Mitochondrial signaling in mammalian cells activated by red and near-IR radiation

Photochemistry and Photobiology

Volumn 84, Issue 5, 2008, Pages 1091-1099

  Karu, Tiina I ^a  

^a INSTITUTE ON LASER AND INFORMATION TECHNOLOGIES   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE;

ANIMAL; CELL NUCLEUS; HUMAN; INFRARED RADIATION; MAMMAL; METABOLISM; MITOCHONDRION; RADIATION EXPOSURE; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL NUCLEUS; ELECTRON TRANSPORT COMPLEX IV; HUMANS; INFRARED RAYS; MAMMALS; MITOCHONDRIA; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 50849098175     PISSN: 00318655     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1751-1097.2008.00394.x     Document Type: Review

References (92)

1. Butow, R. A. N. G. Avadhani (2004) Mitochondrial signaling: The retrograde response. Mol. Cell 14, 1 15.
2. Ryan, M. T. N. J. Hoogenraad (2007) Mitochondrial-nuclear communications. Annu. Rev. Biochem. 76, 701 722.
3. Liu, Z. R. A. Butow (2007) Mitochondrial retrograde signaling. Annu. Rev. Genet. 40, 159 185.
4. Rhoads, D. M. C. C. Subbaiah (2007) Mitochondrial retrograde regulation in plants. Mitochondrion 7, 177 194.
5. 2+ signaling in C2C12 skeletal myocytes in response to mitochondrial genetic and metabolic stress: A novel mode of inter-organelle crosstalk. EMBO J. 18, 522 533.
6. Erol, A. (2005) Retrograde regulation due to mitochondrial dysfunction may be an important mechanism for carcinogenesis. Med. Hypoth. 65, 525 529.
7. Karu, T. I. (1988) Molecular mechanism of the therapeutic effect of low-intensity laser radiation. Lasers Life Sci. 2, 53 74.
8. Karu, T. I. (1989) Photobiology of low-power laser effects. Health Phys. 56, 691 704.
9. Karu, T. I. (1987) Photobiological fundamentals of low-power laser therapy. IEEE J. Quantum Electron. QE-23, 1703 1717.
10. Tuner, J. L. Hode (2002) Laser Therapy. Prima Books AB, Grängesberg, Sweden.
11. Karu, T. (1999) Primary and secondary mechanisms of action of visible-to-near IR radiation on cells. J. Photochem. Photobiol. B Biol. 49, 1 17.
12. Karu, T. I., L. V. Pyatibrat, S. F. Kolyakov N. I. Afanasyeva (2005) Absorption measurements of a cell monolayer relevant to phototherapy: Reduction of cytochrome c oxidase under near IR radiation. J. Photochem. Photobiol. B Biol. 81, 98 106.
13. Wong-Riley, M. T., H. L. Liang, J. T. Eells, B. Chance, M. M. Henry, T. Buchmann, M. Kane H. T. Whelan (2005) Photomodulation directly benefits primary neutrons functionally inactivated by toxins: Role of cytochrome c oxidase. J. Biol. Chem. 280, 4761 4771.
14. Pastore, D., M. Greco S. Passarella (2000) Specific He-Ne laser sensitivity of the purified cytochrome c oxidase. Int. J. Radiat. Biol. 76, 863 870.
15. Karu, T. I., L. V. Pyatibrat N. I. Afanasyeva (2004) A novel mitochondrial signaling pathway activated by visible-to-near infrared radiation. Photochem. Photobiol. 80, 366 372.
16. Schroeder, P., C. Pohl, C. Calles, C. Marks, S. Wild J. Krutmann (2007) Cellular response to infrared radiation involves retrograde mitochondrial signaling. Free Radic. Biol. Med. 43, 128 135.
17. Karu, T. (1990) Effects of visible radiation on cultured cells. Photochem. Photobiol. 52, 1089 1099.
18. Karu, T. (2007) Ten Lectures on Basic Science of Laser Phototherapy. Prima Books AB, Grängesberg, Sweden.
19. Karu, T. I. S. F. Kolyakov (2005) Exact action spectra for cellular responses relevant to phototherapy. Photomed. Laser Surg. 23, 355 361.
20. Karu, T. I., L. V. Pyatibrat, S. F. Kolyakov N. I. Afanasyeva (2008) Absorption measurements of cell monolayers relevant to laser phototherapy: Reduction or oxidation of cytochrome c oxidase under laser radiation at 632.8 nm. Photomed. Laser Surg. 26 (in press).
21. Karu, T. I., L. V. Pyatibrat G. S. Kalendo (2001) Cell attachment modulation by radiation from a pulsed semiconductor light diode (λ = 820 nm) and various chemicals. Lasers Surg. Med. 28, 227 236.
22. Karu, T. I., L. V. Pyatibrat G. S. Kalendo (2001) Thiol reactive agents eliminate stimulation of cell attachment to extracellular matrices induced by irradiation at λ = 820 nm: Possible involvement of cellular redox status into low power laser effects. Laser Ther. 11, 177 187.
23. Karu, T. I., L. V. Pyatibrat N. I. Afanasyeva (2005) Cellular effects of low power laser therapy can be mediated by nitric oxide. Lasers Surg. Med. 36, 307 314.
24. Karu, T. I., L. V. Pyatibrat G. S. Kalendo (2001) Cell attachment to extracellular matrices is modulated by pulsed radiation at 820 nm and chemicals that modify the activity of enzymes in the plasma membrane. Lasers Surg. Med. 29, 274 281.
25. Karu, T. I., L. V. Pyatibrat T. P. Ryabykh (2003) Melatonin modulates the action of near infrared radiation on cell adhesion. J. Pineal Res. 34, 167 172.
26. Karu, T. I., L. V. Pyatibrat G. S. Kalendo (2004) Photobiological modulation of cell attachment via cytochrome c oxidase. Photochem. Photobiol. Sci. 3, 211 216.
27. Karu, T. I., L. V. Pyatibrat G. S. Kalendo (2001) Donors of NO and pulsed radiation at λ = 820 nm exert effects on cells attachment to extracellular matrices. Toxicol. Lett. 121, 57 61.
28. Zhang, Y., S. Song, C.-C. Fong, C.-H. Tsang, Z. Yang M. Yang (2003) cDNA microarray analysis of gene expression proteins in human fibroblast cells irradiation with red light. J. Invest. Dermatol. 120, 849 857.
29. Kato, M., K. Sinizawa S. Yoshikawa (1981) Cytochrome c oxidase is a possible photoacceptor in mitochondria. Photochem. Photobiophys. 2, 263 269.
30. Karu, T. (1998) Introduction. In The Science of Low-Power Laser Therapy. pp. XIII XVIII, Gordon and Breach Science Publishers, Amsterdam.
31. Kondrashova, M. N. (1970) Control of mitochondria respiration at increasing influences on the cell. Biophysics (Moscow) 15, 312 323.
32. Selye, H. (1950) Stress and the general adaptation syndrome. Br. Med. J. 1, 1382 1392.
33. Gordon, S. A. K. Surrey (1960) Red and far-red light action on oxidative phosphorylation. Radiat. Res. 12, 325 339.
34. Passarella, S., E. Casamassima, S. Molinari, D. Pastore, E. Quagliariello, I. M. Catalano A. Cingolani (1984) Increase of proton electrochemical potential and ATP synthesis in rat liver mitochondria irradiated in vitro by helium-neon laser. FEBS Lett. 175, 95 99.
35. Vekshin, N. L. (1991) Light-dependent ATP synthesis in mitochondria. Biochem. Int. 25, 603 611.
36. Vekshin, N. L. G. P. Mironov (1982) Flavin-dependent oxygen uptake in mitochondria under illumination. Biophysics (Moscow) 27, 537 539.
37. Passarella, S., E. Perlino, E. Quagliariello, L. Baldassarre, I. M. Catalano A. Cingolani (1983) Evidence of changes induced by He-Ne laser irradiation in the biochemical properties of rat liver mitochondria. Bioelectrochem. Bioenerg. 10, 185 198.
38. Hu, W.-P., J. J. Wang, C.-L. Yu, C.-C. E. Lan, G. S. Chen H.-S. Yu (2007) He-Ne laser irradiation stimulates cell proliferation through photostimulatory effects in mitochondria. J. Invest. Dermatol. 127, 2048 2057.
39. Passarella, S., A. Ostuni, A. Atlante E. Quagliariello (1988) Increase in the ADP/;ATP exchange in rat liver mitochondria irradiated in vitro by He-Ne laser. Biochem. Biophys. Res. Commun. 156, 978 986.
40. Greco, M., G. Guida, E. Perlino, E. Marra E. Quagliariello (1989) Increase in RNA and protein synthesis by mitochondria irradiated with He-Ne laser. Biochem. Biophys. Res. Commun. 163, 1428 1434.
41. Vacca, R. A., E. Marra, E. Quagliariello M. Greco (1993) Activation of mitochondrial DNA replication by He-Ne laser irradiation. Biochem. Biophys. Res. Commun. 195, 704 709.
42. Vacca, R. A., E. Marra, E. Quagliariello M. Greco (1993) Increase of both transcription and translation activities following separate irradiation of the in vitro system components with He-Ne laser. Biochem. Biophys. Res. Commun. 203, 991 997.
43. Vacca, R. A., E. Marra, S. Passarella, V. A. Petragallo M. Greco (1996) Increase in cytosolic and mitochondrial protein synthesis in rat hepatocytes irradiated in vitro by He-Ne laser. J. Photochem. Photobiol. B Biol. 34, 197 202.
44. - ratio of the cytochrome c oxidase reaction in mitochondria irradiated with He-Ne laser. Biochem. Mol. Biol. Int. 34, 817 826.
45. Morimoto, Y., T. Arai, M. Kikuchi, S. Nakajama H. Nakamura (1994) Effect of low-intensity argon laser irradiation on mitochondrial respiration. Lasers Surg. Med. 15, 191 199.
46. Yu, W., J. O. Naim, H. McGowan, K. Ippolito R. J. Lanzafame (1997) Photomodulation of oxidative metabolism and electron chain enzymes in rat liver mitochondria. Photochem. Photobiol. 66, 866 871.
47. Alexandratou, E., D. Yova, P. Handris, D. Kletsas S. Loukas (2002) Human fibroblast alterations induced by low power laser irradiation at the single cell level using confocal microscopy. Photochem. Photobiol. Sci. 1, 547 552.
48. Gavish, L., Y. Asher, Y. Becker Y. Kleinman (2004) Low level laser irradiation stimulates mitochondrial membrane potential and disperses subnuclear promyelocytic leukemia protein. Lasers Surg. Med. 35, 369 376.
49. Zhang, D. X. D. D. Gutterman (2006) Mitochondrial reactive oxygen species-mediated signaling in endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 292, H2023 H2031.
50. 2+ signaling. Am. J. Physiol. Cell Physiol. 291, C1082 C1088.
51. Schicke, S. M. T. Finkel (2006) Mitochondrial signaling, TOR, and life span. Biol. Chem. 387, 1357 1361.
52. Kudin, A. P., G. Debska-Vilhaber W. S. Kunz (2005) Characterization of superoxide production sites in isolated rat brain and skeletal muscle mitochondria. Biomed. Pharmacother. 59, 163 168.
53. Brookes, P. S., Y. Yoon, J. L. Robotham, M. W. Anders S.-S. Sheu (2004) Calcium, ATP, and ROS: A mitochondrial love-hate triangle. Am. J. Physiol. Cell Physiol. 287, C817 C833.
54. Karu, T. I., L. V. Pyatibrat, G. S. Kalendo R. O. Esenaliev (1996) Effects of monochromatic low-intensity light and laser irradiation on adhesion of HeLa cells in vitro. Lasers Surg. Med. 18, 171 177.
55. Tan, D. X., L. C. Manchester, R. J. Reiter, W. B. Qi, H. Karbownik J. R. Calvo (2000) Significance of melatonin in antioxidative defence system: Reactions and products. Biol. Signals Recept. 9, 137 159.
56. Martin, M., M. Macias, G. Escames, J. Leon D. Acuna-Castroviejo (2000) Melatonin but not vitamins C and E maintains glutathione homeostasic in t-butyl hydroperoxide-induced mitochondrial oxidative stress. FASEB J. 14, 1677 1679.
57. Acuna-Castroviejo, D., M. Martin, M. Macias, G. Excames, J. Leon, H. Khaldy J. Reiter (2001) Melatonin, mitochondria, and cellular bioenergetics. J. Pineal Res. 30, 65 74.
58. Beinert, H., R. W. Shaw, R. E. Hansen C. R. Hartzell (1980) Studies on the origin of the near-infrared (800-900) absorption of cytochrome c oxidase. Biochim. Biophys. Acta 591, 458 470.
59. Karu, T., A. Kurchikov, V. Letokhov V. Mokh (1996) He-Ne laser radiation influences single-channel ionic currents through cell membranes: A patch-clamp study. Lasers Life Sci. 7, 35 48.
60. Karu, T. I., G. S. Kalendo, V. S. Letokhov V. V. Lobko (1982) Biostimulation of HeLa cells by low intensity visible light. Nuovo Cimento D 1, 828 840.
61. Vacca, R. A., L. Moro, V. A. Petragallo, M. Greco, F. Fontana S. Passarella (1997) The irradiation of hepatocytes with He-Ne laser causes an increase of cytosolic free calcium concentration and an increase of cell membrane potential, correlated with it, both increases taking place in an oscillatory manner. Biochem. Mol. Biol. Int. 43, 1005 1014.
62. Cortassa, S., M. A. Aon, R. L. Winslow B. O'Rourke (2004) A mitochondrial oscillator dependent on reactive oxygen species. Biophys. J. 87, 2060 2073.
63. Aon, M. A., S. Cortassa, E. Marban B. O'Rourke (2003) Synchronized whole cell oscillations in mitochondria metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J. Biol. Chem. 278, 44735 44744.
64. Smolyaninova, N. K., T. I. Karu, G. E. Fedoseyeva A. V. Zelenin (1991) Effect of He-Ne laser irradiation on chromatin properties and synthesis of nucleic acids synthesis of human blood lymphocytes. Biomed. Sci. 2, 121 126.
65. Lubart, R., H. Friedmann, T. Levinshal, R. Lavie H. Breitbart (1992) Effect of light on calcium transport in bull sperm cells. J. Photochem. Photobiol. B Biol. 15, 337 341.
66. Cohen, N., R. Lubart, S. Rubinstein H. Breitbart (1998) Light irradiation of mouse spermatozoa: Stimulation of in vitro fertilization and calcium signals. Photochem. Photobiol. 68, 407 413.
67. Breitbart, H., T. Levinshal, N. Cohen, H. Friedmann R. Lubart (1996) Changes in calcium transport in mammalian sperm mitochondria and plasma membrane irradiated at 633 nm (He-Ne laser). J. Photochem. Photobiol. B Biol. 34, 117 121.
68. Lubart, R., H. Friedmann, H. Sinyakov, N. Cohen H. Breitbart (1997) Changes in calcium transport in mammalian sperm mitochondria and plasma membranes caused by 780 nm irradiation. Lasers Surg. Med. 21, 493 499.
69. Schwartz, F., C. Brodie, E. Appel, G. Kazimirsky A. Schainberg (2002) Effect of helium/;neon laser irradiation on nerve growth factor synthesis and secretion in skeletal muscle cultures. J. Photochem. Photobiol. B Biol. 66, 195 200.
70. Yang, W.-Z., J.-Y. Chen, J. T. Yu L.-W. Zhou (2007) Effects of low power laser irradiation on intracellular calcium and histamine release in RBL-2H3 mast cells. Photochem. Photobiol. 83, 979 984.
71. Cooper, C. E. (2002) Nitric oxide and cytochrome oxidase: Substrate, inhibitor or effector? Trends Biochem. Sci. 27, 33 39.
72. • signaling pathway, and the transduction of nitrosative to oxidative cell signaling: An alternative function for cytochrome c oxidase. Free Radic. Biol. Med. 32, 370 374.
73. Giulivi, C., J. J. Pedroso A. Boveris (1998) Production of nitric oxide by mitochondria. J. Biol. Chem. 273, 11038 11043.
74. Brookes, P. S., A.-L. Levonen, S. Shiva, P. S. Sarti V. M. Darley-Usmar (2002) Mitochondria: Regulators of signal transduction by reactive oxygen and nitrogen species. Free Radic. Biol. Med. 33, 755 764.
75. Nicoli, E. M. O. Carruba (2006) Nitric oxide and mitochondrial biogenesis. J. Cell Sci. 119, 2855 2862.
76. Passarella, S., L. Roncali, R. Cicero E. Quagliariello (1988) New ultrastructural conformations of mitochondria irradiated in vitro with a He-Ne laser. Lasers Life Sci. 2, 161 171.
77. Greco, M., E. Perlino, D. Pastore, G. Grida, E. Marra E. Quagliariello (1991) He-Ne laser irradiation of rat level mitochondria gives rise to a new subpopulation of mitochondria: Isolation and first biochemical characterization. J. Photochem. Photobiol. B Biol. 10, 71 78.
78. Manteifel, V. M., L. E. Bakeeva T. I. Karu (1999) He-Ne laser radiation causes changes in mitochondrial ultrastructure in successive generations of yeast cells. Doklady Biophysics (Moscow) 364-366, 58 60.
79. Manteifel, V. M. T. I. Karu (2005) Structure of mitochondria and activity of their respiratory chain in successive generations of yeast cells exposed to He-Ne laser light. Biol. Bull. 32, 556 566.
80. Jazwinski, S. M. (2005) The retrograde response links metabolism with stress responses, chromatin-dependent gene activation, and genome stability in yeast aging. Gene 354, 22 27.
81. Tiphlova, O. T. Karu (1991) Action of low-intensity laser radiation on Escherichia coli. Crit. Rev. Biomed. Eng. 18, 387 412.
82. Quickenden, T. I., L. L. Daniels L. J. Burne (1995) Does low intensity He-Ne laser radiation affect the intracellular pH of intact Escherichia coli cells? SPIE Proc. 2391, 535 544.
83. Trimm, J. L., G. Salama Y. J. Abramson (1986) Sulphydryl oxidation induces rapid calcium release from sarcoplasmic reticulum vesicles. J. Biol. Chem. 261, 16092 16098.
84. Wang, T., X. Zhang J. J. Li (2002) The role of NF-kB in the regulation of cell stress responses. Int. Immunopharmacol. 2, 1509 1520.
85. Liu, X., B. Zhou, S. Mi, L. Xue, J. Shih, J. Lee, J. Chau, F. Un Y. Yen (2007) An increase of cytochrome c oxidase mediated disruption of gemcitabine incorporation into DNA in a resistant κB clone. Biochem. Pharmacol. 73, 1927 1938.
86. Pueyo, M. E., W. Gonzales, A. Nicoletti, F. Savoie, J.-F. Arnal J.-B. Michel (2000) Angiotensin II stimulates endothelial vascular cell adhesion molecule-1 via nuclear factor-κB activation induced by intracellular oxidative stress. Arterioscler. Thromb. Vasc. Biol. 20, 645 651.
87. Aihara, N., M. Yamaguchi K. Kasai (2006) Low-energy irradiation stimulates formation of osteoplast-like cells via RANK expression in vitro. Laser Med. Sci. 21, 24 33.
88. Rizzi, C. F., J. L. Mauriz, D. S. F. Corréa, A. J. Moreira, C. G. Zettler, L. I. Filippin, N. P. Marroni J. González-Gallego (2006) Effects of low-level laser therapy (LLLT) on the nuclear factor (NF)-κB signaling pathway in traumatized muscle. Lasers Surg. Med. 38, 704 713.
89. Karu, T. I., O. A. Tiphlova, G. G. Lukpanova I. M. Parkhomenko (1987) Effect of irradiation with monochromatic visible light on cAMP content in Chinese hamster fibroblasts. Nuovo Cimento D 9, 1245 1252.
90. Eells, J. T., M. M. Henry, P. Summerfelt, M. T. Wong-Riley, E. V. Buchmann, M. Kane, N. T. Whelan H. T. Whelan (2003) Therapeutic photobiomodulation for methanol-induced retinal toxicity. Proc. Natl Acad. Sci. USA 100, 3439 3444.
91. Eells, J., M. T. Wong-Riley, J. VerHoeve, M. Henry, E. V. Buchman, M. P. Kane, L. J. Gould, R. Das, M. Jett, B. D. Hodgson, D. Margolis H. T. Whelan (2004) Mitochondrial signal introduction in accelerated wound and retinal healing by near-infrared light therapy. Mitochondrion 4, 559 567.
92. Liang, H. L., H. T. Whelan, J. T. Eells, H. Meng, E. Buchmann, A. Lerch-Gaggl M. T. Wong-Riley (2006) Photobiomodulation partially rescues visual cortical neurons from cyanide-induced apoptosis. Neuroscience 139, 639 649.