Influence of low-level laser radiation on the physico-chemical indicators of biomembranes
Abstract
Background: The study of physical and molecular mechanisms of the influence of low-level laser radiation (LLLR) of a wide frequency range on biological objects allows to clarify the problem of laser photomodulation at the level of natural biological membranes and their model analogues.
Objectives: Identification of molecular and physical mechanisms of the influence of LLLR of a wide frequency range on biological objects of various levels of complexity.
Materials and methods: Research objects: unicellular organisms S. cerevisiae, concentration of cells in the sample 18×106; model lipid membranes from a mixture of phosphatidylcholine and cardiolipin with different content of components (10%, 20% and 40% cardiolipin), which simulates the surface electrical properties of lipid models. A spectrophotometric study of charge redistribution on the cell surface was carried out using bromothymol blue dye. Complex formation of cytochrome c with model membranes was studied spectrophotometrically at the wavelength of the Soret band (405–410 nm). The influence of low-intensity laser radiation with wavelength and power density, respectively: 337 nm, 2.8 mW/cm2; 532 nm, 9.5 mW/cm2; 70.5 μm, 10.0 mW/cm2 on the yeast cell surface; 632.8 nm, 5.1 mW/cm2 on liposomes with different protein-lipid composition.
Results: LLLR of a wide frequency range causes a change in the surface electrical properties of S. cerevisiae cells, namely, a redistribution of the surface charges of the cell membrane, as a result of which a change in the surface membrane potential is recorded. Irradiation of samples of model lipid membranes with a helium-neon laser leads to a change in the surface characteristics of liposomes, which affects the kinetic parameters of the formation of protein-lipid complexes with the participation of cytochrome c.
Conclusions: The target of laser photomodulation processes is the surface of the biological membrane of both natural cells, for example yeast cells, and model lipid membranes made of a mixture of phospholipids with different content of components. The creation of lipid models based on the protein and lipid composition of natural membranes makes it possible to predict the reaction of cell membranes to the action of LLLR in the model, and to understand the molecular mechanisms of laser photomodulation processes.
Downloads
References
Santos FP, Carvalhos CA and Figueiredo-Dias M. Review New insights into photobiomodulation of the vaginal microbiome-A. Critical Review Int. J. Mol. Sci. 2023;24:13507. https://doi.org/10.3390/ijms241713507
Grangeteau C, Lepinois F, Winckler P, Perrier-Cornet JM, Dupont S, Beney L. Cell death mechanisms induced by photo-oxidation studied at the cell scale in the yeast Saccharomyces cerevisiae. Front Microbiol. 2018;5(9):2640 https://doi.org/10.3389/fmicb.2018.02640
Lubart R, Lavi R, Friedmann H, Rochkind S, Photochemistry and Photobiology of Light Absorption by Living Cells Photomedicine and Laser Surgery. 2006;24(2):179–85 https://doi.org/10.1089/pho.2006.24.179
Zhu R, Avsievich T, Su X, Bykov A, Popov A, Meglinski I. Hemorheological alterations of red blood cells induced by 450-nm and 520-nm laser radiation. J Photochem Photobiol B. 2022;230:112438. https://doi.org/10.1016/j.jphotobiol.2022.112438
Elblbesy MA. Comparative In Vitro Study: Examining 635 nm laser and 265 nm ultraviolet interaction with blood. Photobiomodul Photomed Laser Surg. 2019;37(6):342–8. https://doi.org/10.1089/photob.2018.4611
Cui Y, Guo Z, Zhao Y, Zheng Y, Qiao Y, Cai J et al. Reactive effect of low intensity He-Ne laser upon damaged ultrastructure of human erythrocyte membrane in Fenton system by atomic force microscopy. Acta Biochimica et Biophysica Sin. (Shanghai) 2007;39(7):484–9 https://doi.org/10.1111/j.1745-7270.2007.00309.x
Hamblin MR. Mechanisms and mitochondrial redox signaling in photobiomodulation. Photochemistry and Photobiology. 2018;94(2):199–212. https://doi.org/10.1111/php.12864
Baldassarro VA, Alastra G, Lorenzini L, Giardino L, Calzà L. Photobiomodulation at defined wavelengths regulates mitochondrial membrane potential and redox balance in skin fibroblasts. Oxid Med Cell Longev 2023;24:7638223 https://doi.org/10.1155/2023/7638223
Bensadoun RJ, Epstein JB, Nair RG, Barasch A, Raber-Durlacher JE, Migliorati C et al. Safety and efficacy of photobiomodulation therapy in oncology: A systematic review. Cancer Med. 2020;9(22):8279–300. https://doi.org/10.1002/cam4.3582
Berni M, Brancato AM, Torriani C, Bina V, Annunziata S, Cornella E et al. The Role of Low-Level Laser Therapy in Bone Healing: Systematic Review. Int J Mol Sci. 2023;24(8):7094. https://doi.org/10.3390/ijms24087094
Nejatifard M, Asefi S, Jamali R, Hamblin MR, Fekrazad R. Probable positive effects of the photobiomodulation as an adjunctive treatment in COVID-19: A systematic review. Cytokine. 2021; 137:155312. https://doi.org/10.1016/j.cyto.2020.155312
da Silva TG, Ribeiro RS, Mencalha AL, de Souza Fonseca A. Photobiomodulation at molecular, cellular, and systemic levels. Lasers Med. Sci. 2023;38(136):77. https://doi.org/10.1007/s10103-023-03801-6
Maki Y, Kushibiki T, Sano T, Ogawa T, Komai E, Takahashi S et al. 1270 nm near-infrared light as a novel vaccine adjuvant acts on mitochondrial photoreception in intradermal vaccines. Front. Immunol. 2022;13:1028733. https://doi.org/10.3389/fimmu.2022.1028733
Yokomizo S, Katagiri W, Maki Y, Sano T, Inoue K, Fukushi M, et al. Brief exposure of skin to near-infrared laser augments early vaccine responses. Nanophotonics. 2021;10:3187–97. https://doi.org/10.1515/nanoph-2021-0133
Cronshaw M, Parker S, Grootveld M, Lynch E. Photothermal effects of high-energy photobiomodulation therapies: an in vitro investigation Biomedicines 2023;11(6):1634. https://doi.org/10.3390/biomedicines11061634
Itoh S, Okada H, Kuboi T, Kusaka T. Phototherapy for neonatal hyperbilirubinemia. 2017;59:959–66. https://doi.org/10.1111/ped.13332
Liebert AD, Bicknell BT, Adams RD. Protein conformational modulation by photons: A mechanism for laser treatment effects Medical Hypotheses 82.2014;275–81 https://doi.org/10.1016/j.mehy.2013.12.009
Freitas De Freitas L, Hamblin MR. Proposed mechanisms of photobiomodulation or low-level light therapy. IEEE Journal of Selected Topics in Quantum Electronics. 2016;22(3):348–64. https://doi.org/10.1109/JSTQE.2016.2561201
Huanmei Suna, Jiajun Liua, Yifei Lib, Jing Wanga, Yajun Zhanga Characterization of the heterogeneous adsorption of three drugs on immobilized bovine serum albumin by adsorption energy distribution. Journal of Chromatography B. 2019;1125(1):121727. https://doi.org/10.1016/j.jchromb.2019.121727
Kremer JMH, Esker MWJ, Pathmamanoharan C, Wiersema PH. Vesicles of variable diameter prepared by a modified injection method. Biochemistry. 1977;16(17):3932–5 https://doi.org/10.1021/bi00636a033
Stano P, Bufali S, Pisano C, Bucci F, Barbarino M, Santaniello M, Carminati P, Luisi PL. Novel camptothecin analogue (gimatecan)-containing liposomes prepared by the ethanol injection method. J. Liposome Res, 2004;14(1–2):87–109 https://doi.org/10.1081/LPR-120039794
Matsuzaki K, Murase O, Sugishita K, Yoneyama S, Akada K, Ueha M, Nakamura A, Kobayashi S. Optical characterization of liposomes by right angle light scattering and turbidity measurement Biochimica et Biophysica Acta 1467 (2000) 219–26 https://doi.org/10.1016/S0005-2736(00)00223-6
Gorbenko GP. Kinetics of conformational changes of methemoglobin complexed with liposomes. The Ukrainian Biochemical Journal. 1998;70(3):68–72. (In Ukrainan)
Szeremeta M, Petelska AD, Kotyn´ska J, Pepin´ski W, Naumowicz M, Figaszewski ZA, et al. Changes in surface charge density of blood cells in fatal accidental hypothermia. J Membrane Biol. 2015;248:1175–80. https://doi.org/10.1007%2Fs00232-015-9838-1
Aharon D, Weitman H, Ehrenberg B. The effect of liposomes’ surface electric potential on the uptake of hematoporphyrin Biochimica et Biophysica Acta. 2011;1808:2031–5 https://doi.org/10.1016/j.bbamem.2011.03.015
Dreval VI, Finashin AV, Barannik EA. Study of bromthymol blue binding with plasma membranes. The Ukrainian Biochemical Journal, 1989;61(2):94–8. (In Ukrainan)
Luvisetto S, Cola С, Conover ТЕ, Azzone GF. Tracking of proton flow during transition from anaerobiosis to steady state in rat liver mitochondria. Biochimica et Biophysica Acta. 1990;1018:77–90 https://doi.org/10.1016/0005-2728(90)90113-I
Eddy АА, Barnett JA. A history of research on yeasts 11. The study of solute transport: the first 90 years, simple and facilitated diffusion. Yeast. 2007;24(12):1023–59 https://doi.org/10.1002/yea.1572
De Nobel JG, Barnett JA. Passage of molecules through yeast cell walls: a brief essay-review. Yeast. 1991;7(4):313–23 https://doi.org/10.1002/yea.320070402
De Nobel JG, Klis FM, Munnik T, Priem J, Ende H. An assay of relative cell wall porosity in Saccharomyces cerevisiae, Kluyveromyces lactis and Schizosaccharomyces pombe. Yeast. 199;6(6):483–90 https://doi.org/10.1002/yea.320060605
Camponeschi I, Montanari A, Mazzoni C, Bianchi MM. Light Stress in Yeasts: Signaling and Responses in Creatures of the Night. Int. J. Mol. Sci. 2023;24:6929. https://doi.org/10.3390/ijms24086929
Robertson JB, Davis CR, Johnson CH. Visible light alters yeast metabolic rhythms by inhibiting respiration. Proc Natl Acad Sci USA. 2013;110(52):21130–5 https://doi.org/10.1073/pnas.1313369110
Gierke AM, Hessling M. Photoinactivation by UVA radiation and visible light of Candida auris compared to other fungi. Photochem Photobiol Sci. 2024;23(4):681–92 https://doi.org/10.1007/s43630-024-00543-4
Salichos L, Rokas A. The diversity and evolution of circadian clock proteins in fungi. Mycologia. 2010;102(2):269–78 https://doi.org/10.3852/09-073
Bodvard K, Peeters K, Roger F, Romanov N, et al. Light-sensing via hydrogen peroxide and a peroxiredoxin. Nat. Commun. 2017;24(8):14791 https://doi.org/10.1038/ncomms14791
Mi XQ, Chen JY, Cen Y, Liang ZJ, Zhou LW. A comparative study of 632.8 and 532 nm laser irradiation on some rheological factors in human blood in vitro Journal of Photochemistry and Photobiology B: Biology 74 (2004) 7–12 https://doi.org/10.1016/j.jphotobiol.2004.01.003
Al Musawi MS, Jaafar MS, Al-Gailani, Ahmed NM, Suhaimi FM, Suardi N. Effects of low-level laser irradiation on human blood lymphocytes in vitro Lasers Med Sci. 2017;32(2):405–11 https://doi.org/10.1007/s10103-016-2134-1
Vakifahmetoglu-Norberg H, Ouchida AT, Norberg E. The role of mitochondria in metabolism and cell death, Biochem. Biophys. Res. Commun. 2017;482(3):426–31. https://doi.org/10.1016/j.bbrc.2016.11.088
Hüttemann M, Pecina P, Rainbolt M, Sanderson TH, Kagan VE, Samavati L, et al. The multiple functions of cytochrome c and their regulation in life and death decisions of the mammalian cell: from respiration to apoptosis, Mitochondrion. 2011;11:369–81. https://doi.org/10.1016/j.mito.2011.01.010
Ikon N, Ryan RO. Cardiolipin and mitochondrial cristae organization. Biochim Biophys Acta Biomembr. 2017;1859(6):1156–63. https://doi.org/10.1016/j.bbamem.2017.03.013
Gorbenko GP. Resonance energy transfer study of hemoglobin and cytochrome complexes with lipids. Biochim. Biophis. Acta.1998;12(24):13–4. https://doi.org/10.1016/S0005-2728(98)00140-6
Zaidi S, Hassan MI, Islam A, Ahmad F. The role of key residues in structure, function, and stability of cytochrome-c, Cell. Mol. Life Sci.2014;71:229–55. https://doi.org/10.1007/s00018-013-1341-1.
Bertini I, Cavallaro G, Rosato A. Cytochrome c: occurrence and functions. Chem. Rev. 2006;106:90–115. https://doi.org/10.1021/cr050241v.
Schweitzer-Stenner R. Relating the multi-functionality of cytochrome c to membrane binding and structural conversion, Biophys. Rev. 2018;10:1151–85. https://doi.org/10.1007/s12551-018-0409-4.
Fox CA, Ryan RO. Studies of the cardiolipin interactome. Prog Lipid Res. 2022;88:101195. https://doi.org/10.1016/j.plipres.2022.101195
Gasanoff ES, Yaguzhinsky LS, Garab G. Cardiolipin, Non-Bilayer Structures and Mitochondrial Bioenergetics: Relevance to Cardiovascular Disease. Cells. 2021;10(7):1721. https://doi.org/10.3390/cells10071721
Copyright (c) 2024 L. V. Sichevska, T. M. Ovsyannikova, A. O. Kovalenko, I. A. Zabelina, O. M. Levchenko, O. V. Gurin, V. P. Berest
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
