Carrier-Free Hybrid Nanoparticles for Enhanced Photodynamic Therapy in Oral Carcinoma via Reversal of Hypoxia and Oxidative Resistance
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials
2.2. Synthesis of KPF NPs
2.3. Characterization of KPF NPs
2.4. Cell Culture
2.5. In Vitro Assessment of KPF NPs
2.6. In Vivo Study of KPF
2.7. Results of Statistical Analysis
3. Results
3.1. Synthesis and Characterization of KPF NPs
3.2. In Vitro Study of KPF NPs
3.3. In Vivo Anti-Tumor Study of KPF NPs
3.4. Biological Safety Study
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Miranda-Filho, A.; Bray, F. Global patterns and trends in cancers of the lip, tongue and mouth. Oral Oncol. 2020, 102, 104551. [Google Scholar] [CrossRef] [PubMed]
- D’souza, S.; Addepalli, V. Preventive measures in oral cancer: An overview. Biomed. Pharmacother. 2018, 107, 72–80. [Google Scholar] [CrossRef] [PubMed]
- Togni, L.; Mascitti, M.; Vignini, A.; Alia, S.; Sartini, D.; Barlattani, A. Treatment-Related Dysgeusia in Oral and Oropharyngeal Cancer: A Comprehensive Review. Nutrients 2021, 13, 3325. [Google Scholar] [CrossRef] [PubMed]
- Co, J.L.; Mejia, M.B.; Que, J.C.; Dizon, J.M. Effectiveness of honey on radiation-induced oral mucositis, time to mucositis, weight loss, and treatment interruptions among patients with head and neck malignancies: A meta-analysis and systematic review of literature. Head Neck 2016, 38, 1119–1128. [Google Scholar] [CrossRef]
- Allison, R.R.; Sibata, C.; Gay, H. PDT for cancers of the head and neck. Photodiagnosis Photodyn. Ther. 2009, 6, 1–2. [Google Scholar] [CrossRef]
- Bredell, M.G.; Besic, E.; Maake, C.; Walt, H. The application and challenges of clinical PD-PDT in the head and neck region: A short review. J. Photochem. Photobiol. B 2010, 101, 185–190. [Google Scholar] [CrossRef]
- Li, Y.; Wang, B.; Zheng, S.; He, Y. Photodynamic therapy in the treatment of oral leukoplakia: A systematic review. Photodiagnosis Photodyn. Ther. 2019, 25, 17–22. [Google Scholar] [CrossRef]
- Poh, C.F.; Zhang, L.; Anderson, D.W.; Durham, J.S.; Williams, P.M.; Priddy, R.W.; Berean, K.W.; Ng, S.; Tseng, O.L.; MacAulay, C.; et al. Fluorescence visualization detection of field alterations in tumor margins of oral cancer patients. Clin. Cancer Res. 2006, 12, 6716–6722. [Google Scholar] [CrossRef]
- Heath, B.R.; Michmerhuizen, N.L.; Donnelly, C.R.; Sansanaphongpricha, K.; Sun, D.; Brenner, J.C.; Lei, Y.L. Head and Neck Cancer Immunotherapy beyond the Checkpoint Blockade. J. Dent. Res. 2019, 98, 1073–1080. [Google Scholar] [CrossRef]
- Fu, S.; Li, G.; Zang, W.; Zhou, X.; Shi, K.; Zhai, Y. Pure drug nano-assemblies: A facile carrier-free nanoplatform for efficient cancer therapy. Acta Pharm. Sin. B 2022, 12, 92–106. [Google Scholar] [CrossRef]
- Qi, M.; Chi, M.; Sun, X.; Xie, X.; Weir, M.D.; Oates, T.W.; Zhou, Y.; Wang, L.; Bai, Y.; Xu, H.H. Novel nanomaterial-based antibacterial photodynamic therapies to combat oral bacterial biofilms and infectious diseases. Int. J. Nanomed. 2019, 14, 6937–6956. [Google Scholar] [CrossRef]
- Hong, L.; Li, J.; Luo, Y.; Guo, T.; Zhang, C.; Ou, S.; Long, Y.; Hu, Z. Recent Advances in Strategies for Addressing Hypoxia in Tumor Photodynamic Therapy. Biomolecules 2022, 12, 81. [Google Scholar] [CrossRef] [PubMed]
- Lan, M.; Zhao, S.; Liu, W.; Lee, C.S.; Zhang, W.; Wang, P. Photosensitizers for Photodynamic Therapy. Adv. Healthc. Mater. 2019, 8, e1900132. [Google Scholar] [CrossRef]
- Huang, Y.; Qiu, F.; Chen, R.; Yan, D.; Zhu, X. Fluorescence resonance energy transfer-based drug delivery systems for enhanced photodynamic therapy. J. Mater. Chem. B 2020, 8, 3772–3788. [Google Scholar] [CrossRef]
- Wei, X.; Song, M.; Jiang, G.; Liang, M.; Chen, C.; Yang, Z.; Zou, L. Progress in advanced nanotherapeutics for enhanced photodynamic immunotherapy of tumor. Theranostics 2022, 12, 5272–5298. [Google Scholar] [CrossRef]
- Ibarra, A.M.C.; Cecatto, R.B.; Motta, L.J.; Dos Santos Franco, A.L.; de Fátima Teixeira da Silva, D.; Nunes, F.D.; Hamblin, M.R.; Rodrigues, M.F.S.D. Photodynamic therapy for squamous cell carcinoma of the head and neck: Narrative review focusing on photosensitizers. Lasers Med. Sci. 2022, 37, 1441–1470. [Google Scholar] [CrossRef]
- Jerjes, W.; Upile, T.; Hamdoon, Z.; Abbas, S.; Akram, S.; Mosse, C.A.; Morley, S.; Hopper, C. Photodynamic therapy: The minimally invasive surgical intervention for advanced and/or recurrent tongue base carcinoma. Lasers Surg. Med. 2011, 43, 283–292. [Google Scholar] [CrossRef] [PubMed]
- Gross, S.; Gilead, A.; Scherz, A.; Neeman, M.; Salomon, Y. Monitoring photodynamic therapy of solid tumors online by BOLD-contrast MRI. Nat. Med. 2003, 9, 1327–1331. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Liu, Y.; Bu, W.; Cheng, C.; Zuo, C.; Xiao, Q.; Sun, Y.; Ni, D.; Zhang, C.; Liu, J.; et al. Hypoxia Induced by Upconversion-Based Photodynamic Therapy: Towards Highly Effective Synergistic Bioreductive Therapy in Tumors. Angew. Chem. Int. Ed. Engl. 2015, 54, 8105–8109. [Google Scholar] [CrossRef]
- Cheung, E.C.; Vousden, K.H. The role of ROS in tumour development and progression. Nat. Rev. Cancer 2022, 22, 280–297. [Google Scholar] [CrossRef]
- Niu, B.; Liao, K.; Zhou, Y.; Wen, T.; Quan, G.; Pan, X.; Wu, C. Application of glutathione depletion in cancer therapy: Enhanced ROS-based therapy, ferroptosis, and chemotherapy. Biomaterials 2021, 277, 121110. [Google Scholar] [CrossRef] [PubMed]
- Liu, P.; Hao, L.; Liu, M.; Hu, S. Glutathione-responsive and -exhausting metal nanomedicines for robust synergistic cancer therapy. Front. Bioeng. Biotechnol. 2023, 11, 1161472. [Google Scholar] [CrossRef]
- Bansal, A.; Simon, M.C. Glutathione metabolism in cancer progression and treatment resistance. J. Cell Biol. 2018, 217, 2291–2298. [Google Scholar] [CrossRef] [PubMed]
- Larue, L.; Myrzakhmetov, B.; Ben-Mihoub, A.; Moussaron, A.; Thomas, N.; Arnoux, P.; Baros, F.; Vanderesse, R.; Acherar, S.; Frochot, C. Fighting Hypoxia to Improve PDT. Pharmaceuticals 2019, 12, 163. [Google Scholar] [CrossRef] [PubMed]
- Feng, L.; Cheng, L.; Dong, Z.; Tao, D.; Barnhart, T.E.; Cai, W.; Chen, M.; Liu, Z. Theranostic Liposomes with Hypoxia-Activated Prodrug to Effectively Destruct Hypoxic Tumors Post-Photodynamic Therapy. ACS Nano 2017, 11, 927–937. [Google Scholar] [CrossRef]
- Maas, A.L.; Carter, S.L.; Wileyto, E.P.; Miller, J.; Yuan, M.; Yu, G.; Durham, A.C.; Busch, T.M. Tumor vascular microenvironment determines responsiveness to photodynamic therapy. Cancer Res. 2012, 72, 2079–2088. [Google Scholar] [CrossRef]
- Fan, W.; Huang, P.; Chen, X. Overcoming the Achilles’ heel of photodynamic therapy. Chem. Soc. Rev. 2016, 45, 6488–6519. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.; Zhao, D.; Wang, G.; Wang, Y.; Cao, L.; Sun, J.; Jiang, Q.; He, Z. Recent progress of hypoxia-modulated multifunctional nanomedicines to enhance photodynamic therapy: Opportunities, challenges, and future development. Acta Pharm. Sin. B 2020, 10, 1382–1396. [Google Scholar] [CrossRef]
- Cheng, D.; Ji, Y.; Wang, B.; Jin, T.; Xu, Y.; Qian, X.; Zhu, W. Enzyme/GSH dual-responsive biodegradable nanohybrid for spatiotemporally specific photodynamic and hypoxia-augmented therapy against tumors. Int. J. Pharm. 2021, 603, 120730. [Google Scholar] [CrossRef]
- Liu, C.; Wang, D.; Zhang, S.; Cheng, Y.; Yang, F.; Xing, Y.; Xu, T.; Dong, H.; Zhang, X. Biodegradable Biomimic Copper/Manganese Silicate Nanospheres for Chemodynamic/Photodynamic Synergistic Therapy with Simultaneous Glutathione Depletion and Hypoxia Relief. ACS Nano 2019, 13, 4267–4277. [Google Scholar] [CrossRef]
- Liang, X.; Chen, M.; Bhattarai, P.; Hameed, S.; Tang, Y.; Dai, Z. Complementing Cancer Photodynamic Therapy with Ferroptosis through Iron Oxide Loaded Porphyrin-Grafted Lipid Nanoparticles. ACS Nano 2021, 15, 20164–20180. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Q.; Kuang, G.; Wang, H.; Zhao, Y.; Wei, J.; Shang, L. Multi-Bioinspired MOF Delivery Systems from Microfluidics for Tumor Multimodal Therapy. Adv. Sci. 2023, 10, e2303818. [Google Scholar] [CrossRef]
- Zhu, T.; Shi, L.; Yu, C.; Dong, Y.; Qiu, F.; Shen, L.; Qian, Q.; Zhou, G.; Zhu, X. Ferroptosis Promotes Photodynamic Therapy: Supramolecular Photosensitizer-Inducer Nanodrug for Enhanced Cancer Treatment. Theranostics 2019, 9, 3293–3307. [Google Scholar] [CrossRef] [PubMed]
- Pan, W.L.; Tan, Y.; Meng, W.; Huang, N.H.; Zhao, Y.B.; Yu, Z.Q.; Huang, Z.; Zhang, W.H.; Sun, B.; Chen, J.X. Microenvironment-driven sequential ferroptosis, photodynamic therapy, and chemotherapy for targeted breast cancer therapy by a cancer-cell-membrane-coated nanoscale metal-organic framework. Biomaterials 2022, 283, 121449. [Google Scholar] [CrossRef]
- Shi, L.; Hu, F.; Duan, Y.; Wu, W.; Dong, J.; Meng, X.; Zhu, X.; Liu, B. Hybrid Nanospheres to Overcome Hypoxia and Intrinsic Oxidative Resistance for Enhanced Photodynamic Therapy. ACS Nano 2020, 14, 2183–2190. [Google Scholar] [CrossRef] [PubMed]
- Liu, Q.; Guan, C.; Liu, C.; Li, H.; Wu, J.; Sun, C. Targeting hypoxia-inducible factor-1alpha: A new strategy for triple-negative breast cancer therapy. Biomed. Pharmacother. 2022, 156, 113861. [Google Scholar] [CrossRef]
- Lamplugh, Z.; Fan, Y. Vascular Microenvironment, Tumor Immunity and Immunotherapy. Front. Immunol. 2021, 12, 811485. [Google Scholar] [CrossRef]
- Liao, Z.H.; Zhu, H.Q.; Chen, Y.Y.; Chen, R.L.; Fu, L.X.; Li, L.; Zhou, H.; Zhou, J.L.; Liang, G. The epigallocatechin gallate derivative Y6 inhibits human hepatocellular carcinoma by inhibiting angiogenesis in MAPK/ERK1/2 and PI3K/AKT/HIF-1α/VEGF dependent pathways. J. Ethnopharmacol. 2020, 259, 112852. [Google Scholar] [CrossRef]
- Shen, L.; Huang, Y.; Chen, D.; Qiu, F.; Ma, C.; Jin, X.; Zhu, X.; Zhou, G.; Zhang, Z. pH-Responsive Aerobic Nanoparticles for Effective Photodynamic Therapy. Theranostics 2017, 7, 4537–4550. [Google Scholar] [CrossRef]
- Zhu, T.; Shi, L.; Ma, C.; Xu, L.; Yang, J.; Zhou, G.; Zhu, X.; Shen, L. Fluorinated chitosan-mediated intracellular catalase delivery for enhanced photodynamic therapy of oral cancer. Biomater. Sci. 2021, 9, 658–662. [Google Scholar] [CrossRef] [PubMed]
- Zhu, X.; Wang, M.; Wang, H.; Ding, Y.; Liu, Y.; Fu, Z.; Lin, D.; Lu, C.; Tu, X. Multifunctional Hollow MnO2 @Porphyrin@Bromelain Nanoplatform for Enhanced Photodynamic Therapy. Small 2022, 18, e2204951. [Google Scholar] [CrossRef] [PubMed]
- Tang, X.; Cui, K.; Lu, X.; Wu, P.; Yu, S.; Yang, B.; Xu, Y.; Liang, X. A Novel Hypoxia-inducible Factor 1α Inhibitor KC7F2 Attenuates Oxygen-induced Retinal Neovascularization. Investig. Ophthalmol. Vis. Sci. 2022, 63, 13. [Google Scholar] [CrossRef] [PubMed]
- Cheng, J.; Yang, H.L.; Gu, C.J.; Liu, Y.K.; Shao, J.; Zhu, R.; He, Y.Y.; Zhu, X.Y.; Li, M.Q. Melatonin restricts the viability and angiogenesis of vascular endothelial cells by suppressing HIF-1α/ROS/VEGF. Int. J. Mol. Med. 2019, 43, 945–955. [Google Scholar] [CrossRef] [PubMed]
- Wang, E.L.; Zhang, J.J.; Luo, F.M.; Fu, M.Y.; Li, D.; Peng, J.; Liu, B. Cerebellin-2 promotes endothelial-mesenchymal transition in hypoxic pulmonary hypertension rats by activating NF-κB/HIF-1α/Twist1 pathway. Life Sci. 2023, 328, 121879. [Google Scholar] [CrossRef]
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
Li, X.; Li, Z.; Su, Y.; Zhou, J.; Li, Y.; Zhao, Q.; Yang, X.; Shi, L.; Shen, L. Carrier-Free Hybrid Nanoparticles for Enhanced Photodynamic Therapy in Oral Carcinoma via Reversal of Hypoxia and Oxidative Resistance. Pharmaceutics 2024, 16, 1130. https://doi.org/10.3390/pharmaceutics16091130
Li X, Li Z, Su Y, Zhou J, Li Y, Zhao Q, Yang X, Shi L, Shen L. Carrier-Free Hybrid Nanoparticles for Enhanced Photodynamic Therapy in Oral Carcinoma via Reversal of Hypoxia and Oxidative Resistance. Pharmaceutics. 2024; 16(9):1130. https://doi.org/10.3390/pharmaceutics16091130
Chicago/Turabian StyleLi, Xiao, Zhiyin Li, Yue Su, Jia Zhou, Yuxiang Li, Qianqian Zhao, Xia Yang, Leilei Shi, and Lingyue Shen. 2024. "Carrier-Free Hybrid Nanoparticles for Enhanced Photodynamic Therapy in Oral Carcinoma via Reversal of Hypoxia and Oxidative Resistance" Pharmaceutics 16, no. 9: 1130. https://doi.org/10.3390/pharmaceutics16091130