Bilirubin- and Blue-Green Light-Induced Damage of Human Erythrocytes
Paper #8188 received 28 Feb 2023; revised manuscript received 25 May 2023; accepted for publication 25 May 2023; published online 9 Jun 2023.
1. T. Hansen, M. Maisels, F. Ebbesen, H. Vreman, D. Stevenson, R. Wong, and V. Bhutani, “Sixty years of phototherapy for neonatal jaundice–from serendipitous observation to standardized treatment and rescue for millions,” Journal of Perinatology 40(2), 180–193 (2020).
2. A. Lamola, “A pharmacologic view of phototherapy,” Clinics in Perinatology 43(2), 259–276 (2016).
3. V. Plavskiĭ, A. Tret’yakova, and G. Mostovnikova, “Phototherapeutic systems for the treatment of hyperbilirubinemia of newborns,” Journal of Optical Technology 81(6), 341–348 (2014).
4. S. Itoh, H. Okada, T. Kuboi, and T. Kusaka, “Phototherapy for neonatal hyperbilirubinemia,” Pediatrics International 59(9), 959–966 (2017).
5. V. Bhutani, Committee on Fetus and Newborn, “Phototherapy to prevent severe neonatal hyperbilirubinemia in the newborn infant 35 or more weeks of gestation,” Pediatrics 128(4), 1046–1052 (2011).
6. D. Seidman, J. Moise, Z. Ergaz, A. Laor, H. Vreman, D. Stevenson, and R. Gale, “A prospective randomized controlled study of phototherapy using blue and blue-green light-emitting devices, and conventional halogen-quartz phototherapy,” Journal of Perinatology 23(2), 123–127 (2003).
7. F. Ebbesen, P. Vandborg, P. Madsen, T. Trydal, L. Jakobsen, and H. Vreman, “Effect of phototherapy with turquoise vs. blue LED light of equal irradiance in jaundiced neonates,” Pediatric Research 79(2), 308–312 (2016).
8. V. Plavskii, A. Mikulich, I. Leusenko, A. Tretyakova, L. Plavskaya, N. Serdyuchenko, J. Gao, D. Xiong, and X. Wu, “Spectral range optimization to enhance the effectiveness of phototherapy for neonatal hyperbilirubinemia,” Journal of Applied Spectroscopy 84(1), 92–102 (2017).
9. T. Kuboi, T. Kusaka, H. Okada, M. Arioka, K. Nii, M. Takahashi, S. Yamato, T. Sadamura, A. Nakano, and S. Itoh, “Green light-emitting diode phototherapy for neonatal hyperbilirubinemia: Randomized controlled trial,” Pediatrics International 61(5), 465–470 (2019).
10. S. Kato, O. Iwata, Y. Yamada, H. Kakita, T. Yamada, H. Nakashima, T. Sugiura, S. Suzuki, and H. Togari, “Standardization of phototherapy for neonatal hyperbilirubinemia using multiple-wavelength irradiance integration,” Pediatrics & Neonatology 61(1), 100–105 (2020).
11. F. Ebbesen, P. Vandborg, and M. Donneborg, “The effectiveness of phototherapy using blue-green light for neonatal hyperbilirubinemia – Danish clinical trials,” Seminars in Perinatology 45(1), 151358 (2021).
12. F. Ebbesen, M. Rodrigo-Domingo, A. Moeller, H. Vreman, and M. Donneborg, “Effect of blue LED phototherapy centered at 478 nm versus 459 nm in hyperbilirubinemic neonates: a randomized study,” Pediatric Research 89(3), 598–603 (2021).
13. B. Morris, W. Oh, J. Tyson, D. Stevenson, D. Phelps, and T. O’Shea, “Aggressive vs. conservative phototherapy for infants with extremely low birth weight,” New England Journal of Medicine 359(18), 1885–1896 (2008).
14. J. Tyson, C. Pedroza, J. Langer, C. Green, B. Morris, and D. Stevenson, “Does aggressive phototherapy increase mortality while decreasing profound impairment among the smallest and sickest newborns?” Journal of Perinatology 32(9), 677–684 (2012).
15. C. Arnold, C. Pedroza, and J. E. Tyson, “Phototherapy in ELBW newborns: does it work? Is it safe? The evidence from randomized clisnical trials,” Seminars in Perinatology 38(7), 452–464 (2014).
16. S. Yahia, A. E. Shabaan, M. Gouida, D. El-Ghanam, H. Eldegla, A. El-Bakary, and H. Abdel-Hady, “Influence of hyperbilirubinemia and phototherapy on markers of genotoxicity and apoptosis in full-term infants,” European Journal of Pediatrics 174(4), 459–464 (2015).
17. N. Auger, C. Laverdière, A. Ayoub, E. Lo, and T. M. Luu, “Neonatal phototherapy and future risk of childhood cancer,” International Journal of Cancer 145(8), 2061–2069 (2019).
18. J. Oláh, E. Tóth-Molnár, L. Kemény, and Z. Csoma, “Long-term hazards of neonatal blue-light phototherapy,” British Journal of Dermatology 169(2), 243–249 (2013).
19. N. Ramy, E. A. Ghany, W. Alsharany, A. Nada, R. K. Darwish, W. A. Rabie, and H. Aly, “Jaundice, phototherapy and DNA damage in full-term neonates,” Journal of Perinatology 36(2), 132–136 (2016).
20. T. Newman, Y. Wu, M. Kuzniewicz, B. Grimes, and C. McCulloch, “Childhood seizures after phototherapy,” Pediatrics 142(4), e20180648 (2018).
21. T. Xiong, Y. Qu, S. Cambier, and D. Mu, “The side effects of phototherapy for neonatal jaundice: what do we know? What should we do?” European Journal of Pediatrics 170(10), 1247–1255 (2011).
22. J. Wang, G. Guo, A. Li, W. Q. Cai, and X. Wang, “Challenges of phototherapy for neonatal hyperbilirubinemia,” Experimental and Therapeutic Medicine 21(3), 231 (2021).
23. V. Plavskii, V. Mostovnikov, A. Tret’yakova, and G. Mostovnikova, “Sensitizing effect of Z, Z-bilirubin IXα and its photoproducts on enzymes in model solutions,” Journal of Applied Spectroscopy 75(3), 407–419 (2008).
24. G. Wondrak, M. Jacobson, and E. Jacobson, “Endogenous UVA-photosensitizers: mediators of skin photodamage and novel targets for skin photoprotection,” Photochemical & Photobiological Sciences 5, 215–237 (2006).
25. B. Rosenstein, J. Ducore, and S. Cummings, “The mechanism of bilirubin-photosensitized DNA strand breakage in human cells exposed to phototherapy light,” Mutation Research/DNA Repair Reports 112(6), 397–406 (1983).
26. F. Bohm, F. Drygalla, P. Charlesworth, K. Bohm, T. Truscott, and K. Jokiel, “Bilirubin phototoxicity to human cells by green light phototherapy in vitro,” Photochemistry and Photobiology 62(6), 980–983 (1995).
27. O. Kozlenkova, L. Plavskaya, A. Mikulich, I. Leusenko, A. Tretyakova, and V. Plavskii, “Photodamage of the cells in culture sensitized with bilirubin,” Journal of Physics: Conference Series 741(1), 012063 (2016).
28. E. Bruzell Roll, T. Christensen, “Formation of photoproducts and cytotoxicity of bilirubin irradiated with turquoise and blue phototherapy light,” Acta Paediatrica 94(10), 1448–1454 (2005).
29. T. Christensen, G. Kinn, T. Granli, and I. Amundsen, “Cells, bilirubin and light: formation of bilirubin photoproducts and cellular damage at defined wavelengths,” Acta Pædiatrica 83(1), 7–12 (1994).
30. T. Christensen, E. B. Roll, A. Jaworska, and G. Kinn, “Bilirubin and light induced cell death in a murine lymphoma cell line,” Journal of Photochemistry and Photobiology B: Biology B 58(2–3), 170–174 (2000).
31. G. Odell, R. Brown, and A. Kopelman, “The photodynamic action of bilirubin on erythrocytes,” The Journal of Pediatrics 81(3), 473–483 (1972).
32. M. Deziel, A. Girotti, “Bilirubin photosensitized lysis of resealed erythrocyte membranes,” Photochemistry and Photobiology 31(6), 593–596 (1980).
33. M. Tozzi-Ciancarelli, G. Amicosante, A. Menichelli, S. Di Giulio, and D. Del Principe, “Photodynamic damage induced by bilirubin on human platelets: possible relevance to newborn pathology,” Neonatology 48(6), 336–340 (1985).
34. E. Bruzell Roll, T. Christensen, and O. Gederaas, “Effects of bilirubin and phototherapy on osmotic fragility and haematoporphyrin-induced photohaemolysis of normal erythrocytes and spherocytes,” Acta Paediatrica 94(10), 1443–1447 (2005).
35. K. Nii, H. Okada, S. Itoh, and T. Kusaka, “Characteristics of bilirubin photochemical changes under green light-emitting diodes in humans compared with animal species,” Scientific Reports 11(1), 6391 (2021).
36. V. Plavskii, “Current State and Prospects for Development of Systems for Photodynamic Therapy of Neonatal Hyperbilirubinemia,” Biomedical Engineering 47, 91–95 (2013).
37. A. McDonagh, G. Agati, F. Fusi, and R. Pratesi, “Quantum yields for laser photocyclization of bilirubin in the presence of human serum albumin. Dependence of quantum yield on excitation wavelength,” Photochemistry and Photobiology 50(3), 305–319 (1989).
38. J. Ennever, T. Dresing, “Quantum yields for the cyclization and configurational isomerization of 4E,15Z-bilirubin,” Photochemistry and Photobiology 53(1), 25–32 (1991).
39. S. Onishi, S. Itoh, and K. Isobe, “Wavelength-dependence of the relative rate constants for the main geometric and structural photoisomerization of bilirubin IXa bound to human serum albumin: demonstration of green light at 510 nm as the most effective wavelength in photochemical changes from (ZZ)-bilirubin IXa to (EZ)-cyclobilirubin IXa via (EZ)-bilirubin,” Biochemical Journal 236(1), 23–29 (1986).
40. V. Plavskii, V. Mostovnikov, G. Mostovnikova, and A. Tret’yakova, “Spectral fluorescence and polarization characteristics of Z, Z-bilirubin IXα,” Journal of Applied Spectroscopy 74(1), 120–132 (2007).
41. V. Plavskiĭ, V. Mostovnikov, A. Tret’yakova, and G. Mostovnikova, “Photophysical processes that determine the photoisomerization selectivity of Z, Z-bilirubin IXα in complexes with albumins,” Journal of Optical Technology 74(7), 446–454 (2007).
42. H. Sato, S. Aono, R. Semba, and S. Kashiwamata, “Interaction of bilirubin with human erythrocyte membranes. Bilirubin binding to neuraminidase-and phospholipase-treated membranes,” Biochemical Journal 248(1), 21–26 (1987).
43. H. Sato, S. Kashiwamata, “Interaction of bilirubin with human erythrocyte membranes,” Biochemical Journal 210(2), 489–496 (1983).
44. A. Girotti, “Bilirubin-photosensitized crosslinking of polypeptides in the isolated membrane of the human erythrocyte,” Journal of Biological Chemistry 253(20), 7186–7193 (1978).
45. J. Kruchenok, A. Sobchuk, G. Kurilo, N. Nemkovich, and A. Rubinov, “Study of interference laser field action on erythrocyte membranes by fluorescent probe with intramolecular proton transfer,” Proceedings of SPIE 6257, 62570W (2006).
46. S. Bondarchuk, I. Bondarchuk, Statistical processing of experimental data in MS Excel: tutorial, Tomsk State Pedagogical University Publishing, Tomsk (2018). [in Russian]
47. A. Lamola, J. Esinger, W. Blumberg, S. Patel, and J. Flore, “Fluorometric study of the partition of bilirubin among blood components: basis for rapid microassays of bilirubin and bilirubin binding capacity in whole blood,” Analytical Biochemistry 100(1), 25–42 (1979).
48. J. Vazquez, M. Garcia-Calvo, F. Valdivieso, F. Mayor, and Jr. F. Mayor, “Interaction of bilirubin with the synaptosomal plasma membrane,” Journal of Biological Chemistry 263(3), 1255–1265 (1988).
49. T. Vadetskaya, N. Shukanova, and A. Vorobej, “Role of α-tocopherol and glutathione in membrane defense under photodynamic action on erythrocytes,” Doklady Nacional’noj akademii nauk Belarusi 42, 101–103 (1998). [in Russian]
50. S. V. Lepeshkevich, A. S. Stasheuski, M. V. Parkhats, V. A. Galievsky, and B. M. Dzhagarov, “Does photodissociation of molecular oxygen from myoglobin and hemoglobin yield singlet oxygen?” Journal of Photochemistry and Photobiology B: Biology 120, 130–141(2013).
51. V. Plavskii, A. Mikulich, A. Tretyakova, I. Leusenka, L. Plavskaya, O. Kazyuchits, I. Dobysh, and T. 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).
52. 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).
53. V. Plavskii, N. Barulin, A. Mikulich, A. Tretyakova, T. Ananich, L. Plavskaya, I. Leusenka, A. Sobchuk, V. Sysov, O. Dudinova, A. Vodchits, I. Khodasevich, and V. 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).
54. J. Fernandez, M. Bilgin, and L. Grossweiner, “Singlet oxygen generation by photodynamic agents,” Journal of Photochemistry and Photobiology B: Biology 37(1–2), 131–140 (1997).
55. S. Hustad, M. McKinley, H. McNulty, J. Schneede, J. Strain, J. Scott, and P. Ueland, “Riboflavin, flavin mononucleotide, and flavin adenine dinucleotide in human plasma and erythrocytes at baseline and after low-dose riboflavin supplementation,” Clinical Chemistry 48(9), 1571–1577 (2002).
56. W. Marsh Jr, D. Nelson, and H. Koenig, “Free erythrocyte protoporphyrin (FEP) I. Normal values for adults and evaluation of the hematofluorometer,” American Journal of Clinical Pathology 79(6), 655–660 (1983).
57. G. Hennig, C. Gruber, M. Vogeser, H. Stepp, S. Dittmar, R. Sroka, and G. Brittenham, “Dual-wavelength excitation for fluorescence-based quantification of zinc protoporphyrin IX and protoporphyrin IX in whole blood,” Journal of Biophotonics 7(7), 514–524 (2014).
58. M. Musawi, M. Jafar, B. Al-Gailani, N. Ahmed, F. Suhaimi, and N. Suardi, “In vitro mean red blood cell volume change induced by diode pump solid state low-level laser of 405 nm,” Photomedicine and Laser Surgery 34(5), 211–214 (2016).
59. Т. Machneva, N. Kosmacheva, Yu. Vladimirov, and А. Osipov, “The effects of low power laser radiation on blue, green and red ranges on free radical processes in rat blood in endotoxic shock,” Biochemistry (Moscow), Supplement Series B: Biomedical Chemistry 6(3), 237–246 (2012).
60. A. McDonagh, “The biliverdin–bilirubin antioxidant cycle of cellular protection: Missing a wheel?” Free Radical Biology and Medicine 49(5), 814–820 (2010).
61. A. Dvořák, K. Pospisilova, N. Capkova, L. Muchova, M. Vecka, N. Vrzackova, J. Krízová, J. Zelenka, and L. Vítek, “The effects of bilirubin and lumirubin on metabolic and oxidative stress markers,” Frontiers in Pharmacology 12, 567001 (2021).
62. M. A. Brito, R. F. Silva, and D. Brites, “Bilirubin toxicity to human erythrocytes: a review,” Clinica Chimica Acta 374(1–2), 46–56 (2006) .
63. A. Frolov, G. Gurinovich, “The laws of delayed photohaemolysis sensitized by chlorin e6,” Journal of Photochemistry and Photobiology B: Biology 13(1), 39–50 (1992).
64. N. Peskova, A. Brilkina, A. Gorokhova, N. Shilyagina, O. Kutova, A. Nerush, A. Orlova, L. Klapshina, V. Vodeneev, and I. Balalaeva, “The localization of the photosensitizer determines the dynamics of the secondary production of hydrogen peroxide in cell cytoplasm and mitochondria,” Journal of Photochemistry and Photobiology B: Biology 219, 112208 (2021).
65. V. Plavskii, L. Plavskaya, T. Аnanich, V. Katarkevich, A. Mikulich, I. Leusenko, А. Tretiakova, O. Dudinova, P. Mazmanyan, V. Karapyan, and G. Margaryan, “New approaches to improve efficacy and reduce side effects of phototherapy for neonatal hyperbilirubinemia using led and laser sources,” Photobiology and Photomedicine 26, 63–72 (2019).
66. H. Vreman, S. Kourula, J. Jašprová, L. Ludvíková, P. Klán, L. Muchova, L. Vítek, B. Cline, R. Wong, and D. Stevenson, “The effect of light wavelength on in vitro bilirubin photodegradation and photoisomer production,” Pediatric Research 85(6), 865–873 (2019).
67. G. Agati, F. Fusi, G. Donzelli, and R. Pratesi, “Quantum yield and skin filtering effects on the formation rate of lumirubin,” Journal of Photochemistry and Photobiology B: Biology 18(2–3), 197–203 (1993).
68. V. Glushko, M, Thaler, and M. Ros, “The fluorescence of bilirubin upon interaction with human erythrocyte ghosts,” Biochimica et Biophysica Acta (BBA)-General Subjects 719, 65–73 (1982).
69. R. Bormett, S. Asher, P. Larkin, W. G. Gustafson, N. Ragunathan, T. Freedman, L. Nafie, S. Balasubramanian, S. Boxer, N. Yu, K. Gersonde, R. Noble, B. Springer, and S. Sligar, “Selective examination of heme protein azide ligand-distal globin interactions by vibrational circular dichroism,” Journal of the American Chemical Society 114(17), 6864–6867 (1992).
70. E. Nagababu, J. Mohanty, S. Bhamidipaty, G. Ostera, and J. Rifkind, “Role of the membrane in the formation of heme degradation products in red blood cells,” Life Sciences 86(3–4), 133–138 (2010).
71. L. Huang, T. G. S. Denis, Y. Xuan, Y. Huang, M. Tanaka, A. Zadlo, T. Sarna, and M. Hamblin, “Paradoxical potentiation of methylene blue-mediated antimicrobial photodynamic inactivation by sodium azide: Role of ambient oxygen and azide radicals,” Free Radical Biology and Medicine 53(11), 2062–2071 (2012).
72. M. Hamblin, H. Abrahamse, “Inorganic salts and antimicrobial photodynamic therapy: mechanistic conundrums?” Molecules 23(12), 3190 (2018).
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