The role of vascular myoglobin in nitrite-mediated blood vessel relaxation

Cardiovascular Research

Volumn 89, Issue 3, 2011, Pages 560-565

  Ormerod, Julian O M ^a   Ashrafian, Houman ^b   Maher, Abdul R ^a   Arif, Sayqa ^a   Steeples, Violetta ^b   Born, Gustav V R ^c   Egginton, Stuart ^a   Feelisch, Martin ^d   Watkins, Hugh ^b   Frenneaux, Michael P ^e  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^d UNIVERSITY OF WARWICK   (United Kingdom)

^e UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Myoglobin; Nitric oxide; Nitrite; Vasodilation

Indexed keywords

CARBON DIOXIDE; CARBON MONOXIDE; CYCLIC GMP; MYOGLOBIN; NITRITE; NITRITE REDUCTASE; NITROPRUSSIDE SODIUM;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AORTA; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; VASCULAR RING; VASCULARIZATION; VASODILATATION; WILD TYPE;

ANIMALS; AORTA; CARBON MONOXIDE; DRUG INTERACTIONS; MALE; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOGLOBIN; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRITE REDUCTASES; NITRITES; NITROPRUSSIDE; VASODILATION;

EID: 79551487824     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvq299     Document Type: Article

References (36)

1. Dejam A, Hunter CJ, Tremonti C, Pluta RM, Hon YY, Grimes G et al. Nitrite infusion in humans and nonhuman primates: endocrine effects, pharmacokinetics, and tolerance formation. Circulation 2007;116:1821-1831.
2. Maher AR, Milsom AB, Gunaruwan P, Abozguia K, Ahmed I, Weaver RA et al. Hypoxic modulation of exogenous nitrite-induced vasodilation in humans. Circulation 2008;117:670-677.
3. Bryan NS, Calvert JW, Gundewar S, Lefer DJ. Dietary nitrite restores NO homeosta-sis and is cardioprotective in endothelial nitric oxide synthase-deficient mice. Free Radic Biol Med 2008;104:19144-19149.
4. Duranski MR, Greer JJ, Dejam A, Jaganmohan S, Hogg N, Langston W et al. Cytopro-tective effects of nitrite during in vivo ischemia-reperfusion of the heart and liver. J Clin Invest 2005;115:1232-1240.
5. Shiva S, Sack MN, Greer JJ, Duranski M, Ringwood LA, Burwell L et al. Nitrite augments tolerance to ischemia/reperfusion injury via the modulation of mitochondrial electron transfer. J Exp Med 2007;204:2089-2102.
6. Webb A, Bond R, McLean P, Uppal R, Benjamin N, Ahluwalia A. Reduction of nitrite to nitric oxide during ischemia protects against myocardial ischemia-reperfusion damage. Proc Natl Acad Sci USA 2004;101:13683-13688.
7. Zweier JL, Wang P, Samouilov A, Kuppusamy P. Enzyme-independent formation of nitric oxide in biological tissues. Nat Med 1995;1:804-809.
8. Feelisch M, Fernandez BO, Bryan NS, Garcia-Saura MF, Bauer S, Whitlock DR et al. Tissue processing of nitrite in hypoxia: an intricate interplay of nitric oxide-generating and -scavenging systems. J Biol Chem 2008;283:33927-33934.
9. Kozlov AV, Staniek K, Nohl H. Nitrite reductase activity is a novel function of mammalian mitochondria. FEBS Lett 1999;454:127-130.
10. Li H, Cui H, Kundu TK, Alzawahra W, Zweier JL. Nitric oxide production from nitrite occurs primarily in tissues not in the blood: critical role of xanthine oxidase and aldehyde oxidase. J Biol Chem 2008;283:17855-17863.
11. Petersen MG, Dewilde S, Fago A. Reactions of ferrous neuroglobin and cytoglobin with nitrite under anaerobic conditions. J Inorg Biochem 2008;102:1777-1782.
12. Basu S, Grubina R, Huang J, Conradie J, Huang Z, Jeffers A et al. Catalytic generation of N2O3 by the concerted nitrite reductase and anhydrase activity of hemoglobin. Nat Chem Biol 2007;3:785-794.
13. Cosby K, Partovi KS, Crawford JH, Patel RP, Reiter CD, Martyr S et al. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med 2003;9:1498-1505.
14. Crawford JH, Isbell TS, Huang Z, Shiva S, Chacko BK, Schechter AN et al. Hypoxia, red blood cells, and nitrite regulate NO-dependent hypoxic vasodilation. Blood 2006; 107:566-574.
15. Grubina R, Huang Z, Shiva S, Joshi MS, Azarov I, Basu S et al. Concerted nitric oxide formation and release from the simultaneous reactions of nitrite with deoxy- and oxyhemoglobin. J Biol Chem 2007;282:12916-12927.
16. Huang KT, Keszler A, Patel N, Patel RP, Gladwin MT, Kim-Shapiro DB et al. The reaction between nitrite and deoxyhemoglobin. Reassessment of reaction kinetics and stoichiometry. J Biol Chem 2005;280:31126-31131.
17. Isbell TS, Gladwin MT, Patel RP. Hemoglobin oxygen fractional saturation regulates nitrite-dependent vasodilation of aortic ring bioassays. Am J Physiol Heart Circ Physiol 2007;293:2565-2572.
18. Lundberg JO, Weitzberg E, Gladwin MT. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov 2008;7:156-167.
19. Shiva S, Huang Z, Grubina R, Sun J, Ringwood LA, MacArthur PH et al. Deoxymyo-globin is a nitrite reductase that generates nitric oxide and regulates mitochondrial respiration. Circ Res 2007;100:654-661.
20. Hendgen-Cotta UB, Merx MW, Shiva S, Schmitz J, Becher S, Klare JP et al. Nitrite reductase activity of myoglobin regulates respiration and cellular viability in myocar-dial ischemia-reperfusion injury. Proc Natl Acad Sci USA 2008;105:10256-10261.
21. Alzawahra WF, Talukder MAH, Liu XP, Samouilov A, Zweier JL. Heme proteins mediate the conversion of nitrite to nitric oxide in the vascular wall. Am J Physiol Heart Circ Physiol 2008;295:H499-H508.
22. Bryan NS, Fernandez BO, Bauer SM, Garcia-Saura MF, Milsom AB, Rassaf T et al. Nitrite is a signaling molecule and regulator of gene expression in mammalian tissues. Nat Chem Biol 2005;1:290-297.
23. Wunderlich C, Flogel U, Godecke A, Heger J, Schrader J. Acute inhibition of myoglo-bin impairs contractility and energy state of iNOS-overexpressing hearts. Circ Res 2003;92:1352-1358.
24. Godecke A, Flogel U, Zanger K, Ding Z, Hirchenhain J, Decking UK et al. Disruption of myoglobin in mice induces multiple compensatory mechanisms. Proc Natl Acad Sci USA 1999;96:10495-10500.
25. Diesen DL, Hess DT, Stamler JS. Hypoxic vasodilation by red blood cells. Evidence for an S-nitrosothiol-based signal. Circ Res 2008;103:545-553.
26. Gladwin MT, Shelhamer JH, Schechter AN, Pease-Fye ME, Waclawiw MA, Panza JA et al. Role of circulating nitrite and S-nitrosohemoglobin in the regulation of regional blood flow in humans. Proc Natl Acad Sci USA 2000;97:11482-11487.
27. Gladwin MT, Kim-Shapiro DB. The functional nitrite reductase activity of the heme-globins. Blood 2008;112:2636-2647.
28. Dalsgaard T, Simonsen U, Fago A. Nitrite-dependent vasodilation is facilitated by hypoxia and is independent of known NO-generating nitrite reductase activities. Am J Physiol Heart Circ Physiol 2007;292:H3072-H3078.
29. Bryan NS, Rassaf T, Maloney RE, Rodriguez CM, Saijo F, Rodriguez JR et al. Cellular targets and mechanisms of nitros(yl)ation: an insight into their nature and kinetics in vivo. Proc Natl Acad Sci USA 2004;101:4308-4313.
30. Rodriguez J, Maloney RE, Rassaf T, Bryan NS, Feelisch M. Chemical nature of nitric oxide storage forms in rat vascular tissue. Proc Natl Acad Sci USA 2003;100:336-341.
31. Brunori M. Nitric oxide, cytochrome-c oxidase and myoglobin. Trends Biochem Sci 2001;26:21-23. (Pubitemid 32124705)
32. Lauer T, Preik M, Rassaf T, Strauer BE, Deussen A, Feelisch M et al. Plasma nitrite rather than nitrate reflects regional endothelial nitric oxide synthase activity but lacks intrinsic vasodilator action. Proc Natl Acad Sci USA 2001;98:12814-12819.
33. Rassaf T, Bryan NS, Maloney RE, Specian V, Kelm M, Kalyanaraman B et al. NO adducts in mammalian red blood cells: too much or too little? Nat Med 2003;9: 481-482.
34. Benamar A, Rolletschek H, Borisjuk L, Velange-Macherel MH, Curien G, Mostefai HA et al. Nitrite-nitric oxide control of mitochondrial respiration at the frontier of anoxia. Biochim Biophys Acta 2008;1777:1268-1275.
35. Gonzalez FM, Shiva S, Vincent PS, Ringwood LA, Hsu LY, Hon YY et al. Nitrite anion provides potent cytoprotective and antiapoptotic effects as adjunctive therapy to reperfusion for acute myocardial infarction. Circulation 2008;117:2986-2994.
36. Kaelin WG Jr, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 2008;30:393-402.