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Erschienen in: Lasers in Medical Science 1/2015

01.01.2015 | Original Article

Are the mitochondrial respiratory complexes blocked by NO the targets for the laser and LED therapy?

verfasst von: Evgeny A. Buravlev, Tatyana V. Zhidkova, Anatoly N. Osipov, Yury A. Vladimirov

Erschienen in: Lasers in Medical Science | Ausgabe 1/2015

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Abstract

Effects of laser (442 and 532 nm) and light-emitting diode (LED) (650 nm) radiation on mitochondrial respiration and mitochondrial electron transport rate (complexes II–III and IV) in the presence of nitric oxide (NO) were investigated. It was found that nitric oxide (300 nM–10 μM) suppresses mitochondrial respiration. Laser irradiation of mitochondria (442 nm, 3 J cm−2) partly restored mitochondrial respiration (approximately by 70 %). Irradiation with green laser (532 nm) or red LED (650 nm) in the same dose had no reliable effect. Evaluation of mitochondrial electron transport rate in complexes II–III and IV and effects of nitric oxide demonstrated almost similar sensitivity of complex II–III and IV to NO, with approximately 50 % inhibition at NO concentration of 3 μM. Subsequent laser or LED irradiation (3 J cm−2) showed partial recovery of electron transport only in complex IV and only under irradiation with blue light (442 nm). Our results support the hypothesis of the crucial role of cytochrome c oxidase (complex IV) in photoreactivation of mitochondrial respiration suppressed by NO.
Literatur
1.
Zurück zum Zitat Yan B (2014) Comments on: “Efficacy of low-level laser therapy in the management of orthodontic pain: a systematic review and meta-analysis”. Lasers Med Sci 29(4):1531PubMedCrossRef Yan B (2014) Comments on: “Efficacy of low-level laser therapy in the management of orthodontic pain: a systematic review and meta-analysis”. Lasers Med Sci 29(4):1531PubMedCrossRef
2.
Zurück zum Zitat Ge MK, He WL, Chen J, Wen C, Yin X, Hu ZA, Liu ZP, Zou SJ (2014) Efficacy of low-level laser therapy for accelerating tooth movement during orthodontic treatment: a systematic review and meta-analysis. Lasers Med Sci. doi:10.1007/s10103-014-1538-z Ge MK, He WL, Chen J, Wen C, Yin X, Hu ZA, Liu ZP, Zou SJ (2014) Efficacy of low-level laser therapy for accelerating tooth movement during orthodontic treatment: a systematic review and meta-analysis. Lasers Med Sci. doi:10.​1007/​s10103-014-1538-z
3.
Zurück zum Zitat Carvalho-Lobato P, Garcia VJ, Kasem K, Ustrell-Torrent JM, Tallon-Walton V, Manzanares-Cespedes MC (2014) Tooth movement in orthodontic treatment with low-level laser therapy: a systematic review of human and animal studies. Photomed Laser Surg 32(5):302–309PubMedCrossRef Carvalho-Lobato P, Garcia VJ, Kasem K, Ustrell-Torrent JM, Tallon-Walton V, Manzanares-Cespedes MC (2014) Tooth movement in orthodontic treatment with low-level laser therapy: a systematic review of human and animal studies. Photomed Laser Surg 32(5):302–309PubMedCrossRef
4.
Zurück zum Zitat Beckmann KH, Meyer-Hamme G, Schroder S (2014) Low level laser therapy for the treatment of diabetic foot ulcers: a critical survey. Evid Based Complement Alternat Med : eCAM 2014:626127PubMedCentralPubMedCrossRef Beckmann KH, Meyer-Hamme G, Schroder S (2014) Low level laser therapy for the treatment of diabetic foot ulcers: a critical survey. Evid Based Complement Alternat Med : eCAM 2014:626127PubMedCentralPubMedCrossRef
5.
Zurück zum Zitat Avci P, Gupta GK, Clark J, Wikonkal N, Hamblin MR (2014) Low-level laser (light) therapy (LLLT) for treatment of hair loss. Lasers Surg Med 46(2):144–151PubMedCrossRef Avci P, Gupta GK, Clark J, Wikonkal N, Hamblin MR (2014) Low-level laser (light) therapy (LLLT) for treatment of hair loss. Lasers Surg Med 46(2):144–151PubMedCrossRef
6.
Zurück zum Zitat Karu T (1999) Primary and secondary mechanisms of action of visible to near-IR radiation on cells. J Photochem Photobiol B 49(1):1–17PubMedCrossRef Karu T (1999) Primary and secondary mechanisms of action of visible to near-IR radiation on cells. J Photochem Photobiol B 49(1):1–17PubMedCrossRef
7.
Zurück zum Zitat Vladimirov YA (1994) Three hypotheses about the mechanism of action of laser radiation on cells and the human body. In: Chikin SY (ed) Efferent medicine. Institute of Biomedical Chemistry RAMS, Moscow, pp 51–66 Vladimirov YA (1994) Three hypotheses about the mechanism of action of laser radiation on cells and the human body. In: Chikin SY (ed) Efferent medicine. Institute of Biomedical Chemistry RAMS, Moscow, pp 51–66
8.
Zurück zum Zitat Vladimirov YA, Osipov AN, Klebanov GI (2004) Photobiological principles of therapeutic applications of laser radiation. Biochem Mosc 69(1):81–90CrossRef Vladimirov YA, Osipov AN, Klebanov GI (2004) Photobiological principles of therapeutic applications of laser radiation. Biochem Mosc 69(1):81–90CrossRef
9.
Zurück zum Zitat Vladimirov Y, Borisenko G, Boriskina N, Kazarinov K, Osipov A (2000) NO-hemoglobin may be a light-sensitive source of nitric oxide both in solution and in red blood cells. J Photochem Photobiol B 59:115–122PubMedCrossRef Vladimirov Y, Borisenko G, Boriskina N, Kazarinov K, Osipov A (2000) NO-hemoglobin may be a light-sensitive source of nitric oxide both in solution and in red blood cells. J Photochem Photobiol B 59:115–122PubMedCrossRef
10.
Zurück zum Zitat Borisenko GG, Osipov AN, Kazarinov KD, Vladimirov YA (1997) Photochemical reactions of nitrosyl hemoglobin during exposure to low-power laser irradiation. Biochemistry (Mosc) 62(6):661–666 Borisenko GG, Osipov AN, Kazarinov KD, Vladimirov YA (1997) Photochemical reactions of nitrosyl hemoglobin during exposure to low-power laser irradiation. Biochemistry (Mosc) 62(6):661–666
11.
Zurück zum Zitat Osipov AN, Borisenko GG, Vladimirov YA (2007) Biological activity of hemoprotein nitrosyl complexes. Biochemistry (Mosc) 72(13):1491–1504CrossRef Osipov AN, Borisenko GG, Vladimirov YA (2007) Biological activity of hemoprotein nitrosyl complexes. Biochemistry (Mosc) 72(13):1491–1504CrossRef
12.
Zurück zum Zitat Vladimirov Iu A, Klebanov GI, Borisenko GG, Osipov AN (2004) Molecular and cellular mechanisms of the low intensity laser radiation effect. Biofizika 49(2):339–350PubMed Vladimirov Iu A, Klebanov GI, Borisenko GG, Osipov AN (2004) Molecular and cellular mechanisms of the low intensity laser radiation effect. Biofizika 49(2):339–350PubMed
13.
Zurück zum Zitat Brown GC, Borutaite V (2007) Nitric oxide and mitochondrial respiration in the heart. Cardiovasc Res 75:283–290PubMedCrossRef Brown GC, Borutaite V (2007) Nitric oxide and mitochondrial respiration in the heart. Cardiovasc Res 75:283–290PubMedCrossRef
14.
Zurück zum Zitat Brown GC (2001) Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome c oxidase. Biochim Biophys Acta 1504(1):46–57PubMedCrossRef Brown GC (2001) Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome c oxidase. Biochim Biophys Acta 1504(1):46–57PubMedCrossRef
15.
Zurück zum Zitat Borutaite V, Budriunaite A, Brown GC (2000) Reversal of nitric oxide-, peroxynitrite- and S-nitrosothiol-induced inhibition of mitochondrial respiration or complex I activity by light and thiols. Biochim Biophys Acta 1459(2–3):405–412PubMedCrossRef Borutaite V, Budriunaite A, Brown GC (2000) Reversal of nitric oxide-, peroxynitrite- and S-nitrosothiol-induced inhibition of mitochondrial respiration or complex I activity by light and thiols. Biochim Biophys Acta 1459(2–3):405–412PubMedCrossRef
16.
Zurück zum Zitat Brown GC (1999) Nitric oxide and mitochondrial respiration. Biochim Biophys Acta 1411:351–369PubMedCrossRef Brown GC (1999) Nitric oxide and mitochondrial respiration. Biochim Biophys Acta 1411:351–369PubMedCrossRef
17.
Zurück zum Zitat Karu TI (2010) Multiple roles of cytochrome c oxidase in mammalian cells under action of red and IR-A radiation. IUBMB Life 62(8):607–610PubMedCrossRef Karu TI (2010) Multiple roles of cytochrome c oxidase in mammalian cells under action of red and IR-A radiation. IUBMB Life 62(8):607–610PubMedCrossRef
18.
Zurück zum Zitat Boelens R, Rademaker H, Pel R, Wever R (1982) EPR studies of the photodissociation reactions of cytochrome c oxidase-nitric oxide complexes. Biochim Biophys Acta 679(1):84–94PubMedCrossRef Boelens R, Rademaker H, Pel R, Wever R (1982) EPR studies of the photodissociation reactions of cytochrome c oxidase-nitric oxide complexes. Biochim Biophys Acta 679(1):84–94PubMedCrossRef
19.
Zurück zum Zitat Storrie B, Madden EA (1990) Isolation of subcellular organelles. Methods Enzymol 182:203–225PubMedCrossRef Storrie B, Madden EA (1990) Isolation of subcellular organelles. Methods Enzymol 182:203–225PubMedCrossRef
20.
Zurück zum Zitat Berry EA, Trumpower BL (1987) Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra. Anal Biochem 161(1):1–15PubMedCrossRef Berry EA, Trumpower BL (1987) Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra. Anal Biochem 161(1):1–15PubMedCrossRef
21.
Zurück zum Zitat Douglas DB, Simeon EG (2003) Mechanisms of bacterial lipopolysaccharide-induced endothelial apoptosis. Am J Physiol Lung Cell Mol Physiol 284:L899–L914 Douglas DB, Simeon EG (2003) Mechanisms of bacterial lipopolysaccharide-induced endothelial apoptosis. Am J Physiol Lung Cell Mol Physiol 284:L899–L914
22.
Zurück zum Zitat Karu T (2003) Low-power laser therapy. In: Vo-Dinh T (ed) Biomedical photonics handbook. 1st edn. CRC Press, Boca Raton, pp 48-01‒ 48-25 Karu T (2003) Low-power laser therapy. In: Vo-Dinh T (ed) Biomedical photonics handbook. 1st edn. CRC Press, Boca Raton, pp 48-01‒ 48-25
23.
Zurück zum Zitat Buravlev EA, Zhidkova TV, Vladimirov YA, Osipov AN (2013) Effects of laser and LED radiation on mitochondrial respiration in experimental endotoxic shock. Lasers Med Sci 28(3):785–790PubMedCrossRef Buravlev EA, Zhidkova TV, Vladimirov YA, Osipov AN (2013) Effects of laser and LED radiation on mitochondrial respiration in experimental endotoxic shock. Lasers Med Sci 28(3):785–790PubMedCrossRef
24.
Zurück zum Zitat Borodulin RR, Kubrina LN, Serezhenkov VA, Burbaev DS, Mikoyan VD, Vanin AF (2013) Redox conversions of dinitrosyl iron complexes with natural thiol-containing ligands. Nitric Oxide 35:35–41PubMedCrossRef Borodulin RR, Kubrina LN, Serezhenkov VA, Burbaev DS, Mikoyan VD, Vanin AF (2013) Redox conversions of dinitrosyl iron complexes with natural thiol-containing ligands. Nitric Oxide 35:35–41PubMedCrossRef
25.
Zurück zum Zitat Dungel P, Mittermayr R, Haindl S, Osipov A, Wagner C, Redl H, Kozlov AV (2008) Illumination with blue light reactivates respiratory activity of mitochondria inhibited by nitric oxide, but not by glycerol trinitrate. Arch Biochem Biophys 471(2):109–115PubMedCrossRef Dungel P, Mittermayr R, Haindl S, Osipov A, Wagner C, Redl H, Kozlov AV (2008) Illumination with blue light reactivates respiratory activity of mitochondria inhibited by nitric oxide, but not by glycerol trinitrate. Arch Biochem Biophys 471(2):109–115PubMedCrossRef
26.
Zurück zum Zitat Mittermayr R, Osipov A, Piskernik C, Haindl S, Dungel P, Weber C, Vladimirov YA, Redl H, Kozlov AV (2007) Blue laser light increases perfusion of a skin flap via release of nitric oxide from hemoglobin. Mol Med 13(1–2):22–29PubMedCentralPubMed Mittermayr R, Osipov A, Piskernik C, Haindl S, Dungel P, Weber C, Vladimirov YA, Redl H, Kozlov AV (2007) Blue laser light increases perfusion of a skin flap via release of nitric oxide from hemoglobin. Mol Med 13(1–2):22–29PubMedCentralPubMed
27.
Zurück zum Zitat Kipshidze N, Nikolaychik V, Keelan MH, Shankar LR, Khanna A, Kornowski R, Leon M, Moses J (2001) Low-power helium: neon laser irradiation enhances production of vascular endothelial growth factor and promotes growth of endothelial cells in vitro. Lasers Surg Med 28(4):355–364PubMedCrossRef Kipshidze N, Nikolaychik V, Keelan MH, Shankar LR, Khanna A, Kornowski R, Leon M, Moses J (2001) Low-power helium: neon laser irradiation enhances production of vascular endothelial growth factor and promotes growth of endothelial cells in vitro. Lasers Surg Med 28(4):355–364PubMedCrossRef
28.
Zurück zum Zitat Hopkins JT, McLoda TA, Seegmiller JG, David Baxter G (2004) Low-level laser therapy facilitates superficial wound healing in humans: a triple-blind, sham-controlled study. J Athl Train 39(3):223–229PubMedCentralPubMed Hopkins JT, McLoda TA, Seegmiller JG, David Baxter G (2004) Low-level laser therapy facilitates superficial wound healing in humans: a triple-blind, sham-controlled study. J Athl Train 39(3):223–229PubMedCentralPubMed
29.
Zurück zum Zitat Byrnes KR, Barna L, Chenault VM, Waynant RW, Ilev IK, Longo L, Miracco C, Johnson B, Anders JJ (2004) Photobiomodulation improves cutaneous wound healing in an animal model of type II diabetes. Photomed Laser Surg 22(4):281–290PubMedCrossRef Byrnes KR, Barna L, Chenault VM, Waynant RW, Ilev IK, Longo L, Miracco C, Johnson B, Anders JJ (2004) Photobiomodulation improves cutaneous wound healing in an animal model of type II diabetes. Photomed Laser Surg 22(4):281–290PubMedCrossRef
30.
Zurück zum Zitat Passarella S, Casamassima E, Molinari S, Pastore D, Quagliariello E, Catalano IM, Cingolani A (1984) Increase of proton electrochemical potential and ATP synthesis in rat liver mitochondria irradiated in vitro by helium-neon laser. FEBS Lett 175(1):95–99PubMedCrossRef Passarella S, Casamassima E, Molinari S, Pastore D, Quagliariello E, Catalano IM, Cingolani A (1984) Increase of proton electrochemical potential and ATP synthesis in rat liver mitochondria irradiated in vitro by helium-neon laser. FEBS Lett 175(1):95–99PubMedCrossRef
31.
Zurück zum Zitat Yu W, Naim JO, McGowan M, Ippolito K, Lanzafame RJ (1997) Photomodulation of oxidative metabolism and electron chain enzymes in rat liver mitochondria. Photochem Photobiol 66(6):866–871PubMedCrossRef Yu W, Naim JO, McGowan M, Ippolito K, Lanzafame RJ (1997) Photomodulation of oxidative metabolism and electron chain enzymes in rat liver mitochondria. Photochem Photobiol 66(6):866–871PubMedCrossRef
32.
Zurück zum Zitat Morimoto Y, Arai T, Kikuchi M, Nakajima S, Nakamura H (1994) Effect of low-intensity argon laser irradiation on mitochondrial respiration. Lasers Surg Med 15(2):191–199PubMedCrossRef Morimoto Y, Arai T, Kikuchi M, Nakajima S, Nakamura H (1994) Effect of low-intensity argon laser irradiation on mitochondrial respiration. Lasers Surg Med 15(2):191–199PubMedCrossRef
33.
Zurück zum Zitat Jou MJ, Jou SB, Chen HM, Lin CH, Peng TI (2002) Critical role of mitochondrial reactive oxygen species formation in visible laser irradiation-induced apoptosis in rat brain astrocytes (RBA-1). J Biomed Sci 9(6 Pt 1):507–516PubMedCrossRef Jou MJ, Jou SB, Chen HM, Lin CH, Peng TI (2002) Critical role of mitochondrial reactive oxygen species formation in visible laser irradiation-induced apoptosis in rat brain astrocytes (RBA-1). J Biomed Sci 9(6 Pt 1):507–516PubMedCrossRef
34.
Zurück zum Zitat Jou MJ, Jou SB, Guo MJ, Wu HY, Peng TI (2004) Mitochondrial reactive oxygen species generation and calcium increase induced by visible light in astrocytes. Ann N Y Acad Sci 1011:45–56PubMedCrossRef Jou MJ, Jou SB, Guo MJ, Wu HY, Peng TI (2004) Mitochondrial reactive oxygen species generation and calcium increase induced by visible light in astrocytes. Ann N Y Acad Sci 1011:45–56PubMedCrossRef
35.
Zurück zum Zitat Karima R, Matsumoto S, Higashi H, Matsushima K (1999) The molecular pathogenesis of endotoxic shock and organ failure. Mol Med Today 5(3):123–132PubMedCrossRef Karima R, Matsumoto S, Higashi H, Matsushima K (1999) The molecular pathogenesis of endotoxic shock and organ failure. Mol Med Today 5(3):123–132PubMedCrossRef
36.
Zurück zum Zitat Kirkebøen KA, Strand OA (1999) The role of nitric oxide in sepsis—an overview. Acta Anaesthesiol Scand 43:275–288PubMedCrossRef Kirkebøen KA, Strand OA (1999) The role of nitric oxide in sepsis—an overview. Acta Anaesthesiol Scand 43:275–288PubMedCrossRef
37.
Zurück zum Zitat Kozlov AV, Staniek K, Haindl S, Piskernik C, Ohlinger W, Gille L, Nohl H, Bahrami S, Redl H (2006) Different effects of endotoxic shock on the respiratory function of liver and heart mitochondria in rats. Am J Physiol Gastrointest Liver Physiol 290(3):G543–G549PubMedCrossRef Kozlov AV, Staniek K, Haindl S, Piskernik C, Ohlinger W, Gille L, Nohl H, Bahrami S, Redl H (2006) Different effects of endotoxic shock on the respiratory function of liver and heart mitochondria in rats. Am J Physiol Gastrointest Liver Physiol 290(3):G543–G549PubMedCrossRef
38.
Zurück zum Zitat Wainio WW (1955) Reactions of cytochrome oxidase. J Biol Chem 212(2):723–733PubMed Wainio WW (1955) Reactions of cytochrome oxidase. J Biol Chem 212(2):723–733PubMed
39.
Zurück zum Zitat Vos MH, Lipowski G, Lambry JC, Martin JL, Liebl U (2001) Dynamics of nitric oxide in the active site of reduced cytochrome c oxidase aa3. Biochemistry 40(26):7806–7811PubMedCrossRef Vos MH, Lipowski G, Lambry JC, Martin JL, Liebl U (2001) Dynamics of nitric oxide in the active site of reduced cytochrome c oxidase aa3. Biochemistry 40(26):7806–7811PubMedCrossRef
40.
Zurück zum Zitat Karu TI, Kalendo GS, Letokhov VS, Lobko VV (1982) Biostimulation of HeLa cells by low intensity visible light. Nuov Cim D 1 (828-40) Karu TI, Kalendo GS, Letokhov VS, Lobko VV (1982) Biostimulation of HeLa cells by low intensity visible light. Nuov Cim D 1 (828-40)
41.
Zurück zum Zitat Karu TI, Kalendo GS, Letokhov VS, Lobko VV (1984) Biostimulation of HeLa cells by low intensity visible light. II. Stimulation of DNA and RNA synthesis in a wide spectral range. Nuov Cim D 3:309–318CrossRef Karu TI, Kalendo GS, Letokhov VS, Lobko VV (1984) Biostimulation of HeLa cells by low intensity visible light. II. Stimulation of DNA and RNA synthesis in a wide spectral range. Nuov Cim D 3:309–318CrossRef
42.
Zurück zum Zitat Karu T, Pyatibrat L, Afanasyeva N (2005) Cellular effects of low power laser therapy can be mediated by nitric oxide. Lasers Surg Med 36(4):307–314PubMedCrossRef Karu T, Pyatibrat L, Afanasyeva N (2005) Cellular effects of low power laser therapy can be mediated by nitric oxide. Lasers Surg Med 36(4):307–314PubMedCrossRef
Metadaten
Titel
Are the mitochondrial respiratory complexes blocked by NO the targets for the laser and LED therapy?
verfasst von
Evgeny A. Buravlev
Tatyana V. Zhidkova
Anatoly N. Osipov
Yury A. Vladimirov
Publikationsdatum
01.01.2015
Verlag
Springer London
Erschienen in
Lasers in Medical Science / Ausgabe 1/2015
Print ISSN: 0268-8921
Elektronische ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-014-1639-8

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