The Assessment of Photo-Induced Toxicity of [NaYF4:Yb3+, Er3+] Upconversion Nanoparticles on Model Normal and Cancer Cell Lines in Vitro

Irina Yu. Yanina; Roman A. Verkhovskii; Nikita A. Navolokin; Vyacheslav I. Kochubey

doi:10.18287/JBPE24.10.010309

The Assessment of Photo-Induced Toxicity of [NaYF4:Yb3+, Er3+] Upconversion Nanoparticles on Model Normal and Cancer Cell Lines in Vitro

Irina Yu. Yanina (Login required)
Saratov State University, Russian Federation
Tomsk State University, Russian Federation

Roman A. Verkhovskii
Saratov State University, Russian Federation

Nikita A. Navolokin
Saratov State Medical University, Russian Federation
State Healthcare Institution “Saratov City Clinical Hospital No. 1 named after Yu. Ya. Gordeev”, Russian Federation

Vyacheslav I. Kochubey
Saratov State University, Russian Federation
Tomsk State University, Russian Federation

Paper #9046 received 15 Dec 2023; revised manuscript received 19 Mar 2024; accepted for publication 19 Mar 2024; published online 31 Mar 2024.

DOI: 10.18287/JBPE24.10.010309

Abstract

Upconversion nanoparticles (UCNPs) are promising alternatives to traditional fluorescent labels for cell imaging that have outstanding potential in biological and clinical applications. As we previously established, the co-incubation of synthesized in-house [NaYF₄:Yb³⁺, Er³⁺] UCNPs uncoated and coated by SiO₂ shell with the cell lines resulted in particles’ uptake. Because of the tendency to particle internalization by cells, the assessment of the biocompatibility of UCNPs intended for biomedical applications and their ability to induce desirable biological effects under the appropriate wavelength irradiation is an important step in UCNPs development. The present work is focused on the assessment of [NaYF₄:Yb³⁺, Er³⁺] UCNPs’ phototoxicity and changes in human lung-derived embryonic fibroblast (FLEH-104) and human laryngeal epidermoid carcinoma (Hep-2) cell lines’ morphology in response to the influence of UCNPs.

Keywords

cell lines; upconversion nanoparticles; luminescence; phototoxicity; laser; NIR

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References

1. J. Ferlay, M. Colombet, I. Soerjomataram, D. M. Parkin, M. Piñeros, A. Znaor, and F. Bray, “Cancer statistics for the year 2020: An overview,” International Journal of Cancer 149(4), 778−789 (2021).

2. Cancer, World Health Organization (accessed 15 September 2022). [https://www.who.int/news-room/fact-sheets/detail/cancer].

3. J. G. Hiller, N. J. Perry, G.Poulogiannis, B. Riedel, and E. K. Sloan,“Perioperative events influence cancer recurrence risk after surgery,” Nature Reviews Clinical Oncology 15(4), 205−218 (2018).

4. Y. P. Liu, C. C. Zheng, Y. N. Huang, M. L. He, W. W. Xu, and B. Li, “Molecular mechanisms of chemo- and radiotherapy resistance and the potential implications for cancer treatment,” MedComm 2(3), 315−340 (2021).

5. Y. Wu, Y. Song, R. Wang, and T. Wang, “Molecular mechanisms of tumor resistance to radiotherapy,” Molecular Cancer 22(1), 96 (2023).

6. N. V. Polukonova, M. A. Baryshnikova, D. A. Khochankov, E. V. Stepanova, E. S. Solomko, A. V. Polukonova, D. A. Mudrak, A. M. Mylnikov, A. B. Bucharskaya, G. N. Maslyakova, and N. A. Navolokin, “Activation of Apoptosis and Autophagy by Gratiola Officinalis Extract in Human Tumor Cell Lines,” Journal of Biomedical Photonics & Engineering 7(4), 040307 (2021).

7. H. Modjtahedi, S. Ali, and S. Essapen,“Therapeutic application of monoclonal antibodies in cancer: advances and challenges,” British Medical Bulletin 104, 41−59 (2012).

8. V. M. Tolmachev, V. I. Chernov, and S. M. Deyev, “Targeted nuclear medicine. Seek and destroy,” Russian Chemical Reviews 91(3), RCR5034 (2022).

9. N. Widmer, C. Bardin, E. Chatelut, A. Paci, J. Beijnen, D. Levêque, G. Veal, and A. Astier, “Review of therapeutic drug monitoring of anticancer drugs part two – Targeted therapies,” European Journal of Cancer 50(12), 2020−2036 (2014).

10. E. Raschi, V. Vasina, M. G. Ursino, G. Boriani, A. Martoni, and F. De Ponti, “Anticancer drugs and cardiotoxicity: Insights and perspectives in the era of targeted therapy,” Pharmacology & Therapeutics 125(2), 196−218 (2010).

11. T. A. Baudino, “Targeted Cancer Therapy: The Next Generation of Cancer Treatment,” Current Drug Discovery Technologies 12(1), 3−20 (2015).

12. M. Kim, D. M. Kim, K. S. Kim, W. Jung, and D. E. Kim, “Applications of Cancer Cell-Specific Aptamers in Targeted Delivery of Anticancer Therapeutic Agents,” Molecules 23(4), 830 (2018).

13. H. Sun, X. Zhu, P. Y. Lu, R. R. Rosato, W. Tan, and Y. Zu, “Oligonucleotide aptamers: new tools for targeted cancer therapy,” Molecular Therapy-Nucleic Acids 3(8), e182 (2014).

14. M. C. Skala, J. M. Squirrell, K. M. Vrotsos, J. C. Eickhoff, A. Gendron-Fitzpatrick, K. W. Eliceiri, and N. Ramanujam, “Multiphoton microscopy of endogenous fluorescence differentiates normal, precancerous, and cancerous squamous epithelial tissues,” Cancer Research 65(4), 1180−1186 (2005).

15. S. Maryam, M. S. Nogueira, R. Gautam, S. Krishnamoorthy, S. K. V. Sekar, K. W. Kho, H. Lu, R. N. Riordain, L. Feeley, P. Sheahan, R. Burke, and S. Andersson-Engels, “Label-Free Optical Spectroscopy for Early Detection of Oral Cancer,” Diagnostics 12(12), 2896 (2022).

16. L. Yang, J. Park, M. Marjanovic, E. J. Chaney, D. R. Spillman Jr, H. Phillips, and S. A. Boppart, “Intraoperative Label-Free Multimodal Nonlinear Optical Imaging for Point-of-Procedure Cancer Diagnostics,” IEEE Journal of Selected Topics in Quantum Electronics 27(4), 1−12 (2021).

17. S. Hernot, L. van Manen, P. Debie, J. S. D. Mieog, and A. L. Vahrmeijer, “Latest developments in molecular tracers for fluorescence image-guided cancer surgery,” Lancet Oncology 20(7), e354-e367 (2019).

18. D. Musumeci, C. Platella, C. Riccardi, F. Moccia, and D. Montesarchio, “Fluorescence Sensing Using DNA Aptamers in Cancer Research and Clinical Diagnostics,” Cancers 9(12), 174 (2017).

19. M. Gao, F. Yu, C. Lv, J. Choo, and L. Chen, “Fluorescent chemical probes for accurate tumor diagnosis and targeting therapy,” Chemical Society Reviews 46(8), 2237−2271 (2017).

20. V. Shupletsov, K. Kandurova, V. Dremin, E. Potapova, M. Apanaykin, U. Legchenko, and A. Dunaev, “Fluorescence imaging system for biological tissues diagnosis: phantom and animal studies,” Journal of Biomedical Photonics & Engineering 6(1), 010303 (2020).

21. V. Maryakhina, Y. Korneva, I. Chekurov, and O. Shisterova, “Fluorescent diagnostics of benign breast diseases and breast cancer,” Journal of Biomedical Photonics & Engineering 3(4), 040306 (2017).

22. A. D. Mironova, Y. V. Kargina, Olga S. Pavlova, A. M. Perepukhov, I. O. Sobina, and V. Yu. Timoshenko, “Porous Silicon Nanoparticles with Rare Earth as Potential Contrast Agents for MRI and Luminescent Probes for Bioimaging,” Journal of Biomedical Photonics & Engineering 8(2), 020304 (2022).

23. M. Albota, D. Beljonne, J. L. Brédas, J. E. Ehrlich, J.-Y. Fu, A. A. Heikal, S. E. Hess, T. Kogej, M. D. Levin, S. R. Marder, D. Mccord-Maughon, J. W. Perry, H. RöCkel, M. Rumi, G. Subramaniam, W. W. Webb, X.-L. Wu, and C. Xu, “Design of organic molecules with large two-photon absorption cross sections,” Science 281(5383), 1653−1656 (1998).

24. D. R. Larson, W. R. Zipfel, R. M. Williams, S. W. Clark, M. P. Bruchez, F. W. Wise, and W. W. Webb, “Water-soluble quantum dots for multiphoton fluorescence imaging in vivo,” Science 300(5624), 1434−1436 (2003).

25. R. A. Farrer, F. L. Butterfield, V. W. Chen, and J. T. Fourkas, “Highly efficient multiphoton-absorption-induced luminescence from gold nanoparticles,” Nano Letters 5(6), 1139−1142 (2005).

26. C. Sönnichsen, A. P. Alivisatos, “Gold nanorods as novel nonbleaching plasmon-based orientation sensors for polarized single-particle microscopy,” Nano Letters 5(2), 301−304 (2005).

27. H. Wang, T. B. Huff, D. A. Zweifel, W. He, P. S. Low, A. Wei, and J. X. Cheng, “In vitro and in vivo two-photon luminescence imaging of single gold nanorods,” Proceedings of the National Academy of Sciences 102(44), 15752−15756 (2005).

28. D. Yelin, D. Oron, S. Thiberge, E. Moses, and Y. Silberberg, “Multiphoton plasmon-resonance microscopy,” Optics Express 11(12), 1385−1391 (2003).

29. W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nature Biotechnology 21(11), 1369−1377 (2003).

30. B. Gidwani, V. Sahu, S. S. Shukla, R. Pandey, V. Joshi, V. K. Jain, and A. Vyas, “Quantum dots: Prospectives, toxicity, advances and applications,” Journal of Drug Delivery Science and Technology 61, 102308 (2021).

31. M. J. Abrams, B. A. Murrer, “Metal compounds in therapy and diagnosis,” Science 261(5122), 725−730 (1993).

32. Q. Fan, X. Cui, H. Guo, Y. Xu, G. Zhang, and B. Peng, “Application of rare earth-doped nanoparticles in biological imaging and tumor treatment,” Journal of Biomaterials Applications 35(2), 237−263 (2020).

33. N. Zhou, J. Ni, and R. He, “Advances of Upconversion Nanoparticles for Molecular Imaging,” Nano Biomedicine & Engineering 5(3), 131 (2013).

34. S. A. Hilderbrand, F. Shao, C. Salthouse, U. Mahmood, and R. Weissleder, “Upconverting luminescent nanomaterials: application to in vivo bioimaging,” Chemical Communications (28), 4188−4190 (2009).

35. S. Andersson-Engels, H. Liu, C. T. Xu, P. Svenmarker, A. Gisselsson, P. Kjellman, L. Andersson, R. in’t Zandt, F. Olsson, and S. Fredriksson, “In vivo luminescence imaging and tomography using upconverting nanoparticles as contrast agents,” In 2012 Asia Communications and Photonics Conference (ACP), AS3E.2 (2012).

36. M. A. Syroeshkin, F. Kuriakose, E. A. Saverina, V. A. Timofeeva, M. P. Egorov, and I. V. Alabugin, “Upconversion of Reductants,” Angewandte Chemie International Edition 58(17), 5532−5550 (2019).

37. S. Han, R. Deng, X. Xie, and X. Liu, “Enhancing luminescence in lanthanide-doped upconversion nanoparticles,” Angewandte Chemie International Edition 53(44), 11702−11715 (2014).

38. P. P. Nampi, A. Vakurov, L. E. Mackenzie, N. S. Scrutton, P. A. Millner, G. Jose, and S. Saha, “Selective cellular imaging with lanthanide-based upconversion nanoparticles,” Journal of Biophotonics 12, e201800256 (2019).

39. H. Li, Q. Chen, J. Zhao, and K. Urmila, “Fabricating upconversion fluorescent nanoparticles modified substrate for dynamical control of cancer cells and pathogenic bacteria,” Journal of Biophotonics 10(8), 1034−1042 (2017).

40. A. K. S. Braz, D. S. Moura, A. S. L. Gomes, T. Y. Ohulchanskyy, G. Chen, M. Liu, J. Damasco, R. E. de Araujo, and P. N. Prasad, “TiO2 -coated fluoride nanoparticles for dental multimodal optical imaging,” Journal of Biophotonics 11(4), e201700029 (2018).

41. Y. Yang, T. Zhang, and D. Xing, “Single 808 nm near-infrared-triggered multifunctional upconverting phototheranostic nanocomposite for imaging-guided high-efficiency treatment of tumors,” Journal of Biophotonics 14 (9), e202100134 (2021).

42. Y. Hu, J. F. Honek, B. C. Wilson, and Q-B. Lu, “Design, synthesis and photocytotoxicity of upconversion nanoparticles: Potential applications for near-infrared photodynamic and photothermal therapy,” Journal of Biophotonics 12, e201900129 (2019).

43. R. Liang, M. Wei, D. G. Evans, and X. Duan, “Inorganic nanomaterials for bioimaging, targeted drug delivery and therapeutics,” Chemical Communications 50(91), 14071 (2014).

44. U. Kostiv, M. Šlouf, H. Macková, A. Zhigunov, H. Engstová, K. Smolková, P. Ježek, and D. Horák, “Silica-coated upconversion lanthanide nanoparticles: The influence of crystal design on morphology, structure and optical properties,” Beilstein Journal of Nanotechnology 6, 2290−2299 (2015).

45. M. Tou, Z. Luo, S. Bai, F. Liu, Q. Chai, S. Li, and Z. Li, “Sequentially coating upconversion NaYF4:Yb,Tm nanocrystals with SiO2 and ZnO layers for NIR-driven photocatalytic and antibacterial applications,” Materials Science and Engineering: C 70, 1141−1148 (2017).

46. T. Jang, M. J. Kim, and S. H. Sohn, “Silica nanoparticle coating of NaYF4:(Yb3+, Er3+) upconversion phosphor,” Journal of Nanomaterials 2022, 8961362 (2022).

47. P. Kowalik, D. Elbaum, J. Mikulski, et al., “Upconversion fluorescence imaging of HeLa cells using ROS-generating SiO2-coated lanthanide-doped NaYF4nanoconstructs,” RSC Advances 7(48), 30262−30273 (2017).

48. R. A. Verkhovskii, R. A. Anisimov, M. V. Lomova, D. K. Tuchina, E. N. Lazareva, A. A. Doronkina, A. M. Mylnikov, N. A. Navolokin, V. I. Kochubey, and I. Yu. Yanina, “Cytotoxicity of various types of coated upconversion nanoparticles. Overview,” Izvestiya of Saratov University. Physics 22(4), 357–373 (2022). [in Russian].

49. I. Yu. Yanina, E. A. Sagaidachnaya, I. V. Vidyasheva, N. A. Navolokin, V. I. Kochubey, and V. V. Tuchin, “Phototoxicity and luminescence of the upconversion nanoparticles embedded in the cells,” Proceedings of SPIE 10877, 108770Y (2019).

50. E. A. Sagaidachnaya, J. G. Konyukhova, N. I. Kazadaeva, A. A. Doronkina, I. Yu. Yanina, A. A. Skaptsov, A. B. Pravdin, and V. I. Kochubey, “Effect of hydrothermal synthesis conditions on up-conversion luminescence intensity of β-NaYF4 : Er3+, Yb3+ particles,” Quantum Electronics 50(2), 109–113 (2020).

51. A. E. Guller, A. N. Generalova, E. V. Petersen, A. V. Nechaev, I. A. Trusova, N. N. Landyshev, A. Nadort, E. A. Grebenik, S. M. Deyev, A. B. Shekhter, and A. V. Zvyagin, “Cytotoxicity and non-specific cellular uptake of bare and surface-modified upconversion nanoparticles in human skin cells,” Nano Research 8, 1546−1562 (2015).