Critical redox and allosteric aspects of nitric oxide interactions with hemoglobin

Antioxidants and Redox Signaling

Volumn 6, Issue 6, 2004, Pages 979-991

  Bonaventura, Celia ^a   Fago, Angela ^b   Henkens, Robert ^a   Crumbliss, Alvin L ^c  

^a DUKE UNIVERSITY MARINE LABORATORY   (United States)

^b AARHUS UNIVERSITY   (Denmark)

^c DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FERRIC ION; FERROUS ION; HEME; HEMOGLOBIN; IRON; NITRIC OXIDE; SULFUR;

ALLOSTERISM; BINDING AFFINITY; BLOOD PRESSURE REGULATION; COMPLEX FORMATION; DEGRADATION; HUMAN; MOLECULAR INTERACTION; NITROSYLATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; REACTION ANALYSIS; REVIEW; SIGNAL TRANSDUCTION;

ALLOSTERIC SITE; ANIMALS; ELECTRONS; HEME; HEMOGLOBINS; HUMANS; MODELS, BIOLOGICAL; MODELS, CHEMICAL; NITRIC OXIDE; OXIDATION-REDUCTION; OXYGEN; PROTEIN BINDING; SIGNAL TRANSDUCTION;

EID: 7244243908     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2004.6.979     Document Type: Review

References (84)

1. Addison AW and Stephanos JJ. Nitrosyliron(III) hemoglobin: autoreduction and spectroscopy. Biochemistry 25: 4104-4113, 1986.
2. Alayash AI, Fratantoni JC, Bonaventura C, Bonaventura J, and Bucci E. Consequences of chemical modifications on the free radical reactions of human hemoglobin. Arch Biochem Biophys 298: 114-120, 1992.
3. Antonini E and Brunori M. Hemoglobin and Myoglobin in their Reactions with Ligands. Amsterdam: North-Holland Publishing Company, 1971.
4. Antonini E, Wyman J, Brunori M, Taylor JF, Rossi-Fanelli A, and Caputo A. Studies on the oxidation-reduction potentials of heme proteins. I. Human hemoglobin. J Biol Chem 239: 907-912, 1964.
5. Antonini E, Brunori M, Wyman J, and Noble RW. Preparation and kinetic properties of intermediates in the reaction of hemoglobin with ligands. J Biol Chem 241: 3236-3238, 1966.
6. - donation by S-nitrosothiols: implications for regulation of physiological functions by S-nitrosylation and acceleration of disulfide formation. Arch Biochem Biophys 318: 279-285, 1995.
7. Barnett DJ, McAninly J, and Williams DLH. Transnityrosation between nitrosothiols and thiols. J Chem Soc [Perkin 2]: 1131-1133, 1994.
8. Bartberger MD, Liu W, Ford E, Miranda KM, Switzer C, Fukuto JM, Farmer PJ, Wink DA, and Houk KN. The reduction potential of nitric oxide (NO) and its importance to NO biochemistry. Proc Natl Acad Sci USA 99: 10958-10963, 2002.
9. Benesch RE, Edalji R, Kwong S, and Benesch R. Oxygen affinity as an index of hemoglobin S polymerization: a new micromethod. Anal Biochem 89: 162-173, 1978.
10. 0 and Deer Lodge β2(NA2)His→Arg. Biochemistry 37: 496-506, 1998.
11. Bonaventura C, Ferruzzi G, Tesh S, and Stevens RD. Effects of 5-nitrosation on oxygen binding by normal and sickle cell hemoglobin. J Biol Chem 274: 24742-24748, 1999.
12. Bonaventura C, Godette G, Tesh S, Holm DE, Bonaventura J, Crumbliss AL, Pearce LL, and Peterson J. Internal electron transfer between hemes and Cu(II) bound at cysteine β93 promotes methemoglobin reduction by carbon monoxide. J Biol Chem 274: 5499-5507, 1999.
13. Bonaventura C, Godette G, Ferruzzi G, Tesh S, Stevens RD, and Henkens R. Responses of normal and sickle cell hemoglobin to S-nitroscysteine: implications for therapeutic applications of NO in treatment of sickle cell disease. Biophys Chem 98: 165-181, 2002.
14. 0 and hemoglobin S. Implications for interactions of nitric oxide with normal and sickle red blood cells. J Biol Chem 277: 14557-14563, 2002.
15. Cassoly R and Gibson Q. Conformation, co-operativity and ligand binding in human hemoglobin. J Mol Biol 91: 301-313, 1975.
16. 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.
17. Desbois A and Banerjee R. Effects of polyvalent anion binding to hemoglobin on oxygen and oxidation-reduction equilibria and their relevance to allosteric transition. J Mol Biol 92: 479-493, 1975.
18. Dong S, Zhu Y, and Song S. Electrode processes of hemoglobin at a platinum electrode covered by Brilliant Cresyl Blue. Bioelectrochem Bioenerg 21: 233-243, 1989.
19. Dou Y, Maillett DH, Eich RF, and Olson JS. Myoglobin as a model system for designing heme protein based blood substitutes. Biophys Chem 98: 127-148, 2002.
20. Fago A, Crumbliss AL, Peterson J, Pearce LL, and Bonaventura C. The case of the missing NO-hemoglobin: spectral changes suggestive of heme redox reactions reflect changes in NO-heme geometry. Proc Natl Acad Sci USA 100: 12087-12092, 2003.
21. Faulkner KM, Bonaventura C, and Crumbliss AL. A spectroelectrochemical method for evaluating factors which regulate the redox potential of hemoglobins. Inorg Chim Acta 226: 187-194, 1994.
22. Feelisch M and Stamler JS. Donors of nitrogen oxides. In: Methods in Nitric Oxide Research, edited by Feelisch M and Stamler JS. New York: John Wiley & Sons, 1996, pp. 71-115.
23. Ferranti P, Malorni A, Mamone G, Sannolo N, and Marino G. Characterisation of S-nitrosohaemoglobin by mass spectrometry. FEBS Lett 400: 19-24, 1997.
24. 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.
25. Garel MC, Beuzard Y, Thillet J, Domenget C, Martin J, Galacteros F, and Rosa J. Binding of 21 thiol reagents to human hemoglobin in solution and in intact cells. Eur J Biochem 123: 513-519, 1982.
26. Garel MC, Domenget C, Galacteros F, Martin-Caburi J, and Beuzard Y. Inhibition of erythrocyte sickling by thiol reagents. Mol Pharmacol 26: 559-565, 1984.
27. Gibson QH and Roughton FJ. Further studies on the kinetics and equilibria of the reaction of nitric oxide with haemoproteins. Proc R Soc Lond B Biol Sci 163: 197-205, 1965.
28. Gladwin MT, Ognibene FP, Pannell LK, Nichols JS, Pease-Fye ME, Shelhamer JH, and Schechter AN. Relative role of heme nitrosylation and β-cysteine 93 nitrosation in the transport and metabolism of nitric oxide by hemoglobin in the human circulation. Proc Natl Acad Sci U S A 97: 9943-9948, 2000.
29. 2/NO-linked allosteric function. J Biol Chem 277: 27818-27828, 2002.
30. Gow AJ and Stamler JS. Reactions between nitric oxide and haemoglobin under physiological conditions. Nature 391: 169-173, 1998.
31. 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.
32. Man TH, Hyduke DR, Vaughn MW, Fukuto JM, and Liao JC. Nitric oxide reaction with red blood cells and hemoglobin under heterogeneous conditions. Proc Natl Acad Sci U S A 99: 7763-7768, 2002.
33. Henry Y and Banerjee R. Electron paramagnetic studies of nitric oxide haemoglobin derivatives: isolated subunits and nitric oxide hybrids. J Mol Biol 73: 469-482, 1973.
34. Herold S. Interaction of nitrogen monoxide with hemoglobin and the artefactual production of S-nitroso-hemoglobin. C R Biol 326: 533-541, 2003.
35. Herold S and Rehmann FJ. Kinetic and mechanistic studies of the reactions of nitrogen monoxide and nitrite with ferryl myoglobin. J Biol Inorg Chem 6: 543-555, 2001.
36. Herold S and Rock G. Reactions of deoxy-, oxy-, and methemoglobin with nitrogen monoxide. Mechanistic studies of the S-nitrosothiol formation under different mixing conditions. J Biol Chem 278: 6623-6634, 2003.
37. Hille R, Palmer G, and Olson JS. Chain equivalence in reaction of nitric oxide with hemoglobin. J Biol Chem 252: 403-405, 1977.
38. Hille R, Olson JS, and Palmer G. Spectral transitions of nitrosyl hemes during ligand binding to hemoglobin. J Biol Chem 254: 12110-12120, 1979.
39. Ignarro LJ, Adams JB, Horwitz PM, and Wood KS. Activation of soluble guanylate cyclase by NO-hemoproteins involves NO-heme exchange. Comparison of heme-containing and heme-deficient enzyme forms. J Biol Chem 261: 4997-5002, 1986.
40. 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 U SA 84: 9265-9269, 1987.
41. Ignarro LJ, Byrns RE, Buga GM, and Wood KS. Endothelium-derived 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.
42. 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.
43. 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.
44. Khan I, Dantsker D, Samuni U, Friedman AJ, Bonaventura C, Manjula B, Acharya SA, and Friedman JM. β93-modified hemoglobin: kinetic and conformational consequences. Biochemistry 40: 7581-7592, 2001.
45. Kharnitov VG, Bonaventura J, and Sharma VS. Interactions of nitric oxide with heme proteins using UV-VIS spectroscopy. In: Methods in Nitric Oxide Research, edited by Feelisch M and Stamler JS. New York: John Wiley & Sons, 1996, pp. 39-45.
46. Kiese M. Methemoglobinemias: A Comprehensive Treatise. Cleveland, OH: CRC Press, 1974.
47. Lancaster JR Jr. Simulation of the diffusion and reaction of endogenously produced nitric oxide. Proc Natl Acad Sci USA 91: 8137-8141, 1994.
48. Lipton AJ, Johnson MA, Macdonald T, Lieberman MW, Gozal D, and Gaston B. S-Nitrosothiols signal the ventilatory response to hypoxia. Nature 413: 171-174, 2001.
49. Lipton SA, Choi YB, Pan ZH, Lei SZ, Chen HS, Sucher NJ, Loscalzo J, Singel DJ, and Stamler JS. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364: 626-632, 1993.
50. Liu X, Samouilov A, Lancaster JR Jr, and Zweier JL. Nitric oxide uptake by erythrocytes is primarily limited by extracellular diffusion not membrane resistance. J Biol Chem 277: 26194-26199, 2002.
51. Martin W, Smith JA, and White DG. The mechanisms by which haemoglobin inhibits the relaxation of rabbit aorta induced by nitrovasodilators, nitric oxide, or bovine retractor penis inhibitory factor. Br J Pharmacol 89: 563-571, 1986.
52. McAninly J, Williams DL, Askew SC, Butler AR, and Russell C. Metal ion catalysis in nitrosothiol (RSNO) decomposition. J Chem Soc Chem Commun 1758-1759, 1993.
53. McMahon TJ, Stone AE, Bonaventura J, Singel, DJ, and Stamler, JS. Functional coupling of oxygen binding and vasoactivity in S-nitrosohemoglobin. J Biol Chem 275: 16738-16745, 2000.
54. McMahon TJ, Moon RE, Luschinger BP, Carraway MS, Stone AE, Stolp BW, Gow AJ, Pawloski JR, Watke P, Singel DJ, Piantadosi CA, and Stamler JS. Nitric oxide in the human respiratory cycle. Nat Med 8: 711-717, 2002.
55. Misra HP and Fridovich I. The generation of superoxide radical during the autoxidation of hemoglobin. J Biol Chem 247: 6960-6962, 1972.
56. Moncada S, Palmer RM, and Higgs EA. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43: 109-142, 1991.
57. Monod J, Wyman J, and Changeux JP. On the nature of allosteric transitions: a plausible model. J Mol Biol 12: 88-118, 1965.
58. Moore EG and Gibson QH. Cooperativity in the dissociation of nitric oxide from hemoglobin. J Biol Chem 251: 2788-2794, 1976.
59. 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: 46349-46356, 2003.
60. 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.
61. 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.
62. Pawloski JR, Hess DT, and Stamler JS. Export by red blood cells of nitric oxide bioactivity. Nature 409: 622-626, 2001.
63. Perutz MF. Nature of haem-haem interaction. Nature 237: 495-499, 1972.
64. Perutz MF, Fersht AR, Simon SR, and Roberts GC. Influence of globin structure on the state of the heme. II. Allosteric transitions in methemoglobin. Biochemistry: 13: 2174-2186, 1974.
65. Perutz MF, Kilmartin JV, Nagai K, Szabo A, and Simon SR. Influence of globin structures on the state of the heme. Ferrous low spin derivatives. Biochemistry 15: 378-387, 1976.
66. Rassaf T, Bryan NS, Maloney RE, Specian V, Kelm M, Kalanyaraman B, Rodriguez J, and Feelisch M. NO adducts in mammalian red blood cells: too much or too little? Nat Med 9: 481-482, 2003.
67. Reischl E. High sulfhydryl content in turtle erythrocytes: is there a relation with resistance to hypoxia? Comp Biochem Physiol [B] 85: 723-726, 1986.
68. Romeo AA, Filosa A, Capobianco JA, and English AM. Metal chelators inhibit S-nitrosation of Cys β93 in oxyhemoglobin. J Am Chem Soc 123: 1782-1783, 2001.
69. Rubbo H, Tarpey M, and Freeman BA. Nitric oxide and reactive oxygen species in vascular injury. In: Free Radicals and Oxidative Stress: Environment, Drugs and Food Additives, edited by Rice-Evans C, Halliwell B, and Lunt GG. London: Portland Press, 1995, pp. 33-45.
70. Sharma VS, Traylor TG, Gardiner R, and Mizukami H. Reaction of nitric oxide with heme proteins and model compounds of hemoglobin. Biochemistry 26: 3837-3843, 1987.
71. Spencer NY, Zeng H, Patel RP, and Hogg N. Reaction of S-nitrosoglutathione with the heme group of deoxyhemoglobin. J Biol Chem 275: 36562-36567, 2000.
72. Stamler JS. S-Nitrosothiols and the bioregulatory actions of nitrogen oxides through reactions with thiol groups. Curr Top Microbiol Immunol 196: 19-36, 1995.
73. Stamler JS, Jia L, Eu JP, McMahon TJ, Demchenko IT, Bonaventura J, Gernert K, and Piantadosi CA. Blood flow regulation by 5-nitrosohemoglobin in the physiological oxygen gradient. Science 276: 2034-2037, 1997.
74. Szabo A and Perutz MF. Equilibrium between six- and five-coordinated hemes in nitrosylhemoglobin: interpretation of electron spin resonance spectra. Biochemistry 15: 4427-4428, 1976.
75. Taketa F, Antholine WE, and Chen JY. Chain nonequivalence in binding of nitric oxide to hemoglobin. J Biol Chem 253: 5448-5451, 1978.
76. Taylor JF and Hastings AB. Oxidation-reduction potentials of the methemoglobin-hemoglobin system. J Biol Chem 131: 649-662, 1939.
77. Vandegriff KD and Winslow RM. Theoretical analysis of oxygen transport: a new strategy for the design of hemoglobin-based red cell substitutes. In: Blood Substitutes: Physiological Basis of Efficacy, edited by Winslow RM, Vandegriff KD, and Intaglietta M. Boston: Birkhauser, 1995, 143-154.
78. Vandegriff KD, Malavalli A, Wooldridge J, Lohman J, and Winslow RM. MP4, a new nonvasoactive PEG-Hb conjugate. Transfusion 43: 509-516, 2003.
79. Vaughn MW, Huang KT, Kuo L, and Liao JC. Erythrocytes possess an intrinsic barrier to nitric oxide consumption. J Biol Chem 275: 2342-2348, 2000.
80. Wink DA and Mitchell JB. Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic Biol Med 25: 434-456, 1998.
81. Winterbourn CC. Free-radical production and oxidative reactions of hemoglobin. Environ Health Perspect 64: 321-330, 1985.
82. Wolzt M, MacAllister RJ, Davis D, Feelisch M, Moncada S, Vallance P, and Hobbs AJ. Biochemical characterization of S-nitrosohemoglobin. Mechanisms underlying synthesis, NO release, and biological activity. J Biol Chem 274: 28983-28990, 1999.
83. 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 β-93 thiol of human hemoglobin during cycles of oxygenation and deoxygenation. Proc Natl Acad Sci USA 100: 11303-11308, 2003.
84. Yonetani T, Tsuneshige A, Zhou Y, and Chen X. Electron paramagnetic resonance and oxygen binding studies of α-nitrosyl hemoglobin. A novel oxygen carrier having NO-assisted allosteric functions. J Biol Chem 273: 20323-20333, 1998.