] [PubMed]
- Alemi, F.; Zarezadeh, R.; Sadigh, A.R.; Hamishehkar, H.; Rahimi, M.; Majidinia, M.; Asemi, Z.; Ebrahimi-Kalan, A.; Yousefi, B.; Rashtchizadeh, N. Graphene oxide and reduced graphene oxide: Efficient cargo platforms for cancer theranostics. J. Drug Deliv. Sci. Technol. 2020, 60, 101974. [Google Scholar] [CrossRef]
- Su, S.; Wang, J.; Wei, J.; Martínez-Zaguilán, R.; Qiu, J.; Wang, S. Efficient photothermal therapy of brain cancer through porphyrin functionalized graphene oxide. New J. Chem. 2015, 39, 5743–5749. [Google Scholar] [CrossRef]
- Liu, J.; Yuan, X.; Deng, L.; Yin, Z.; Tian, X.; Bhattacharyya, S.; Liu, H.; Luo, Y.; Luo, L. Graphene oxide activated by 980 nm laser for cascading two-photon photodynamic therapy and photothermal therapy against breast cancer. Appl. Mater. Today 2020, 20, 100665. [Google Scholar] [CrossRef]
- Gong, T.; Wang, X.; Ma, Q.; Li, J.; Li, M.; Huang, Y.; Liang, W.; Su, D.; Guo, R. Triformyl cholic acid and folic acid functionalized magnetic graphene oxide nanocomposites: Multiple-targeted dual-modal synergistic chemotherapy/photothermal therapy for liver cancer. J. Inorg. Biochem. 2021, 223, 111558. [Google Scholar] [CrossRef]
- Deng, X.; Liang, H.; Yang, W.; Shao, Z. Polarization and function of tumor-associated macrophages mediate graphene oxide-induced photothermal cancer therapy. J. Photochem. Photobiol. B Biol. 2020, 208, 111913. [Google Scholar] [CrossRef]
- Wang, C.; Wang, X.; Chen, Y.; Fang, Z. In-vitro photothermal therapy using plant extract polyphenols functionalized graphene sheets for treatment of lung cancer. J. Photochem. Photobiol. B Biol. 2020, 204, 111587. [Google Scholar] [CrossRef]
- Yang, J.; Xia, X.; He, K.; Zhang, M.; Qin, S.; Luo, M.; Wu, L. Green synthesis of reduced graphene oxide (RGO) using the plant extract of Salvia spinosa and evaluation of photothermal effect on pancreatic cancer cells. J. Mol. Struct. 2021, 1245, 131064. [Google Scholar] [CrossRef]
- Shakerian Ardakani, T.; Meidanchi, A.; Shokri, A.; Shakeri-Zadeh, A. Fe3O4@Au/reduced graphene oxide nanostructures: Combinatorial effects of radiotherapy and photothermal therapy on oral squamous carcinoma KB cell line. Ceram. Int. 2020, 46, 28676–28685. [Google Scholar] [CrossRef]
- Tian, B.; Wang, C.; Zhang, S.; Feng, L.; Liu, Z. Photothermally Enhanced Photodynamic Therapy Delivered by Nano-Graphene Oxide. ACS Nano 2011, 5, 7000–7009. [Google Scholar] [CrossRef] [PubMed]
- Li, F.; Park, S.-J.; Ling, D.; Park, W.; Han, J.Y.; Na, K.; Char, K. Hyaluronic acid-conjugated graphene oxide/photosensitizer nanohybrids for cancer targeted photodynamic therapy. J. Mater. Chem. B 2013, 1, 1678–1686. [Google Scholar] [CrossRef]
- Zhou, L.; Jiang, H.; Wei, S.; Ge, X.; Zhou, J.; Shen, J. High-efficiency loading of hypocrellin B on graphene oxide for photodynamic therapy. Carbon 2012, 50, 5594–5604. [Google Scholar] [CrossRef]
- Hosseinzadeh, R.; Khorsandi, K.; Hosseinzadeh, G. Graphene oxide-methylene blue nanocomposite in photodynamic therapy of human breast cancer. J. Biomol. Struct. Dyn. 2018, 36, 2216–2223. [Google Scholar] [CrossRef]
- Guo, S.; Song, Z.; Ji, D.-K.; Reina, G.; Fauny, J.-D.; Nishina, Y.; Ménard-Moyon, C.; Bianco, A. Combined Photothermal and Photodynamic Therapy for Cancer Treatment Using a Multifunctional Graphene Oxide. Pharmaceutics 2022, 14, 1365. [Google Scholar] [CrossRef]
- Guo, W.; Chen, Z.; Feng, X.; Shen, G.; Huang, H.; Liang, Y.; Zhao, B.; Li, G.; Hu, Y. Graphene oxide (GO)-based nanosheets with combined chemo/photothermal/photodynamic therapy to overcome gastric cancer (GC) paclitaxel resistance by reducing mitochondria-derived adenosine-triphosphate (ATP). J. Nanobiotechnol. 2021, 19, 146. [Google Scholar] [CrossRef]
- Ma, M.; Cheng, L.; Zhao, A.; Zhang, H.; Zhang, A. Pluronic-based graphene oxide-methylene blue nanocomposite for photodynamic/photothermal combined therapy of cancer cells. Photodiagnosis Photodyn. Ther. 2020, 29, 101640. [Google Scholar] [CrossRef]
- Shih, C.-Y.; Huang, W.-L.; Chiang, I.T.; Su, W.-C.; Teng, H. Biocompatible hole scavenger–assisted graphene oxide dots for photodynamic cancer therapy. Nanoscale 2021, 13, 8431–8441. [Google Scholar] [CrossRef]
- Liu, F.; Xu, C.; Li, J.; Zhang, Z.; Jin, X.; Wang, B. Nanoarchitectonics of versatile platform based on graphene oxide for precise and enhanced synergistic cancer photothermal-photodynamic/chemotherapy. J. Mol. Struct. 2023, 1294, 136499. [Google Scholar] [CrossRef]
- Mukherjee, S.; Sriram, P.; Barui, A.K.; Nethi, S.K.; Veeriah, V.; Chatterjee, S.; Suresh, K.I.; Patra, C.R. Graphene Oxides Show Angiogenic Properties. Adv. Healthc. Mater. 2015, 4, 1722–1732. [Google Scholar] [CrossRef]
- Qian, Y.; Song, J.; Zhao, X.; Chen, W.; Ouyang, Y.; Yuan, W.; Fan, C. 3D Fabrication with Integration Molding of a Graphene Oxide/Polycaprolactone Nanoscaffold for Neurite Regeneration and Angiogenesis. Adv. Sci. 2018, 5, 1700499. [Google Scholar] [CrossRef]
- Cibecchini, G.; Veronesi, M.; Catelani, T.; Bandiera, T.; Guarnieri, D.; Pompa, P.P. Antiangiogenic Effect of Graphene Oxide in Primary Human Endothelial Cells. ACS Appl. Mater. Interfaces 2020, 12, 22507–22518. [Google Scholar] [CrossRef] [PubMed]
- Al-Janabi, A.H.A.; Hayati Roodbari, N.; Homayouni Tabrizi, M. Investigating the anticancer and anti-angiogenic effects of graphene oxide nanoparticles containing 6-gingerol modified with chitosan and folate. Cancer Nanotechnol. 2023, 14, 69. [Google Scholar] [CrossRef]
- Fiorillo, M.; Verre, A.F.; Iliut, M.; Peiris-Pagés, M.; Ozsvari, B.; Gandara, R.; Cappello, A.R.; Sotgia, F.; Vijayaraghavan, A.; Lisanti, M.P. Graphene oxide selectively targets cancer stem cells, across multiple tumor types: Implications for non-toxic cancer treatment, via “differentiation-based nano-therapy”. Oncotarget 2015, 6, 3553–3562. [Google Scholar] [CrossRef]
- Zuchowska, A.; Buta, A.; Dabrowski, B.; Jastrzebska, E.; Zukowski, K.; Brzozka, Z. 3D and 2D cell models in a novel microfluidic tool for evaluation of highly chemically and microbiologically pure graphene oxide (GO) as an effective drug carrier. Sens. Actuators B Chem. 2020, 302, 127064. [Google Scholar] [CrossRef]
- Kim, C.-H.; Suhito, I.R.; Angeline, N.; Han, Y.; Son, H.; Luo, Z.; Kim, T.-H. Vertically Coated Graphene Oxide Micro-Well Arrays for Highly Efficient Cancer Spheroid Formation and Drug Screening. Adv. Healthc. Mater. 2020, 9, 1901751. [Google Scholar] [CrossRef] [PubMed]
- Grilli, F.; Hassan, E.M.; Variola, F.; Zou, S. Harnessing graphene oxide nanocarriers for siRNA delivery in a 3D spheroid model of lung cancer. Biomater. Sci. 2023, 11, 6635–6649. [Google Scholar] [CrossRef]
- De Lázaro, I.; Sharp, P.; Gurcan, C.; Ceylan, A.; Stylianou, M.; Kisby, T.; Chen, Y.; Vranic, S.; Barr, K.; Taheri, H.; et al. Deep Tissue Translocation of Graphene Oxide Sheets in Human Glioblastoma 3D Spheroids and an Orthotopic Xenograft Model. Adv. Ther. 2021, 4, 2000109. [Google Scholar] [CrossRef]
- Wang, X.; Zhou, W.; Li, X.; Ren, J.; Ji, G.; Du, J.; Tian, W.; Liu, Q.; Hao, A. Graphene oxide suppresses the growth and malignancy of glioblastoma stem cell-like spheroids via epigenetic mechanisms. J. Transl. Med. 2020, 18, 200. [Google Scholar] [CrossRef] [PubMed]
- Dolatkhah, M.; Hashemzadeh, N.; Barar, J.; Adibkia, K.; Aghanejad, A.; Barzegar-Jalali, M.; Omidian, H.; Omidi, Y. Stimuli-responsive graphene oxide and methotrexate-loaded magnetic nanoparticles for breast cancer-targeted therapy. Nanomedicine 2021, 16, 2155–2174. [Google Scholar] [CrossRef]
- Liu, X.; Yang, C.; Chen, P.; Zhang, L.; Cao, Y. The uses of transcriptomics and lipidomics indicated that direct contact with graphene oxide altered lipid homeostasis through ER stress in 3D human brain organoids. Sci. Total Environ. 2022, 849, 157815. [Google Scholar] [CrossRef] [PubMed]
- Park, S.; Kim, Y.J.; Sharma, H.; Kim, D.; Gwon, Y.; Kim, W.; Park, S.; Ha, C.W.; Choung, Y.H.; Kim, J. Graphene Hybrid Inner Ear Organoid with Enhanced Maturity. Nano Lett. 2023, 23, 5573–5580. [Google Scholar] [CrossRef]
- Lee, J.M.; Park, D.Y.; Yang, L.; Kim, E.-J.; Ahrberg, C.D.; Lee, K.-B.; Chung, B.G. Generation of uniform-sized multicellular tumor spheroids using hydrogel microwells for advanced drug screening. Sci. Rep. 2018, 8, 17145. [Google Scholar] [CrossRef] [PubMed]
- Zhang, S.; Ma, B.; Wang, S.; Duan, J.; Qiu, J.; Li, D.; Sang, Y.; Ge, S.; Liu, H. Mass-production of fluorescent chitosan/graphene oxide hybrid microspheres for in vitro 3D expansion of human umbilical cord mesenchymal stem cells. Chem. Eng. J. 2018, 331, 675–684. [Google Scholar] [CrossRef]
- Fiorica, C.; Mauro, N.; Pitarresi, G.; Scialabba, C.; Palumbo, F.S.; Giammona, G. Double-Network-Structured Graphene Oxide-Containing Nanogels as Photothermal Agents for the Treatment of Colorectal Cancer. Biomacromolecules 2017, 18, 1010–1018. [Google Scholar] [CrossRef]
- Askari, E.; Naghib, S.M.; Seyfoori, A.; Maleki, A.; Rahmanian, M. Ultrasonic-assisted synthesis and in vitro biological assessments of a novel herceptin-stabilized graphene using three dimensional cell spheroid. Ultrason. Sonochem. 2019, 58, 104615. [Google Scholar] [CrossRef]
- Kumarasamy, M.; Sosnik, A. Heterocellular spheroids of the neurovascular blood-brain barrier as a platform for personalized nanoneuromedicine. iScience 2021, 24, 102183. [Google Scholar] [CrossRef]
- Jeon, H.; Zhu, R.; Kim, G.; Wang, Y. Chirality-enhanced transport and drug delivery of graphene nanocarriers to tumor-like cellular spheroid. Front Chem. 2023, 11, 1207579. [Google Scholar] [CrossRef]
- Yu, L.; Tian, X.; Gao, D.; Lang, Y.; Zhang, X.-X.; Yang, C.; Gu, M.-M.; Shi, J.; Zhou, P.-K.; Shang, Z.-F. Oral administration of hydroxylated-graphene quantum dots induces intestinal injury accompanying the loss of intestinal stem cells and proliferative progenitor cells. Nanotoxicology 2019, 13, 1409–1421. [Google Scholar] [CrossRef]
- Lee, J.M.; Choi, J.W.; Ahrberg, C.D.; Choi, H.W.; Ha, J.H.; Mun, S.G.; Mo, S.J.; Chung, B.G. Generation of tumor spheroids using a droplet-based microfluidic device for photothermal therapy. Microsyst. Nanoeng. 2020, 6, 52. [Google Scholar] [CrossRef] [PubMed]
- Santhosh, M.; Choi, J.-H.; Choi, J.-W. Magnetic-Assisted Cell Alignment within a Magnetic Nanoparticle-Decorated Reduced Graphene Oxide/Collagen 3D Nanocomposite Hydrogel. Nanomaterials 2019, 9, 1293. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Liu, K.; Feng, L.; Liu, Z.; Xu, L. Comparison of nanomedicine-based chemotherapy, photodynamic therapy and photothermal therapy using reduced graphene oxide for the model system. Biomater. Sci. 2017, 5, 331–340. [Google Scholar] [CrossRef] [PubMed]
- Wychowaniec, J.K.; Litowczenko, J.; Tadyszak, K.; Natu, V.; Aparicio, C.; Peplińska, B.; Barsoum, M.W.; Otyepka, M.; Scheibe, B. Unique cellular network formation guided by heterostructures based on reduced graphene oxide—Ti(3)C(2)T(x) MXene hydrogels. Acta Biomater. 2020, 115, 104–115. [Google Scholar] [CrossRef] [PubMed]
- Souza, S.O.L.D.; Oliveira, S.M.D.; Lehman, C.P.; Silva, M.C.D.; Silva, L.M.; Oréfice, R.L. Tuning the structure and properties of cell-embedded gelatin hydrogels for tumor organoids. Polímeros 2023, 33, e20230014. [Google Scholar] [CrossRef]
- Bao, L.; Cui, X.; Wang, X.; Wu, J.; Guo, M.; Yan, N.; Chen, C. Carbon Nanotubes Promote the Development of Intestinal Organoids through Regulating Extracellular Matrix Viscoelasticity and Intracellular Energy Metabolism. ACS Nano 2021, 15, 15858–15873. [Google Scholar] [CrossRef]
- Rastogi, S.K.; Garg, R.; Scopelliti, M.G.; Pinto, B.I.; Hartung, J.E.; Kim, S.; Murphey, C.G.E.; Johnson, N.; San Roman, D.; Bezanilla, F.; et al. Remote nongenetic optical modulation of neuronal activity using fuzzy graphene. Proc. Natl. Acad. Sci. USA 2020, 117, 13339–13349. [Google Scholar] [CrossRef]
- Xiao, M.; Li, X.; Song, Q.; Zhang, Q.; Lazzarino, M.; Cheng, G.; Ulloa Severino, F.P.; Torre, V. A Fully 3D Interconnected Graphene-Carbon Nanotube Web Allows the Study of Glioma Infiltration in Bioengineered 3D Cortex-Like Networks. Adv. Mater. 2018, 30, e1806132. [Google Scholar] [CrossRef]
- Li, N.; Zhang, Q.; Gao, S.; Song, Q.; Huang, R.; Wang, L.; Liu, L.; Dai, J.; Tang, M.; Cheng, G. Three-dimensional graphene foam as a biocompatible and conductive scaffold for neural stem cells. Sci. Rep. 2013, 3, 1604. [Google Scholar] [CrossRef]
- Kalmykov, A.; Huang, C.; Bliley, J.; Shiwarski, D.; Tashman, J.; Abdullah, A.; Rastogi, S.K.; Shukla, S.; Mataev, E.; Feinberg, A.W.; et al. Organ-on-e-chip: Three-dimensional self-rolled biosensor array for electrical interrogations of human electrogenic spheroids. Sci. Adv. 2019, 5, eaax0729. [Google Scholar] [CrossRef]
- Yin, F.; Hu, K.; Chen, Y.; Yu, M.; Wang, D.; Wang, Q.; Yong, K.-T.; Lu, F.; Liang, Y.; Li, Z. SiRNA Delivery with PEGylated Graphene Oxide Nanosheets for Combined Photothermal and Genetherapy for Pancreatic Cancer. Theranostics 2017, 7, 1133–1148. [Google Scholar] [CrossRef] [PubMed]
- Thapa, R.K.; Ku, S.K.; Choi, H.-G.; Yong, C.S.; Byeon, J.H.; Kim, J.O. Vibrating droplet generation to assemble zwitterion-coated gold-graphene oxide stealth nanovesicles for effective pancreatic cancer chemo-phototherapy. Nanoscale 2018, 10, 1742–1749. [Google Scholar] [CrossRef] [PubMed]
- Papi, M.; Palmieri, V.; Digiacomo, L.; Giulimondi, F.; Palchetti, S.; Ciasca, G.; Perini, G.; Caputo, D.; Cartillone, M.C.; Cascone, C.; et al. Converting the personalized biomolecular corona of graphene oxide nanoflakes into a high-throughput diagnostic test for early cancer detection. Nanoscale 2019, 11, 15339–15346. [Google Scholar] [CrossRef] [PubMed]
- Prasad, K.S.; Cao, X.; Gao, N.; Jin, Q.; Sanjay, S.T.; Henao-Pabon, G.; Li, X. A low-cost nanomaterial-based electrochemical immunosensor on paper for high-sensitivity early detection of pancreatic cancer. Sens. Actuators B Chem. 2020, 305, 127516. [Google Scholar] [CrossRef]
- Yoon, H.J.; Kim, T.H.; Zhang, Z.; Azizi, E.; Pham, T.M.; Paoletti, C.; Lin, J.; Ramnath, N.; Wicha, M.S.; Hayes, D.F.; et al. Sensitive capture of circulating tumour cells by functionalized graphene oxide nanosheets. Nat. Nanotechnol. 2013, 8, 735–741. [Google Scholar] [CrossRef]
- Quagliarini, E.; Caputo, D.; Cammarata, R.; Caracciolo, G.; Pozzi, D. Coupling magnetic levitation of graphene oxide–protein complexes with blood levels of glucose for early detection of pancreatic adenocarcinoma. Cancer Nanotechnol. 2023, 14, 16. [Google Scholar] [CrossRef]
- Jia, X.; Xu, W.; Ye, Z.; Wang, Y.; Dong, Q.; Wang, E.; Li, D.; Wang, J. Functionalized Graphene@Gold Nanostar/Lipid for Pancreatic Cancer Gene and Photothermal Synergistic Therapy under Photoacoustic/Photothermal Imaging Dual-Modal Guidance. Small 2020, 16, 2003707. [Google Scholar] [CrossRef]
- Haqiqian, M.H.; Sardari, D.; Houshyari, M.; Moghadasali, R. Nano-sheets of Graphene Oxide Enhance the Combined Effect of Hyperthermia and Radiation Treatment in Pancreatic Cancer Cell Lines. Curr. Nanosci. 2021, 17, 779–788. [Google Scholar] [CrossRef]
- Wójcik, B.; Sawosz, E.; Szczepaniak, J.; Strojny, B.; Sosnowska, M.; Daniluk, K.; Zielińska-Górska, M.; Bałaban, J.; Chwalibog, A.; Wierzbicki, M. Effects of Metallic and Carbon-Based Nanomaterials on Human Pancreatic Cancer Cell Lines AsPC-1 and BxPC-3. Int. J. Mol. Sci. 2021, 22, 12100. [Google Scholar] [CrossRef]
- Caputo, D.; Coppola, A.; Quagliarini, E.; Di Santo, R.; Capriotti, A.L.; Cammarata, R.; Laganà, A.; Papi, M.; Digiacomo, L.; Coppola, R.; et al. Multiplexed Detection of Pancreatic Cancer by Combining a Nanoparticle-Enabled Blood Test and Plasma Levels of Acute-Phase Proteins. Cancers 2022, 14, 4658. [Google Scholar] [CrossRef] [PubMed]
- Caputo, D.; Digiacomo, L.; Cascone, C.; Pozzi, D.; Palchetti, S.; Di Santo, R.; Quagliarini, E.; Coppola, R.; Mahmoudi, M.; Caracciolo, G. Synergistic Analysis of Protein Corona and Haemoglobin Levels Detects Pancreatic Cancer. Cancers 2020, 13, 93. [Google Scholar] [CrossRef]
- Di Santo, R.; Digiacomo, L.; Quagliarini, E.; Capriotti, A.L.; Laganà, A.; Zenezini Chiozzi, R.; Caputo, D.; Cascone, C.; Coppola, R.; Pozzi, D.; et al. Personalized Graphene Oxide-Protein Corona in the Human Plasma of Pancreatic Cancer Patients. Front. Bioeng. Biotechnol. 2020, 8, 491. [Google Scholar] [CrossRef] [PubMed]
- Kang, S.; Kim, K.M.; Jung, K.; Son, Y.; Mhin, S.; Ryu, J.H.; Shim, K.B.; Lee, B.; Han, H.; Song, T. Graphene Oxide Quantum Dots Derived from Coal for Bioimaging: Facile and Green Approach. Sci. Rep. 2019, 9, 4101. [Google Scholar] [CrossRef] [PubMed]
- Nigam, P.; Waghmode, S.; Louis, M.; Wangnoo, S.; Chavan, P.; Sarkar, D. Graphene quantum dots conjugated albumin nanoparticles for targeted drug delivery and imaging of pancreatic cancer. J. Mater. Chem. B 2014, 2, 3190–3195. [Google Scholar] [CrossRef]
- Garriga, R.; Jurewicz, I.; Seyedin, S.; Bardi, N.; Totti, S.; Matta-Domjan, B.; Velliou, E.G.; Alkhorayef, M.A.; Cebolla, V.L.; Razal, J.M.; et al. Multifunctional, biocompatible and pH-responsive carbon nanotube- and graphene oxide/tectomer hybrid composites and coatings. Nanoscale 2017, 9, 7791–7804. [Google Scholar] [CrossRef] [PubMed]
- Ajgaonkar, R.; Lee, B.; Valimukhametova, A.; Nguyen, S.; Gonzalez-Rodriguez, R.; Coffer, J.; Akkaraju, G.R.; Naumov, A.V. Detection of Pancreatic Cancer miRNA with Biocompatible Nitrogen-Doped Graphene Quantum Dots. Materials 2022, 15, 5760. [Google Scholar] [CrossRef] [PubMed]
- Yoon, H.J.; Shanker, A.; Wang, Y.; Kozminsky, M.; Jin, Q.; Palanisamy, N.; Burness, M.L.; Azizi, E.; Simeone, D.M.; Wicha, M.S.; et al. Tunable Thermal-Sensitive Polymer-Graphene Oxide Composite for Efficient Capture and Release of Viable Circulating Tumor Cells. Adv. Mater. 2016, 28, 4891–4897. [Google Scholar] [CrossRef]
- Du, X.; Zheng, X.; Zhang, Z.; Wu, X.; Sun, L.; Zhou, J.; Liu, M. A Label-Free Electrochemical Immunosensor for Detection of the Tumor Marker CA242 Based on Reduced Graphene Oxide-Gold-Palladium Nanocomposite. Nanomaterials 2019, 9, 1335. [Google Scholar] [CrossRef]
- Wu, J.; Li, Z.; Li, Y.; Pettitt, A.; Zhou, F. Photothermal Effects of Reduced Graphene Oxide on Pancreatic Cancer. Technol. Cancer Res. Treat. 2018, 17, 1533034618768637. [Google Scholar] [CrossRef] [PubMed]
- Yu, Y.; Liang, C.; Wan, Q.Q.; Jin, D.; Liu, X.; Zhang, Z.; Sun, Z.Y.; Zhang, G.J. Integrated FET sensing microsystem for specific detection of pancreatic cancer exosomal miRNA10b. Anal. Chim. Acta 2023, 1284, 341995. [Google Scholar] [CrossRef] [PubMed]
- Akin, M.; Bekmezci, M.; Bayat, R.; Coguplugil, Z.K.; Sen, F.; Karimi, F.; Karimi-Maleh, H. Mobile device integrated graphene oxide quantum dots based electrochemical biosensor design for detection of miR-141 as a pancreatic cancer biomarker. Electrochim. Acta 2022, 435, 141390. [Google Scholar] [CrossRef]
- Xiao, G.; Ge, H.; Yang, Q.; Zhang, Z.; Cheng, L.; Cao, S.; Ji, J.; Zhang, J.; Yue, Z. Light-addressable photoelectrochemical sensors for multichannel detections of GPC1, CEA and GSH and its applications in early diagnosis of pancreatic cancer. Sens. Actuators B Chem. 2022, 372, 132663. [Google Scholar] [CrossRef]
- Chiu, N.-F.; Lin, T.-L.; Kuo, C.-T. Highly sensitive carboxyl-graphene oxide-based surface plasmon resonance immunosensor for the detection of lung cancer for cytokeratin 19 biomarker in human plasma. Sens. Actuators B Chem. 2018, 265, 264–272. [Google Scholar] [CrossRef]
- Gieseck Iii, R.L.; Hannan, N.R.F.; Bort, R.; Hanley, N.A.; Drake, R.A.L.; Cameron, G.W.W.; Wynn, T.A.; Vallier, L. Maturation of Induced Pluripotent Stem Cell Derived Hepatocytes by 3D-Culture. PLoS ONE 2014, 9, e86372. [Google Scholar] [CrossRef] [PubMed]
- Georgakopoulos, N.; Prior, N.; Angres, B.; Mastrogiovanni, G.; Cagan, A.; Harrison, D.; Hindley, C.J.; Arnes-Benito, R.; Liau, S.-S.; Curd, A.; et al. Long-term expansion, genomic stability and in vivo safety of adult human pancreas organoids. BMC Dev. Biol. 2020, 20, 4. [Google Scholar] [CrossRef] [PubMed]
- Sachs, N.; Clevers, H. Organoid cultures for the analysis of cancer phenotypes. Curr. Opin. Genet. Dev. 2014, 24, 68–73. [Google Scholar] [CrossRef]
- Romero-Calvo, I.; Weber, C.R.; Ray, M.; Brown, M.; Kirby, K.; Nandi, R.K.; Long, T.M.; Sparrow, S.M.; Ugolkov, A.; Qiang, W.; et al. Human Organoids Share Structural and Genetic Features with Primary Pancreatic Adenocarcinoma Tumors. Mol. Cancer Res. 2019, 17, 70–83. [Google Scholar] [CrossRef]
- Usman, O.H.; Zhang, L.; Xie, G.; Kocher, H.M.; Hwang, C.-i.; Wang, Y.J.; Mallory, X.; Irianto, J. Genomic heterogeneity in pancreatic cancer organoids and its stability with culture. NPJ Genom. Med. 2022, 7, 71. [Google Scholar] [CrossRef]
- Lai Benjamin, F.L.; Lu Rick, X.; Hu, Y.; Davenport, H.L.; Dou, W.; Wang, E.Y.; Radulovich, N.; Tsao, M.S.; Sun, Y.; Radisic, M. Recapitulating pancreatic tumor microenvironment through synergistic use of patient organoids and organ-on-a-chip vasculature. Adv. Funct. Mater. 2020, 30, 2000545. [Google Scholar] [CrossRef] [PubMed]
- Martinez Paino, I.M.; Santos, F.; Zucolotto, V. Biocompatibility and toxicology effects of graphene oxide in cancer, normal, and primary immune cells. J. Biomed. Mater. Res. A 2017, 105, 728–736. [Google Scholar] [CrossRef] [PubMed]
- Shams, M.; Guiney, L.M.; Huang, L.; Ramesh, M.; Yang, X.; Hersam, M.C.; Chowdhury, I. Influence of functional groups on the degradation of graphene oxide nanomaterials. Environ. Sci. Nano 2019, 6, 2203–2214. [Google Scholar] [CrossRef]
- Kumar, S.; Kumar, S.; Srivastava, S.; Yadav, B.K.; Lee, S.H.; Sharma, J.G.; Doval, D.C.; Malhotra, B.D. Reduced graphene oxide modified smart conducting paper for cancer biosensor. Biosens. Bioelectron. 2015, 73, 114–122. [Google Scholar] [CrossRef] [PubMed]
- Kang, S.; Lee, J.; Ryu, S.; Kwon, Y.; Kim, K.-H.; Jeong, D.H.; Paik, S.R.; Kim, B.-S. Gold Nanoparticle/Graphene Oxide Hybrid Sheets Attached on Mesenchymal Stem Cells for Effective Photothermal Cancer Therapy. Chem. Mater. 2017, 29, 3461–3476. [Google Scholar] [CrossRef]
- Neklyudov, V.V.; Khafizov, N.R.; Sedov, I.A.; Dimiev, A.M. New insights into the solubility of graphene oxide in water and alcohols. Phys. Chem. Chem. Phys. 2017, 19, 17000–17008. [Google Scholar] [CrossRef] [PubMed]
- Ali, J.; Li, Y.; Shang, E.; Wang, X.; Zhao, J.; Mohiuddin, M.; Xia, X. Aggregation of graphene oxide and its environmental implications in the aquatic environment. Chin. Chem. Lett. 2023, 34, 107327. [Google Scholar] [CrossRef]
- Ghulam, A.N.; Dos Santos, O.A.; Hazeem, L.; Pizzorno Backx, B.; Bououdina, M.; Bellucci, S. Graphene oxide (GO) materials—Applications and toxicity on living organisms and environment. J. Funct. Biomater. 2022, 13, 77. [Google Scholar] [CrossRef]
- Tiwari, S.K.; Mishra, R.K.; Ha, S.K.; Huczko, A. Evolution of graphene oxide and graphene: From imagination to industrialization. ChemNanoMat 2018, 4, 598–620. [Google Scholar] [CrossRef]
- Cho, H.; Kim, S.-m.; Liang, H.; Kim, S. Electric-potential-induced uniformity in graphene oxide deposition on porous alumina substrates. Ceram. Int. 2020, 46, 14828–14839. [Google Scholar] [CrossRef]
- Huch, M.; Bonfanti, P.; Boj, S.F.; Sato, T.; Loomans, C.J.; Van De Wetering, M.; Sojoodi, M.; Li, V.S.; Schuijers, J.; Gracanin, A. Unlimited in vitro expansion of adult bi-potent pancreas progenitors through the Lgr5/R-spondin axis. EMBO J. 2013, 32, 2708–2721. [Google Scholar] [CrossRef]
- Ren, Y.; Yang, X.; Ma, Z.; Sun, X.; Zhang, Y.; Li, W.; Yang, H.; Qiang, L.; Yang, Z.; Liu, Y.; et al. Developments and Opportunities for 3D Bioprinted Organoids. Int. J. Bioprint. 2021, 7, 364. [Google Scholar] [CrossRef]
- Zheng, F.; Xiao, Y.; Liu, H.; Fan, Y.; Dao, M. Patient-Specific Organoid and Organ-on-a-Chip: 3D Cell-Culture Meets 3D Printing and Numerical Simulation. Adv. Biol. 2021, 5, 2000024. [Google Scholar] [CrossRef] [PubMed]
- Rawal, P.; Tripathi, D.M.; Ramakrishna, S.; Kaur, S. Prospects for 3D bioprinting of organoids. Bio-Des. Manuf. 2021, 4, 627–640. [Google Scholar] [CrossRef]
- Hirt, C.K.; Booij, T.H.; Grob, L.; Simmler, P.; Toussaint, N.C.; Keller, D.; Taube, D.; Ludwig, V.; Goryachkin, A.; Pauli, C. Drug screening and genome editing in human pancreatic cancer organoids identifies drug-gene interactions and candidates for off-label therapy. Cell Genom. 2022, 2, 100095. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Wu, W.; Wang, Y.; Han, S.; Yuan, Y.; Huang, J.; Shuai, X.; Peng, Z. Recent development of gene therapy for pancreatic cancer using non-viral nanovectors. Biomater. Sci. 2021, 9, 6673–6690. [Google Scholar] [CrossRef] [PubMed]
- Cui, L.; Chen, Z.; Zhu, Z.; Lin, X.; Chen, X.; Yang, C.J. Stabilization of ssRNA on graphene oxide surface: An effective way to design highly robust RNA probes. Anal. Chem. 2013, 85, 2269–2275. [Google Scholar] [CrossRef]
- Vincent, M.; De Lázaro, I.; Kostarelos, K. Graphene materials as 2D non-viral gene transfer vector platforms. Gene Ther. 2017, 24, 123–132. [Google Scholar] [CrossRef] [PubMed]
- Beelen, N.A.; Aberle, M.R.; Bruno, V.; Olde Damink, S.W.M.; Bos, G.M.J.; Rensen, S.S.; Wieten, L. Antibody-dependent cellular cytotoxicity-inducing antibodies enhance the natural killer cell anti-cancer response against patient-derived pancreatic cancer organoids. Front. Immunol. 2023, 14, 1133796. [Google Scholar] [CrossRef]
- Liu, W.; Zhang, X.; Zhou, L.; Shang, L.; Su, Z. Reduced graphene oxide (rGO) hybridized hydrogel as a near-infrared (NIR)/pH dual-responsive platform for combined chemo-photothermal therapy. J. Colloid Interface Sci. 2019, 536, 160–170. [Google Scholar] [CrossRef]
- Costa, V.C.d.S. Preclinical Testing of Theranostic Graphene-Based Magnetic Nanocarriers in 2D and 3D Hepatocellular Carcinoma Models; University of Minho: Braga, Portugal, 2021. [Google Scholar]
- Darrigues, E.; Nima, Z.A.; Griffin, R.J.; Anderson, J.M.; Biris, A.S.; Rodriguez, A. 3D cultures for modeling nanomaterial-based photothermal therapy. Nanoscale Horiz. 2020, 5, 400–430. [Google Scholar] [CrossRef] [PubMed]
- You, M.; Zhu, H.; Li, Z.; Ye, E. Photothermal Nanomaterials for Oncological Hyperthermia. In Photothermal Nanomaterials; The Royal Society of Chemistry: London, UK, 2022; pp. 321–333. [Google Scholar]
- Zhou, C.; Wu, H.; Wang, M.; Huang, C.; Yang, D.; Jia, N. Functionalized graphene oxide/Fe3O4 hybrids for cellular magnetic resonance imaging and fluorescence labeling. Mater. Sci. Eng. C 2017, 78, 817–825. [Google Scholar] [CrossRef] [PubMed]
- Thakkar, S.; Sharma, D.; Kalia, K.; Tekade, R.K. Tumor microenvironment targeted nanotherapeutics for cancer therapy and diagnosis: A review. Acta Biomater. 2020, 101, 43–68. [Google Scholar] [CrossRef] [PubMed]
- Barar, J.; Omidi, Y. Dysregulated pH in tumor microenvironment checkmates cancer therapy. BioImpacts BI 2013, 3, 149. [Google Scholar]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Mai, S.; Inkielewicz-Stepniak, I. Graphene Oxide Nanoparticles and Organoids: A Prospective Advanced Model for Pancreatic Cancer Research. Int. J. Mol. Sci. 2024, 25, 1066. https://doi.org/10.3390/ijms25021066
Mai S, Inkielewicz-Stepniak I. Graphene Oxide Nanoparticles and Organoids: A Prospective Advanced Model for Pancreatic Cancer Research. International Journal of Molecular Sciences. 2024; 25(2):1066. https://doi.org/10.3390/ijms25021066
Chicago/Turabian StyleMai, Shaoshan, and Iwona Inkielewicz-Stepniak. 2024. "Graphene Oxide Nanoparticles and Organoids: A Prospective Advanced Model for Pancreatic Cancer Research" International Journal of Molecular Sciences 25, no. 2: 1066. https://doi.org/10.3390/ijms25021066