In Vitro and In Vivo Evaluation of PEGylated Starch-Coated Iron Oxide Nanoparticles for Enhanced Photothermal Cancer Therapy
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials
2.2. Preparation of PEGylated Starch-Coated Iron Oxide Nanoparticles (PEG–Starch–IONPs)
2.3. Physical Characterization of PEG–Starch–IONPs
2.4. In Vitro Photothermal Activity of PEG–Starch–IONPs
2.5. Cellular Analyses of the Photothermal Toxicity by PEG–Starch–IONPs
2.6. Animal Studies
2.6.1. Pharmacokinetics (PK)
2.6.2. In Vivo Photothermal Activity of PEG–Starch–IONPs
2.6.3. Assessment of the Tumor Accumulation of PEG–Starch–IONPs
2.6.4. Tumor Growth Inhibition by PEG–Starch–IONPs-Based PTT
2.7. Statistical Analyses
3. Results and Discussions
3.1. Physical Characterization of PEG–Starch–IONPs
3.2. In Vitro Photothermal Activity of PEG–Starch–IONPs
3.3. Cellular Analyses of the Photothermal Toxicity by PEG–Starch–IONPs
3.4. Pharmacokinetic Studies
3.5. In Vivo Photothermal Activity of PEG–Starch–IONPs
3.6. Preliminary PEG–Starch–IONPs-Based PTT Efficacy Studies
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Zhi, D.; Yang, T.; O’hagan, J.; Zhang, S.; Donnelly, R.F. Photothermal therapy. J. Control. Release 2020, 325, 52–71. [Google Scholar] [CrossRef]
- Liu, Y.; Bhattarai, P.; Dai, Z.; Chen, X. Photothermal therapy and photoacoustic imaging via nanotheranostics in fighting cancer. Chem. Soc. Rev. 2019, 48, 2053–2108. [Google Scholar] [CrossRef]
- Jung, H.S.; Verwilst, P.; Sharma, A.; Shin, J.; Sessler, J.L.; Kim, J.S. Organic molecule-based photothermal agents: An expanding photothermal therapy universe. Chem. Soc. Rev. 2018, 47, 2280–2297. [Google Scholar] [CrossRef]
- Chen, Q.; Wen, J.; Li, H.; Xu, Y.; Liu, F.; Sun, S. Recent advances in different modal imaging-guided photothermal therapy. Biomaterials 2016, 106, 144–166. [Google Scholar] [CrossRef]
- Chen, J.; Ning, C.; Zhou, Z.; Yu, P.; Zhu, Y.; Tan, G.; Mao, C. Nanomaterials as photothermal therapeutic agents. Prog. Mater. Sci. 2019, 99, 1–26. [Google Scholar] [CrossRef] [PubMed]
- Estelrich, J.; Busquets, M.A. Iron oxide nanoparticles in photothermal therapy. Molecules 2018, 23, 1567. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ren, X.; Chen, H.; Yang, V.; Sun, D. Iron oxide nanoparticle-based theranostics for cancer imaging and therapy. Front. Chem. Sci. Eng. 2014, 8, 253–264. [Google Scholar] [CrossRef]
- Sim, T.; Lim, C.; Hoang, N.H.; Shin, Y.; Kim, J.C.; Park, J.Y.; Her, J.; Lee, E.S.; Youn, Y.S.; Oh, K.T. An on-demand pH-sensitive nanocluster for cancer treatment by combining photothermal therapy and chemotherapy. Pharmaceutics 2020, 12, 839. [Google Scholar] [CrossRef] [PubMed]
- Qiao, R.; Yang, C.; Gao, M. Superparamagnetic iron oxide nanoparticles: From preparations to in vivo MRI applications. J. Mater. Chem. 2009, 19, 6274–6293. [Google Scholar] [CrossRef]
- Chertok, B.; Moffat, B.A.; David, A.E.; Yu, F.; Bergemann, C.; Ross, B.D.; Yang, V.C. Iron oxide nanoparticles as a drug delivery vehicle for MRI monitored magnetic targeting of brain tumors. Biomaterials 2008, 29, 487–496. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.-X.J. Superparamagnetic iron oxide based MRI contrast agents: Current status of clinical application. Quant. Imaging Med. Surg. 2011, 1, 35. [Google Scholar] [PubMed]
- Xie, W.; Guo, Z.; Gao, F.; Gao, Q.; Wang, D.; Liaw, B.S.; Cai, Q.; Sun, X.; Wang, X.; Zhao, L. Shape-, size- and structure-controlled synthesis and biocompatibility of iron oxide nanoparticles for magnetic theranostics. Theranostics 2018, 8, 3284–3307. [Google Scholar] [CrossRef] [PubMed]
- Sadhukha, T.; Wiedmann, T.S.; Panyam, J. Enhancing therapeutic efficacy through designed aggregation of nanoparticles. Biomaterials 2014, 35, 7860–7869. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arias, L.S.; Pessan, J.P.; Vieira, A.P.M.; Lima, T.M.T.d.; Delbem, A.C.B.; Monteiro, D.R. Iron oxide nanoparticles for biomedical applications: A perspective on synthesis, drugs, antimicrobial activity, and toxicity. Antibiotics 2018, 7, 46. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Karakoti, A.; Hench, L.; Seal, S. The potential toxicity of nanomaterials—the role of surfaces. JOM 2006, 58, 77–82. [Google Scholar] [CrossRef]
- Alphandéry, E. Iron oxide nanoparticles for therapeutic applications. Drug Discov. Today 2020, 25, 141–149. [Google Scholar] [CrossRef]
- Liu, G.; Gao, J.; Ai, H.; Chen, X. Applications and potential toxicity of magnetic iron oxide nanoparticles. Small 2013, 9, 1533–1545. [Google Scholar] [CrossRef] [PubMed]
- Wáng, Y.X.J.; Idée, J.-M. A comprehensive literatures update of clinical researches of superparamagnetic resonance iron oxide nanoparticles for magnetic resonance imaging. Quant. Imaging Med. Surg. 2017, 7, 88. [Google Scholar] [CrossRef] [Green Version]
- Min, K.A.; Yu, F.; Yang, V.C.; Zhang, X.; Rosania, G.R. Transcellular transport of heparin-coated magnetic iron oxide nanoparticles (Hep-MION) under the influence of an applied magnetic field. Pharmaceutics 2010, 2, 119–135. [Google Scholar] [CrossRef]
- Zhang, J.; Shin, M.C.; David, A.E.; Zhou, J.; Lee, K.; He, H.; Yang, V.C. Long-circulating heparin-functionalized magnetic nanoparticles for potential application as a protein drug delivery platform. Mol. Pharm. 2013, 10, 3892–3902. [Google Scholar] [CrossRef] [Green Version]
- Dadfar, S.M.; Roemhild, K.; Drude, N.I.; von Stillfried, S.; Knüchel, R.; Kiessling, F.; Lammers, T. Iron oxide nanoparticles: Diagnostic, therapeutic and theranostic applications. Adv. Drug Deliv. Rev. 2019, 138, 302–325. [Google Scholar] [CrossRef]
- Alavijeh, M.S.; Maghsoudpour, A.; Khayat, M.; Rad, I.; Hatamie, S. Distribution of “molybdenum disulfide/cobalt ferrite” nanocomposite in animal model of breast cancer, following injection via differential infusion flow rates. J. Pharm. Investig. 2020, 50, 583–592. [Google Scholar] [CrossRef]
- Vallabani, N.S.; Singh, S. Recent advances and future prospects of iron oxide nanoparticles in biomedicine and diagnostics. 3 Biotech 2018, 8, 1–23. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Espinosa, A.; Di Corato, R.; Kolosnjaj-Tabi, J.; Flaud, P.; Pellegrino, T.; Wilhelm, C. Duality of iron oxide nanoparticles in cancer therapy: Amplification of heating efficiency by magnetic hyperthermia and photothermal bimodal treatment. ACS Nano 2016, 10, 2436–2446. [Google Scholar] [CrossRef]
- Soenen, S.J.; Parak, W.J.; Rejman, J.; Manshian, B. (Intra) cellular stability of inorganic nanoparticles: Effects on cytotoxicity, particle functionality, and biomedical applications. Chem. Rev. 2015, 115, 2109–2135. [Google Scholar] [CrossRef] [PubMed]
- Levy, M.; Luciani, N.; Alloyeau, D.; Elgrabli, D.; Deveaux, V.; Pechoux, C.; Chat, S.; Wang, G.; Vats, N.; Gendron, F. Long term in vivo biotransformation of iron oxide nanoparticles. Biomaterials 2011, 32, 3988–3999. [Google Scholar] [CrossRef] [PubMed]
- Volatron, J.; Carn, F.; Kolosnjaj-Tabi, J.; Javed, Y.; Vuong, Q.L.; Gossuin, Y.; Ménager, C.; Luciani, N.; Charron, G.; Hémadi, M. Ferritin protein regulates the degradation of iron oxide nanoparticles. Small 2017, 13, 1602030. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Lovell, J.F.; Yoon, J.; Chen, X. Clinical development and potential of photothermal and photodynamic therapies for cancer. Nat. Rev. Clin. Oncol. 2020, 17, 657–674. [Google Scholar] [CrossRef] [PubMed]
- Cole, A.J.; David, A.E.; Wang, J.; Galbán, C.J.; Hill, H.L.; Yang, V.C. Polyethylene glycol modified, cross-linked starch-coated iron oxide nanoparticles for enhanced magnetic tumor targeting. Biomaterials 2011, 32, 2183–2193. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- García-Jimeno, S.; Estelrich, J. Ferrofluid based on polyethylene glycol-coated iron oxide nanoparticles: Characterization and properties. Colloids Surf. A Physicochem. Eng. Asp. 2013, 420, 74–81. [Google Scholar] [CrossRef]
- Li, X.; Xia, S.; Zhou, W.; Ji, R.; Zhan, W. Targeted Fe-doped silica nanoparticles as a novel ultrasound–magnetic resonance dual-mode imaging contrast agent for HER2-positive breast cancer. Int. J. Nanomed. 2019, 14, 2397. [Google Scholar] [CrossRef] [Green Version]
- Jani, K.; Kaushal, N.; Sadoqi, M.; Long, G.; Chen, Z.-S.; Squillante, E. Formulation and characterization of oleic acid magnetic PEG PLGA nanoparticles for targeting glioblastoma multiforme. J. Magn. Magn. Mater. 2021, 533, 167970. [Google Scholar] [CrossRef]
- Zhang, J.; Shin, M.C.; Yang, V.C. Magnetic targeting of novel heparinized iron oxide nanoparticles evaluated in a 9L-glioma mouse model. Pharm. Res. 2014, 31, 579–592. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Prochazkova, S.; Vårum, K.M.; Ostgaard, K. Quantitative determination of chitosans by ninhydrin. Carbohydr. Polym. 1999, 38, 115–122. [Google Scholar] [CrossRef]
- Kurfürst, M.M. Detection and molecular weight determination of polyethylene glycol-modified hirudin by staining after sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Anal. Biochem. 1992, 200, 244–248. [Google Scholar] [CrossRef]
- Min, K.A.; Shin, M.C.; Yu, F.; Yang, M.; David, A.E.; Yang, V.C.; Rosania, G.R. Pulsed magnetic field improves the transport of iron oxide nanoparticles through cell barriers. ACS Nano 2013, 7, 2161–2171. [Google Scholar] [CrossRef] [Green Version]
- Cho, K.H.; Shin, M.C.; Min, K.A. Externally Controlled Cellular Transport of Magnetic Iron Oxide Particles with Polysaccharide Surface Coatings. Cell Biochem. Biophys. 2019, 77, 213–225. [Google Scholar] [CrossRef]
- Atlihan-Gundogdu, E.; Ilem-Ozdemir, D.; Ekinci, M.; Ozgenc, E.; Demir, E.S.; Sánchez-Dengra, B.; González-Alvárez, I. Recent developments in cancer therapy and diagnosis. J. Pharm. Investig. 2020, 50, 349–361. [Google Scholar] [CrossRef]
- Le Corre, D.; Bras, J.; Dufresne, A. Starch nanoparticles: A review. Biomacromolecules 2010, 11, 1139–1153. [Google Scholar] [CrossRef] [PubMed]
- Kiio, T.M.; Park, S. Physical properties of nanoparticles do matter. J. Pharm. Investig. 2021, 51, 35–51. [Google Scholar] [CrossRef]
- Kim, D.K.; Mikhaylova, M.; Zhang, Y.; Muhammed, M. Protective coating of superparamagnetic iron oxide nanoparticles. Chem. Mater. 2003, 15, 1617–1627. [Google Scholar] [CrossRef]
- D’souza, A.A.; Shegokar, R. Polyethylene glycol (PEG): A versatile polymer for pharmaceutical applications. Expert Opin. Drug Deliv. 2016, 13, 1257–1275. [Google Scholar] [CrossRef] [PubMed]
- Riley, T.; Govender, T.; Stolnik, S.; Xiong, C.; Garnett, M.; Illum, L.; Davis, S. Colloidal stability and drug incorporation aspects of micellar-like PLA–PEG nanoparticles. Colloids Surf. B Biointerfaces 1999, 16, 147–159. [Google Scholar] [CrossRef]
- Roohi, F.; Lohrke, J.; Ide, A.; Schütz, G.; Dassler, K. Studying the effect of particle size and coating type on the blood kinetics of superparamagnetic iron oxide nanoparticles. Int. J. Nanomed. 2012, 7, 4447. [Google Scholar]
- Gupta, A.K.; Wells, S. Surface-modified superparamagnetic nanoparticles for drug delivery: Preparation, characterization, and cytotoxicity studies. IEEE Trans. Nanobiosci. 2004, 3, 66–73. [Google Scholar] [CrossRef] [PubMed]
- Larsen, E.K.; Nielsen, T.; Wittenborn, T.; Birkedal, H.; Vorup-Jensen, T.; Jakobsen, M.H.; Østergaard, L.; Horsman, M.R.; Besenbacher, F.; Howard, K.A. Size-dependent accumulation of PEGylated silane-coated magnetic iron oxide nanoparticles in murine tumors. ACS Nano 2009, 3, 1947–1951. [Google Scholar] [CrossRef]
- Briley-Saebo, K.C.; Mani, V.; Hyafil, F.; Cornily, J.C.; Fayad, Z.A. Fractionated Feridex and positive contrast: In vivo MR imaging of atherosclerosis. Magn. Reson. Med. 2008, 59, 721–730. [Google Scholar] [CrossRef] [PubMed]
- Owens, D.E., III; Peppas, N.A. Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int. J. Pharm. 2006, 307, 93–102. [Google Scholar] [CrossRef]
- Yoo, J.-W.; Chambers, E.; Mitragotri, S. Factors that control the circulation time of nanoparticles in blood: Challenges, solutions and future prospects. Curr. Pharm. Des. 2010, 16, 2298–2307. [Google Scholar] [CrossRef] [PubMed]
- Sato, I.; Umemura, M.; Mitsudo, K.; Kioi, M.; Nakashima, H.; Iwai, T.; Feng, X.; Oda, K.; Miyajima, A.; Makino, A. Hyperthermia generated with ferucarbotran (Resovist®) in an alternating magnetic field enhances cisplatin-induced apoptosis of cultured human oral cancer cells. J. Physiol. Sci. 2014, 64, 177–183. [Google Scholar] [CrossRef]
- Song, Y.; Li, D.; Lu, Y.; Jiang, K.; Yang, Y.; Xu, Y.; Dong, L.; Yan, X.; Ling, D.; Yang, X. Ferrimagnetic mPEG-b-PHEP copolymer micelles loaded with iron oxide nanocubes and emodin for enhanced magnetic hyperthermia–chemotherapy. Nat. Sci. Rev. 2020, 7, 723–736. [Google Scholar] [CrossRef] [Green Version]
Samples | Hydrodynamic Diameter (nm) | PDI | Zeta Potential (mV) | Amine Content (nmol/mg Fe) | PEG Content (nmol/mg Fe) |
---|---|---|---|---|---|
Starch–IONPs | 105.2 (±5.9) | 0.11 | −3.3 (±0.2) | - | - |
PEG–Starch–IONPs | 154.4 (±8.3) | 0.10 | +24.9 (±5.1) | 255 (±28.8) | 5.3 (±0.4) |
Laser Power (W) | Maximum Tumor Temperature (°C) | ||
---|---|---|---|
Control | Starch-IONPs | PEG–Starch–IONPs | |
1.0 | 38.4 (±3.5) | 40.2 (±2.1) | 48.9 (±3.3) |
0.9 | 36.9 (±3.3) | 38.5 (±2.3) | 46.6 (±3.4) |
0.8 | 33.4 (±2.8) | 34.9 (±3.1) | 42.3 (±3.1) |
0.7 | 28.2 (±1.9) | 29.4 (±2.2) | 37.8 (±2.5) |
0.6 | 25.8 (±1.4) | 26.6 (±1.3) | 34.2 (±3.4) |
Control | 25.1(±1.2) | 25.2 (±1.8) | 25.4 (±1.3) |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 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
Amatya, R.; Hwang, S.; Park, T.; Min, K.A.; Shin, M.C. In Vitro and In Vivo Evaluation of PEGylated Starch-Coated Iron Oxide Nanoparticles for Enhanced Photothermal Cancer Therapy. Pharmaceutics 2021, 13, 871. https://doi.org/10.3390/pharmaceutics13060871
Amatya R, Hwang S, Park T, Min KA, Shin MC. In Vitro and In Vivo Evaluation of PEGylated Starch-Coated Iron Oxide Nanoparticles for Enhanced Photothermal Cancer Therapy. Pharmaceutics. 2021; 13(6):871. https://doi.org/10.3390/pharmaceutics13060871
Chicago/Turabian StyleAmatya, Reeju, Seungmi Hwang, Taehoon Park, Kyoung Ah Min, and Meong Cheol Shin. 2021. "In Vitro and In Vivo Evaluation of PEGylated Starch-Coated Iron Oxide Nanoparticles for Enhanced Photothermal Cancer Therapy" Pharmaceutics 13, no. 6: 871. https://doi.org/10.3390/pharmaceutics13060871
APA StyleAmatya, R., Hwang, S., Park, T., Min, K. A., & Shin, M. C. (2021). In Vitro and In Vivo Evaluation of PEGylated Starch-Coated Iron Oxide Nanoparticles for Enhanced Photothermal Cancer Therapy. Pharmaceutics, 13(6), 871. https://doi.org/10.3390/pharmaceutics13060871