Nitric oxide stimulates myoglobin gene and protein expression in vascular smooth muscle

Biochemical Journal

Volumn 423, Issue 2, 2009, Pages 169-177

  Rayner, Benjamin S ^a   Hua, Susan ^b   Sabaretnam, Tharani ^a   Witting, Paul K ^a,b  

^a Department of Microbiology and Infectious Diseases   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Endothelial function; Haem protein; Nitric oxide metabolism; Vascular smooth muscle; Vasodilation

Indexed keywords

APOPTOSIS; CELL SIGNALLING; CELL VIABILITY; CONCENTRATION OF; ENDOTHELIAL FUNCTION; HAEM PROTEIN; HAEMOGLOBINS; HOMOEOSTASIS; IN-CELL; INDIRECT IMMUNOFLUORESCENCE MICROSCOPY; L-ARGININE; MITOCHONDRIAL FUNCTION; N-O COMPLEXES; NITROSO; NO CONCENTRATION; PROTEIN EXPRESSIONS; SMOOTH MUSCLES; TIME-DEPENDENT; TRANSCRIPTIONAL ACTIVATIONS; UP-REGULATION; VASCULAR SMOOTH MUSCLE; VASCULAR SMOOTH MUSCLE CELLS; VASCULAR SMOOTH MUSCLES; VASODILATION; VESSEL LUMEN; VESSEL WALLS; WESTERN-BLOT ANALYSIS;

ACTIVATION ANALYSIS; AMINO ACIDS; ANIMAL CELL CULTURE; BIOCHEMISTRY; BLOOD VESSEL PROSTHESES; CELL CULTURE; CELL DEATH; GENE EXPRESSION; METABOLISM; MOLECULAR OXYGEN; MUSCLE; NITRIC OXIDE; PHYSIOLOGY; SELF ASSEMBLY;

CELL MEMBRANES;

HEMOGLOBIN; MYOGLOBIN; NITRIC OXIDE;

ANIMAL CELL; ARTICLE; CELL DENSITY; CELL VIABILITY; CONTROLLED STUDY; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; UPREGULATION; VASCULAR SMOOTH MUSCLE; WESTERN BLOTTING;

ANIMALS; AORTA; CELL CULTURE TECHNIQUES; CELL MEMBRANE; CELL SURVIVAL; CELLS, CULTURED; GENE EXPRESSION; HUMANS; MUSCLE, SMOOTH, VASCULAR; MYOGLOBIN; NITRIC OXIDE; RATS; UP-REGULATION;

RATTUS;

EID: 70350114568     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20090716     Document Type: Article

References (54)

1. Furchgott, R. F. and Zawadzki, J. V. (1980) The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288, 373-376
2. Ignarro, L. J., Buga, G. M., Wood, K. S., Byrns, R. E. and Chaudhuri, G. (1987) Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. U.S.A. 84, 9265-9269
3. Zhao, Y., Brandish, P. E., Ballou, D. P. and Marletta, M. A. (1999) A molecular basis for nitric oxide sensing by soluble guanylate cyclase. Proc. Natl. Acad. Sci. U.S.A. 96, 14753-14758
4. Gow, A. J. and Stamler, J. S. (1998) Reactions between nitric oxide and haemoglobin under physiological conditions. Nature 391, 169-173
5. Gross, S. S. and Lane, P. (1999) Physiological reactions of nitric oxide and hemoglobin: a radical rethink. Proc. Natl. Acad. Sci. U.S.A. 96, 9967-9969
6. Wittenberg, B. A. and Wittenberg, J. B. (1989) Transport of oxygen in muscle. Ann. Rev. Physiol. 51, 857-878
7. Qiu, Y., Sutton, L. and Riggs, A. F. (1998) Identification of myoglobin in human smooth muscle. J. Biol. Chem. 273, 23426-23432
8. Brunori, M. (2001) Nitric oxide moves myoglobin centre stage. Trends Biochem. Sci. 26, 209-210
9. Andriambeloson, E. and Witting, P. K. (2002) Chemical regulation of nitric oxide: a role for intracellular myoglobin? Redox Report 7, 131-136
10. Doyle, M. P. and Hoekstra, J. W. (1981) Oxidation of nitrogen oxides by bound dioxygen in hemoproteins J. Inorg. Biochem. 14, 351-358
11. Kalyanaraman, B. (1996) Detection of nitric oxide by electron spin resonance in chemical, photochemical, cellular, physiological, and pathophysiological systems. Methods Enzymol. 268, 168-187
12. Schreiter, E. R., Rodriguez, M. M., Weichsel, A., Montfort, W. R. and Bonaventura, J. (2007) S-nitrosylation-induced conformational change in blackfin tuna myoglobin. J. Biol. Chem. 282, 19773-19780
13. Rayner, B. S., Wu, B.-J., Raftery, M., Stocker, R. and Witting, P. K. (2005) Human S-nitroso-oxymyoglobin is a store of vasoactive nitric oxide. J. Biol. Chem. 280, 9985-9993
14. Flögel, U., Merx, M. W., Gödecke, A., Decking, U. K. and Schrader, J. (2001) Myoglobin: a scavenger of bioactive NO. Proc. Natl. Acad. Sci. U.S.A. 98, 735-740
15. Thomas, S. R., Chen, K. and Keaney, Jr, J. F. (2002) Hydrogen peroxide activates endothelial nitric-oxide synthase through coordinated phosphorylation and dephosphorylation via a phosphoinositide 3-kinase-dependent signaling pathway. J. Biol. Chem. 277, 6017-6024
16. Rayner, B. S., Duong, T. T. H., Myers, S. J. and Witting, P. K. (2006) Protective effect of a phenolic antioxidant on neuronal cell apoptosis resulting from experimental hypoxia re-oxygenation injury. J. Neurochem. 97, 211-221
17. Duong, T. T., Antao, S., Ellis, N. A., Myers, S. J. and Witting, P. K. (2008) Supplementation with a synthetic polyphenol limits oxidative stress and enhances neuronal cell viability in response to hypoxia-re-oxygenation injury. Brain Res. 1219, 8-18
18. Purcell, A. W., Aguilar, M. I. and Hearn, M. T. (1999) Probing the binding behavior and conformational states of globular proteins in reversed-phase high-performance liquid chromatography. Anal. Chem. 71, 2440-2451
19. Travascio, P., Witting, P. K., Mauk, A. G. and Sen, D. (2001) The peroxidase activity of a hemin-DNA oligonucleotide complex: free radical damage to specific guanine bases of the DNA. J. Am. Chem. Soc. 123, 1337-1348
20. Yang, G., Sun, X. and Wang, R. (2004) Hydrogen sulfide-induced apoptosis of human aorta smooth muscle cells via the activation of mitogen-activated protein kinases and caspase-3. FASEB J. 18, 1782-1784
21. Witting, P. K., Rayner, B. S., Wu, B.-J., Ellis, N. A. and Stocker, R. (2007) Hydrogen peroxide promotes vascular dysfunction through decreasing nitric oxide bioavailability. Cell Physiol. Biochem. 20, 255-268
22. Berkels, R., Purol-Schnabel, S. and Roesen, R. (2001) A new method to measure nitrate/nitrite with a NO-sensitive electrode. J. Appl. Physiol. 90, 317-320
23. Witting, P. K., Pettersson, K., Ostlund-Lindqvist, A. M., Westerlund, C., Wagberg, M. and Stocker, R. (1999) Dissociation of atherogenesis from aortic accumulation of lipid hydro(pero)xides in Watanabe heritable hyperlipidemic rabbits. J. Clin. Invest. 104, 213-220
24. Suarna, C., Dean, R. T., May, J. and Stocker, R. (1995) Human atherosclerotic plaque contains both oxidized lipids and relatively large amounts of alpha-tocopherol and ascorbate. Arterioscler. Thromb. Vasc. Biol. 15, 1616-1624
25. Singel, D. J. and Stamler, J. S. (2005) Chemical physiology of blood flow regulation by red blood cells: the role of nitric oxide and S-nitrosohemoglobin. Annu. Rev. Physiol. 67, 99-145
26. Antonini, E. and Brunori, M. (1971) Hemoglobin and Myoglobin in Their Reactions with Ligands, North-Holland Publishing Co., Amsterdam
27. Shiva, S., Huang, Z., Grubina, R., Sun, J., Ringwood, L. A., MacArthur, P. H., Xu, X., Murphy, E., Darley-Usmar, V. M. and Gladwin, M. T. (2007) Deoxymyoglobin is a nitrite reductase that generates nitric oxide and regulates mitochondrial respiration. Circ. Res. 100, 654-661
28. Duranski, M. R., Greer, J. J., Dejam, A., Jaganmohan, S., Hogg, N., Langston, W., Patel, R. P., Yet, S. F., Wang, X., Kevil, C. G. et al. (2005) Cytoprotective effects of nitrite during in vivo ischemia-reperfusion of the heart and liver. J. Clin. Invest. 115, 1232-1240
29. Hendgen-Cotta, U. B., Merx, M. W., Shiva, S., Schmitz, J., Becher, S., Klare, J. P., Steinhoff, H. J., Goedecke, A., Schrader, J., Gladwin, M. T. et al. (2008) Nitrite reductase activity of myoglobin regulates respiration and cellular viability in myocardial ischemia-reperfusion injury. Proc. Natl. Acad. Sci. U.S.A. 105, 10256-10261
30. a Erratum (2008) Proc. Natl. Acad. Sci. U.S.A. 105, 12636
31. Godecke, A., Molojavyi, A., Heger, J., Flogel, U., Ding, Z., Jacoby, C. and Schrader, J. (2003) Myoglobin protects the heart from inducible nitric-oxide synthase (iNOS)-mediated nitrosative stress. J. Biol. Chem. 278, 21761-21766
32. Wunderlich, C., Flogel, U., Godecke, A., Heger, J. and Schrader, J. (2003) Acute inhibition of myoglobin impairs contractility and energy state of iNOS-overexpressing hearts. Circ. Res. 92, 1352-1358
33. Andréka, P., Tran, T., Webster, P. A. and Bishopric, N. H. (2004) Nitric oxide and promotion of cardiac myocyte apoptosis. Mol. Cell. Biochem. 263, 35-53
34. Lin, P. C., Kreutzer, U. and Jue, T. (2007) Myoglobin translational diffusion in rat myocardium and its implication on intracellular oxygen transport. J. Physiol. 578, 595-603
35. Wittenberg, J. B. and Wittenberg, B. A. (2003) Myoglobin function reassessed. J. Exp. Biol. 206, 2011-2020
36. Godecke, A., Flogel, U., Zanger, K., Ding, Z., Hirchenhain, J., Decking, U. K. and Schrader, J. (1999) Disruption of myoglobin in mice induces multiple compensatory mechanisms. Proc. Natl. Acad. Sci. U.S.A. 96, 10495-10500
37. Hazarika, S., Angelo, M., Li, Y., Aldrich, A. J., Odronic, S. I., Yan, Z., Stamler, J. S. and Annex, B. H. (2008) Myocyte specific overexpression of myoglobin impairs angiogenesis after hind-limb ischemia. Arterioscler. Thromb. Vasc. Biol. 28, 2144-2150
38. Kondo, T., Kobayashi, K. and Murohara, T. (2004) Nitric oxide signaling during myocardial angiogenesis. Mol. Cell. Biochem. 264, 25-34
39. Dulak, J. and Jozkowicz, A. (2003) Regulation of vascular endothelial growth factor synthesis by nitric oxide: facts and controversies. Antioxid. Redox Signaling 5, 123-132
40. Bassel-Duby, R., Hernandez, M. D., Yang, Q., Rochelle, J. M., Seldin, M. F. and Williams, R. S. (1994) Myocyte nuclear factor, a novel winged-helix transcription factor under both developmental and neural regulation in striated myocytes. Mol. Cell. Biol. 14, 4596-4605
41. Vogt, M., Puntschart, A., Geiser, J., Zuleger, C., Billeter, R. and Hoppeler, H. (2001) Molecular adaptations in human skeletal muscle to endurance training under simulated hypoxic conditions. J. Appl. Physiol. 91, 173-182
42. Grayson, J., Williams, R. S., Yu, Y. T. and Bassel-Duby, R. (1995) Synergistic interactions between heterologous upstream activation elements and specific TATA sequences in a muscle-specific promoter. Mol. Cell. Biol. 15, 1870-1878
43. Bassel-Duby, R., Hernandez, M. D., Gonzalez, M. A., Krueger, J. K. and Williams, R. S. (1992) A 40-kilodalton protein binds specifically to an upstream sequence element essential for muscle-specific transcription of the human myoglobin promoter. Mol. Cell. Biol. 12, 5024-5032
44. van Weel, V., Deckers, M. M., Grimbergen, J. M., van Leuven, K. J., Lardenoye, J. H., Schlingemann, R. O., van Nieuw, A., Amerongen, G. P., van Bockel, J. H., van Hinsbergh, V. W. and Quax, P. H. (2004) Vascular endothelial growth factor overexpression in ischemic skeletal muscle enhances myoglobin expression in vivo. Circ. Res. 95, 58-66
45. Robach, P., Cairo, G., Gelfi, C., Bernuzzi, F., Pilegaard, H., Vigano, A., Santambrogio, P., Cerretelli, P., Calbet, J. A., Moutereau, S. and Lundby, C. (2007) Strong iron demand during hypoxia-induced erythropoiesis is associated with down-regulation of iron-related proteins and myoglobin in human skeletal muscle. Blood 109, 4724-4731
46. Mason, M. G., Nicholls, P., Wilson, M. T. and Cooper, C. E. (2006) Nitric oxide inhibition of respiration involves both competitive (heme) and noncompetitive (copper) binding to cytochrome c oxidase. Proc. Natl. Acad. Sci. U.S.A. 103, 708-713
47. Brunori, M., Giuffrè, A., Forte, E., Mastronicola, D., Barone, M. C. and Sarti, P. (2004) Control of cytochrome c oxidase activity by nitric oxide. Biochim. Biophys. Acta 1655, 365-371
48. Antunes, F., Boveris, A. and Cadenas, E. (2007) On the biologic role of the reaction of NO with oxidized cytochrome c oxidase. Antiox. Redox Signaling 9, 1569-1579
49. Dahm, C. C., Moore, K. and Murphy, M. M. (2006) Persistent S-nitrosation of complex I and other mitochondrial membrane proteins by S-nitrosothiols but not nitric oxide or peroxynitrite: implications for the interaction of nitric oxide with mitochondria. J. Biol. Chem. 281, 10056-10065
50. Ignarro, L. J., Cirino, G., Casini, A. and Napoli, C. (1999) Nitric oxide as a signaling molecule in the vascular system: an overview. J. Cardiovasc. Pharmacol. 34, 879-886
51. Liu, X., Yan, Q., Baskerville, K. L. and Zweier, J. L. (2007) Estimation of nitric oxide concentration in blood for different rates of generation. Evidence that intravascular nitric oxide levels are too low to exert physiological effects. J. Biol. Chem. 282, 8831-8836
52. Joshi, M. S., Lancaster, Jr, J. R., Liu, X. and Ferguson, Jr, T. B. (2001) In situ measurement of nitric oxide production in cardiac isografts and rejecting allografts by an electrochemical method. Nitric Oxide 5, 561-565
53. Gomez-Jimenez, J., Salgado, A., Mourelle, M., Martin, M. C., Segura, R. M., Peracaula, R. and Moncada, S. (1995) L-arginine: nitric oxide pathway in endotoxemia and human septic shock. Crit. Care Med. 23, 253-258
54. Ochoa, J. B., Udekwu, A. O., Billiar, T. R., Curran, R. D., Cerra, F. B., Simmons, R. L. and Peitzman, A. B. (1991) Nitrogen oxide levels in patients after trauma and during sepsis. Ann. Surg. 214, 621-626