Nitrite as a vascular endocrine nitric oxide reservoir that contributes to hypoxic signaling, cytoprotection, and vasodilation

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 291, Issue 5, 2006, Pages

  Gladwin, Mark T ^a,b   Raat, Nicolaas J H ^a,b   Shiva, Sruti ^a,b   Dezfulian, Cameron ^a,b,c   Hogg, Neil ^d   Kim Shapiro, Daniel B ^e   Patel, Rakesh P ^f  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c JOHNS HOPKINS HOSPITAL   (United States)

^d MEDICAL COLLEGE OF WISCONSIN   (United States)

^e WAKE FOREST UNIVERSITY   (United States)

^f University of Alabama at Birmingham   (United States)

Author keywords

Cysteine 93; Hemoglobin; Hypoxia; S nitrosated albumin

Indexed keywords

HEMOGLOBIN; NITRIC OXIDE; NITRITE; NITRITE REDUCTASE;

CELL PROTECTION; CIRCULATION; HEART INFARCTION; HUMAN; ISCHEMIA; NONHUMAN; PRIORITY JOURNAL; REPERFUSION; REVIEW; VASODILATATION;

ANIMALS; CELL HYPOXIA; CYTOPROTECTION; ENDOCRINE SYSTEM; HEMOGLOBINS; HUMANS; MODELS, BIOLOGICAL; NITRIC OXIDE; NITRITES; VASODILATION;

EID: 33751198519     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00407.2006     Document Type: Review

References (103)

1. Azarov I, Huang KT, Basu S, Gladwin MT, Hogg N, and Kim-Shapiro DB. Nitric oxide scavenging by red blood cells as a function of hematocrit and oxygenation. J Biol Chem 280: 39024-39032, 2005.
2. Baker PR, Lin Y, Schopfer FJ, Woodcock SR, Groeger AL, Batthyany C, Sweeney S, Long MH, Iles KE, Baker LM, Branchaud BP, Chen YE, and Freeman BA. Fatty acid transduction of nitric oxide signaling: multiple nitrated unsaturated fatty acid derivatives exist in human blood and urine and serve as endogenous peroxisome proliferatoractivated receptor ligands. J Biol Chem 280: 42464-42475, 2005.
3. Basireddy M, Isbell TS, Teng X, Patel RP, and Agarwal A. Effects of sodium nitrite on ischemia-reperfusion injury in the rat kidney. Am J Physiol Renal Physiol 290: F779-F786, 2006.
4. Beier S, Classen HG, Loeffler K, Schumacher E, and Thoni H. Antihypertensive effect of oral nitrite uptake in the spontaneously hypertensive rat. Arzneimittelforschung 45: 258-261, 1995.
5. Bjorne HH, Petersson J, Phillipson M, Weitzberg E, Holm L, and Lundberg JO. Nitrite in saliva increases gastric mucosal blood flow and mucus thickness. J Clin Invest 113: 106-114, 2004.
6. Bonaventura C, Ferruzzi G, Tesh S, and Stevens RD. Effects of S-nitrosation on oxygen binding by normal and sickle cell hemoglobin. J Biol Chem 274: 24742-24748, 1999.
7. Brooks J. The action of nitrite on haemoglobin in the absence of oxygen. Proc R Soc Med 123: 368-382, 1937.
8. Bryan NS, Fernandez FO, Bauer SM, Garcia-Saura MF, Milsom AB, Rassaf T, Maloney RE, Bharti A, Rodriguez JR, and Feelisch M. Nitrite is a signaling molecule and regulator of gene expression in mammalian tissues. Nat Chem Biol 1: 290-297, 2005.
9. Cannon RO III, Schechter AN, Panza JA, Ognibene FP, Pease-Fye ME, Waclawiw MA, Shelhamer JH, and Gladwin MT. Effects of inhaled nitric oxide on regional blood flow are consistent with intravascular nitric oxide delivery. J Clin Invest 108: 279-287, 2001.
10. 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, and Gladwin MT. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med 9: 1498-1505, 2003.
11. Crawford JH, Chacko BK, Pruitt HM, Piknova B, Hogg N, and Patel RP. Transduction of NO-bioactivity by the red blood cell in sepsis: novel mechanisms of vasodilation during acute inflammatory disease. Blood 104: 1375-1382, 2004.
12. 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, and Patel RP. Hypoxia, red blood cells, and nitrite regulate NO-dependent hypoxic vasodilation. Blood 107: 566-574, 2006.
13. Crawford JH, White CR, and Patel RP. Vasoactivity of S-nitrosohemoglobin: role of oxygen, heme, and NO oxidation states. Blood 101: 4408-4415, 2003.
14. Deem S, Kim JU, Manjula BN, Acharya AS, Kerr ME, Patel RP, Gladwin MT, and Swenson ER. Effects of S-nitrosation and crosslinking of hemoglobin on hypoxic pulmonary vasoconstriction in isolated rat lungs. Circ Res 91: 626-632, 2002.
15. Dejam A, Kleinbongard P, Rassaf T, Hamada S, Gharini P, Rodriguez J, Feelisch M, and Kelm M. Thiols enhance NO formation from nitrate photolysis. Free Radic Biol Med 35: 1551-1559, 2003.
16. Dietrich HH, Ellsworth ML, Sprague RS, and Dacey RG Jr. Red blood cell regulation of microvascular tone through adenosine triphosphate. Am J Physiol Heart Circ Physiol 278: H1294-H1298, 2000.
17. Doyle MP, Pickering RA, DeWeert TM, Hoekstra JW, and Pater D. Kinetics and mechanism of the oxidation of human deoxyhemoglobin by nitrites. J Biol Chem 256: 12393-12398, 1981.
18. Duranski MR, Greer JJ, Dejam A, Jaganmohan S, Hogg N, Langston W, Patel RP, Yet SF, Wang X, Kevil CG, Gladwin MT, and Lefer DJ. Cytoprotective effects of nitrite during in vivo ischemiareperfusion of the heart and liver. J Clin Invest 115: 1232-1240, 2005.
19. Ellsworth ML, Forrester T, Ellis CG, and Dietrich HH. The erythrocyte as a regulator of vascular tone. Am J Physiol Heart Circ Physiol 269: H2155-H2161, 1995.
20. Fox-Robichaud A, Payne D, Hasan SU, Ostrovsky L, Fairhead T, Reinhardt P, and Kubes P. Inhaled NO as a viable antiadhesive therapy for ischemia/reperfusion injury of distal microvascular beds. J Clin Invest 101: 2497-2505, 1998.
21. Furchgott RF and Bhadrakom S. Reactions of strips of rabbit aorta to epinephrine, isopropylarterenol, sodium nitrite and other drugs. J Pharmacol Exp Ther 108: 129-143, 1953.
22. Furchgott RF and Zawadzki JV. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288: 373-376, 1980.
23. Gladwin MT. Nitrite as an intrinsic signaling molecule. Nat Chem Biol 1: 245-246, 2005.
24. Gladwin MT, Crawford JH, and Patel RP. The biochemistry of nitric oxide, nitrite, and hemoglobin: role in blood flow regulation. Free Radic Biol Med 36: 707-717, 2004.
25. Gladwin MT, Lancaster JR, Freeman BA, and Schechter AN. Nitric oxide's reactions with hemoglobin: a view through the SNO-storm. Nat Med 9: 496-500, 2003.
26. Gladwin MT, Ognibene FP, Pannell LK, Nichols JS, Pease-Fye ME, Shelhamer JH, and Schechter AN. Relative role of heme nitrosylation and beta-cysteine 93 nitrosation in the transport and metabolism of nitric oxide by hemoglobin in the human circulation. Proc Natl Acad Sci USA 97: 9943-9948, 2000.
27. Gladwin MT and Schechter AN. NO contest: nitrite versus S-nitrosohemoglobin. Circ Res 94: 851-855, 2004.
28. Gladwin MT, Schechter AN, Kim-Shapiro DB, Patel RP, Hogg N, Shiva S, Cannon RO III, Kelm M, Wink DA, Espey MG, Oldfield EH, Pluta RM, Freeman BA, Lancaster JR Jr, Feelisch M, and Lundberg JO. The emerging biology of the nitrite anion. Nat Chem Biol 1: 308-314, 2005.
29. Gladwin MT, Shelhamer JH, Schechter AN, Pease-Fye ME, Waclawiw MA, Panza JA, Ognibene FP, and Cannon RO III. Role of circulating nitrite and S-nitrosohemoglobin in the regulation of regional blood flow in humans. Proc Natl Acad Sci USA 97: 11482-11487, 2000.
30. 2/NO-linked allosteric function. J Biol Chem 277: 27818-27828, 2002.
31. Godber BL, Doel JJ, Sapkota GP, Blake DR, Stevens CR, Eisenthal R, and Harrison R. Reduction of nitrite to nitric oxide catalyzed by xanthine oxidoreductase. J Biol Chem 275: 7757-7763, 2000.
32. Gonzalez-Alonso J, Olsen DB, and Saltin B. Erythrocyte and the regulation of human skeletal muscle blood flow and oxygen delivery: role of circulating ATP. Circ Res 91: 1046-1055, 2002.
33. Gow AJ, Luchsinger BP, Pawloski JR, Singel DJ, and Stamler JS. The oxyhemoglobin reaction of nitric oxide. Proc Natl Acad Sci USA 96: 9027-9032, 1999.
34. Gow AJ and Stamler JS. Reactions between nitric oxide and haemoglobin under physiological conditions. Nature 391: 169-173, 1998.
35. Gruetter CA, Barry BK, McNamara DB, Kadowitz PJ, and Ignarro LJ. Coronary arterial relaxation and guanylate cyclase activation by cigarette smoke, N′-nitrosonornicotine and nitric oxide. J Pharmacol Exp Ther 214: 9-15, 1980.
36. Hataishi R, Rodrigues AC, Neilan TG, Morgan JG, Buys E, Sruti S, Tambouret R, Jassal DS, Raher MJ, Furutani E, Ichinose F, Gladwin MT, Rosenzweig A, Zapol WM, Picard MH, Bloch KD, and Scherrer-Crosbie M. Inhaled nitric oxide decreases infarction size and improves left ventricular function in a murine model of myocardial ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 291: H379-H384, 2006.
37. Huang KT, Azarov I, Basu S, Huang J, and Kim-Shapiro DB. Lack of allosterically controlled intramolecular transfer of nitric oxide from the heme to cysteine in the beta subunit of hemoglobin. Blood 107: 2602-2604, 2006.
38. Huang KT, Han TH, Hyduke DR, Vaughn MW, Van Herle H, Hein TW, Zhang C, Kuo L, and Liao JC. Modulation of nitric oxide bioavailability by erythrocytes. Proc Natl Acad Sci USA 98: 11771-11776, 2001.
39. Huang KT, Keszler A, Patel N, Patel RP, Gladwin MT, Kim-Shapiro DB, and Hogg N. The reaction between nitrite and deoxyhemoglobin. Reassessment of reaction kinetics and stoichiometry. J Biol Chem 280: 31126-31131, 2005.
40. Huang Z, Louderback JG, Goyal M, Azizi F, King SB, and Kim-Shapiro DB. Nitric oxide binding to oxygenated hemoglobin under physiological conditions. Biochim Biophys Acta 1568: 252-260, 2001.
41. Huang Z, Shiva S, Kim-Shapiro DB, Patel RP, Ringwood LA, Irby CE, Huang KT, Ho C, Hogg N, Schechter AN, and Gladwin MT. Enzymatic function of hemoglobin as a nitrite reductase that produces NO under allosteric control. J Clin Invest 115: 2099-2107, 2005.
42. Huang Z, Ucer KB, Murphy T, Williams RT, King SB, and Kim-Shapiro DB. Kinetics of nitric oxide binding to R-state hemoglobin. Biochem Biophys Res Commun 292: 812-818, 2002.
43. Hunter CJ, Dejam A, Blood AB, Shields H, Kim-Shapiro DB, Machado RF, Tarekegn S, Mulla N, Hopper AO, Schechter AN, Power GG, and Gladwin MT. Inhaled nebulized nitrite is a hypoxia-sensitive NO-dependent selective pulmonary vasodilator. Nat Med 10: 1122-1127, 2004.
44. Ignarro LJ, Buga GM, Wood KS, Byrns RE, and Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 84: 9265-9269, 1987.
45. Ignarro LJ, Byrns RE, Buga GM, and Wood KS. Endotheliumderived relaxing factor from pulmonary artery and vein possesses pharmacologic and chemical properties identical to those of nitric oxide radical. Circ Res 61: 866-879, 1987.
46. Ignarro LJ and Gruetter CA. Requirement of thiols for activation of coronary arterial guanylate cyclase by glyceryl trinitrate and sodium nitrite: possible involvement of S-nitrosothiols. Biochim Biophys Acta 631: 221-231, 1980.
47. Ignarro LJ, Lippton H, Edwards JC, Baricos WH, Hyman AL, Kadowitz PJ, and Gruetter CA. Mechanism of vascular smooth muscle relaxation by organic nitrates, nitrites, nitroprusside and nitric oxide: evidence for the involvement of S-nitrosothiols as active intermediates. J Pharmacol Exp Ther 218: 739-749, 1981.
48. 2 delivery mediated by hemoglobin oxygenation. Am J Physiol Heart Circ Physiol 280: H2833-H2839, 2001.
49. Jensen FB and Agnisola C. Perfusion of the isolated trout heart coronary circulation with red blood cells: effects of oxygen supply and nitrite on coronary flow and myocardial oxygen consumption. J Exp Biol 208: 3665-3674, 2005.
50. Jia L, Bonaventura C, Bonaventura J, and Stamler JS. S- nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 380: 221-226, 1996.
51. Joshi MS, Ferguson TB Jr, Han TH, Hyduke DR, Liao JC, Rassaf T, Bryan N, Feelisch M, and Lancaster JR Jr. Nitric oxide is consumed, rather than conserved, by reaction with oxyhemoglobin under physiological conditions. Proc Natl Acad Sci USA 99: 10341-10346, 2002.
52. Kavdia M and Popel AS. Venular endothelium-derived NO can affect paired arteriole: a computational model. Am J Physiol Heart Circ Physiol 290: H716-H723, 2006.
53. Kim-Shapiro DB. Hemoglobin-nitric oxide cooperativity: is NO the third respiratory ligand? Free Radic Biol Med 36: 402-412, 2004.
54. Kim-Shapiro DB, Schechter AN, and Gladwin MT. Unraveling the reactions of nitric oxide, nitrite, and hemoglobin in physiology and therapeutics. Arterioscler Thromb Vasc Biol 26: 697-705, 2006.
55. Kozlov AV, Costantino G, Sobhian B, Szalay L, Umar F, Nohl H, Bahrami S, and Redl H. Mechanisms of vasodilatation induced by nitrite instillation in intestinal lumen: possible role of hemoglobin. Antioxid Redox Signal 7: 515-521, 2005.
56. Kubes P, Payne D, Grisham MB, Jourd-Heuil D, and Fox-Robichaud A. Inhaled NO impacts vascular but not extravascular compartments in postischemic peripheral organs. Am J Physiol Heart Circ Physiol 277: H676-H682, 1999.
57. Lauer T, Preik M, Rassaf T, Strauer BE, Deussen A, Feelisch M, and Kelm M. Plasma nitrite rather than nitrate reflects regional endothelial nitric oxide synthase activity but lacks intrinsic vasodilator action. Proc Natl Acad Sci USA 98: 12814-12819, 2001.
58. Lim DG, Sweeney S, Bloodsworth A, White CR, Chumley PH, Krishna NR, Schopfer F, O'Donnell VB, Eiserich JP, and Freeman BA. Nitrolinoleate, a nitric oxide-derived mediator of cell function: synthesis, characterization, and vasomotor activity. Proc Natl Acad Sci USA 99: 15941-15946, 2002.
59. Lippton HL, Gruetter CA, Ignarro LJ, Meyer RL, and Kadowitz PJ. Vasodilator actions of several N-nitroso compounds. Can J Physiol Pharmacol 60: 68-75, 1982.
60. Lundberg JON, Weitzberg E, Lundberg JM, and Alving K. Intragastric nitric oxide production in humans: measurements in expelled air. Gut 35: 1543-1546, 1994.
61. McMahon TJ. Hemoglobin and nitric oxide. N Engl J Med 349: 402-405, 2003.
62. Millar TM, Stevens CR, Benjamin N, Eisenthal R, Harrison R, and Blake DR. Xanthine oxidoreductase catalyses the reduction of nitrates and nitrite to nitric oxide under hypoxic conditions. FEBS Lett 427: 225-228, 1998.
63. Mittal CK, Arnold WP, and Murad F. Characterization of protein inhibitors of guanylate cyclase activation from rat heart and bovine lung. J Biol Chem 253: 1266-1271, 1978.
64. Modin A, Bjorne H, Herulf M, Alving K, Weitzberg E, and Lundberg JO. Nitrite-derived nitric oxide: a possible mediator of 'acidic-metabolic' vasodilation. Acta Physiol Scand 171: 9-16, 2001.
65. Monod J, Wyman J, and Changeux JP. On the nature of allosteric transitions: a plausible model. J Mol Biol 12: 88-118, 1965.
66. Nagababu E, Ramasamy S, Abernethy DR, and Rifkind JM. Active nitric oxide produced in the red cell under hypoxic conditions by deoxyhemoglobin mediated nitrite reduction. J Biol Chem 278: 46439-46356, 2003.
67. Nagababu E, Ramasamy S, and Rifkind JM. S-nitrosohemoglobin: a mechanism for its formation in conjunction with nitrite reduction by deoxyhemoglobin. Nitric Oxide 15: 20-29, 2006.
68. Ng ES, Jourd'heuil D, McCord JM, Hernandez D, Yasui M, Knight D, and Kubes P. Enhanced S-nitroso-albumin formation from inhaled NO during ischemia/reperfusion. Circ Res 94: 559-565, 2004.
69. Okamoto M, Tsuchiya K, Kanematsu Y, Izawa Y, Yoshizumi M, Kagawa S, and Tamaki T. Nitrite-derived nitric oxide formation after ischemia-reperfusion injury in kidney. Am J Physiol Renal Physiol 288: F182-F187, 2005.
70. Olson JS, Foley EW, Rogge C, Tsai AL, Doyle MP, and Lemon DD. No scavenging and the hypertensive effect of hemoglobin-based blood substitutes. Free Radic Biol Med 36: 685-697, 2004.
71. Palmer RM, Ashton DS, and Moncada S. Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature 333: 664-666, 1988.
72. Palmer RM, Ferrige AG, and Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327: 524-526, 1987.
73. Patel RP, Hogg N, Spencer NY, Kalyanaraman B, Matalon S, and Darley-Usmar VM. Biochemical characterization of human S-nitrosohemoglobin. Effects on oxygen binding and transnitrosation. J Biol Chem 274: 15487-15492, 1999.
74. Pawloski JR. Hemoglobin and nitric oxide. N Engl J Med 349: 402-405, 2003.
75. Quezado ZM, Natanson C, Karzai W, Danner RL, Koev CA, Fitz Y, Dolan DP, Richmond S, Banks SM, Wilson L, and Eichacker PQ. Cardiopulmonary effects of inhaled nitric oxide in normal dogs and during E. coli pneumonia and sepsis. J Appl Physiol 84: 107-115, 1998.
76. Rassaf T, Bryan NS, Kelm M, and Feelisch M. Concomitant presence of N-nitroso and S-nitroso proteins in human plasma. Free Radic Biol Med 33: 1590-1596, 2002.
77. Rassaf T, Bryan NS, Maloney RE, Specian V, Kelm M, Kalyanaraman B, Rodriguez J, and Feelisch M. NO adducts in mammalian red blood cells: too much or too little? Nat Med 9: 481-483, 2003.
78. Rassaf T, Preik M, Kleinbongard P, Lauer T, Heiss C, Strauer BE, Feelisch M, and Kelm M. Evidence for in vivo transport of bioactive nitric oxide in human plasma. J Clin Invest 109: 1241-1248, 2002.
79. Ross JM, Fairchild HM, Weldy J, and Guyton AC. Autoregulation of blood flow by oxygen lack. Am J Physiol 202: 21-24, 1962.
80. Roy CS and Brown JG. Blood pressure and its variations in the arterioles, capillaries, and smaller veins. J Physiol (Lond) 2: 323-359, 1879.
81. Scharfstein JS, Keaney JF Jr, Slivka A, Welch GN, Vita JA, Stamler JS, and Loscalzo J. In vivo transfer of nitric oxide between a plasma protein-bound reservoir and low molecular weight thiols. J Clin Invest 94: 1432-1439, 1994.
82. Schopfer FJ, Baker PR, Giles G, Chumley P, Batthyany C, Crawford J, Patel RP, Hogg N, Branchaud BP, Lancaster JR Jr, and Freeman BA. Fatty acid transduction of nitric oxide signaling Nitrolinoleic acid is a hydrophobically stabilized nitric oxide donor. J Biol Chem 280: 19289-19297, 2005.
83. Schopfer FJ, Lin Y, Baker PR, Cui T, Garcia-Barrio M, Zhang J, Chen K, Chen YE, and Freeman BA. Nitrolinoleic acid: an endogenous peroxisome proliferator-activated receptor gamma ligand. Proc Natl Acad Sci USA 102: 2340-2345, 2005.
84. Segal SS and Duling BR. Communication between feed arteries and microvessels in hamster striated muscle: segmental vascular responses are functionally coordinated. Circ Res 59: 283-290, 1986.
85. Segal SS and Duling BR. Conduction of vasomotor responses in arterioles: a role for cell-to-cell coupling? Am J Physiol Heart Circ Physiol 256: H838-H845, 1989.
86. Segal SS and Duling BR. Flow control among microvessels coordinated by intercellular conduction. Science 234: 868-870, 1986.
87. Stamler JS, Jaraki O, Osborne J, Simon DI, Keaney J, Vita J, Singel D, Valeri CR, and Loscalzo J. Nitric oxide circulates in mammalian plasma primarily as an S-nitroso adduct of serum albumin. Proc Natl Acad Sci USA 89: 7674-7677, 1992.
88. Stamler JS, Jia L, Eu JP, McMahon TJ, Demchenko IT, Bonaventura J, Gernert K, and Piantadosi CA. Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 276: 2034-2037, 1997.
89. Takahashi Y, Kobayashi H, Tanaka N, Sato T, Takizawa N, and Tomita T. Nitrosyl hemoglobin in blood of normoxic and hypoxic sheep during nitric oxide inhalation. Am J Physiol Heart Circ Physiol 274: H349-H357, 1998.
90. Troncy E, Francoeur M, Salazkin I, Yang F, Charbonneau M, Leclerc G, Vinay P, and Blaise G. Extra-pulmonary effects of inhaled nitric oxide in swine with and without phenylephrine. Br J Anaesth 79: 631-640, 1997.
91. Tsai AG, Johnson PC, and Intaglietta M. Oxygen gradients in the microcirculation. Physiol Rev 83: 933-963, 2003.
92. Tsuchiya K, Kanematsu Y, Yoshizumi M, Ohnishi H, Kirima K, Izawa Y, Shikishima M, Ishida T, Kondo S, Kagami S, Takiguchi Y, and Tamaki T. Nitrite is an alternative source of NO in vivo. Am J Physiol Heart Circ Physiol 288: H2163-H2170, 2005.
93. Tsuchiya K, Takiguchi Y, Okamoto M, Izawa Y, Kanematsu Y, Yoshizumi M, and Tamaki T. Malfunction of vascular control in lifestyle-related diseases: formation of systemic hemoglobin-nitric oxide complex (HbNO) from dietary nitrite. J Pharm Sci 96: 395-400, 2004.
94. Tune JD, Gorman MW, and Feigl EO. Matching coronary blood flow to myocardial oxygen consumption. J Appl Physiol 97: 404-415, 2004.
95. + channels, nitric oxide, and adenosine are not required for local metabolic coronary vasodilation. Am J Physiol Heart Circ Physiol 280: H868-H875, 2001.
96. Wang X, Tanus-Santos JE, Reiter CD, Dejam A, Shiva S, Smith RD, Hogg N, and Gladwin MT. Biological activity of nitric oxide in the plasmatic compartment. Proc Natl Acad Sci USA 101: 11477-11482, 2004.
97. Webb A, Bond R, McLean P, Uppal R, Benjamin N, and Ahluwalia A. Reduction of nitrite to nitric oxide during ischemia protects against myocardial ischemia-reperfusion damage. Proc Natl Acad Sci USA 101: 13683-13688, 2004.
98. Weiss S, Wilkins RW, and Haynes FW. The nature of circulatory collapse induced by sodium nitrite. J Clin Invest 16: 73-84, 1937.
99. Xu X, Cho M, Spencer NY, Patel N, Huang Z, Shields H, King SB, Gladwin MT, Hogg N, and Kim-Shapiro DB. Measurements of nitric oxide on the heme iron and beta-93 thiol of human hemoglobin during cycles of oxygenation and deoxygenation. Proc Natl Acad Sci USA 100: 11303-11308, 2003.
100. Zhang Y and Hogg N. Mixing artifacts from the bolus addition of nitric oxide to oxymyoglobin: implications for S-nitrosothiol formation. Free Radic Biol Med 32: 1212-1219, 2002.
101. Zuzak KJ, Gladwin MT, Cannon RO III, and Levin IW. Imaging hemoglobin oxygen saturation in sickle cell disease patients using noninvasive visible reflectance hyperspectral techniques: effects of nitric oxide. Am J Physiol Heart Circ Physiol 285: H1183-H1189, 2003.
102. Zuzak KJ, Schaeberle MD, Gladwin MT, Cannon RO III, and Levin IW. Noninvasive determination of spatially resolved and time-resolved tissue perfusion in humans during nitric oxide inhibition and inhalation by use of a visible-reflectance hyperspectral imaging technique. Circulation 104: 2905-2910, 2001.
103. Zweier JL, Wang P, Samouilov A, and Kuppusamy P. Enzyme-independent formation of nitric oxide in biological tissues. Nat Med 1: 804-809, 1995.