Development of Biodegradable GQDs-hMSNs for Fluorescence Imaging and Dual Cancer Treatment via Photodynamic Therapy and Drug Delivery
Abstract
:1. Introduction
2. Resultes and Discussion
2.1. Design of GQDs-hMSNs and Synthesis
2.2. Characterization of GQDs-hMSNs
2.2.1. Size Distribution and Surface Morphology
2.2.2. Functional Group Formation and Elemental Composition
2.2.3. Optical Properties and pH Effects
2.3. GQDs-hMSNs Biodegradation
2.4. Cell Viability, In Vitro Cell Imaging, PDT Treatment, and Mock Drug Delivery of GQDs-hMSNs
3. Methods and Materials
3.1. Materials and Sample Preparations
3.2. Instrumentation Used for the Characterization and Analysis of GQDs-hMSNs
3.3. Synthesis of GQDs-hMSNs
3.4. Cell Toxicity
3.5. Cell Imaging, PDT, and Drug Delivery
4. Conclusions
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Sung, H.; Ferlay, J.; Siegel, R.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2021, 71, 209. [Google Scholar] [CrossRef]
- Palesh, O.; Scheiber, C.; Kesler, S.; Mustian, K.; Koopman, C.; Schapira, L. Management of side effects during and post-treatment in breast cancer survivors. Breast J. 2017, 24, 167. [Google Scholar] [CrossRef]
- Liu, Y.; Wang, X.; He, D.; Cheng, Y. Protection against chemotherapy-and radiotherapy-induced side effects: A review based on the mechanisms and therapeutic opportunities of phytochemicals. Phytomedicine 2021, 80, 153402. [Google Scholar] [CrossRef]
- CDC. Cancer Patients: Diagnosis and Treatment|CDC. Available online: https://www.cdc.gov/cancer/survivors/patients/index.htm (accessed on 31 March 2022).
- NIH. Side Effects of Cancer Treatment—National Cancer Institute. Available online: https://www.cdc.gov/cancer/survivors/patients/side-effects-of-treatment.htm (accessed on 31 March 2022).
- Pucci, C.; Martinelli, C.; Ciofani, G. Innovative approaches for cancer treatment: Current perspectives and new challenges. Ecancermedicalscience 2019, 13, 961. [Google Scholar] [CrossRef] [PubMed]
- Barroso-Sousa, R.; Tolaney, S. Clinical development of new antibody-drug conjugates in breast cancer: To infinity and beyond. BioDrugs 2021, 35, 159. [Google Scholar] [CrossRef]
- Broadfield, L.; Pane, A.; Talebi, A.; Swinnen, J.; Fendt, S. Lipid metabolism in cancer: New perspectives and emerging mechanisms. Dev. Cell 2021, 56, 1363. [Google Scholar] [CrossRef]
- Gavas, S.; Quazi, S.; Karpinski, T. Nanoparticles for cancer therapy: Current progress and challenges. Nanoscale Res. Lett. 2021, 16, 173. [Google Scholar] [CrossRef]
- Jain, R.; Vithalani, R.; Patel, D.; Lad, U.; Modi, C.; Suthar, D.; Solanki, J.; Surati, K. Highly fluorescent nitrogen-doped graphene quantum dots (N-GQDs) as an efficient nanoprobe for imaging of microbial cells. Fuller. Nanotub. Carbon Nanostruct. 2021, 29, 588–595. [Google Scholar] [CrossRef]
- Fan, Z.; Li, S.; Yuan, F.; Fan, L. Fluorescent graphene quantum dots for biosensing and bioimaging. RSC Adv. 2015, 5, 19773. [Google Scholar] [CrossRef]
- Wang, Z.; Liu, Z.; Gu, B.; Gao, B.; Wang, T.; Zheng, X.; Wang, G.; Guo, Q.; Chen, D. Ultraviolet light-driven controllable doping of graphene quantum dots with tunable emission wavelength for fluorescence bio-imaging. Mater. Lett. 2020, 266, 127468. [Google Scholar] [CrossRef]
- El-Shaheny, R.; Yoshida, S.; Fuchigami, T. Graphene quantum dots as a nanoprobe for analysis of o- and p-nitrophenols in environmental water adopting conventional fluorometry and smartphone image processing-assisted paper-based analytical device. In-depth study of sensing mechanisms. Microchem. J. 2020, 158, 105241. [Google Scholar] [CrossRef]
- Su, J.; Zhang, X.; Tong, X.; Wang, X.; Yang, P.; Yao, F.; Guo, R.; Yuan, C. Preparation of graphene quantum dots with high quantum yield by a facile one-step method and applications for cell imaging. Mater. Lett. 2020, 271, 127806. [Google Scholar] [CrossRef]
- Fan, H.; Yu, X.; Wang, K.; Yin, Y.; Tang, Y.; Tang, Y.; Liang, X. Graphene quantum dots (GQDs)-based nanomaterials for improving photodynamic therapy in cancer treatment. Eur. J. Med. Chem. 2019, 182, 111620. [Google Scholar] [CrossRef]
- Tabish, T.; Scotton, C.; Ferguson, D.; Lin, L.; van der Veen, A.; Lory, S.; Ali, M.; Jabeen, F.; Ali, M.; Winyard, P.; et al. Biocompatibility and toxicity of graphene quantum dots for potential application in photodynamic therapy. Nanomedicine 2018, 13, 1923. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aggarwal, V.; Singh Tuli, G.; Varol, A.; Thakral, F.; Betul Yerer, M.; Sak, K.; Varol, M.; Jain, A.; Khan, A.; Sethi, G. Role of reactive oxygen species in cancer progression: Molecular mechanisms and recent advancements. Biomolecules 2019, 9, 735. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Perillo, B.; Di Donato, M.; Pezone, A.; Di Zazzo, E.; Giovannelli, P.; Galasso, G.; Castoria, G.; Migliaccio, A. ROS in cancer therapy: The bright side of the moon. Exp. Mol. Med. 2020, 52, 192. [Google Scholar] [CrossRef] [PubMed]
- Lin, L.; Wang, J.; Song, J.; Liu, Y.; Zhu, G.; Dai, Y.; Shen, Z.; Tian, R.; Song, J.; Wang, Z.; et al. Cooperation of endogenous and exogenous reactive oxygen species induced by zinc peroxide nanoparticles to enhance oxidative stress-based cancer therapy. Theragnostics 2019, 9, 7200–7209. [Google Scholar] [CrossRef]
- Zhang, C.; Wang, X.; Du, J.; Gu, Z.; Zhao, Y. Reactive oxygen species—Regulating strategies based on nanomaterials for disease treatment. Adv. Sci. 2020, 8, 2002797. [Google Scholar] [CrossRef] [PubMed]
- Sarbadhikary, P.; George, B.; Abrahamse, H. Recent advances in photosensitizers as multifunctional theranostic agents for imaging-guided photodynamic therapy of cancer. Theranostics 2021, 11, 9054. [Google Scholar] [CrossRef] [PubMed]
- Mroz, P.; Yaroslavsky, A.; Kharkwal, G.; Hamblin, M. Cell death pathways in photodynamic therapy of cancer. Cancers 2011, 3, 2516. [Google Scholar] [CrossRef] [PubMed]
- Choi, S.; Baek, S.; Chang, S.; Song, Y.; Rafique, R.; Lee, K.; Park, T. Synthesis of upconversion nanoparticles conjugated with graphene quantum dots and their use against cancer cell imaging and photodynamic therapy. Biosens. Bioelectron. 2017, 93, 267. [Google Scholar] [CrossRef]
- Li, Z.; Wang, D.; Xu, M.; Wang, J.; Hu, X.; Sadat, A.; Tedesco, A.; Morais, P.; Bi, H. Fluorine-containing graphene quantum dots with a high singlet oxygen generation applied for photodynamic therapy. J. Mater. Chem. B 2020, 8, 2598. [Google Scholar] [CrossRef] [PubMed]
- Wang, M.; Li, B.; Du, T.; Bu, H.; Tang, Y.; Huang, Q. Fluorescence imaging-guided cancer photothermal therapy using polydopamine and graphene quantum dot-capped Prussian blue nanocubes. RSC Adv. 2021, 11, 8420. [Google Scholar] [CrossRef]
- Zhao, C.; Song, X.; Liu, Y.; Fu, Y.; Ye, L.; Wang, N.; Wang, F.; Li, L.; Mohammadniaei, M.; Zhang, M.; et al. Synthesis of graphene quantum dots and their application in drug delivery. J. Nanobiotechnol. 2020, 18, 142. [Google Scholar] [CrossRef] [PubMed]
- Tian, P.; Tang, L.; Teng, K.; Lau, S. Graphene quantum dots from chemistry to applications. Mater. Today Chem. 2018, 10, 221–258. [Google Scholar] [CrossRef]
- Yan, C.; Hu, X.; Guan, P.; Hou, T.; Chen, P.; Wan, D.; Zhang, X.; Wang, J.; Wang, C. Highly biocompatible graphene quantum dots: Green synthesis, toxicity comparison and fluorescence imaging. J. Mater. Sci. 2020, 55, 1198–1215. [Google Scholar] [CrossRef]
- Malavika, J.; Shobana, C.; Sundarraj, S.; Ganeshbabu, M.; Kumar, P.; Selvan, R. Green synthesis of multifunctional carbon quantum dots: An approach in cancer theranostics. Biomater. Adv. 2022, 136, 212756. [Google Scholar] [CrossRef]
- Liu, Q.; Zhou, Y.; Li, M.; Zhao, L.; Ren, J.; Li, D.; Tan, Z.; Wang, K.; Li, H.; Hussain, M.; et al. Polyethyleneimine hybrid thing-shell hollow mesoporous silica nanoparticles as vaccine self-adjuvants for cancer immunotherapy. ACS Appl. Mater. Interfaces 2019, 11, 47798. [Google Scholar] [CrossRef] [PubMed]
- Möller, K.; Bein, T. Degradable drug carriers: Vanishing mesoporous silica nanoparticles. Chem. Mater. 2019, 31, 4364. [Google Scholar] [CrossRef]
- Zhang, B.; Liu, Q.; Liu, M.; Shi, P.; Zhu, L.; Zhang, L.; Li, R. Biodegradable hybrid mesoporous silica nanoparticles for gene/chemo-synergetic therapy of breast cancer. J. Biomater. Appl. 2019, 33, 1382. [Google Scholar] [CrossRef]
- Gao, F.; Wu, J.; Niu, S.; Sun, T.; Li, F.; Bai, Y.; Jin, L.; Lin, L.; Shi, Q.; Zhu, L.; et al. Biodegradable, pH-sensitive hollow mesoporous organosilica nanoparticle (HMON) with controlled release of Pirfenidone and ultrasound-target-microbubble-destruction (UTMD) for pancreatic cancer treatment. Theranostics 2019, 9, 6002. [Google Scholar] [CrossRef] [PubMed]
- Lu, N.; Fan, W.; Yi, X.; Wang, S.; Wang, Z.; Tian, R.; Jacobson, O.; Liu, Y.; Yung, B.; Zhang, G.; et al. Biodegradable hollow mesoporous organosilica nanotheranostics for mild hyperthermia-induced bubble-enhanced oxygen-sensitized radiotherapy. ACS Nano 2018, 12, 1580. [Google Scholar] [CrossRef] [PubMed]
- Liberman, A.; Mendez, N.; Trogler, W.; Kummel, A. Synthesis and surface functionalization of silica nanoparticles for nanomedicine. Surf. Sci. Rep. 2014, 69, 132. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, J.; Shen, S.; Kong, F.; Jiang, T.; Tang, C.; Yin, C. Effects of pore size on in vitro and in vivo anticancer efficacies of mesoporous silica nanoparticles. RSC Adv. 2018, 8, 24633. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gao, Y.; Zhong, S.; Xu, L.; He, S.; Dou, Y.; Zhao, S.; Chen, P.; Cui, X. Mesoporous silica nanoparticles capped with graphene quantum dots as multifunctional drug carriers for photo-thermal and redox-responsive release. Micropor. Mesopor. Mater. 2019, 278, 130. [Google Scholar] [CrossRef]
- Vallet-Regí, M.; Colilla, M.; Izquierdo-Barba, I.; Manzano, M. Mesoporous silica nanoparticles for drug delivery: Current insights. Molecules 2018, 23, 47. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, J.; Luo, Z.; Zhang, J.; Luo, T.; Zhou, J.; Zhao, X.; Cai, K. Hollow mesoporous silica nanoparticles facilitated drug delivery via cascade pH stimuli in tumor microenvironment for tumor therapy. Biomaterials 2016, 83, 51. [Google Scholar] [CrossRef]
- Flak, D.; Przysiecka, L. GQDs-MSNs nanocomposite nanoparticles for simultaneous intracellular drug delivery and fluorescent imaging. J. Nanopart. Res. 2018, 20, 306. [Google Scholar] [CrossRef] [Green Version]
- Dong, J.; Yao, X.; Sun, S.; Zhong, Y.; Qian, C.; Yang, D. In vivo targeting of breast cancer with a vasculature-specific GQDs/hMSN nanoplatform. RSC Adv. 2019, 9, 11576. [Google Scholar] [CrossRef] [Green Version]
- Dong, J.; Zhang, Y.; Guo, P.; Xu, H.; Wang, Y.; Yang, D. GQDs/hMSN nanoplatform; singlet oxygen generation for photodynamic therapy. J. Drug Deliv. Sci. Technol. 2020, 61, 102127. [Google Scholar] [CrossRef]
- Yang, D.; Yao, X.; Dong, J.; Wang, N.; Du, Y.; Sun, S.; Gao, L.; Zhong, Y.; Qian, C.; Hong, H. Design and investigation of core/shell GQDs/hMSN nanoparticles as an enhanced drug delivery platform in triple-negative breast cancer. Bioconjug. Chem. 2018, 29, 2776. [Google Scholar] [CrossRef]
- Chen, F.; Gao, W.; Qui, X.; Zhang, H.; Liu, L.; Liao, P.; Fu, W.; Luo, Y. Graphene quantum dots in biomedical applications: Recent advances and future challenges. Front. Lab. Med. 2017, 1, 192. [Google Scholar] [CrossRef]
- Wang, Z.; Scheuring, M.; Mabin, M.; Shahni, R.; Wang, Z.D.; Ugrinov, A.; Butz, J.; Chu, Q.R. Renewable cyclobutane-1,3-dicarboxylic acid (CBDA) building block synthesized from furfural via photocyclization. ACS Sustain. Chem. Eng. 2020, 8, 8909. [Google Scholar] [CrossRef]
- Han, Y.; Lu, Z.; Teng, Z.; Liang, J.; Guo, Z.; Wang, D.; Han, M.; Yang, W. Unraveling the growth mechanism of silica particles in the Stöber method: In situ seeded growth model. Langmuir 2017, 33, 5879. [Google Scholar] [CrossRef]
- Britannica. Available online: https://www.britannica.com/science/nanoparticle (accessed on 20 April 2022).
- Bharti, C.; Nagaich, U.; Pal, A.; Gulati, N. Mesoporous silica nanoparticles in target drug delivery system: A review. Int. J. Pharm. Investig. 2015, 5, 124. [Google Scholar] [CrossRef] [Green Version]
- Shang, L.; Nienhaus, K.; Nienhaus, G. Engineered nanoparticles interaction with cells: Size matters. J. Nanobiotechnol. 2014, 12, 5. [Google Scholar] [CrossRef] [Green Version]
- Zhang, D.; Wei, L.; Zhong, M.; Xiao, L.; Li, H.; Wang, J. The morphology and surface charge-dependent cellular uptake efficiency of upconversion nanostructures revealed by single-particle optical microscopy. Chem. Sci. 2018, 9, 5260. [Google Scholar] [CrossRef] [Green Version]
- Fröhlich, E. The role of surface charge in cellular uptake and cytotoxicity of medical nanoparticles. Int. J. Nanomed. 2012, 7, 5577. [Google Scholar] [CrossRef] [Green Version]
- Sivasubramanian, M.; Chuang, Y.; Lo, L. Evolution of nanoparticle-mediated photodynamic therapy: From superficial to deep-seated cancers. Molecules 2019, 24, 520. [Google Scholar] [CrossRef] [Green Version]
- Jovanovic, S.; Syrgiannis, Z.; Budimir, M.; Milivojevic, D.; Jovanovic, D.; Pavlovic, V.; Papan, J.; Bartenwerfer, M.; Mojsin, M.; Stevanovic, M.; et al. Graphene quantum dots as singlet oxygen producer or radical quencher—The matter of functionalization with urea/thiourea. Mater. Sci. Eng. C 2020, 109, 110539. [Google Scholar] [CrossRef]
- Guo, H.; Qian, H.; Sun, S.; Sun, D.; Yin, H.; Cai, X.; Liu, Z.; Wu, J.; Jiang, T.; Liu, X. Hollow mesoporous silica nanoparticles for intracellular delivery of fluorescent dye. Chem. Cent. J. 2011, 5, 1. [Google Scholar] [CrossRef] [Green Version]
- Asefa, T.; Tao, Z. Biocompatibility of mesoporous silica nanoparticles. Chem. Res. Toxicol. 2012, 25, 2265–2284. [Google Scholar] [CrossRef] [PubMed]
- Zhang, C.; Xie, H.; Zhang, Z.; Wen, B.; Cao, H.; Che, Q.; Guo, J.; and Su, Z. Applications and biocompatibility of mesoporous silica nanocarriers in the field of medicine. Front. Pharmacol. 2022, 13, 829796. [Google Scholar] [CrossRef]
- Zhou, Y.; Chang, C.; Liu, Z.; Zhao, Q.; Xu, Q.; Li, C.; Chen, Y.; Zhang, Y.; Lu, B. Hyaluronic acid-functionalized hollow mesoporous silica nanoparticles as pH-sensitive nanocarriers for cancer chemo-photodynamic therapy. Langmuir 2021, 37, 2619. [Google Scholar] [CrossRef] [PubMed]
- Croissant, J.; Brinker, C. Biodegradable silica-based nanoparticles: Dissolution kinetics and selective bond cleavage. Enzymes 2018, 43, 181. [Google Scholar]
- Kong, M.; Tang, J.; Qiao, Q.; Wu, T.; Qi, Y.; Tan, S.; Gao, X.; Zhang, Z. Biodegradable hollow mesoporous silica nanoparticles for regulating tumor microenvironment and enhancing antitumor efficiency. Theranostics 2017, 7, 3276. [Google Scholar] [CrossRef]
- Sukhanova, A.; Bozrova, S.; Sokolov, P.; Berestovoy, M.; Karaulov, A.; Nabiev, I. Dependence of nanoparticle toxicity on their physical and chemical properties. Nanoscale Res. Lett. 2018, 13, 44. [Google Scholar] [CrossRef] [Green Version]
- Beganskiene, A.; Sirutkaitis, V.; Kurtinaitiene, M.; Juskenas, R.; Kareiva, A. FTIR, TEM and NMR investigations of Stöber silica nanoparticles. Mater. Sci. 2004, 10, 287. [Google Scholar]
- Mehmood, Y.; Khan, I.; Shahzad, Y.; Khalid, S.; Asghar, S.; Irfan, M.; Asif, M.; Khalid, I.; Yousaf, A.; Hussain, T. Facile synthesis of mesoporous silica nanoparticles using modified sol-gel method: Optimization and in vitro cytotoxicity studies. Pak. J. Pharm. Sci. 2019, 32, 1805. [Google Scholar]
- Rameli, N.; Jumbri, K.; Wahab, R.; Ramli, A.; Huyop, F. Synthesis and characterization of mesoporous silica nanoparticles using ionic liquids as a template. J. Phys. Conf. Ser. 2018, 1123, 012068. [Google Scholar] [CrossRef]
- Fang, J.; Liu, Y.; Chen, Y.; Ouyang, D.; Yang, G.; Yu, T. Graphene quantum dots-gated hollow mesoporous carbon nanoplatform targetinging drug delivery and synergistic chemo-photothermal therapy. Int. J. Nanomed. 2018, 13, 5991. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yao, X.; Tian, Z.; Liu, J.; Zhu, Y.; Hanagata, N. Mesoporous silica nanoparticles capped with graphene quantum dots for potential chemo-photothermal synergistic cancer therapy. Langmuir 2017, 33, 591. [Google Scholar] [CrossRef] [PubMed]
- Hao, N.; Jayawardana, K.; Chen, X.; De Zoysa, T.; Yan, M. One-step synthesis of amine-functionalized hollow mesoporous silica nanoparticles as efficient antibacterial and anticancer materials. ACS Appl. Mater. Interfaces 2015, 7, 1040. [Google Scholar] [CrossRef]
- Reagen, S.; Wu, Y.; Liu, X.; Shahni, R.; Bogenschuetz, J.; Wu, X.; Chu, Q.; Oncel, N.; Zhang, J.; Hou, X.; et al. Synthesis of highly near-infrared fluorescent graphene quantum dots using biomass-derived materials for in vitro cell imaging and metal ion detection. ACS Appl. Mater. Inter. 2021, 13, 43952. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Elliot, Q.; Wang, Z.; Setien, R.; Puttkammer, J.; Ugrinov, A.; Lee, J.; Webster, D.; Chu, Q.R. Fufural-derived diacid prepared by photoreaction for sustainable materials synthesis. ACS Sustain. Chem. Eng. 2018, 6, 8136. [Google Scholar] [CrossRef]
- Thiramanas, R.; Jiang, S.; Simon, J.; Landfester, K.; Mailänder, V. Silica nanocapsules with different sizes and physicochemical properties as suitable nanocarriers for uptake in T-cells. Int. J. Nanomed. 2020, 15, 6069–6084. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 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
Reagen, S.; Wu, Y.; Sun, D.; Munoz, C.; Oncel, N.; Combs, C.; Zhao, J.X. Development of Biodegradable GQDs-hMSNs for Fluorescence Imaging and Dual Cancer Treatment via Photodynamic Therapy and Drug Delivery. Int. J. Mol. Sci. 2022, 23, 14931. https://doi.org/10.3390/ijms232314931
Reagen S, Wu Y, Sun D, Munoz C, Oncel N, Combs C, Zhao JX. Development of Biodegradable GQDs-hMSNs for Fluorescence Imaging and Dual Cancer Treatment via Photodynamic Therapy and Drug Delivery. International Journal of Molecular Sciences. 2022; 23(23):14931. https://doi.org/10.3390/ijms232314931
Chicago/Turabian StyleReagen, Sarah, Yingfen Wu, Di Sun, Carlos Munoz, Nuri Oncel, Colin Combs, and Julia Xiaojun Zhao. 2022. "Development of Biodegradable GQDs-hMSNs for Fluorescence Imaging and Dual Cancer Treatment via Photodynamic Therapy and Drug Delivery" International Journal of Molecular Sciences 23, no. 23: 14931. https://doi.org/10.3390/ijms232314931