Journal of Molecular and Cellular Cardiology
Volume 47, Issue 2 , Pages 256-263 , August 2009

Enhancement of nitric oxide release from nitrosyl hemoglobin and nitrosyl myoglobin by red/near infrared radiation: Potential role in cardioprotection

  • Nicole L. Lohr

      Affiliations

    • Department of Anesthesiology, the Medical College of Wisconsin, MEB 4245, 8701 Watertown Plank Road, Milwaukee, Wisconsin 53226, USA
    • Department of Internal Medicine, the Medical College of Wisconsin, Milwaukee WI, USA
    • Corresponding Author InformationCorresponding author. Department of Anesthesiology, the Medical College of WI, MEB 4245, 8701 Watertown Plank Road, Milwaukee, Wisconsin 53226, USA. Tel.: +1 414 456 5739; fax: +1 414 456 6507.
  • ,
  • Agnes Keszler

      Affiliations

    • Department of Biophysics, the Medical College of Wisconsin, Milwaukee Wisconsin, USA
  • ,
  • Phillip Pratt

      Affiliations

    • Department of Anesthesiology, the Medical College of Wisconsin, MEB 4245, 8701 Watertown Plank Road, Milwaukee, Wisconsin 53226, USA
    • Department of Pharmacology, the Medical College of Wisconsin, Milwaukee Wisconsin, USA
  • ,
  • Martin Bienengraber

      Affiliations

    • Department of Anesthesiology, the Medical College of Wisconsin, MEB 4245, 8701 Watertown Plank Road, Milwaukee, Wisconsin 53226, USA
    • Department of Pharmacology, the Medical College of Wisconsin, Milwaukee Wisconsin, USA
  • ,
  • David C. Warltier

      Affiliations

    • Department of Anesthesiology, the Medical College of Wisconsin, MEB 4245, 8701 Watertown Plank Road, Milwaukee, Wisconsin 53226, USA
    • Department of Pharmacology, the Medical College of Wisconsin, Milwaukee Wisconsin, USA
  • ,
  • Neil Hogg

      Affiliations

    • Department of Biophysics, the Medical College of Wisconsin, Milwaukee Wisconsin, USA

Received 20 January 2009 ,Revised 16 March 2009 ,Accepted 19 March 2009.

References 

  1. Massion PB, et al. Nitric oxide and cardiac function: ten years after, and continuing. Circ. Res. 2003;93(5):388–398
  2. Dweik RA, et al. Nitric oxide synthesis in the lung. Regulation by oxygen through a kinetic mechanism. J. Clin. Invest. 1998;101(3):660–666
  3. Lundberg JO, Weitzberg E, Gladwin MT. The nitrate–nitrite–nitric oxide pathway in physiology and therapeutics. Nat. Rev. Drug Discov. 2008;7(2):156–167
  4. Nagababu E, et al. Active nitric oxide produced in the red cell under hypoxic conditions by deoxyhemoglobin-mediated nitrite reduction. J. Biol. Chem. 2003;278(47):46349–46356
  5. Cosby K, et al. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. [see. comment] Nat. Med. 2003;9(12):1498–1505
  6. Shiva S, et al. Deoxymyoglobin is a nitrite reductase that generates nitric oxide and regulates mitochondrial respiration. Circ. Res. 2007;100(5):654–661
  7. Schwengel RH, et al. Characterization of pulsed-dye laser-mediated vasodilatation in a rabbit femoral artery model of vasoconstriction. Lasers Surg. Med. 1993;13(3):284–295
  8. Castello PR, et al. Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes. Cell Metab. 2006;3(4):277–287
  9. Castello PR, et al. Oxygen-regulated isoforms of cytochrome c oxidase have differential effects on its nitric oxide production and on hypoxic signaling. Proc. Natl. Acad. Sci. U. S. A. 2008;105(24):8203–8208
  10. Gautier C, et al. Endothelial nitric oxide synthase reduces nitrite anions to NO under anoxia. Biochem. Biophys. Res. Commun. 2006;341(3):816–821
  11. Huang KT, et al. The reaction between nitrite and deoxyhemoglobin. Reassessment of reaction kinetics and stoichiometry. J. Biol. Chem. 2005;280(35):31126–31131
  12. Crawford JH, et al. Hypoxia, red blood cells, and nitrite regulate NO-dependent hypoxic vasodilation. Blood. 2006;107(2):566–574
  13. Huang Z, et al. Enzymatic function of hemoglobin as a nitrite reductase that produces NO under allosteric control. J. Clin. Invest. 2005;115(8):2099–2107
  14. Gladwin MT, Crawford JH, Patel RP. The biochemistry of nitric oxide, nitrite, and hemoglobin: role in blood flow regulation. Free Radic. Biol. Med. 2004;36(6):707–717
  15. Owen-Reece H, et al. Near infrared spectroscopy. Br. J. Anaesth. 1999;82(3):418–426
  16. Bozkurt A, Onaral B. Safety assessment of near infrared light emitting diodes for diffuse optical measurements. Biomed. Eng. Online. 2004;3(1):9
  17. Stadler I, et al. Alteration of skin temperature during low-level laser irradiation at 830 nm in a mouse model. Photomed. Laser Surg. 2004;22(3):227–231
  18. Wong-Riley MT, et al. Photobiomodulation directly benefits primary neurons functionally inactivated by toxins: role of cytochrome c oxidase. J. Biol. Chem. 2005;280(6):4761–4771
  19. Whelan HT, et al. NASA light-emitting diodes for the prevention of oral mucositis in pediatric bone marrow transplant patients. J. Clin. Laser Med. Surg. 2002;20(6):319–324
  20. Bibikova A, Belkin V, Oron U. Enhancement of angiogenesis in regenerating gastrocnemius muscle of the toad (Bufo viridis) by low-energy laser irradiation. Anat. Embryol. (Berl.). 1994;190(6):597–602
  21. Ad N, Oron U. Impact of low level laser irradiation on infarct size in the rat following myocardial infarction. Int. J. Cardiol. 2001;80(2–3):109–116
  22. Karu TI, Pyatibrat LV, Kalendo GS. Photobiological modulation of cell attachment via cytochrome c oxidase. Photochem. Photobiol. Sci. 2004;3(2):211–216
  23. Karu TI, et al. Absorption measurements of a cell monolayer relevant to phototherapy: reduction of cytochrome c oxidase under near IR radiation. J. Photochem. Photobiol. B. 2005;81(2):98–106
  24. Sarti P, et al. Nitric oxide and cytochrome c oxidase: mechanisms of inhibition and NO degradation. Biochem. Biophys. Res. Commun. 2000;274(1):183–187
  25. Rossi-Fanelli A, Antonini E, Caputo A. Studies on the relations between molecular and functional properties of hemoglobin. I. The effect of salts on the molecular weight of human hemoglobin. J. Biol. Chem. 1961;236:391–396
  26. Antonini E, Brunori M. In: Hemoglobin and myoglobin in their reactions with ligands [by] Eraldo Antonini and Maurizio Brunori. Amsterdam: North-Holland Pub. Co.; 1971;p. 436
  27. Tanaka K, et al. Mechanism of preconditioning by isoflurane in rabbits: a direct role for reactive oxygen species. Anesthesiology. 2002;97(6):1485–1490
  28. Wallenstein S, Zucker CL, Fleiss JL. Some statistical methods useful in circulation research. Circ. Res. 1980;47:1–9
  29. Duranski MR, et al. Cytoprotective effects of nitrite during in vivo ischemia–reperfusion of the heart and liver. J. Clin. Invest. 2005;115(5):1232–1240
  30. Gonzalez FM, et al. Nitrite anion provides potent cytoprotective and antiapoptotic effects as adjunctive therapy to reperfusion for acute myocardial infarction. Circulation. 2008;117(23):2986–2994
  31. Baker JE, et al. Nitrite confers protection against myocardial infarction: role of xanthine oxidoreductase, NADPH oxidase and K (ATP) channels. J. Mol. Cell. Cardiol. 2007;43(4):437–444
  32. Cohen MV, Liu GS, Downey JM. Preconditioning causes improved wall motion as well as smaller infarcts after transient coronary occlusion in rabbits. Circulation. 1991;84(1):341–349
  33. Chou HJ, Yates RL. A rapid and selective method for determining potential nitrosating agents in cosmetic products by chemiluminescence detection of nitric oxide. J. AOAC Int. 1998;81(2):368–372
  34. Keszler A, et al. The reaction between nitrite and oxyhemoglobin: a mechanistic study. J. Biol. Chem. 2008;283(15):9615–9622
  35. Doyle MP, et al. Kinetics and mechanism of the oxidation of human deoxyhemoglobin by nitrites. J. Biol. Chem. 1981;256(23):12393–12398
  36. Huang TH. NMR studies of the quaternary structure and heterogeneity of nitrosyl- and methemoglobin. J. Biol. Chem. 1979;254(22):11467–11474
  37. Piknova B, et al. Electron paramagnetic resonance analysis of nitrosylhemoglobin in humans during NO inhalation. J. Biol. Chem. 2005;280(49):40583–40588
  38. Nakanishi AL, et al. Electron spin resonance analysis of heme-nitrosyl and reduced iron-sulfur centered complexes in allogeneic, heterotopic cardiac transplants: effects of treatment with pyrrolidine dithiocarbamate. Free Radic. Biol. Med. 1998;25(2):201–207
  39. Tiravanti E, Samouilov A, Zweier JL. Nitrosyl-heme complexes are formed in the ischemic heart: evidence of nitrite-derived nitric oxide formation, storage, and signaling in post-ischemic tissues. J. Biol. Chem. 2004;279(12):11065–11073
  40. Hoffman BM, Gibson QH. On the photosensitivity of liganded hemoproteins and their metal-substituted analogues. Proc. Natl. Acad. Sci. U. S. A. 1978;75(1):21–25
  41. Gibson QH, Ainsworth S. Photosensitivity of haem compounds. Nature. 1957;180(4599):1416–1417
  42. Cohen MV, Yang XM, Downey JM. Nitric oxide is a preconditioning mimetic and cardioprotectant and is the basis of many available infarct-sparing strategies. Cardiovasc. Res. 2006;70(2):231–239
  43. Cooper CE, et al. Nitric oxide ejects electrons from the binuclear centre of cytochrome c oxidase by reacting with oxidised copper: a general mechanism for the interaction of copper proteins with nitric oxide?. FEBS Lett. 1997;414(2):281–284
  44. Osipov AN, Borisenko GG, Vladimirov YA. Biological activity of hemoprotein nitrosyl complexes. Biochemistry (Mosc.). 2007;72(13):1491–1504
  45. Sarti P, et al. Nitric oxide and cytochrome oxidase: reaction mechanisms from the enzyme to the cell. Free Radic. Biol. Med. 2003;34(5):509–520
  46. Mason MG, et al. Nitric oxide inhibition of respiration involves both competitive (heme) and noncompetitive (copper) binding to cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 2006;103(3):708–713
  47. Wink DA, Mitchell JB. Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic. Biol. Med. 1998;25(4–5):434–456
  48. Brown GC, Borutaite V. Nitric oxide inhibition of mitochondrial respiration and its role in cell death. Free Radic. Biol. Med. 2002;33(11):1440–1450
  49. Zhao X, et al. Endothelial nitric oxide synthase (NOS3) knockout decreases NOS2 induction, limiting hyperoxygenation and conferring protection in the postischemic heart. Am. J. Physiol. Heart Circ. Physiol. 2007;292(3):H1541–H1550

PII: S0022-2828(09)00117-5

doi: 10.1016/j.yjmcc.2009.03.009

Journal of Molecular and Cellular Cardiology
Volume 47, Issue 2 , Pages 256-263 , August 2009