Abstract
The number of cells attached to glass substrates increases if HeLa cell suspensions are irradiated with monochromatic visible-to-near infrared radiation (600–860 nm, 52 J m−2) prior to plating. The well-structured relationship between this biological response and the radiation wavelength (action spectrum with maxima at 620, 680, 760, and 820 nm) suggests the existence of a photoacceptor responsible for the enhancement of attachment (presumably cytochrome c oxidase, the terminal enzyme of the respiratory chain) and, secondly, the existence of signaling pathways between the mitochondria, the plasma membrane, and the nucleus of the cell. Treating the cell suspension with ouabain (a Na+, K+-ATPase inhibitor), amiloride (an inhibitor of N+/H+ exchangers), or sodium azide (a cytochrome c oxidase inhibitor) prior to irradiation significantly modifies the action spectrum of cell attachment enhancement. The action of the chemicals under study also depends on their concentration and radiation fluence. Our results point to the existence of at least three signaling pathways (reaction channels) relating together the cell attachment, the respiratory chain, and the Na+, K+-ATPase and N+/H+ exchanger activities.
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F. B. Michaelis, L. Delgrano, Biochemical aspects of the attachment of a pig-kidney monolayer cell line to glass surfaces, Exp. Cell Res., 1971, 65, 43–48.
R. J. Klebe, Cell attachment to collagen: the requirement for energy, J. Cell Physiol., 1975, 86, 231–236.
T. I. Karu, L. V. Pyatibrat, G. S. Kalendo, R. O. Esenaliev, Effects of monochromatic low-intensity light and laser irradiation on adhesion of HeLa cells in vitro, Lasers Surg. Med., 1996, 18, 171–177.
T. Karu, Primary and secondary mechanisms of action of visible-to-near IR radiation on cells, J. Photochem. Photobiol., B, 1999, 49, 1–17.
T. I. Karu, Photobiology of low power laser effects, Health Phys., 1989, 56, 691–704.
J. Tuner and L. Hode, Laser Therapy, Prima Books, Grängesberg, 2002
N. Ad, U. Oron, Impact of low level laser irradiation on infarct size in the rat following myocardial infraction, Int. J. Cardiol., 2001, 80, 109–116.
S. Rochkind, M. Nissan, M. Alon, M. Shamm, K. Salate, Effects of laser irradiation on the spinal cord for the regeneration of crushed peripheral nerve in rats, Lasers Surg. Med., 2001, 28, 216–219.
S. K. Snyder, K. R. Byrnes, R. C. Borke, A. Sanches, J. J. Anders, Quantitation of calcitonin gene-related peptide RNA and neuronal cell death in facial motor nuclei following axotomy and 633 nm low power laser treatment, Lasers Surg. Med., 2002, 31, 216–222.
T. I. Karu, L. V. Pyatibrat, G. S. Kalendo, Cell attachment modulation by radiation from a pulsed semiconductor light diode (λ = 820 nm) and various chemicals, Lasers Surg. Med., 2001, 28, 227–236.
M. T. T. Wong-Ripley, X. Bai, E. Buchmann, H. T. Whelan, Light-emitting diode treatment reverses the effect of TTX on cytochrome c oxidase in neurons, NeuroReport, 2001, 12, 3033–3037.
J. T. Eells, M. M. Henry, P. Summerfell, M. T. T. Wong-Ripley, E. V. Buchmann, M. Kane, N. T. Whelan, H. T. Whelan, Therapeutic photobiomodulation for methanol-induced retinal toxicology, Proc. Natl. Acad. Sci. U. S. A., 2003, 100, 3439–3444.
G. Shefer, T. A. Patridge, L. Heslop, J. G. Gross, U. Oron, O. Halevy, Low energy laser irradiation promotes the survival and cell cycle entry of skeletal muscle satellite cells, J. Cell Sci., 2002, 115, 1461–1469.
R. G. Contreras, L. Shoshani, C. Flores-Maldonado, A. Lazaro, M. Cereijido, Relatonship between Na+/K+-ATPase and cell attachment, J. Cell Sci., 1999, 112, 4223–4232.
Z. Xie, A. Askari, Na+/K+-ATPase as a signal transducer, Eur. J. Biochem., 2002, 269, 2434–2439.
Z. H. Nemeth, E. A. Deitch, Q. Lu, C. Szabo, G. Hasko, NHE blokade inhibits chemokine production and NF-?B activation in immunostimulated endothelial cells, Am. J. Physiol.: Cell Physiol., 2002, 283, C396–C403.
J. Orlowski, S. Grinstein, NHEs of mammalian cells, J. Biol. Chem., 1997, 272, 22-373–22-376.
L. B. Margolis, I. A. Rozovskaya, E. Cragoe, Intracellular pH and cell adhesion to solid substrata, FEBS Lett., 1988, 234, 449–450.
M. A. Shwartz, C. Lechene, Adhesion is required for protein kinase C-dependent activation of the Na+/H+ antiporter by platelet-derived growth factor, Proc. Natl. Acad. Sci. U. S. A., 1992, 89, 6138–6141.
S. I. Galkina, G. F. Sudina, L. B. Margolis, Regulation of intracellular pH by phospholipase A2 and protein kinase C upon neutrophil adhesion to solid substrata, FEBS Lett., 1996, 393, 117–120.
M. Haas, A. Askari, Z. Xie, Involvement of Ser and epidermal growth factor receptor in the signal transducing function of Na+/K+-ATP-ase, J. Biol. Chem., 2000, 275, 27-832–27-837.
J. S. Chun, B. S. Jacobson, Requirement for diacylglycerol and protein kinase c in HeLa cell-substratum adhesion and their feedback amplification of arachidonic acid production for optimum cell spreading, Mol. Biol. Cell, 1993, 4, 271–281.
J. R. Crawford, B. S. Jacobson, Extracellular calcium regulates HeLa cell morphology during adhesion to gelatin: role of translocation and phosphorylation of cytosolic phospholipase A2, Mol. Biol. Cell, 1998, 9, 3429–3443.
T. I. Karu, L. V. Pyatibrat, G. S. Kalendo, Biostimulation of HeLa cells by low-intensity visible light. V. Stimulation of cell proliferation in vitro by He-Ne laser radiation, Nuovo Cimento Soc. Ital. Phys., D, 1987, 9, 1485–1494.
K. M. Hartmann, Action spectroscopy, in Biophysics, ed. W. Hoppe, W. Lohmann, H. Marke and H. Ziegler, Springer-Verlag, Heidelberg, 1983. pp. 115–151.
L. Weiss, Studies on cellular adhesion in tissue culture. XI. Some effects of ouabain, Exp. Cell Res., 1972, 71, 281–288.
R. Belusa, Z-M. Wang, T. Matsubara, B. Sahlgren, I. Dulubova, A. C. Nairn, E. Ruosalahti, P. Greengard, A. Aperia, Mutation of the protein kinase C phosphorylation site on rat a1 Na+,K+-ATPase alters regulation of intracellular Na+ and pH and influences cell shape and adhesivness, J. Biol. Chem., 1997, 272, 20-179–20-184.
R. Belusa, O. Aizman, R. M. Andersson, A. Aperia, Changes in Na+,K+-ATPase activity influence cell attachment to fibronectin, Am. J. Physiol.: Cell Physiol., 2000, 282, C302–C309.
C. Levinson, H. G. Hempling, The role of ion transport in the regulation of respiration in the Ehrlich mouse ascites-tumor cell, Biochem. Biophys. Acta, 1967, 135, 306–318.
M. Kajikawa, S. Fujimoto, Y. Tsuura, E. Mhukai, T. Takeda, Y. Hamamoto, M. Takehiro, J. Fujita, Y. Yamada, Y. Seino, Ouabain suppresses glucose-induced mitochondrial ATP production and insulin release by generating reactive oxygen species in pancreatic islets, Diabetes, 2002, 51, 2522–2529.
M. Humphries, P. Newham, The structure of cell-adhesion molecules, Trends Cell Biol., 1998, 8, 78–84.
G. Orend, R. Chiquet-Ehrismann, Adhesion modulation by antiadhesive molecules of the extracellular matrix, Exp. Cell Res., 2000, 261, 104–110.
A. Sucheta, K. E. Georgiadis, O. Einarsdottir, Mechanism of cytochrome c oxidase- catalyzed reduction of dioxygen to water: evidence for peroxy and ferryl intermediates at room temperature, Biochemistry, 1997, 36, 554–556.
T. I. Karu, N. I. Afanasyeva, S. F. Kolyakov, L. V. Pyatibrat, L. Welser, Changes in absorbance of monolayer of living cells induced by laser radiation at 633, 670, and 820 nm, IEEE J. Sel. Top. Quantum Electron., 2001, 7, 982–988.
T. I. Karu, S. F. Kolyakov, L. V. Pyatibrat, E. L. Mikhailov, O. N. Kompanets, Irradiation with a diode 820 nm induces changes in circular dichroism spectra (250–780 nm) of living cells, IEEE J. Sel. Top. Quantum Electron., 2001, 7, 976–981.
T. I. Karu, L. V. Pyatibrat, T. P. Ryabykh, Melatonin modulates the action of near infrared radiation on cell adhesion, J. Pineal Res., 2003, 34, 167–172.
G. Palmer, Current issues in the chemistry of cytochrome c oxidase, J. Bioenerg. Biomembr., 1993, 25, 145–151.
J. N. Koshmieder, S. P. Falsig, J. Damgaard, A. Schousboe, E. K. Hoffmann, Increases in [Ca2+]i and changes in intracellular pH during chemical anoxia in mouse neocortical neurons in primary culture, J. Neurosci. Res., 1999, 56, 358–370.
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Karu, T.I., Pyatibrat, L.V. & Kalendo, G.S. Photobiological modulation of cell attachment via cytochrome c oxidase. Photochem Photobiol Sci 3, 211–216 (2004). https://doi.org/10.1039/b306126d
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DOI: https://doi.org/10.1039/b306126d