α-Hemoglobin-stabilizing Protein (AHSP) perturbs the proximal heme pocket of oxy-α-hemoglobin and weakens the iron-oxygen bond

Journal of Biological Chemistry

Volumn 288, Issue 27, 2013, Pages 19986-20001

  Dickson, Claire F ^a   Rich, Anne M ^b   D'Avigdor, William M H ^c   Collins, Daniel A T ^a   Lowry, Jason A ^c   Mollan, Todd L ^d   Khandros, Eugene ^e   Olson, John S ^d   Weiss, Mitchell J ^e   MacKay, Joel P ^c   Lay, Peter A ^b   Gell, David A ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

^d RICE UNIVERSITY   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL SHIFT; DISSOCIATION; EQUILIBRIUM CONSTANTS; EXTENDED X RAY ABSORPTION FINE STRUCTURE SPECTROSCOPY; HEMOGLOBIN; IRON METALLOGRAPHY; LIGANDS; OXYGEN; PORPHYRINS; PROTEINS; RATE CONSTANTS;

AUTOOXIDATION; AUTOOXIDATION RATE; CONFORMATIONAL CHANGE; DISSOCIATION RATES; LIGAND BINDING; MOLECULAR CHAPERONES; NMR CHEMICAL SHIFTS; OXYGEN BONDS;

IRON COMPOUNDS;

ALPHA HEMOGLOBIN STABILIZING PROTEIN; HELICASE; HEME; HEMOGLOBIN; HISTIDINE; IRON; IRON OXIDE; OXY ALPHA HEMOGLOBIN; OXYGEN; PROLINE; UNCLASSIFIED DRUG;

ARTICLE; AUTOOXIDATION; BINDING AFFINITY; CHEMICAL BOND; CONTROLLED STUDY; GEOMETRY; HUMAN; HUMAN CELL; IMAGE ANALYSIS; MOLECULAR IMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OXIDATION REDUCTION REACTION; OXYGEN DISSOCIATION CURVE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; X RAY ABSORPTION SPECTROSCOPY;

EID: 84880056136     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.437509     Document Type: Article

References (85)

1. Feng, L., Gell, D. A., Zhou, S., Gu, L., Kong, Y., Li, J., Hu, M., Yan, N., Lee, C., Rich, A. M., Armstrong, R. S., Lay, P. A., Gow, A. J., Weiss, M. J., Mackay, J. P., and Shi, Y. (2004) Molecular mechanism of AHSP-mediated stabilization of α-hemoglobin. Cell 119, 629-640
2. Feng, L., Zhou, S., Gu, L., Gell, D. A., Mackay, J. P., Weiss, M. J., Gow, A. J., and Shi, Y. (2005) Structure of oxidized α-haemoglobin bound to AHSP reveals a protective mechanism for haem. Nature 435, 697-701
3. Gell, D., Kong, Y., Eaton, S. A., Weiss, M. J., and Mackay, J. P. (2002) Biophysical characterization of the α-globin binding protein α-hemoglobin stabilizing protein. J. Biol. Chem. 277, 40602-40609
4. Kihm, A. J., Kong, Y., Hong, W., Russell, J. E., Rouda, S., Adachi, K., Simon, M. C., Blobel, G. A., and Weiss, M. J. (2002) An abundant erythroid protein that stabilizes free α-haemoglobin. Nature 417, 758-763
5. dos Santos, C. O., Duarte, A. S., Saad, S. T., and Costa, F. F. (2004) Expression of α-hemoglobin stabilizing protein gene during human erythropoiesis. Exp. Hematol. 32, 157-162
6. Kong, Y., Zhou, S., Kihm, A. J., Katein, A. M., Yu, X., Gell, D. A., Mackay, J. P., Adachi, K., Foster-Brown, L., Louden, C. S., Gow, A. J., and Weiss, M. J. (2004) Loss of α-hemoglobin-stabilizing protein impairs erythropoiesis and exacerbates β-thalassemia. J. Clin. Invest. 114, 1457-1466
7. Lai, M. I., Jiang, J., Silver, N., Best, S., Menzel, S., Mijovic, A., Colella, S., Ragoussis, J., Garner, C., Weiss, M. J., and Thein, S. L. (2006) α-Haemoglobin stabilising protein is a quantitative trait gene that modifies the phenotype of β-thalassaemia. Br. J. Haematol. 133, 675-682
8. Giordano, P. C., Zweegman, S., Akkermans, N., Arkesteijn, S. G., van Delft, P., Versteegh, F. G., Wajcman, H., and Harteveld, C. L. (2007) The first case of Hb Groene Hart [α119(H2)Pro→Ser, CCT→TCT (α1)] homozygosity confirms that α thalassemia phenotype is associated with this abnormal hemoglobin variant. Hemoglobin 31, 179-182
9. Yu, X., Kong, Y., Dore, L. C., Abdulmalik, O., Katein, A. M., Zhou, S., Choi, J. K., Gell, D., Mackay, J. P., Gow, A. J., and Weiss, M. J. (2007) An erythroid chaperone that facilitates folding of α-globin subunits for hemoglobin synthesis. J. Clin. Invest. 117, 1856-1865
10. Nasimuzzaman, M., Khandros, E., Wang, X., Kong, Y., Zhao, H., Weiss, D., Rivella, S., Weiss, M. J., and Persons, D. A. (2010) Analysis ofα hemoglobin stabilizing protein overexpression in murine β-thalassemia. Am. J. Hematol. 85, 820-822
11. Khandros, E., Mollan, T. L., Yu, X., Wang, X., Yao, Y., D'Souza, J., Gell, D. A., Olson, J. S., and Weiss, M. J. (2012) Insights into hemoglobin assembly through in vivo mutagenesis of α-hemoglobin stabilizing protein. J. Biol. Chem. 287, 11325-11337
12. Yu, X., Mollan, T. L., Butler, A., Gow, A. J., Olson, J. S., and Weiss, M. J. (2009) Analysis of human α globin gene mutations that impair binding to the α hemoglobin stabilizing protein. Blood 113, 5961-5969
13. Giulivi, C., and Davies, K. J. (1994) Hydrogen peroxide-mediated ferrylhemoglobin generation in vitro and in red blood cells. Methods Enzymol. 231, 490-496
14. Nagababu, E., and Rifkind, J. M. (2000) Reaction of hydrogen peroxide with ferrylhemoglobin. Superoxide production and heme degradation. Biochemistry 39, 12503-12511
15. Reeder, B. J., Svistunenko, D. A., Cooper, C. E., and Wilson, M. T. (2004) The radical and redox chemistry of myoglobin and hemoglobin. From in vitro studies to human pathology. Antioxid. Redox. Signal 6, 954-966
16. Svistunenko, D. A. (2005) Reaction of haem containing proteins and enzymes with hydroperoxides. The radical view. Biochim. Biophys. Acta 1707, 127-155
17. Reeder, B. J. (2010) The redox activity of hemoglobins. From physiologic functions to pathologic mechanisms. Antioxid. Redox. Signal 13, 1087-1123
18. Joshi, W., Leb, L., Piotrowski, J., Fortier, N., and Snyder, L. M. (1983) Increased sensitivity of isolated β subunits of normal human hemoglobin to oxidative damage and crosslinkage with spectrin. J. Lab. Clin. Med. 102, 46-52
19. Scott, M. D., van den Berg, J. J., Repka, T., Rouyer-Fessard, P., Hebbel, R. P., Beuzard, Y., and Lubin, B. H. (1993) Effect of excess α-hemoglobin chains on cellular and membrane oxidation in modelβ-thalassemic erythrocytes. J. Clin. Invest. 91, 1706-1712
20. Mollan, T. L., Banerjee, S., Wu, G., Parker Siburt, C. J., Tsai, A. L., Olson, J. S., Weiss, M. J., Crumbliss, A. L., and Alayash, A. I. (2013)α-Hemoglobin stabilizing protein (AHSP) markedly decreases the redox potential and reactivity of β subunits of human HbA with hydrogen peroxide. J. Biol. Chem. 288, 4288-4298
21. Amer, J., Goldfarb, A., and Fibach, E. (2003) Flow cytometric measurement of reactive oxygen species production by normal and thalassaemic red blood cells. Eur. J. Haematol. 70, 84-90
22. Srinoun, K., Svasti, S., Chumworathayee, W., Vadolas, J., Vattanaviboon, P., Fucharoen, S., and Winichagoon, P. (2009) Imbalanced globin chain synthesis determines erythroid cell pathology in thalassemic mice. Haematologica 94, 1211-1219
23. Leecharoenkiat, A., Wannatung, T., Lithanatudom, P., Svasti, S., Fucha-roen, S., Chokchaichamnankit, D., Srisomsap, C., and Smith, D. R. (2011) Increased oxidative metabolism is associated with erythroid precursor expansion in β0-thalassaemia/Hb E disease. Blood Cells Mol. Dis. 47, 143-157
24. De Franceschi, L., Bertoldi, M., De Falco, L., Santos Franco, S., Ronzoni, L., Turrini, F., Colancecco, A., Camaschella, C., Cappellini, M. D., and Iolascon, A. (2011) Oxidative stress modulates heme synthesis and induces peroxiredoxin-2 as a novel cytoprotective response in β-thalassemic erythropoiesis. Haematologica 96, 1595-1604
25. Gell, D. A., Feng, L., Zhou, S., Jeffrey, P. D., Bendak, K., Gow, A., Weiss, M. J., Shi, Y., and Mackay, J. P. (2009) A cis-proline in α-hemoglobin stabilizing protein directs the structural reorganization of α-hemoglobin. J. Biol. Chem. 284, 29462-29469
26. Hamdane, D., Vasseur-Godbillon, C., Baudin-Creuza, V., Hoa, G. H., and Marden, M. C. (2007) Reversible hexacoordination of α-hemoglobin- stabilizing protein (AHSP)/α-hemoglobin versus pressure. Evidence for protection of the α-chains by their chaperone. J. Biol. Chem. 282, 6398-6404
27. Mollan, T. L., Khandros, E., Weiss, M. J., and Olson, J. S. (2012) The kinetics of α-globin binding to α hemoglobin stabilizing protein (AHSP) indicate preferential stabilization of a hemichrome folding intermediate. J. Biol. Chem. 287, 11338-11350
28. Vasseur-Godbillon, C., Hamdane, D., Marden, M. C., and Baudin-Creuza, V. (2006) High-yield expression in Escherichia coli of soluble humanα- hemoglobin complexed with its molecular chaperone. Protein Eng. Des. Sel. 19, 91-97
29. Zhou, S., Olson, J. S., Fabian, M., Weiss, M. J., and Gow, A. J. (2006) Biochemical fates of α hemoglobin bound to α-hemoglobin-stabilizing protein AHSP. J. Biol. Chem. 281, 32611-32618
30. Simplaceanu, V., Lukin, J. A., Fang, T. Y., Zou, M., Ho, N. T., and Ho, C. (2000) Chain-selective isotopic labeling for NMR studies of large multimeric proteins. Application to hemoglobin. Biophys. J. 79, 1146-1154
31. Looker, D., Mathews, A. J., Neway, J. O., and Stetler, G. L. (1994) Expression of recombinant human hemoglobin in Escherichia coli. Methods Enzymol. 231, 364-374
32. Cai, M., Huang, Y., Sakaguchi, K., Clore, G. M., Gronenborn, A. M., and Craigie, R. (1998) An efficient and cost-effective isotope labeling protocol for proteins expressed in Escherichia coli. J. Biomol. NMR 11, 97-102
33. Shen, T. J., Ho, N. T., Zou, M., Sun, D. P., Cottam, P. F., Simplaceanu, V., Tam, M. F., Bell, D. A., Jr., and Ho, C. (1997) Production of human normal adult and fetal hemoglobins in Escherichia coli. Protein Eng. 10, 1085-1097
34. Gill, S. C., and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326
35. Eaton, W. A., and Hofrichter, J. (1981) Polarized absorption and linear dichroism spectroscopy of hemoglobin. Methods Enzymol. 76, 175-261
36. Folta-Stogniew, E., and Williams, K. R. (1999) Determination of molecular masses of proteins in solution. Implementation of an HPLC size exclusion chromatography and laser light scattering service in a core laboratory. J. Biomol. Tech. 10, 51-63
37. Goddard, T. D., and Kneller, D. G. (2006) SPARKY, University of California at San Francisco
38. Pelton, J. G., Torchia, D. A., Meadow, N. D., and Roseman, S. (1993) Tautomeric states of the active-site histidines of phosphorylated and unphosphorylated IIIGlc, a signal-transducing protein from Escherichia coli, using two-dimensional heteronuclear NMR techniques. Protein Sci. 2, 543-558
39. Cramer, S. P., Tench, O., Yocum, M., and George, G. N. (1988) A 13- element Ge detector for fluorescence EXAFS. Nucl. Instrum. Methods Phys. Res. A 266, 586-591
40. Zhang, Y., Pavlosky, M. A., Brown, C. A., Westre, T. E., Hedman, B., Hodgson, K. O., and Solomon, E. I. (1992) Spectroscopic and theoretical description of the electronic structure of the S = 3/2 nitrosyl complex of non-heme iron enzymes. J. Am. Chem. Soc. 114, 9189-9191
41. Rich, A. M., Armstrong, R. S., Ellis, P. J., Freeman, H. C., and Lay, P. A. (1998) Determination of iron-ligand bond lengths in horse heart met-and deoxymyoglobin using multiple-scattering XAFS analyses. Inorg. Chem. 37, 5743-5753
42. Ellis, P. J., and Freeman, H. C. (1995) XFIT. An interactive EXAFS analysis program. J. Synchrotron. Radiat. 2, 190-195
43. Jameson, G. B., Molinaro, F. S., Ibers, J. A., Collman, J. P., Brauman, J. I., Rose, E., and Suslick, K. S. (1980) Models for the active site of oxygenbinding hemoproteins. Dioxygen binding properties and the structures of (2-methylimidazole)-meso-tetra(α,α,α,α-o- pivalamidophenyl)porphyrinatoiron( II)-ethanol and its dioxygen adduct. J. Am. Chem. Soc. 102, 3224-3237
44. Penner-Hahn, J. (2004) in Comprehensive Coordination Chemistry II; From Biology to Nanotechnology (Lever, A. B. P., ed.) pp. 159, Elsevier, Oxford
45. Birukou, I., Schweers, R. L., and Olson, J. S. (2010) Distal histidine stabilizes bound O2 and acts as a gate for ligand entry in both subunits of adult human hemoglobin. J. Biol. Chem. 285, 8840-8854
46. Santiveri, C. M., Pérez-Cañadillas, J. M., Vadivelu, M. K., Allen, M. D., Rutherford, T. J., Watkins, N. A., and Bycroft, M. (2004)NMRstructure of the α-hemoglobin stabilizing protein. Insights into conformational heterogeneity and binding. J. Biol. Chem. 279, 34963-34970
47. Martineau, L., and Craescu, C. T. (1992) Sequential assignment of the proton NMR spectrum of isolated α(CO) chains from human adult hemoglobin. Eur. J. Biochem. 205, 661-670
48. Antonini, E., Bucci, E., Fronticelli, C., Chiancone, E., Wyman, J., and Rossi-Fanelli, A. (1966) The properties and interactions of the isolated α- and β-chains of human haemoglobin. V. The reaction of α- and β-chains. J. Mol. Biol. 17, 29-46
49. Valdes, R., Jr., and Ackers, G. K. (1977) Thermodynamic studies on subunit assembly in human hemoglobin. Self-association of oxygenated chains (αSH and βSH). Determination of stoichiometries and equilibrium constants as a function of temperature. J. Biol. Chem. 252, 74-81
50. Bucci, E., and Fronticelli, C. (1965) A new method for the preparation of α and β subunits of human hemoglobin. J. Biol. Chem. 240, PC551-552
51. Brunori, M., Noble, R. W., Antonini, E., and Wyman, J. (1966) The reactions of the isolated α and β chains of human hemoglobin with oxygen and carbon monoxide. J. Biol. Chem. 241, 5238-5243
52. Shen, Y., Delaglio, F., Cornilescu, G., and Bax, A. (2009) TALOS+. A hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR 44, 213-223
53. Park, S. Y., Yokoyama, T., Shibayama, N., Shiro, Y., and Tame, J. R. (2006) 1.25 Å resolution crystal structures of human haemoglobin in the oxy-, deoxy-, and carbonmonoxy forms. J. Mol. Biol. 360, 690-701
54. Kabsch, W., and Sander, C. (1983) Dictionary of protein secondary structure. Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637
55. Dalvit, C., Tennant, L., and Wright, P. E. (1987) 1Hresonances of proximal histidine in CO complexes of hemoglobins provide a sensitive probe of coordination geometry. FEBS Lett. 213, 289-292
56. Dalvit, C., and Wright, P. E. (1987) Assignment of resonances in the 1H nuclear magnetic resonance spectrum of the carbon monoxide complex of human hemoglobin α-chains. J. Mol. Biol. 194, 329-339
57. Lukin, J. A., Simplaceanu, V., Zou, M., Ho, N. T., and Ho, C. (2000) NMR reveals hydrogen bonds between oxygen and distal histidines in oxyhemoglobin. Proc. Natl. Acad. Sci. U.S.A. 97, 10354-10358
58. Levina, A., Armstrong, R. S., and Lay, P. A. (2005) Three-dimensional structure determination using multiple-scattering analysis of XAFS. Applications to metalloproteins and coordination chemistry. Coord. Chem. Rev. 249, 141-160
59. George, G. N., Pickering, I. J., Pushie, M. J., Nienaber, K., Hackett, M. J., Ascone, I., Hedman, B., Hodgson, K. O., Aitken, J. B., Levina, A., Glover, C., and Lay, P. A. (2012) X-ray-induced photo-chemistry and X-ray absorption spectroscopy of biological samples. J. Synchrotron. Radiat. 19, 875-886
60. Rich, A. M. (1997) Determination of Fe-ligand bond lengths and angles in hemeproteins using x-ray absorption Spectroscopy. Ph.D thesis, School of Chemistry, The University of Sydney, Sydney
61. Reed, C. A., and Cheung, S. K. (1977) On the bonding of FeO2 in hemoglobin and related dioxygen complexes. Proc. Natl. Acad. Sci. U.S.A. 74, 1780-1784
62. Spiro, T. G., and Strekas, T. C. (1974) Resonance Raman spectra of heme proteins. Effects of oxidation and spin state. J. Am. Chem. Soc. 96, 338-345
63. Binsted, N., Strange, R. W., and Hasnain, S. S. (1992) Constrained and restrained refinement in EXAFS data analysis with curved wave theory. Biochemistry 31, 12117-12125
64. Chance, M. R., Miller, L. M., Fischetti, R. F., Scheuring, E., Huang, W. X., Sclavi, B., Hai, Y., and Sullivan, M. (1996) Global mapping of structural solutions provided by the extended x-ray absorption fine structure ab initio code FEFF 6.01. Structure of the cryogenic photoproduct of the myoglobin-carbon monoxide complex. Biochemistry 35, 9014-9023
65. Hasnain, S. S., and Hodgson, K. O. (1999) Structure of metal centres in proteins at subatomic resolution. J. Synchrotron Radiat. 6, 852-864
66. Rich, A. M., Armstrong, R. S., Ellis, P. J., and Lay, P. A. (1998) Determination of the Fe-ligand bond lengths and Fe-N-O bond angles in horse heart ferric and ferrous nitrosylmyoglobin using multiple-scattering XAFS analyses. J. Am. Chem. Soc. 120, 10827-10836
67. Vojtechovský, J., Chu, K., Berendzen, J., Sweet, R. M., and Schlichting, I. (1999) Crystal structures of myoglobin-ligand complexes at near-atomic resolution. Biophys. J. 77, 2153-2174
68. Kachalova, G. S., Popov, A. N., and Bartunik, H. D. (1999) A steric mechanism for inhibition of CO binding to heme proteins. Science 284, 473-476
69. Li, R., Nagai, Y., and Nagai, M. (2000) Changes of tyrosine and tryptophan residues in human hemoglobin by oxygen binding. Near-and far-UV circular dichroism of isolated chains and recombined hemoglobin. J. Inorg. Biochem. 82, 93-101
70. Beychok, S., Tyuma, I., Benesch, R. E., and Benesch, R. (1967) Optically active absorption bands of hemoglobin and its subunits. J. Biol. Chem. 242, 2460-2462
71. Geraci, G., and Li, T. K. (1969) Circular dichroism of isolated and recombined hemoglobin chains. Biochemistry 8, 1848-1854
72. Geraci, G., and Parkhurst, L. J. (1981) Circular dichroism spectra of hemoglobins. Methods Enzymol. 76, 262-275
73. Tran, A. T., Kolczak, U., and La Mar, G. N. (2003) Solution 1HNMRstudy of the active site molecular structure and magnetic properties of the cyanomet complex of the isolated α-chain from human hemoglobin A. Biochim. Biophys. Acta 1650, 59-72
74. Tran, A. T., Kolczak, U., and La Mar, G. N. (2004) Solution 1HNMRstudy of the active site molecular structure and magnetic properties of the cyanomet complex of the isolated, tetrameric β-chain from human adult hemoglobin. Biochim. Biophys. Acta 1701, 75-87
75. Azevedo, E. P., Pereira, H. M., Garratt, R. C., Kelly, J. W., Foguel, D., and Palhano, F. L. (2011) Dissecting the structure, thermodynamic stability, and aggregation properties of the A25T transthyretin (A25T-TTR) variant involved in leptomeningeal amyloidosis. Identifying protein partners that co-aggregate during A25T-TTR fibrillogenesis in cerebrospinal fluid. Biochemistry 50, 11070-11083
76. Olson, J. S., and Phillips, G. N., Jr. (1997) Myoglobin discriminates betweenO2, NO, andCOby electrostatic interactions with the bound ligand. J. Biol. Inorg. Chem. 2, 544-552
77. Capece, L., Marti, M. A., Crespo, A., Doctorovich, F., and Estrin, D. A. (2006) Heme protein oxygen affinity regulation exerted by proximal effects. J. Am. Chem. Soc. 128, 12455-12461
78. Schulman, H. M., Martinez-Medellin, J., and Sidloi, R. (1974) The oxidation state of newly synthesized hemoglobin. Biochem. Biophys. Res. Commun. 56, 220-226
79. Gill, F. M., and Schwartz, E. (1973) Free α-globin pool in human bone marrow. J. Clin. Invest. 52, 3057-3063
80. Vasseur, C., Pissard, S., Domingues-Hamdi, E., Marden, M. C., Galactéros, F., and Baudin-Creuza, V. (2011) Evaluation of the free α-hemoglobin pool in red blood cells. A new test providing a scale of β-thalassemia severity. Am. J. Hematol. 86, 199-202
81. Tomoda, A., Sugimoto, K., Suhara, M., Takeshita, M., and Yoneyama, Y. (1978) Haemichrome formation from haemoglobin subunits by hydrogen peroxide. Biochem. J. 171, 329-335
82. Straub, A. C., Lohman, A. W., Billaud, M., Johnstone, S. R., Dwyer, S. T., Lee, M. Y., Bortz, P. S., Best, A. K., Columbus, L., Gaston, B., and Isakson, B. E. (2012) Endothelial cell expression of haemoglobin α regulates nitric oxide signalling. Nature 491, 473-477
83. Doherty, D. H., Doyle, M. P., Curry, S. R., Vali, R. J., Fattor, T. J., Olson, J. S., and Lemon, D. D. (1998) Rate of reaction with nitric oxide determines the hypertensive effect of cell-free hemoglobin. Nat. Biotechnol. 16, 672-676
84. Eich, R. F., Li, T., Lemon, D. D., Doherty, D. H., Curry, S. R., Aitken, J. F., Mathews, A. J., Johnson, K. A., Smith, R. D., Phillips, G. N., Jr., and Olson, J. S. (1996) Mechanism of NO-induced oxidation of myoglobin and hemoglobin. Biochemistry 35, 6976-6983
85. Kim-Shapiro, D. B., Schechter, A. N., and Gladwin, M. T. (2006) Unraveling the reactions of nitric oxide, nitrite, and hemoglobin in physiology and therapeutics. Arterioscler. Thromb. Vasc. Biol. 26, 697-705