Factors Determining the Increased Sensitivity of Cancer Cells to the Action of Optical Radiation in Blue Spectral Region
Vitaly Yu. Plavskii
(Login required)
State Scientific Institution “B.I. Stepanov Institute of Physics of the National Academy of Sciences of Belarus”, Minsk, Republic of Belarus
Aliaksandr V. Mikulich
State Scientific Institution “B.I. Stepanov Institute of Physics of the National Academy of Sciences of Belarus”, Minsk, Republic of Belarus
DOI: 10.18287/JBPE25.11.020305
Abstract
The majority of studies state that inactivating effect of blue light is more pronounced in relation to cancer cells. We show, for the first time, that one of the reasons for increased sensitivity of cancer cells to blue light is higher concentrations of endogenous porphyrin sensitizers in them, which is confirmed by fluorescence methods. This leads to higher levels of light-induced production of reactive oxygen species in cancer cells, detected by chemiluminescence, and higher rate of light-induced decrease in metabolic activity of cancer cells compared to normal cells. The decisive role of endogenous porphyrins is evidenced by higher rate of photoinactivation of cells and more intense chemiluminescent signal when cells are exposed to laser radiation with wavelength of λ = 405 nm, corresponding to the maximum of absorption spectrum of porphyrins, compared with λ = 445 nm, corresponding to the maximum of absorption spectrum of flavins.
Keywords
Full Text:
PDFReferences
1. H. Serrage, V. Heiskanen, W. M. Palin, P. R. Cooper, M. R. Milward, M. Hadis, and M. R. Hamblin, “Under the spotlight: mechanisms of photobiomodulation concentrating on blue and green light,” Photochemical & Photobiological Sciences 18(8), 1877–1909 (2019).
2. Z. Chen, S. Huang, and M. Liu, “The review of the light parameters and mechanisms of Photobiomodulation on melanoma cells,” Photodermatology, Photoimmunology & Photomedicine 38(1), 3–11 (2022).
3. J. Yang, Q. Fu, H. Jiang, Y. Li, and M. Liu, “Progress of phototherapy for osteosarcoma and application prospect of blue light photobiomodulation therapy,” Frontiers in Oncology 12, 1022973 (2022).
4. N. Matsumoto, K. Yoshikawa, M. Shimada, N. Kurita, H. Sato, T. Iwata, J. Higashijima, M. Chikakiyo, M. Nishi, H. Kashihara, C. Takasu, S. Eto, A. Takahashi, M. Akutagawa, and T. Emoto, “Effect of light irradiation by light emitting diode on colon cancer cells,” Anticancer Research 34(9), 4709–4716 (2014).
5. P. Oh, H. Kim, E. Kim, H. Hwang, H. H. Ryu, S. Lim, M. Sohn, and H. Jeong, “Inhibitory effect of blue light emitting diode on migration and invasion of cancer cells,” Journal of Cellular Physiology 232(12), 3444–3453 (2017).
6. T. Yoshimoto, Y. Morine, C. Takasu, R. Feng, T. Ikemoto, K. Yoshikawa, S. Iwahashi, Y. Saito, H. Kashihara, M. Akutagawa, T. Emoto, Y. Kinouchi, and M. Shimada, “Blue light-emitting diodes induce autophagy in colon cancer cells by Opsin 3,” Annals of Gastroenterological Surgery 2(2), 154–161 (2018).
7. G. Yan, L. Zhang, C. Feng, R. Gong, E. Idiiatullina, Q. Huang, M. He, S. Guo, F. Yang, Y. Li, F. Ding, W. Ma, V. Pavlov, Z. Han, Z. Wang, C. Xu, B. Cai, Y. Yuan, and L. Yang, “Blue light emitting diodes irradiation causes cell death in colorectal cancer by inducing ROS production and DNA damage,” The International Journal of Biochemistry & Cell Biology 103, 81–88 (2018).
8. C. Li, G. Zhu, Z. Cui, J. Zhang, S. Zhang, and Y. Wei, “The strong inhibitory effect of combining anti-cancer drugs AT406 and rocaglamide with blue LED irradiation on colorectal cancer cells,” Photodiagnosis and Photodynamic Therapy 30, 101797 (2020).
9. M. Nishi, M. Shimada, K. Yoshikawa, J. Higashijima, T. Nakao, C. Takasu, S. Eto, and H. Teraoku, “Effect of light irradiation by light emitting diode on colon cancer cells and cancer stem cells,” Journal of Clinical Oncology 33(3_suppl), 271–271 (2015).
10. T. Yoshimoto, M. Shimada, T. Tokunaga, T. Nakao, M. Nishi, C. Takasu, H. Kashihara, Y. Wada, S. Okikawa, and K. Yoshikawa, “Blue light irradiation inhibits the growth of colon cancer and activation of cancer‑associated fibroblasts,” Oncology Reports 47(5), 104 (2022).
11. H. Kim, Y. Kim, T.-H. Kim, S.-Y. Heo, W.-K. Jung, and H. W. Kang, “Stimulatory effects of wavelength-dependent photobiomodulation on proliferation and angiogenesis of colorectal cancer,” Journal of Photochemistry and Photobiology B: Biology 234, 112527 (2022).
12. M. Ohara, Y. Kawashima, O. Katoh, and H. Watanabe, “Blue light inhibits the growth of B16 melanoma cells,” Japanese Journal of Cancer Research 93(5), 551–558 (2002).
13. M. Ohara, T. Fujikura, and H. Fujiwara, “Augmentation of the inhibitory effect of blue light on the growth of B16 melanoma cells by riboflavin,” International Journal of Oncology 22(6), 1291–1295 (2003).
14. P.-S. Oh, K. S. Na, H. Hwang, H.-S. Jeong, S. Lim, M.-H. Sohn, and H.-J. Jeong, “Effect of blue light emitting diodes on melanoma cells: Involvement of apoptotic signaling,” Journal of Photochemistry and Photobiology B: Biology 142, 197–203 (2015).
15. Z. Chen, H. Qin, S. Lin, Z. Lu, X. Fan, X. Liu, and M. Liu, “Comparative transcriptome analysis of gene expression patterns on B16F10 melanoma cells under Photobiomodulation of different light modes,” Journal of Photochemistry and Photobiology B: Biology 216, 112127 (2021).
16. Z. Chen, W. Li, X. Hu, and M. Liu, “Irradiance plays a significant role in photobiomodulation of B16F10 melanoma cells by increasing reactive oxygen species and inhibiting mitochondrial function,” Biomedical Optics Express 11(1), 27 (2020).
17. A. Sparsa, K. Faucher, V. Sol, H. Durox, S. Boulinguez, V. Doffoel-Hantz, C.-A. Calliste, J. Cook-Moreau, P. Krausz, F. G. Sturtz, C. Bedane, M.-O. Jauberteau-Marchan, M.-H. Ratinaud, and J.-M. Bonnetblanc, “Blue light is phototoxic for B16F10 murine melanoma and bovine endothelial cell lines by direct cytocidal effect,” Anticancer Research 30(1), 143–147 (2010).
18. S. L. Hopkins, B. Siewert, S. H. C. Askes, P. Veldhuizen, R. Zwier, M. Heger, and S. Bonnet, “An in vitro cell irradiation protocol for testing photopharmaceuticals and the effect of blue, green, and red light on human cancer cell lines,” Photochemical & Photobiological Sciences 15(5), 644–653 (2016).
19. K. Sato, Y. Minai, and H. Watanabe, “Effect of monochromatic visible light on intracellular superoxide anion production and mitochondrial membrane potential of B16F1 and B16F10 murine melanoma cells,” Cell Biology International 37(6), 633–637 (2013).
20. S. Zhou, R. Yamada, and K. Sakamoto, “Low energy multiple blue light-emitting diode light Irradiation promotes melanin synthesis and induces DNA damage in B16F10 melanoma cells,” PLOS ONE 18(2), e0281062 (2023).
21. Z. Chen, R. Zhang, H. Qin, H. Jiang, A. Wang, X. Zhang, S. Huang, M. Sun, X. Fan, Z. Lu, Y. Li, S. Liu, and M. Liu, “The pulse light mode enhances the effect of photobiomodulation on B16F10 melanoma cells through autophagy pathway,” Lasers in Medical Science 38(1), 71 (2023).
22. J. B. Lewis, J. C. Wataha, R. L. W. Messer, G. B. Caughman, T. Yamamoto, and S. D. Hsu, “Blue light differentially alters cellular redox properties,” Journal of Biomedical Materials Research Part B: Applied Biomaterials 72B(2), 223–229 (2005).
23. T. Nishio, R. Kishi, K. Sato, and K. Sato, “Blue light exposure enhances oxidative stress, causes DNA damage, and induces apoptosis signaling in B16F1 melanoma cells,” Mutation Research/Genetic Toxicology and Environmental Mutagenesis 883–884, 503562 (2022).
24. V. Y. Plavskii, O. N. Dudinova, L. G. Plavskaya, A. I. Tretyakova, A. V. Mikulich, R. K. Nahorny, A. D. Svechko, T. S. Ananich, A. N. Sobchuk, S. V. Yakimchuk, and I. A. Leusenka, “Spectral dependence of inhibitory effect of blue light on cancer cells and efficacy of light-induced intracellular generation of reactive oxygen species in vitro,” Journal of Biomedical Research & Environmental Sciences 5(11), 1531–1555 (2024).
25. Y. Omata, J. B. Lewis, S. Rotenberg, P. E. Lockwood, R. L. W. Messer, M. Noda, S. D. Hsu, H. Sano, and J. C. Wataha, “Intra- and extracellular reactive oxygen species generated by blue light,” Journal of Biomedical Materials Research Part A 77A(3), 470–477 (2006).
26. A. D. Patel, S. Rotenberg, R. L. Messer, J. C. Wataha, K. U. Ogbureke, V. V. McCloud, P. Lockwood, S. Hsu, and J. B. Lewis, “Blue light activates phase 2 response proteins and slows growth of a431 epidermoid carcinoma xenografts,” Anticancer Research 34(11), 6305–6313 (2014).
27. M. Tartaglione, M. Eléxpuru Zabaleta, R. Lazzarini, F. Piva, E. Busilacchi, A. Poloni, C. Ledda, V. Rapisarda, L. Santarelli, and M. Bracci, “Apoptotic mechanism activated by blue light and cisplatinum in cutaneous squamous cell carcinoma cells,” International Journal of Molecular Medicine 47(4), 48 (2021).
28. D. B. Lockwood, J. C. Wataha, J. B. Lewis, W. Y. Tseng, R. L. W. Messer, and S. D. Hsu, “Blue light generates reactive oxygen species (ROS) differentially in tumor vs. normal epithelial cells,” Dental Materials 21(7), 683–688 (2005).
29. V. Y. Plavskii, L. G. Plavskaya, O. N. Dudinova, A. I. Tretyakova, A. V. Mikulich, A. N. Sobchuk, R. K. Nahorny, T. S. Ananich, A. D. Svechko, S. V. Yakimchuk, and I. A. Leusenko, “Endogenous photoacceptors sensitizing photobiological reactions in somatic cells,” Journal of Applied Spectroscopy 90(2), 334–345 (2023).
30. I. Golovynska, S. Golovynskyi, and J. Qu, “Comparing the impact of NIR , visible and UV light on ROS upregulation via photoacceptors of mitochondrial complexes in normal, immune and cancer cells,” Photochemistry and Photobiology 99(1), 106–119 (2023).
31. Y.-J. Kim, J. Song, D.-H. Lee, S. H. Um, and S. H. Bhang, “Suppressing cancer by damaging cancer cell DNA using LED irradiation,” Journal of Photochemistry and Photobiology B: Biology 243, 112714 (2023).
32. S.-W. Choe, K. Park, C. Park, J. Ryu, and H. Choi, “Combinational light emitting diode-high frequency focused ultrasound treatment for HeLa cell,” Computer Assisted Surgery 22(sup1), 79–85 (2017).
33. J. C. Wataha, J. B. Lewis, P. E. Lockwood, S. Hsu, R. L. Messer, F. A. Rueggeberg, and S. Bouillaguet, “Blue light differentially modulates cell survival and growth,” Journal of Dental Research 83(2), 104–108 (2004).
34. C. Feng, R. Gong, Q. Zheng, G. Yan, M. He, H. Lei, X. Li, L. Zhang, Z. Xu, S. Liu, M. Yu, T. Ma, M. Gao, D. Bamba, E. Idiiatullina, N. Zagidullin, V. Pavlov, C. Xu, Y. Yuan, and L. Yang, “Synergistic anti-tumor effects of arsenic trioxide and blue LED irradiation on human osteosarcoma,” International Journal of Biological Sciences 15(2), 386–394 (2019).
35. M. He, G. Yan, Y. Wang, R. Gong, H. Lei, S. Yu, X. He, G. Li, W. Du, T. Ma, M. Gao, M. Yu, S. Liu, Z. Xu, E. Idiiatullina, N. Zagidullin, V. Pavlov, B. Cai, Y. Yuan, and L. Yang, “Blue LED causes autophagic cell death in human osteosarcoma by increasing ROS generation and dephosphorylating EGFR,” Journal of Cellular and Molecular Medicine 25(11), 4962–4973 (2021).
36. M. Takeuchi, T. Nishisho, S. Toki, S. Kawaguchi, S. Tamaki, T. Oya, Y. Uto, T. Katagiri, and K. Sairyo, “Blue light induces apoptosis and autophagy by promoting ROS-mediated mitochondrial dysfunction in synovial sarcoma,” Cancer Medicine 12(8), 9668–9683 (2023).
37. J. Yang, H. Jiang, Q. Fu, H. Qin, Y. Li, and M. Liu, “Blue light photobiomodulation induced apoptosis by increasing ROS level and regulating SOCS3 and PTEN/PI3K/AKT pathway in osteosarcoma cells,” Journal of Photochemistry and Photobiology B: Biology 249, 112814 (2023).
38. P.-S. Oh, H. Hwang, H.-S. Jeong, J. Kwon, H.-S. Kim, M. Kim, S. Lim, M.-H. Sohn, and H.-J. Jeong, “Blue light emitting diode induces apoptosis in lymphoid cells by stimulating autophagy,” The International Journal of Biochemistry & Cell Biology 70, 13–22 (2016).
39. J. Zhuang, J. Liu, X. Gao, and H. Li, “Inhibition of proliferation in U937 cells treated by blue light irradiation and combined blue light irradiation/drug,” International Journal of Molecular Sciences 19(5), 1464 (2018).
40. P. Oh, E. Kim, F. Boud, S. Lim, and H. Jeong, “Blue light inhibits proliferation of metastatic cancer cells by regulating translational initiation: a synergistic property with anticancer drugs,” Photochemistry and Photobiology 99(6), 1438–1447 (2023).
41. P.-S. Oh, H.-J. Jeong, “Therapeutic application of light emitting diode: Photo-oncomic approach,” Journal of Photochemistry and Photobiology B: Biology 192, 1–7 (2019).
42. H. Tanaka, T. Takahashi, K. Okamoto, M. Tokuda, F. Yamaguchi, and Y. Hirata, “Suppression of cancer cell proliferation by high-intensity blue LED light,” Physica Status Solidi C 8(2), 359–361 (2011).
43. J. Zhuang, Y. Liu, Q. Yuan, J. Liu, Y. Liu, H. Li, and D. Wang, “Blue light-induced apoptosis of human promyelocytic leukemia cells via the mitochondrial-mediated signaling pathway,” Oncology Letters (2018).
44. J. Zhuang, L. Xia, Z. Zou, and J. Yin, “Blue light induces ROS mediated apoptosis and degradation of AML1-ETO oncoprotein in Kasumi-1 cells,” Medical Oncology 39(5), 52 (2022).
45. J. Zhuang, J. Liu, Y. Liu, H. Li, D. Wang, and L. Teng, “Enhanced proliferation inhibition of HL60 cells treated by synergistic all-trans retinoic acid/blue light/nanodiamonds,” RSC Advances 7(62), 38895–38901 (2017).
46. M. Ohara, Y. Kawashima, H. Watanabe, and S. Kitajima, “Effects of blue-light-exposure on growth of extracorporeally circulated leukemic cells in rats with leukemia induced by 1-ethyl-1-nitrosourea,” International Journal of Molecular Medicine (2002).
47. M. Shakibaie, M. Vaezjalali, H. Rafii-Tabar, and P. Sasanpour, “Synergistic effect of phototherapy and chemotherapy on bladder cancer cells,” Journal of Photochemistry and Photobiology B: Biology 193, 148–154 (2019).
48. Y. Xia, W. Yu, F. Cheng, T. Rao, Y. Ruan, R. Yuan, J. Ning, X. Zhou, F. Lin, and D. Zheng, “Photobiomodulation with blue laser inhibits bladder cancer progression,” Frontiers in Oncology 11, 701122 (2021).
49. Y. M. Kim, S. Ko, Y. Shin, Y. Kim, T. Kim, J. Jung, S. Lee, N. G. Kim, K. Park, and J. H. Ryu, “Light-emitting diode irradiation induces AKT/mTOR-mediated apoptosis in human pancreatic cancer cells and xenograft mouse model,” Journal of Cellular Physiology 236(2), 1362–1374 (2021).
50. M. Shakibaie, M. Vaezjalali, H. Rafii-Tabar, and P. Sasanpour, “Phototherapy alters the oncogenic metabolic activity of breast cancer cells,” Photodiagnosis and Photodynamic Therapy 30, 101695 (2020).
51. T. G. Farias, M. C. Sales, A. J. C. Borges, A. L. Mencalha, and A. S. Fonseca, “Effects of low-power red laser and blue LED on oxidative stress and cell death in human breast cancer cells,” Laser Physics Letters 22(5), 055601 (2025).
52. M. He, G. Li, X. He, Y. Wang, H. Lei, Q. Wang, G. Yan, R. Gong, G. Liu, T. Li, B. Cai, L. Li, and Y. Yuan, “Blue LED causes cell death in human hepatoma by inducing DNA damage,” (2020).
53. Y. Teng, Z. Li, J. Liu, L. Teng, and H. Li, “Proliferation inhibition and apoptosis of liver cancer cells treated by blue light irradiation,” Medical Oncology 40(8), 227 (2023).
54. F. Yang, J. Tu, J.-Q. Pan, H.-L. Luo, Y.-H. Liu, J. Wan, J. Zhang, P.-F. Wei, T. Jiang, Y.-H. Chen, and L.-P. Wang, “Light-controlled inhibition of malignant glioma by opsin gene transfer,” Cell Death & Disease 4(10), e893–e893 (2013).
55. M. Esmaeeli, M. Ahmadi-Zeidabadi, M. JalalKamali, H. Eskandary, and M. Shojaei, “Inhibitory effect of photobiomodulation on the proliferation rate of the u87 glioblastoma cell line,” International Journal of Optics and Photonics 15(2), 197–208 (2021).
56. F. Y. Ang, Y. Fukuzaki, B. Yamanoha, and S. Kogure, “Immunocytochemical studies on the effect of 405-nm low-power laser irradiation on human-derived A-172 glioblastoma cells,” Lasers in Medical Science 27(5), 935–942 (2012).
57. E. K. Toruner, H. Kayhan, and F. S. Ezgu, “The effect of a geometric-shaped tool with blue led light on the activation of human dermal fibroblasts and cancer cells,” Journal of Photochemistry and Photobiology 8, 100087 (2021).
58. S. Mo, H. J. Ku, S.-H. Choi, H. J. Jeong, D.-G. Park, M. H. Oh, and J. C. Ahn, “470 nm LED irradiation inhibits the invasiveness of CD133-positive human colorectal cancer stem cells by suppressing the cyclooxygenase-2/prostaglandin E2 pathway,” Anticancer Research 41(3), 1407–1420 (2021).
59. M. Feith, T. Vičar, J. Gumulec, M. Raudenská, A. Gjörloff Wingren, M. Masařík, and J. Balvan, “Quantitative phase dynamics of cancer cell populations affected by blue light,” Applied Sciences 10(7), 2597 (2020).
60. C.-C. Lan, E. Y. Lu, H.-J. Pan, and C.-H. Lee, “Directional migration of cancer cells induced by a blue light intensity gradient,” Biomedical Optics Express 6(7), 2624 (2015).
61. H. Jiang, H. Qin, M. Sun, S. Lin, J. Yang, and M. Liu, “Effect of blue light on the cell viability of A549 lung cancer cells and investigations into its possible mechanism,” Journal of Biophotonics 16(9), e202300047 (2023).
62. W. Zhang, J. Dong, “Suppressing epithelial-mesenchymal-transition blue light therapy for reducing macrophage-mediated cancerous pulmonary fibrosis: An in-vitro study,” Journal of Biophotonics 16(12), e202300253 (2023).
63. E. Kvam, “Induction of oxidative DNA base damage in human skin cells by UV and near visible radiation,” Carcinogenesis 18(12), 2379–2384 (1997).
64. S. Passarella, T. Karu, “Absorption of monochromatic and narrow band radiation in the visible and near IR by both mitochondrial and non-mitochondrial photoacceptors results in photobiomodulation,” Journal of Photochemistry and Photobiology B: Biology 140, 344–358 (2014).
65. M. R. Hamblin, “Mechanisms and mitochondrial redox signaling in photobiomodulation,” Photochemistry and Photobiology 94(2), 199–212 (2018).
66. F. Dos Santos Ferreira, F. C. Cadoná, A. R. Aurélio, T. N. De Oliveira Martins, and H. M. F. Pivetta, “Photobiomodulation-blue and red LED: protection or cellular toxicity? In vitro study with human fibroblasts,” Lasers in Medical Science 37(1), 523–530 (2022).
67. S. Suh, E. H. Choi, and N. Atanaskova Mesinkovska, “The expression of opsins in the human skin and its implications for photobiomodulation: a systematic review,” Photodermatology, Photoimmunology & Photomedicine 36(5), 329–338 (2020).
68. R. Karthikeyan, W. I. L. Davies, and L. Gunhaga, “Non-image-forming functional roles of OPN3, OPN4 and OPN5 photopigments,” Journal of Photochemistry and Photobiology 15, 100177 (2023).
69. A. Mat, H. H. Vu, E. Wolf, and K. Tessmar-Raible, “All light, everywhere? Photoreceptors at nonconventional sites,” Physiology 39(1), 30–43 (2024).
70. A. Liebert, V. Pang, B. Bicknell, C. McLachlan, J. Mitrofanis, and H. Kiat, “A perspective on the potential of opsins as an integral mechanism of photobiomodulation: It’s not just the eyes,” Photobiomodulation, Photomedicine, and Laser Surgery 40(2), 123–135 (2022).
71. S. K. Sharma, S. Sardana, and M. R. Hamblin, “Role of opsins and light or heat activated transient receptor potential ion channels in the mechanisms of photobiomodulation and infrared therapy,” Journal of Photochemistry and Photobiology 13, 100160 (2023).
72. E. L. Bastos, F. H. Quina, and M. S. Baptista, “Endogenous photosensitizers in human skin,” Chemical Reviews 123(16), 9720–9785 (2023).
73. V. Y. Plavskii, A. V. Mikulich, A. I. Tretyakova, I. A. Leusenka, L. G. Plavskaya, O. A. Kazyuchits, I. I. Dobysh, and T. P. Krasnenkova, “Porphyrins and flavins as endogenous acceptors of optical radiation of blue spectral region determining photoinactivation of microbial cells,” Journal of Photochemistry and Photobiology B: Biology 183, 172–183 (2018).
74. V. Plavskii, A. Mikulich, N. Barulin, T. Ananich, L. Plavskaya, A. Tretyakova, and I. Leusenka, “Comparative effect of low-intensity laser radiation in green and red spectral regions on functional characteristics of sturgeon sperm,” Photochemistry and Photobiology 96(6), 1294–1313 (2020).
75. J. V. Kruchenok, O. N. Dudinova, and V. Y. Plavskii, “Bilirubin- and blue-green light-induced damage of human erythrocytes,” Journal of Biomedical Photonics & Engineering 9(2), 020303 (2023).
76. V. Yu. Plavskii, N. V. Barulin, A. V. Mikulich, A. I. Tretyakova, T. S. Ananich, L. G. Plavskaya, I. A. Leusenka, A. N. Sobchuk, V. A. Sysov, O. N. Dudinova, A. I. Vodchits, I. A. Khodasevich, and V. A. Orlovich, “Effect of continuous wave, quasi-continuous wave and pulsed laser radiation on functional characteristics of fish spermatozoa,” Journal of Photochemistry and Photobiology B: Biology 216, 112112 (2021).
77. V. Y. Plavskii, A. N. Sobchuk, A. V. Mikulich, O. N. Dudinova, L. G. Plavskaya, A. I. Tretyakova, R. K. Nahorny, T. S. Ananich, A. D. Svechko, S. V. Yakimchuk, and I. A. Leusenka, “Identification by methods of steady-state and kinetic spectrofluorimetry of endogenous porphyrins and flavins sensitizing the formation of reactive oxygen species in cancer cells,” Photochemistry and Photobiology 100(5), 1310–1327 (2024).
78. M. Eichler, R. Lavi, A. Shainberg, and R. Lubart, “Flavins are source of visible-light-induced free radical formation in cells,” Lasers in Surgery and Medicine 37(4), 314–319 (2005).
79. R. Lavi, M. Sinyakov, A. Samuni, S. Shatz, H. Friedmann, A. Shainberg, H. Breitbart, and R. Lubart, “ESR detection of1 o2 reveals enhanced redox activity in illuminated cell cultures,” Free Radical Research 38(9), 893–902 (2004).
80. P. N. Tonolli, W. K. Martins, H. C. Junqueira, M. N. Silva, D. Severino, C. Santacruz-Perez, I. Watanabe, and M. S. Baptista, “Lipofuscin in keratinocytes: Production, properties, and consequences of the photosensitization with visible light,” Free Radical Biology and Medicine 160, 277–292 (2020).
81. S. Nagahama, T. Yanamoto, M. Sano, and T. Mukai, “Wavelength dependence of InGaN laser diode characteristics,” Japanese Journal of Applied Physics 40(5R), 3075 (2001).
82. P. N. Tonolli, C. M. Vera Palomino, H. C. Junqueira, and M. S. Baptista, “The phototoxicity action spectra of visible light in HaCaT keratinocytes,” Journal of Photochemistry and Photobiology B: Biology 243, 112703 (2023).
83. T. Mosmann, “Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays,” Journal of Immunological Methods 65(1–2), 55–63 (1983).
84. C. Lu, G. Song, J.-M. Lin, “Reactive oxygen species and their chemiluminescence-detection methods,” TrAC Trends in Analytical Chemistry 25(10), 985–995 (2006).
85. W. Yu, L. Zhao, “Chemiluminescence detection of reactive oxygen species generation and potential environmental applications,” TrAC Trends in Analytical Chemistry 136, 116197 (2021).
86. B. Myrzakhmetov, P. Arnoux, S. Mordon, S. Acherar, I. Tsoy, and C. Frochot, “Photophysical properties of protoporphyrin ix, pyropheophorbide-a, and photofrin® in different conditions,” Pharmaceuticals 14(2), 138 (2021).
87. T. Nishimura, K. Hara, N. Honda, S. Okazaki, H. Hazama, and K. Awazu, “Determination and analysis of singlet oxygen quantum yields of talaporfin sodium, protoporphyrin IX, and lipidated protoporphyrin IX using near-infrared luminescence spectroscopy,” Lasers in Medical Science 35(6), 1289–1297 (2020).
88. J. Baier, T. Maisch, M. Maier, E. Engel, M. Landthaler, and W. Bäumler, “Singlet oxygen generation by UVA light exposure of endogenous photosensitizers,” Biophysical Journal 91(4), 1452–1459 (2006).
89. I. A. Menon, M. A. C. Becker, S. D. Persad, and H. F. Haberman, “Quantitation of hydrogen peroxide formed during UV-visible irradiation of protoporphyrin, coproporphyrin and uroporphyrin,” Clinica Chimica Acta 186(3), 375–381 (1990).
90. J. Hühner, Á. Ingles-Prieto, C. Neusüß, M. Lämmerhofer, and H. Janovjak, “Quantification of riboflavin, flavin mononucleotide, and flavin adenine dinucleotide in mammalian model cells by CE with LED-induced fluorescence detection,” Electrophoresis 36(4), 518–525 (2015).
91. J. R. Woodward, N. Ikeya, “Radical pair based magnetic field effects in cells: the importance of photoexcitation conditions and single cell measurements,” bioRxiv (2022).
92. N. E. Uzunbajakava, D. J. Tobin, N. V. Botchkareva, C. Dierickx, P. Bjerring, and G. Town, “Highlighting nuances of blue light phototherapy: Mechanisms and safety considerations,” Journal of Biophotonics 16(2), e202200257 (2023).
93. T. Karu, “Photobiological fundamentals of low-power laser therapy,” IEEE Journal of Quantum Electronics 23(10), 1703–1717 (1987).
94. C. Opländer, S. Hidding, F. B. Werners, M. Born, N. Pallua, and C. V. Suschek, “Effects of blue light irradiation on human dermal fibroblasts,” Journal of Photochemistry and Photobiology B: Biology 103(2), 118–125 (2011).
95. J. Liebmann, M. Born, and V. Kolb-Bachofen, “Blue-light irradiation regulates proliferation and differentiation in human skin cells,” Journal of Investigative Dermatology 130(1), 259–269 (2010).
96. M. L. Cunningham, N. I. Krinsky, S. M. Giovanazzi, and M. J. Peak, “Superoxide anion is generated from cellular metabolites by solar radiation and its components,” Journal of Free Radicals in Biology & Medicine 1(5–6), 381–385 (1985).
97. K. Sato, H. Taguchi, T. Maeda, H. Minami, Y. Asada, Y. Watanabe, and K. Yoshikawa, “The primary cytotoxicity in ultraviolet-a-irradiated riboflavin solution is derived from hydrogen peroxide,” Journal of Investigative Dermatology 105(4), 608–612 (1995).
98. A. Blum, L. I. Grossweiner, “Singlet oxygen generation by hematoporphyrin IX, uroporphyrin I and hematoporphyrin derivative at 546 nm in phosphate buffer and in the presence of egg phosphatidylcholine liposomes,” Photochemistry and Photobiology 41(1), 27–32 (1985).
99. C. R. Lambert, E. Reddi, J. D. Spikes, M. A. J. Rodgers, and G. Jori, “The effects of porphyrin structure and aggregation state on photosensitized processes in aqueous and micellar media,” Photochemistry and Photobiology 44(5), 595–601 (1986).
100. J. M. Fernandez, M. D. Bilgin, and L. I. Grossweiner, “Singlet oxygen generation by photodynamic agents,” Journal of Photochemistry and Photobiology B: Biology 37(1–2), 131–140 (1997).
101. C. Tanielian, C. Wolff, and M. Esch, “Singlet oxygen production in water: Aggregation and charge-transfer effects,” The Journal of Physical Chemistry 100(16), 6555–6560 (1996).
102. G. R. Buettner, L. W. Oberley, “Superoxide formation by protoporphyrin as seen by spin trapping,” FEBS Letters 98(1), 18–20 (1979).
103. P. A. W. Van Den Berg, J. Widengren, M. A. Hink, R. Rigler, and A. J. W. G. Visser, “Fluorescence correlation spectroscopy of flavins and flavoenzymes: photochemical and photophysical aspects,” Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 57(11), 2135–2144 (2001).
104. C. Rimington, “Spectral-absorption coefficients of some porphyrins in the soret-band region,” Biochemical Journal 75(3), 620–623 (1960).
105. Z. Ji, G. Yang, V. Vasovic, B. Cunderlikova, Z. Suo, J. M. Nesland, and Q. Peng, “Subcellular localization pattern of protoporphyrin IX is an important determinant for its photodynamic efficiency of human carcinoma and normal cell lines,” Journal of Photochemistry and Photobiology B: Biology 84(3), 213–220 (2006).
106. J. Horilova, B. Cunderlikova, and A. Marcek Chorvatova, “Time- and spectrally resolved characteristics of flavin fluorescence in U87MG cancer cells in culture,” Journal of Biomedical Optics 20(5), 051017 (2014).
107. V. Yu. Plavskii, V. A. Mostovnikov, G. R. Mostovnikova, A. I. Tret’yakova, and A. V. Mikulich, “Formation of an equilibrium complex of lactate dehydrogenase with chlorin e6,” Journal of Applied Spectroscopy 70(5), 758–764 (2003).
108. V. Yu. Plavskii, V. A. Mostovnikov, G. R. Mostovnikova, A. I. Tret’yakova, and A. V. Mikulich, “Spectral-luminescent properties of chlorin e6 and malate dehydrogenase complexes,” Journal of Applied Spectroscopy 71(6), 818–828 (2004).
109. N. Olfat, M. Ashoori, and A. Saedisomeolia, “Riboflavin is an antioxidant: a review update,” British Journal of Nutrition 128(10), 1887–1895 (2022).
110. M. R. Hamblin, J. Viveiros, C. Yang, A. Ahmadi, R. A. Ganz, and M. J. Tolkoff, “Helicobacter pylori accumulates photoactive porphyrins and is killed by visible light,” Antimicrobial Agents and Chemotherapy 49(7), 2822–2827 (2005).
111. K. Hoenes, U. Wenzel, B. Spellerberg, and M. Hessling, “Photoinactivation sensitivity of staphylococcus carnosus to visible-light irradiation as a function of wavelength,” Photochemistry and Photobiology 96(1), 156–169 (2020).
112. P. Ramakrishnan, M. Maclean, S. J. MacGregor, J. G. Anderson, and M. H. Grant, “Cytotoxic responses to 405nm light exposure in mammalian and bacterial cells: Involvement of reactive oxygen species,” Toxicology in Vitro 33, 54–62 (2016).
Сontact
34 Moskovskoe shosse, Samara, 443086, Russian Federation
Email: j-bpe@ssau.ru
Phone: +7-846-267-4550
© 2014-2025 J-BPE