Photo- and X-ray Induced Cytotoxicity of CeF3-YF3-TbF3 Nanoparticle-Polyvinylpyrrolidone—“Radachlorin” Composites for Combined Photodynamic Therapy
Abstract
:1. Introduction
2. Materials and Methods
2.1. Experimental Technique
2.2. Synthesis of the Nanoparticles
3. Results
3.1. Characterization of Ce0.5Y0.35Tb0.15F3 Nanoparticles
3.2. Spectral-Kinetic Characteristics of Nanoparticles Ce0.5Y0.35Tb0.15F3
3.3. Evaluation of the Survival of A549 Cells in the Presence of Ce0.5Y0.35Tb0.15F3 Nanoparticles and Radachlorin
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Kustov, A.V.; Smirnova, N.L.; Privalov, O.A.; Moryganova, T.M.; Strelnikov, A.I.; Morshnev, P.K.; Berezin, D.B. Transurethral resection of non-muscle invasive bladder tumors combined with fluorescence diagnosis and photodynamic therapy with chlorin e6-type photosensitizers. J. Clin. Med. 2021, 11, 233. [Google Scholar] [CrossRef]
- Kustov, D.M.; Kozlikina, E.I.; Efendiev, K.T.; Loshchenov, M.V.; Grachev, P.V.; Maklygina, Y.S.; Loschenov, V.B. Laser-induced fluorescent visualization and photodynamic therapy in surgical treatment of glial brain tumors. Biomed. Opt. Express 2021, 12, 1761–1773. [Google Scholar] [CrossRef] [PubMed]
- Algorri, J.F.; Ochoa, M.; Roldán-Varona, P.; Rodríguez-Cobo, L.; López-Higuera, J.M. Photodynamic therapy: A compendium of latest reviews. Cancers 2021, 13, 4447. [Google Scholar] [CrossRef] [PubMed]
- Correia, J.H.; Rodrigues, J.A.; Pimenta, S.; Dong, T.; Yang, Z. Photodynamic therapy review: Principles, photosensitizers, applications, and future directions. Pharmaceutics 2021, 13, 1332. [Google Scholar] [CrossRef] [PubMed]
- Kustov, A.V.; Berezin, D.B.; Zorin, V.P.; Morshnev, P.K.; Kukushkina, N.Y.V.; Krestyaninov, M.A.; Kozlovtseva, E.A. Monocationic chlorin as a promising photosensitizer for antitumor and antimicrobial photodynamic therapy. Pharmaceutics 2022, 15, 61. [Google Scholar] [CrossRef]
- Berezin, D.B.; Kruchin, S.O.; Kukushkina, N.Y.V.; Venediktov, E.A.; Koifman, M.O.; Kustov, A.V. Water-Soluble Dicationic Deuteroporphyrin Derivative for Antimicrobial PDT: Singlet Oxygen Generation, Passive Carrier Interaction and Nosocomial Bacterial Strains Photoinactivation. Photochem 2023, 3, 171–186. [Google Scholar] [CrossRef]
- Ji, B.; Wei, M.; Yang, B. Recent advances in nanomedicines for photodynamic therapy (PDT)-driven cancer immunotherapy. Theranostics 2022, 12, 434. [Google Scholar] [CrossRef]
- Hemmer, E.; Benayas, A.; Légaré, F.; Vetrone, F. Exploiting the biological windows: Current perspectives on fluorescent bioprobes emitting above 1000 nm. Nanoscale Horiz. 2016, 1, 168–184. [Google Scholar] [CrossRef]
- Del Rosal, B.; Villa, I.; Jaque, D.; Sanz-Rodríguez, F. In vivo autofluorescence in the biological windows: The role of pigmentation. J. Biophotonics 2016, 9, 1059–1067. [Google Scholar] [CrossRef]
- Bashkatov, A.N.; Genina, E.A.; Tuchin, V.V. Optical properties of skin, subcutaneous, and muscle tissues: A review. J. Innov. Opt. Health Sci. 2011, 4, 9–38. [Google Scholar] [CrossRef]
- Ginner, L.; Gesperger, J.; Wöhrer, A.; Drexler, W.; Baumann, B.; Leitgeb, R.; Niederleithner, M. Ex-vivo Alzheimer’ s disease brain tissue investigation: A multiscale approach using 1060-nm swept source optical coherence tomography for a direct correlation to histology. Neurophotonics 2020, 7, 035004. [Google Scholar]
- He, W.; Frueh, J.; Wu, Z.; He, Q. How leucocyte cell membrane modified janus microcapsules are phagocytosed by cancer cells. ACS Appl. Mater. Interfaces 2016, 8, 4407–4415. [Google Scholar] [CrossRef] [PubMed]
- Zhang, X.; Lan, B.; Wang, S.; Gao, P.; Liu, T.; Rong, J.; Lu, H. Low-dose x-ray excited photodynamic therapy based on naluf4: Tb3+–rose bengal nanocomposite. Bioconjugate Chem. 2019, 30, 2191–2200. [Google Scholar] [CrossRef]
- Orsi, D.; Rimoldi, T.; Pinelli, S.; Alinovi, R.; Goldoni, M.; Benecchi, G.; Cristofolini, L. New CeF3–ZnO nanocomposites for self-lighted photodynamic therapy that block adenocarcinoma cell life cycle. Nanomedicine 2018, 13, 2311–2326. [Google Scholar] [CrossRef] [PubMed]
- Ahmadi, H.; Bagherzadeh, M.; Raeisi, M.; Payami, F. Preparation and characterization and photoluminescence properties of CeF3@ZnS nanocomposites. J. Mater. Sci. Mater. Electron. 2020, 31, 3215–3220. [Google Scholar] [CrossRef]
- Pudovkin, M.S.; Zelenikhin, P.V.; Krasheninnikova, A.O.; Korableva, S.L.; Nizamutdinov, A.S.; Alakshin, E.M.; Kadirov, M.K. Photoinduced toxicity of PrF3 and LaF3 nanoparticles. Opt. Spectrosc. 2016, 121, 538–543. [Google Scholar] [CrossRef]
- Pudovkin, M.S.; Zelenikhin, P.V.; Shtyreva, V.V.; Evtugyn, V.G.; Salnikov, V.V.; Nizamutdinov, A.S.; Semashko, V.V. Cellular uptake and cytotoxicity of unmodified Pr3+: LaF3 nanoparticles. J. Nanoparticle Res. 2019, 21, 184. [Google Scholar] [CrossRef]
- Pudovkin, M.S.; Korableva, S.L.; Krasheninnicova, A.O.; Nizamutdinov, A.S.; Semashko, V.V.; Zelenihin, P.V.; Nevzorova, T. AToxicity of laser irradiated photoactive fluoride PrF3 nanoparticles toward bacteria. J. Phys. Conf. Ser. 2014, 560, 012011. [Google Scholar] [CrossRef]
- Yu, J.; Yin, W.; Peng, T.; Chang, Y.N.; Zu, Y.; Li, J.; He, X.; Ma, X.; Gu, Z.; Zhao, Y. Biodistribution, excretion, and toxicity of polyethyleneimine modified NaYF4:Yb,Er upconversion nanoparticles in mice via different administration routes. Nanoscale 2017, 9, 4497–4507. [Google Scholar] [CrossRef]
- Li, H.; Wei, M.; Lv, X.; Hu, Y.; Shao, J.; Song, X.; Dong, X. Cerium-based nanoparticles for cancer photodynamic therapy. J. Innov. Opt. Health Sci. 2022, 15, 2230009. [Google Scholar] [CrossRef]
- Ca, N.X.; Vinh, N.D.; Bharti, S.; Tan, P.M.; Hien, N.T.; Hoa, V.X.; Do, P.V. Optical properties of Ce3+ and Tb3+ co-doped ZnS quantum dots. J. Alloys Compd. 2021, 883, 160764. [Google Scholar] [CrossRef]
- Akman, P.; Ulusan, S.; Banerjee, S.; Yilmaz, A. Core/shell type, Ce3+ and Tb3+ doped GdBO3 system: Synthesis and Celecoxib drug delivery application. Microporous Mesoporous Mater. 2020, 308, 110528. [Google Scholar] [CrossRef]
- Nizamutdinov, A.S.; Madirov, E.I.; Lukinova, E.V.; Kiyamov, A.G.; Andreeva, D.D.; Pudovkin, M.S.; Semashko, V.V. Spectral-Kinetic Properties and Energy Transfer in Nanoparticles of Y0.5–xCe0.5TbxF3 Solid Solution. J. Appl. Spectrosc. 2020, 87, 481–487. [Google Scholar] [CrossRef]
- Nizamutdinov, A.; Lukinova, E.; Shamsutdinov, N.; Zelenikhin, P.; Khusainova, A.; Gafurov, M.; Pudovkin, M. CeF3-YF3-TbF3 Nanoparticle-Polymer–“Radachlorin” Conjugates for Combined Photodynamic Therapy: Synthesis, Characterization, and Biological Activity. J. Compos. Sci. 2023, 7, 255. [Google Scholar] [CrossRef]
- Rimoldi, T.; Orsi, D.; Lagonegro, P.; Ghezzi, B.; Galli, C.; Rossi, F.; Cristofolini, L. CeF3-ZnO scintillating nanocomposite for self-lighted photodynamic therapy of cancer. J. Mater. Sci. Mater. Med. 2016, 27, 1–9. [Google Scholar] [CrossRef]
- Xiang, H.; Xue, F.; Yi, T.; Tham, H.P.; Liu, J.G.; Zhao, Y. Cu2–x S Nanocrystals Cross-Linked with Chlorin e6-Functionalized Polyethylenimine for Synergistic Photodynamic and Photothermal Therapy of Cancer. ACS Appl. Mater. Interfaces 2018, 10, 16344–16351. [Google Scholar] [CrossRef] [PubMed]
- Zhiyentayev, T.M.; Boltaev, U.T.; Solov’eva, A.B.; Aksenova, N.A.; Glagolev, N.N.; Chernjak, A.V.; Melik-Nubarov, N.S. Complexes of chlorin e6 with pluronics and polyvinylpyrrolidone: Structure and photodynamic activity in cell culture. Photochem. Photobiol. 2014, 90, 171–182. [Google Scholar] [CrossRef]
- Hädener, M.; Gjuroski, I.; Furrer, J.; Vermathen, M. Interactions of polyvinylpyrrolidone with chlorin e6-based photosensitizers studied by NMR and electronic absorption spectroscopy. J. Phys. Chem. B 2015, 119, 12117–12128. [Google Scholar] [CrossRef]
- Solov’eva, A.B.; Khasanova, O.V.; Aksenova, N.A.; Chernyak, A.V.; Volkov, V.I.; Timofeeva, V.A.; Timashev, P.S. The Influence of Effect of Polysaccharides and Polyvinylpyrrolidone on the Photocatalytic Activity of Chlorin e6 in Tryptophan Oxidation. Russ. J. Phys. Chem. A 2019, 93, 2507–2514. [Google Scholar] [CrossRef]
- Tsvetkov, V.B.; Solov’eva, A.B.; Melik-Nubarov, N.S. Computer modeling of the complexes of Chlorin e6 with amphiphilic polymers. Phys. Chem. Chem. Phys. 2014, 16, 10903–10913. [Google Scholar] [CrossRef]
- Gadzhimagomedova, Z.; Polyakov, V.; Pankin, I.; Butova, V.; Kirsanova, D.; Soldatov, M.; Soldatov, A. BaGdF5 Nanophosphors Doped with Different Concentrations of Eu3+ for Application in X-ray Photodynamic Therapy. Int. J. Mol. Sci. 2021, 22, 13040. [Google Scholar] [CrossRef]
- Abràmoff, M.D.; Magalhães, P.J.; Ram, S.J. Image Processing with ImageJ. Biophotonics Int. 2004, 11, 36–42. [Google Scholar]
- Freshney, R.I. Culture of Animal Cells: A Manual of Basic Technique and Specialized Applications; John Wiley & Sons: Hoboken, NJ, USA, 2015. [Google Scholar]
- Alakshin, E.M.; Klochkov, A.V.; Kondratyeva, E.I.; Korableva, S.L.; Kiiamov, A.G.; Nuzhina, D.S.; Kodjikian, S. Microwave-assisted hydrothermal synthesis and annealing of DyF3 nanoparticles. J. Nanomater. 2016, 2016, 7148307. [Google Scholar] [CrossRef]
- Wang, X.; Sheng, T.; Fu, Z.; Li, W. Highly uniform YF3: Ln3+ (Ln = Ce3+, Tb3+) walnut-like microcrystals: Hydrothermal synthesis and luminescent properties. Mater. Res. Bull. 2013, 48, 2143–2148. [Google Scholar] [CrossRef]
- Efendiev, K.T.; Alekseeva, P.M.; Shiryaev, A.A.; Skobeltsin, A.S.; Solonina, I.L.; Fatyanova, A.S.; Loschenov, V.B. Preliminary low-dose photodynamic exposure to skin cancer with chlorin e6 photosensitizer. Photodiagnosis Photodyn. Ther. 2022, 38, 102894. [Google Scholar] [CrossRef]
- Dubey, T.; Gorantla, N.V.; Chandrashekara, K.T.; Chinnathambi, S. Photodynamic exposure of Rose-Bengal inhibits Tau aggregation and modulates cytoskeletal network in neuronal cells. Sci. Rep. 2020, 10, 12380. [Google Scholar] [CrossRef]
- Wen, J.; Duan, C.K.; Ning, L.; Huang, Y.; Zhan, S.; Zhang, J.; Yin, M. Spectroscopic distinctions between two types of Ce3+ ions in X2-Y2SiO5: A theoretical investigation. J. Phys. Chem. A 2014, 118, 4988–4994. [Google Scholar] [CrossRef]
- Camus-Génot, V.; Lhoste, J.; Moury, R.; Galven, C.; Hémon-Ribaud, A.; Pascual, S.; Guiet, A. Facile preparation of 3D interconnected macroporous CeF3. J. Solid State Chem. 2023, 324, 124099. [Google Scholar] [CrossRef]
- Momma, K.; Izumi, F. VESTA 3 for three-dimensional visualization of crystal, volumetric and morphology data. J. Appl. Crystallogr. 2011, 44, 1272–1276. [Google Scholar] [CrossRef]
- Zhang, X.; Huang, Y.; Gong, M. Dual-emitting Ce3+, Tb3+ co-doped LaOBr phosphor: Luminescence, energy transfer and ratiometric temperature sensing. Chem. Eng. J. 2017, 307, 291–299. [Google Scholar] [CrossRef]
- Pudovkin, M.S.; Ginkel, A.K.; Morozov, O.A.; Kiiamov, A.G.; Kuznetsov, M.D. Highly-sensitive lifetime optical thermometers based on Nd3+, Yb3+: YF3 phosphors. J. Lumin. 2022, 249, 119037. [Google Scholar] [CrossRef]
- Guo, B.; Zhang, Z.W.; Jiang, D.G.; Li, Y.N.; Sun, X.Y. Generation of bright white-light by energy-transfer strategy in Ca19Zn2(PO4)14: Ce3+, Tb3+, Mn2+ phosphors. J. Lumin. 2019, 206, 244–249. [Google Scholar] [CrossRef]
- Ren, Y.; Rosch, J.G.; Landry, M.R.; Winter, H.; Khan, S.; Pratx, G.; Sun, C. Tb-Doped core–shell–shell nanophosphors for enhanced X-ray induced luminescence and sensitization of radiodynamic therapy. Biomater. Sci. 2021, 9, 496–505. [Google Scholar] [CrossRef] [PubMed]
- Sahoo, H. Förster resonance energy transfer–A spectroscopic nanoruler: Principle and applications. J. Photochem. Photobiol. C Photochem. Rev. 2011, 12, 20–30. [Google Scholar] [CrossRef]
- Clegg, R.M. Förster resonance energy transfer—FRET what is it, why do it, and how it’s done. Lab. Tech. Biochem. Mol. Biol. 2009, 33, 1–57. [Google Scholar]
- Tang, Y.A.; Hu, J.; Elmenoufy, A.H.; Yang, X. Highly efficient FRET system capable of deep photodynamic therapy established on X-ray excited mesoporous LaF3: Tb scintillating nanoparticles. ACS Appl. Mater. Interfaces 2015, 7, 12261–12269. [Google Scholar] [CrossRef]
- Zhang, W.; Zhang, X.; Shen, Y.; Shi, F.; Song, C.; Liu, T.; Lu, H. Ultra-high FRET efficiency NaGdF4: Tb3+-Rose Bengal biocompatible nanocomposite for X-ray excited photodynamic therapy application. Biomaterials 2018, 184, 31–40. [Google Scholar] [CrossRef]
- Li, X.; Zhang, W.; Dong, L.; Liu, D.; Qi, Z. Low temperature molten salt synthesis of CeF3 and CeF3: Tb3+ phosphors with efficient luminescence properties. J. Lumin. 2019, 205, 122–128. [Google Scholar] [CrossRef]
- Cooper, D.R.; Kudinov, K.; Tyagi, P.; Hill, C.K.; Bradforth, S.E.; Nadeau, J.L. Photoluminescence of cerium fluoride and cerium-doped lanthanum fluoride nanoparticles and investigation of energy transfer to photosensitizer molecules. Phys. Chem. Chem. Phys. 2014, 16, 12441–12453. [Google Scholar] [CrossRef]
- Kim, S.; Ohulchanskyy, T.Y.; Pudavar, H.E.; Pandey, R.K.; Prasad, P.N. Organically modified silica nanoparticles co-encapsulating photosensitizing drug and aggregation-enhanced two-photon absorbing fluorescent dye aggregates for two-photon photodynamic therapy. J. Am. Chem. Soc. 2007, 129, 2669–2675. [Google Scholar] [CrossRef]
Amount of Rch, µL | Distance r, nm | |
---|---|---|
Unmodified | Coated with PVP | |
10 | 8.1 ± 1.2 | 6.3 ± 1.2 |
30 | 6.4 ± 1.2 | 4.6 ± 1.2 |
50 | 5.8 ± 1.2 | 4.2 ± 1.2 |
70 | 5.9 ± 1.2 | 5.0 ± 1.2 |
90 | 5.0 ± 1.2 | 3.7 ± 1.2 |
110 | 4.8 ± 1.2 | 3.6 ± 1.2 |
140 | 4.7 ± 1.2 | 3.5 ± 1.2 |
160 | 4.6 ± 1.2 | 3.5 ± 1.2 |
160 µL Rch + 0.5 mL H2O | 4.3 ± 1.2 | 3.5 ± 1.2 |
160 µL Rch + 1.0 mL H2O | 5.0 ± 1.2 | 3.5 ± 1.2 |
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Khusainova, A.I.; Nizamutdinov, A.S.; Shamsutdinov, N.I.; Kalinichenko, S.; Safin, D.I.; Gafurov, M.; Lukinova, E.V.; Batygov, S.K.; Kuznetsov, S.V.; Zinchenko, S.V.; et al. Photo- and X-ray Induced Cytotoxicity of CeF3-YF3-TbF3 Nanoparticle-Polyvinylpyrrolidone—“Radachlorin” Composites for Combined Photodynamic Therapy. Materials 2024, 17, 316. https://doi.org/10.3390/ma17020316
Khusainova AI, Nizamutdinov AS, Shamsutdinov NI, Kalinichenko S, Safin DI, Gafurov M, Lukinova EV, Batygov SK, Kuznetsov SV, Zinchenko SV, et al. Photo- and X-ray Induced Cytotoxicity of CeF3-YF3-TbF3 Nanoparticle-Polyvinylpyrrolidone—“Radachlorin” Composites for Combined Photodynamic Therapy. Materials. 2024; 17(2):316. https://doi.org/10.3390/ma17020316
Chicago/Turabian StyleKhusainova, Alina I., Alexey S. Nizamutdinov, Nail I. Shamsutdinov, Svetlana Kalinichenko, Damir I. Safin, Marat Gafurov, Elena V. Lukinova, Sergey Kh. Batygov, Sergey V. Kuznetsov, Sergey V. Zinchenko, and et al. 2024. "Photo- and X-ray Induced Cytotoxicity of CeF3-YF3-TbF3 Nanoparticle-Polyvinylpyrrolidone—“Radachlorin” Composites for Combined Photodynamic Therapy" Materials 17, no. 2: 316. https://doi.org/10.3390/ma17020316
APA StyleKhusainova, A. I., Nizamutdinov, A. S., Shamsutdinov, N. I., Kalinichenko, S., Safin, D. I., Gafurov, M., Lukinova, E. V., Batygov, S. K., Kuznetsov, S. V., Zinchenko, S. V., Zelenikhin, P. V., & Pudovkin, M. (2024). Photo- and X-ray Induced Cytotoxicity of CeF3-YF3-TbF3 Nanoparticle-Polyvinylpyrrolidone—“Radachlorin” Composites for Combined Photodynamic Therapy. Materials, 17(2), 316. https://doi.org/10.3390/ma17020316