Antioxidant functions for the hemoglobin β93 cysteine residue in erythrocytes and in the vascular compartment in vivo

Free Radical Biology and Medicine

Volumn 55, Issue , 2013, Pages 119-129

  Vitturi, Dario A ^a   Sun, Chiao Wang ^b   Harper, Victoria M ^a   Thrash Williams, Bessy ^a   Cantu Medellin, Nadiezhda ^a   Chacko, Balu K ^a   Peng, Ning ^c   Dai, Yanying ^c   Wyss, J Michael ^c   Townes, Tim ^b   Patel, Rakesh P ^a,c  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Antioxidant; Endotoxemia; Erythrocytes; Free radicals; Hemoglobin; Inflammation; Oxidative stress

Indexed keywords

5,5 DIMETHYL 1 PYRROLINE 1 OXIDE; ALANINE; CATALASE; CYSTEINE; CYSTEINE DERIVATIVE; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; HEMOGLOBIN; HEMOGLOBIN BETA93 CYSTEINE; HEMOGLOBIN DERIVATIVE; HYDROGEN PEROXIDE; LIPOPOLYSACCHARIDE; PEROXIREDOXIN 2; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; TOSYLCHLORAMIDE SODIUM; UNCLASSIFIED DRUG;

ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ERYTHROCYTE; HYPOTENSION; IN VIVO STUDY; LUNG; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SCAVENGING SYSTEM; VASCULITIS;

ANIMALS; ANTIOXIDANTS; CYSTEINE; ERYTHROCYTES; HEMOGLOBINS; HYDROGEN PEROXIDE; INFLAMMATION; LIPOPOLYSACCHARIDES; LUNG; MALE; MICE; OXIDATION-REDUCTION; OXIDATIVE STRESS;

MUS; VERTEBRATA;

EID: 84871672504     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.11.003     Document Type: Article

References (63)

1. M.R. Condon, J.E. Kim, E.A. Deitch, G.W. Machiedo, and Z. Spolarics Appearance of an erythrocyte population with decreased deformability and hemoglobin content following sepsis Am. J. Physiol. Heart Circ. Physiol 284 2003 H2177 2184
2. E. Fibach, and E. Rachmilewitz The role of oxidative stress in hemolytic anemia Curr. Mol. Med. 8 2008 609 619
3. E. Nagy, J.W. Eaton, V. Jeney, M.P. Soares, Z. Varga, Z. Galajda, J. Szentmiklosi, G. Mehes, T. Csonka, A. Smith, G.M. Vercellotti, G. Balla, and J. Balla Red cells, hemoglobin, heme, iron, and atherogenesis Arterioscler. Thromb. Vasc. Biol. 30 2010 1347 1353
4. Z. Spolarics, M.R. Condon, M. Siddiqi, G.W. Machiedo, and E.A. Deitch Red blood cell dysfunction in septic glucose-6-phosphate dehydrogenase-deficient mice Am. J. Physiol. Heart Circ. Physiol 286 2004 H2118 2126
5. R. Kiefmann, J.M. Rifkind, E. Nagababu, and J. Bhattacharya Red blood cells induce hypoxic lung inflammation Blood 111 2008 5205 5214
6. R.M. Johnson, Y.S. Ho, D.Y. Yu, F.A. Kuypers, Y. Ravindranath, and G.W. Goyette The effects of disruption of genes for peroxiredoxin-2, glutathione peroxidase-1, and catalase on erythrocyte oxidative metabolism Free Radic. Biol. Med. 48 2010 519 525
7. G. Jacobasch, and S.M. Rapoport Hemolytic anemias due to erythrocyte enzyme deficiencies Mol. Aspects Med. 17 1996 143 170
8. 2 in red blood cells Antioxid. Redox Signaling 12 2010 1235 1246
9. E. Reischl, A.L. Dafre, J.L. Franco, and D. Wilhelm Filho Distribution, adaptation and physiological meaning of thiols from vertebrate hemoglobins Comp. Biochem. Physiol. C Toxicol. Pharmacol 146 2007 22 53
10. J.F. Storz, R.E. Weber, and A. Fago Oxygenation properties and oxidation rates of mouse hemoglobins that differ in reactive cysteine content Comp. Biochem. Physiol. A Mol. Integr. Physiol 161 2012 265 270
11. R.E. Benesch, and R. Benesch The influence of oxygenation on the reactivity of the -SH groups of hemoglobin Biochemistry 1 1962 735 738
12. G. Guidotti The rates of reaction of the sulfhydryl groups of human hemoglobin J. Biol. Chem 240 1965 3924 3927
13. A. Riggs The binding of N-ethylmaleimide by human hemoglobin and its effect upon the oxygen equilibrium J. Biol. Chem 236 1961 1948 1954
14. R. Rossi, L. Lusini, F. Giannerini, D. Giustarini, G. Lungarella, and P. Di Simplicio A method to study kinetics of transnitrosation with nitrosoglutathione: reactions with hemoglobin and other thiols Anal. Biochem. 254 1997 215 220
15. E. Antonini, and M. Brunori On the rate of a conformation change associated with ligand binding in hemoglobin J. Biol. Chem. 244 1969 3909 3912
16. G. Geraci, and L.J. Parkhurst Effects of heme-globin and chain-chain interactions on the conformation of human hemoglobin: a kinetic study Biochemistry 12 1973 3414 3418
17. S.A. Morell, P. Hoffman, V.E. Ayers, and F. Taketa Reversible changes in the NEM-reactive -SH groups of hemoglobin on oxygenation-deoxygenation Proc. Natl. Acad. Sci. USA 48 1962 1057 1061
18. C. Balagopalakrishna, O.O. Abugo, J. Horsky, P.T. Manoharan, E. Nagababu, and J.M. Rifkind Superoxide produced in the heme pocket of the beta-chain of hemoglobin reacts with the beta-93 cysteine to produce a thiyl radical Biochemistry 37 1998 13194 13202
19. C. Bonaventura, G. Godette, S. Tesh, D.E. Holm, J. Bonaventura, A.L. Crumbliss, L.L. Pearce, and J. Peterson Internal electron transfer between hemes and Cu(II) bound at cysteine beta93 promotes methemoglobin reduction by carbon monoxide J. Biol. Chem. 274 1999 5499 5507
20. J.M. Rifkind Copper and the autoxidation of hemoglobin Biochemistry 13 1974 2475 2481
21. C.C. Winterbourn, and R.W. Carrell Oxidation of human haemoglobin by copper: mechanism and suggested role of the thiol group of residue beta-93 Biochem. J 165 1977 141 148
22. S. Bhattacharjee, L.J. Deterding, J. Jiang, M.G. Bonini, K.B. Tomer, D.C. Ramirez, and R.P. Mason Electron transfer between a tyrosyl radical and a cysteine residue in hemoproteins: spin trapping analysis J. Am. Chem. Soc. 129 2007 13493 13501
23. Y. Jia, P.W. Buehler, R.A. Boykins, R.M. Venable, and A.I. Alayash Structural basis of peroxide-mediated changes in human hemoglobin: a novel oxidative pathway J. Biol. Chem. 282 2007 4894 4907
24. O. Augusto, S. Lopes de Menezes, E. Linares, N. Romero, R. Radi, and A. Denicola EPR detection of glutathiyl and hemoglobin-cysteinyl radicals during the interaction of peroxynitrite with human erythrocytes Biochemistry 41 2002 14323 14328
25. T.S. Isbell, C.W. Sun, L.C. Wu, X. Teng, D.A. Vitturi, B.G. Branch, C.G. Kevil, N. Peng, J.M. Wyss, N. Ambalavanan, L. Schwiebert, J. Ren, K.M. Pawlik, M.B. Renfrow, R.P. Patel, and T.M. Townes SNO-hemoglobin is not essential for red blood cell-dependent hypoxic vasodilation Nat. Med 14 2008 773 777
26. K.M. Robinson, and J.S. Beckman Synthesis of peroxynitrite from nitrite and hydrogen peroxide Methods Enzymol. 396 2005 207 214
27. E.L. Thomas, M.B. Grisham, and M.M. Jefferson Preparation and characterization of chloramines Methods Enzymol. 132 1986 569 585
28. J.H. Crawford, C.R. White, and R.P. Patel Vasoactivity of S-nitrosohemoglobin: role of oxygen, heme, and NO oxidation states Blood 101 2003 4408 4415
29. N. Cantu-Medellin, D.A. Vitturi, C. Rodriguez, S. Murphy, S. Dorman, S. Shiva, Y. Zhou, Y. Jia, A.F. Palmer, and R.P. Patel Effects of T- and R-state stabilization on deoxyhemoglobin-nitrite reactions and stimulation of nitric oxide signaling Nitric Oxide 25 2011 59 69
30. J.M. Dypbukt, C. Bishop, W.M. Brooks, B. Thong, H. Eriksson, and A.J. Kettle A sensitive and selective assay for chloramine production by myeloperoxidase Free Radic. Biol. Med. 39 2005 1468 1477
31. M.M. Stacey, A.V. Peskin, M.C. Vissers, and C.C. Winterbourn Chloramines and hypochlorous acid oxidize erythrocyte peroxiredoxin 2 Free Radic. Biol. Med. 47 2009 1468 1476
32. F.M. Low, M.B. Hampton, A.V. Peskin, and C.C. Winterbourn Peroxiredoxin 2 functions as a noncatalytic scavenger of low-level hydrogen peroxide in the erythrocyte Blood 109 2007 2611 2617
33. A. Landar, J.Y. Oh, N.M. Giles, A. Isom, M. Kirk, S. Barnes, and V.M. Darley-Usmar A sensitive method for the quantitative measurement of protein thiol modification in response to oxidative stress Free Radic. Biol. Med. 40 2006 459 468
34. S.P. Heximer, R.H. Knutsen, X. Sun, K.M. Kaltenbronn, M.H. Rhee, N. Peng, A. Oliveira-dos-Santos, J.M. Penninger, A.J. Muslin, T.H. Steinberg, J.M. Wyss, R.P. Mecham, and K.J. Blumer Hypertension and prolonged vasoconstrictor signaling in RGS2-deficient mice J. Clin. Invest. 111 2003 445 452
35. B. Manta, M. Hugo, C. Ortiz, G. Ferrer-Sueta, M. Trujillo, and A. Denicola The peroxidase and peroxynitrite reductase activity of human erythrocyte peroxiredoxin 2 Arch. Biochem. Biophys. 484 2009 146 154
36. Y. Tampo, S. Kotamraju, C.R. Chitambar, S.V. Kalivendi, A. Keszler, J. Joseph, and B. Kalyanaraman Oxidative stress-induced iron signaling is responsible for peroxide-dependent oxidation of dichlorodihydrofluorescein in endothelial cells: role of transferrin receptor-dependent iron uptake in apoptosis Circ. Res. 92 2003 56 63
37. P. Wardman Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: progress, pitfalls, and prospects Free Radic. Biol. Med 43 2007 995 1022
38. J.D. MacMicking, C. Nathan, G. Hom, N. Chartrain, D.S. Fletcher, M. Trumbauer, K. Stevens, Q.-w. Xie, K. Sokol, N. Hutchinson, H. Chen, and J.S. Mudget Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase Cell 81 1995 641 650
39. F.B. Jensen The dual roles of red blood cells in tissue oxygen delivery: oxygen carriers and regulators of local blood flow J. Exp. Biol 212 2009 3387 3393
40. T. Niwa, C. Naito, A.H. Mawjood, and K. Imai Increased glutathionyl hemoglobin in diabetes mellitus and hyperlipidemia demonstrated by liquid chromatography/electrospray ionization-mass spectrometry Clin. Chem. 46 2000 82 88
41. F. Takayama, S. Tsutsui, M. Horie, K. Shimokata, and T. Niwa Glutathionyl hemoglobin in uremic patients undergoing hemodialysis and continuous ambulatory peritoneal dialysis Kidney Int. Suppl. 78 2001 S155 S158
42. D. Giustarini, I. Dalle-Donne, R. Colombo, S. Petralia, S. Giampaoletti, A. Milzani, and R. Rossi Protein glutathionylation in erythrocytes Clin. Chem. 49 2003 327 330
43. Y. Iuchi, F. Okada, K. Onuma, T. Onoda, H. Asao, M. Kobayashi, and J. Fujii Elevated oxidative stress in erythrocytes due to a SOD1 deficiency causes anaemia and triggers autoantibody production Biochem. J. 402 2007 219 227
44. T.H. Lee, S.U. Kim, S.L. Yu, S.H. Kim, D.S. Park, H.B. Moon, S.H. Dho, K.S. Kwon, H.J. Kwon, Y.H. Han, S. Jeong, S.W. Kang, H.S. Shin, K.K. Lee, S.G. Rhee, and D.Y. Yu Peroxiredoxin II is essential for sustaining life span of erythrocytes in mice Blood 101 2003 5033 5038
45. G. Ferrer-Sueta, and R. Radi Chemical biology of peroxynitrite: kinetics, diffusion, and radicals ACS Chem. Biol. 4 2009 161 177
46. D.I. Pattison, and M.J. Davies Reactions of myeloperoxidase-derived oxidants with biological substrates: gaining chemical insight into human inflammatory diseases Curr. Med. Chem. 13 2006 3271 3290
47. T. Pimenova, C.P. Pereira, P. Gehrig, P.W. Buehler, D.J. Schaer, and R. Zenobi Quantitative mass spectrometry defines an oxidative hotspot in hemoglobin that is specifically protected by haptoglobin J. Proteome Res. 9 2010 4061 4070
48. L.J. Deterding, D.C. Ramirez, J.R. Dubin, R.P. Mason, and K.B. Tomer Identification of free radicals on hemoglobin from its self-peroxidation using mass spectrometry and immuno-spin trapping: observation of a histidinyl radical J. Biol. Chem. 279 2004 11600 11607
49. D.C. Ramirez, Y.R. Chen, and R.P. Mason Immunochemical detection of hemoglobin-derived radicals formed by reaction with hydrogen peroxide: involvement of a protein-tyrosyl radical Free Radic. Biol. Med. 34 2003 830 839
50. Cooper, C.E.; Schaer, D.J.; Buehler, P.W.; Wilson, M.T.; Reeder, B.J.; Silkstone, G.; Svistunenko, D.A.; Bulow, L.; Alayash, A.I. Haptoglobin binding stabilizes hemoglobin ferryl iron and the globin radical on tyrosine β145. Antioxid. Redox Signaling (in press); 2012.
51. B.J. Reeder, M. Grey, R.L. Silaghi-Dumitrescu, D.A. Svistunenko, L. Bulow, C.E. Cooper, and M.T. Wilson Tyrosine residues as redox cofactors in human hemoglobin: implications for engineering nontoxic blood substitutes J. Biol. Chem. 283 2008 30780 30787
52. -: EPR SPIN trapping studies J. Biol. Chem 280 2005 40684 40698
53. A.V. Peskin, and C.C. Winterbourn Kinetics of the reactions of hypochlorous acid and amino acid chloramines with thiols, methionine, and ascorbate Free Radic. Biol. Med. 30 2001 572 579
54. R.M. Bateman, J.E. Jagger, M.D. Sharpe, M.L. Ellsworth, S. Mehta, and C.G. Ellis Erythrocyte deformability is a nitric oxide-mediated factor in decreased capillary density during sepsis Am. J. Physiol. Heart Circ. Physiol 280 2001 H2848 H2856
55. A. Chatterjee, C. Dimitropoulou, F. Drakopanayiotakis, G. Antonova, C. Snead, J. Cannon, R.C. Venema, and J.D. Catravas Heat shock protein 90 inhibitors prolong survival, attenuate inflammation, and reduce lung injury in murine sepsis Am. J. Respir. Crit. Care Med. 176 2007 667 675
56. J.H. Crawford, B.K. Chacko, H.M. Pruitt, B. Piknova, N. Hogg, and R.P. Patel Transduction of NO-bioactivity by the red blood cell in sepsis: novel mechanisms of vasodilation during acute inflammatory disease Blood 104 2004 1375 1382
57. E. Nagababu, and J.M. Rifkind Reaction of hydrogen peroxide with ferrylhemoglobin: superoxide production and heme degradation Biochemistry 39 2000 12503 12511
58. L. Liu, Y. Yan, M. Zeng, J. Zhang, M.A. Hanes, G. Ahearn, T.J. McMahon, T. Dickfeld, H.E. Marshall, L.G. Que, and J.S. Stamler Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock Cell 116 2004 617 628
59. B.S. van Asbeck, J. Hoidal, G.M. Vercellotti, B.A. Schwartz, C.F. Moldow, and H.S. Jacob Protection against lethal hyperoxia by tracheal insufflation of erythrocytes: role of red cell glutathione Science 227 1985 756 759
60. S.J. Weiss Neutrophil-mediated methemoglobin formation in the erythrocyte: the role of superoxide and hydrogen peroxide J. Biol. Chem. 257 1982 2947 2953
61. M.B. Grisham, M.M. Jefferson, and E.L. Thomas Role of monochloramine in the oxidation of erythrocyte hemoglobin by stimulated neutrophils J. Biol. Chem. 259 1984 6757 6765
62. K.M. Toth, D.P. Clifford, E.M. Berger, C.W. White, and J.E. Repine Intact human erythrocytes prevent hydrogen peroxide-mediated damage to isolated perfused rat lungs and cultured bovine pulmonary artery endothelial cells J. Clin. Invest. 74 1984 292 295
63. M.C. Vissers, and C.C. Winterbourn Oxidation of intracellular glutathione after exposure of human red blood cells to hypochlorous acid Biochem. J 307 Pt 1 1995 57 62