Nitrite enhances RBC hypoxic ATP synthesis and the release of ATP into the vasculature: A new mechanism for nitrite-induced vasodilation

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 297, Issue 4, 2009, Pages

  Cao, Zeling ^a   Bell, Jeffrey B ^a   Mohanty, Joy G ^a   Nagababu, Enika ^a   Rifkind, Joseph M ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Adenosine 5 triphosphate; Anerobic glycolysis; Hypoxia; Nitric oxide; Nitrite reduction; Red blood cell

Indexed keywords

ADENOSINE TRIPHOSPHATE; APYRASE; DEOXYHEMOGLOBIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLYCOLYTIC ENZYME; HEMOGLOBIN; N(G) NITROARGININE METHYL ESTER; NITRITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; ERYTHROCYTE COUNT; HEART MUSCLE ISCHEMIA; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN SYNTHESIS; RAT; VASCULARIZATION; VASODILATATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; APYRASE; BLOOD PRESSURE; CELL HYPOXIA; ENZYME INHIBITORS; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; HEMOGLOBINS; HYDROLYSIS; INJECTIONS, INTRAVENOUS; MALE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; NITRITES; RATS; RATS, WISTAR; TIME FACTORS; VASODILATION;

EID: 70349610358     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01233.2008     Document Type: Article

References (53)

1. Basu S, Grubina R, Huang J, Conradie J, Huang Z, Jeffers A, Jiang A, He X, Azarov I, Seibert R, Mehta A, Patel R, King SB, Hogg N, Ghosh A, Gladwin MT, Kim-Shapiro DB. Catalytic generation of N2O3 by the concerted nitrite reductase and anhydrase activity of hemoglobin. Nat Chem Biol 3: 785-794, 2007. (Pubitemid 350126874)
2. Bergfeld GR, Forrester T. Release of ATP from human erythrocytes in response to a brief period of hypoxia and hypercapnia. Cardiovasc Res 26: 40-47, 1992.
3. Blood AB, Power GG. In vitro and in vivo kinetic handling of nitrite in blood: effects of varying hemoglobin oxygen saturation. Am J Physiol Heart Circ Physiol 293: H1508-H1517, 2007.
4. Boland B, Himpens B, Vincent MF, Gillis JM, Casteels R. ATP activates P2x-contracting and P2y-relaxing purinoceptors in the smooth muscle of mouse vas deferens. Br J Pharmacol 107: 1152-1158, 1992.
5. Campanella ME, Chu H, Low PS. Assembly and regulation of a glycolytic enzyme complex on the human erythrocyte membrane. Proc Natl Acad Sci USA 102: 2402-2407, 2005. (Pubitemid 40279388)
6. Chetrite G, Cassoly R. Affinity of hemoglobin for the cytoplasmic fragment of human erythrocyte membrane band 3. Equilibrium measurements at physiological pH using matrix-bound proteins: the effects of ionic strength, deoxygenation and of 2,3-diphosphoglycerate. J Mol Biol 185: 639-644, 1985. (Pubitemid 15241169)
7. Clementi ME, Giardina B, Colucci D, Galtieri A, Misiti F. Amyloidbeta peptide affects the oxygen dependence of erythrocyte metabolism: a role for caspase 3. Int J Biochem Cell Biol 39: 727-735, 2007. (Pubitemid 46389495)
8. Cosby K, Partovi KS, Crawford JH, Patel RP, Reiter CD, Martyr S, Yang BK, Waclawiw MA, Zalos G, Xu X, Huang KT, Shields H, Kim-Shapiro DB, Schechter AN, Cannon RO III, Gladwin MT. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med 9: 1498-1505, 2003. (Pubitemid 38004777)
9. Crawford JH, Isbell TS, Huang Z, Shiva S, Chacko BK, Schechter AN, Darley-Usmar VM, Kerby JD, Lang JD Jr, Kraus D, Ho C, Gladwin MT, Patel RP. Hypoxia, red blood cells, and nitrite regulate NO-dependent hypoxic vasodilation. Blood 107: 566-574, 2006. (Pubitemid 43076380)
10. Dietrich HH, Ellsworth ML, Sprague RS, Dacey RG Jr. Red blood cell regulation of microvascular tone through adenosine triphosphate. Am J Physiol Heart Circ Physiol 278: H1294-H1298, 2000.
11. Doyle MP, Hoekstra JW. Oxidation of nitrogen oxides by bound dioxygen in hemoproteins. J Inorg Biochem 14: 351-358, 1981.
12. Duranski MR, Greer JJ, Dejam A, Jaganmohan S, Hogg N, Langston W, Patel RP, Yet SF, Wang X, Kevil CG, Gladwin MT, Lefer DJ. Cytoprotective effects of nitrite during in vivo ischemia-reperfusion of the heart and liver. J Clin Invest 115: 1232-1240, 2005. (Pubitemid 40629041)
13. Eich RF, Li T, Lemon DD, Doherty DH, Curry SR, Aitken JF, Mathews AJ, Johnson KA, Smith RD, Phillips GN Jr, Olson JS. Mechanism of NO-induced oxidation of myoglobin and hemoglobin. Biochemistry 35: 6976-6983, 1996. (Pubitemid 26182085)
14. 2-purinergic receptors. Proc Natl Acad Sci USA 84: 5630-5634, 1987.
15. +)-ATPase and band 3 protein. Biochim Biophys Acta 649: 557-571, 1981.
16. Gladwin MT, Crawford JH, Patel RP. The biochemistry of nitric oxide, nitrite, and hemoglobin: role in blood flow regulation. Free Radic Biol Med 36: 707-717, 2004. (Pubitemid 38264415)
17. Hoffman JF. ATP compartmentation in human erythrocytes. Curr Opin Hematol 4: 112-115, 1997.
18. Hsu LL, Champion HC, Campbell-Lee SA, Bivalacqua TJ, Manci EA, Diwan BA, Schimel DM, Cochard AE, Wang X, Schechter AN, Noguchi CT, Gladwin MT. Hemolysis in sickle cell mice causes pulmonary hypertension due to global impairment in nitric oxide bioavailability. Blood 109: 3088-3098, 2007. (Pubitemid 46482112)
19. Ignarro LJ. Nitric oxide as a unique signaling molecule in the vascular system: a historical overview. J Physiol Pharmacol 53: 503-514, 2002.
20. Ignarro LJ, Cirino G, Casini A, Napoli C. Nitric oxide as a signaling molecule in the vascular system: an overview. J Cardiovasc Pharmacol 34: 879-886, 1999.
21. 2 delivery mediated by hemoglobin oxygenation. Am J Physiol Heart Circ Physiol 280: H2833-H2839, 2001.
22. Jia L, Bonaventura C, Bonaventura J, Stamler JS. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 380: 221-226, 1996. (Pubitemid 26090643)
23. Keszler A, Piknova B, Schechter AN, Hogg N. The reaction between nitrite and oxyhemoglobin: a mechanistic study. J Biol Chem 283: 9615-9622, 2008.
24. Kim-Shapiro DB, Schechter AN, Gladwin MT. Unraveling the reactions of nitric oxide, nitrite, and hemoglobin in physiology and therapeutics. Arterioscler Thromb Vasc Biol 26: 697-705, 2006.
25. Kleinbongard P, Dejam A, Lauer T, Rassaf T, Schindler A, Picker O, Scheeren T, Godecke A, Schrader J, Schulz R, Heusch G, Schaub GA, Bryan NS, Feelisch M, Kelm M. Plasma nitrite reflects constitutive nitric oxide synthase activity in mammals. Free Radic Biol Med 35: 790-796, 2003. (Pubitemid 37329482)
26. Kleinbongard P, Keymel S, Kelm M. New functional aspects of the L-arginine-nitric oxide metabolism within the circulating blood. Thromb Haemost 98: 970-974, 2007. (Pubitemid 350091124)
27. Mandal D, Baudin-Creuza V, Bhattacharyya A, Pathak S, Delaunay J, Kundu M, Basu J. Caspase 3-mediated proteolysis of the N-terminal cytoplasmic domain of the human erythroid anion exchanger 1 (band 3). J Biol Chem 278: 52551-52558, 2003. (Pubitemid 38035851)
28. Mandel P, Chambon P, Karon H, Kulic I, Serter M. Free nucleotides in red blood cells and reticulocytes. [In French.] Folia Haematol Int Mag Klin Morphol Blutforsch 78: 525-543, 1962.
29. Matsumoto T, Nakane T, Chiba S. Pharmacological analysis of responses to ATP in the isolated and perfused canine coronary artery. Eur J Pharmacol 334: 173-180, 1997. (Pubitemid 27451986)
30. 2-linked transition of hemoglobin. FEBS Lett 390: 25-28, 1996.
31. Misiti F, Orsini F, Clementi ME, Masala D, Tellone E, Galtieri A, Giardina B. Amyloid peptide inhibits ATP release from human erythrocytes. Biochem Cell Biol 86: 501-508, 2008.
32. Motte S, Pirotton S, Boeynaems JM. Heterogeneity of ATP receptors in aortic endothelial cells. Involvement of P2y and P2u receptors in inositol phosphate response. Circ Res 72: 504-510, 1993. (Pubitemid 23052148)
33. Nagababu E, Ramasamy S, Abernethy DR, Rifkind JM. Active nitric oxide produced in the red cell under hypoxic conditions by deoxyhemoglobin-mediated nitrite reduction. J Biol Chem 278: 46349-46356, 2003. (Pubitemid 37452205)
34. Nagababu E, Ramasamy S, Rifkind JM. S-nitrosohemoglobin: a mechanism for its formation in conjunction with nitrite reduction by deoxyhemoglobin. Nitric Oxide 15: 20-29, 2006.
35. Nagababu E, Ramasamy S, Rifkind JM. Intermediates detected by visible spectroscopy during the reaction of nitrite with deoxyhemoglobin: the effect of nitrite concentration and diphosphoglycerate. Biochemistry 46: 11650-11659, 2007. (Pubitemid 47585511)
36. Nagababu E, Rifkind JM. Measurement of plasma nitrite by chemiluminescence without interference of S-, N-nitroso and nitrated species. Free Radic Biol Med 42: 1146-1154, 2007. (Pubitemid 46428509)
37. Olearczyk JJ, Ellsworth ML, Stephenson AH, Lonigro AJ, Sprague RS. Nitric oxide inhibits ATP release from erythrocytes. J Pharmacol Exp Ther 309: 1079-1084, 2004.
38. Olearczyk JJ, Stephenson AH, Lonigro AJ, Sprague RS. Heterotrimeric G protein Gi is involved in a signal transduction pathway for ATP release from erythrocytes. Am J Physiol Heart Circ Physiol 286: H940-H945, 2004.
39. Olearczyk JJ, Stephenson AH, Lonigro AJ, Sprague RS. NO inhibits signal transduction pathway for ATP release from erythrocytes via its action on heterotrimeric G protein Gi. Am J Physiol Heart Circ Physiol 287: H748-H754, 2004. (Pubitemid 38955308)
40. Pluta RM, Dejam A, Grimes G, Gladwin MT, Oldfield EH. Nitrite infusions to prevent delayed cerebral vasospasm in a primate model of subarachnoid hemorrhage. JAMA 293: 1477-1484, 2005. (Pubitemid 40393292)
41. Reisin IL, Prat AG, Abraham EH, Amara JF, Gregory RJ, Ausiello DA, Cantiello HF. The cystic fibrosis transmembrane conductance regulator is a dual ATP and chloride channel. J Biol Chem 269: 20584-20591, 1994. (Pubitemid 24260468)
42. Rifkind JM, Nagababu E, Barbiro-Michaely E, Ramasamy S, Pluta RM, Mayevsky A. Nitrite infusion increases cerebral blood flow and decreases mean arterial blood pressure in rats: a role for red cell NO. Nitric Oxide 16: 448-456, 2007.
43. Roy CS, Brown JG. The blood-pressure and its variations in the arterioles, capillaries and smaller veins. J Physiol 2: 323-446, 1880.
44. Salgado MT, Nagababu E, Rifkind JM. Quantification of intermediates formed during the reduction of nitrite by deoxyhemoglobin. J Biol Chem 284: 12710-12718, 2009.
45. Spagnuolo C, Rinelli P, Coletta M, Chiancone E, Ascoli F. Oxidation reaction of human oxyhemoglobin with nitrite: a reexamination. Biochim Biophys Acta 911: 59-65, 1987.
46. Sprague RS, Bowles EA, Olearczyk JJ, Stephenson AH, Lonigro AJ. The role of G protein beta subunits in the release of ATP from human erythrocytes. J Physiol Pharmacol 53: 667-674, 2002.
47. Sprague RS, Ellsworth ML, Stephenson AH, Kleinhenz ME, Lonigro AJ. Deformation-induced ATP release from red blood cells requires CFTR activity. Am J Physiol Heart Circ Physiol 275: H1726-H1732, 1998.
48. Sprague RS, Ellsworth ML, Stephenson AH, Lonigro AJ. Participation of cAMP in a signal-transduction pathway relating erythrocyte deformation to ATP release. Am J Physiol Cell Physiol 281: C1158-C1164, 2001. (Pubitemid 32948102)
49. Sprague RS, Ellsworth ML, Stephenson AH, Lonigro AJ. ATP: the red blood cell link to NO and local control of the pulmonary circulation. Am J Physiol Heart Circ Physiol 271: H2717-H2722, 1996.
50. Sprague RS, Olearczyk JJ, Spence DM, Stephenson AH, Sprung RW, Lonigro AJ. Extracellular ATP signaling in the rabbit lung: erythrocytes as determinants of vascular resistance. Am J Physiol Heart Circ Physiol 285: H693-H700, 2003.
51. Tsai IH, Murthy SN, Steck TL. Effect of red cell membrane binding on the catalytic activity of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 257: 1438-1442, 1982.
52. Walder JA, Chatterjee R, Steck TL, Low PS, Musso GF, Kaiser ET, Rogers PH, Arnone A. The interaction of hemoglobin with the cytoplasmic domain of band 3 of the human erythrocyte membrane. J Biol Chem 259: 10238-10246, 1984. (Pubitemid 14065325)
53. Waugh SM, Low PS. Hemichrome binding to band 3: nucleation of Heinz bodies on the erythrocyte membrane. Biochemistry 24: 34-39, 1985.