Post-translational transformation of methionine to aspartate is catalyzed by heme iron and driven by peroxide: A novel subunit-specific mechanism in hemoglobin

Journal of Biological Chemistry

Volumn 289, Issue 32, 2014, Pages 22342-22357

  Strader, Michael Brad ^a   Hicks, Wayne A ^a   Kassa, Tigist ^a   Singleton, Eileen ^b   Soman, Jayashree ^b   Olson, John S ^b   Weiss, Mitchell J ^c   Mollan, Todd L ^a   Wilson, Michael T ^d   Alayash, Abdu I ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^b RICE UNIVERSITY   (United States)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^d UNIVERSITY OF ESSEX   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; HEMOGLOBIN; OXIDATION; PEROXIDES;

ASPARTATES; HEME COMPLEXES; HEME IRON; HEME POCKETS; HEMOGLOBINOPATHIES; MUTANT HEMOGLOBIN; OXIDATIVE MECHANISM;

PORPHYRINS;

ASPARTIC ACID; HEME; HEMOGLOBIN; HEMOGLOBIN A; HEMOGLOBIN EVANS; HEMOGLOBIN F; HEMOGLOBIN VARIANT; HYDROGEN PEROXIDE; IRON; METHIONINE; PROTEIN SUBUNIT;

ADULT; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MISSENSE MUTATION; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PROTEIN PROCESSING; PROTEIN SUBUNIT; PROTEOMICS; STATIC ELECTRICITY; X RAY CRYSTALLOGRAPHY;

ADULT; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ASPARTIC ACID; CRYSTALLOGRAPHY, X-RAY; FETAL HEMOGLOBIN; HEME; HEMOGLOBIN A; HEMOGLOBINS; HEMOGLOBINS, ABNORMAL; HUMANS; HYDROGEN PEROXIDE; IRON; METHIONINE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; OXIDATION-REDUCTION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SUBUNITS; PROTEOMICS; STATIC ELECTRICITY;

EID: 84905833490     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.568980     Document Type: Article

References (48)

1. Bunn, H. F., and Forget, B. G., (1986) in Hemoglobin: Molecular, Genetic, and Clinical Aspects (Dyson, J., ed) W. B. Saunders Co., Philadelphia
2. Zurbriggen, K., Schmugge, M., Schmid, M., Durka, S., Kleinert, P., Kuster, T., Heizmann, C. W., and Troxler, H. (2005) Analysis of minor hemoglobins by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Clin. Chem. 51, 989-996
3. Rees, D. C., Rochette, J., Schofield, C., Green, B., Morris, M., Parker, N. E., Sasaki, H., Tanaka, A., Ohba, Y., and Clegg, J. B. (1996) A novel silent posttranslational mechanism converts methionine to aspartate in hemoglobin Bristol 67[E11] Val-Met3Asp). Blood 88, 341-348
4. Fucci, L., Oliver, C. N., Coon, M. J., and Stadtman, E. R. (1983) Inactivation of key metabolic enzymes by mixed-function oxidation reactions: possible implication in protein turnover and ageing. Proc. Natl. Acad. Sci. U.S.A. 80, 1521-1525
5. Stadtman, E. R. (1990) Metal ion-catalyzed oxidation of proteins: biochemical mechanism and biological consequences. Free Radic. Biol. Med. 9, 315-325
6. Levine, R. L. (1983) Oxidative modification of glutamine synthetase. II. Characterization of the ascorbate model system. J. Biol. Chem. 258, 11828-11833
7. Stadtman, E. R. (1992) Protein oxidation and aging. Science 257, 1220-1224
8. Miyazaki, A., Nakanishi, T., Kishikawa, M., Shimizu, A., Ohba, Y., Tanaka, A., and Sasaki, H. (1996) Post-translational modification from methionine to aspartic acid residue on a variant hemoglobin, Hb Bristol, a proof by ESI-MS-MS. J. Mass Spectrom. 31, 1311-1313
9. Steadman, J. H., Yates, A., and Huehns, E. R. (1970) Idiopathic heinz body anaemia: Hb-Bristol 67 (E11) Val3Asp). Br. J. Haematol. 18, 435-446
10. Sakuragawa, M., Ohba, Y., Miyaji, T., Yamamoto, K., and Miwa, S. (1984) AJapanese boy with hemolytic anemia due to an unstable hemoglobin (Hb Bristol). Nihon Ketsueki Gakkai Zasshi 47, 896-902
11. Ohba, Y., Matsuoka, M., Miyaji, T., Shibuya, T., and Sakuragawa, M. (1985) Hemoglobin Bristol or-67(E11) Val3Asp in Japan. Hemoglobin 9, 79-85
12. Molchanova, T. P., Postnikov YuV, Pobedimskaya, D. D., Smetanina, N. S., Moschan, A. A., Kazanetz, E. G., Tokarev YuN, and Huisman, T. H. (1993) Hb Alesha or2(2)67(E11)Val3Met: a new unstable hemoglobin variant identified through sequencing of amplified DNA. Hemoglobin 17, 217-225
13. Wilson, J. B., Webber, B. B., Kutlar, A., Reese, A. L., McKie, V. C., Lutcher, C. L., Felice, A. E., and Huisman, T. H. (1989) Hb Evans or(2) 62(E11)Val3Met(2); an unstable hemoglobin causing a mild hemolytic anemia. Hemoglobin 13, 557-566
14. Zanotto, M. I., Calvo, K., Schvartzman, G., Deana, A., Noguera, N. L., Brags, I., and Milani, A. (2010) Hemolytic anemia due to hemoglobin Evans in an Argentinean family. n. Arch. Argentinos de Pediatria 108, 130-133
15. Crowley, M. A., Mollan, T. L., Abdulmalik, O. Y., Butler, A. D., Goodwin, E. F., Sarkar, A., Stolle, C. A., Gow, A. J., Olson, J. S., and Weiss, M. J. (2011) A hemoglobin variant associated with neonatal cyanosis and anemia. N. Engl. J. Med. 364, 1837-1843
16. Thom, C. S., Dickson, C. F., Gell, D. A., and Weiss, M. J. (2013) Hemoglobin variants: biochemical properties and clinical correlates. Cold Spring Harbor Perspect. Med. 3, a011858
17. Wiedermann, B. L., and Olson, J. S. (1975) Acceleration of tetramer formation by the binding of inositol hexaphosphate to hemoglobin dimers. J. Biol. Chem. 250, 5273-5275
18. Aebi, H., and Packer, L. (1984) [13]Catalase in vitro. Methods Enzymol. 105, 121-126
19. Shen, T. J., Ho, N. T., Simplaceanu, V., Zou, M., Green, B. N., Tam, M. F., and Ho, C. (1993) Production of unmodified human adult hemoglobin in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 90, 8108-8112
20. 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
21. 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
22. 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)-Hemoglobin stabilizing protein (AHSP) markedly decreases the redox potential and reactivity of α subunits of human HbA with hydrogen peroxide. J. Biol. Chem. 288, 4288-4298
23. Banerjee, R., Alpert, Y., Leterrier, F., and Williams, R. J. (1969) Visible absorption and electron spin resonance spectra of the isolated chains of human hemoglobin. Discussion of chain-mediated heme-heme interaction. Biochemistry 8, 2862-2867
24. Jiang, Z.-Y., Woollard, A. C., and Wolff, S. P. (1990) Hydrogen peroxide production during experimental protein glycation. FEBS Lett. 268, 69-71
25. Berzofsky, J. A., Peisach, J., and Blumberg, W. E. (1971) Sulfheme proteins. I. Optical and magnetic properties of sulfmyoglobin and its derivatives. J. Biol. Chem. 246, 3367-3377
26. Slotta, D. J., McFarland, M. A., and Markey, S. P. (2010) MassSieve: Panning MS/MS peptide data for proteins. Proteomics 10, 3035-3039
27. Birukou, I., Soman, J., and Olson, J. S. (2011) Blocking the gate to ligand entry in human hemoglobin. J. Biol. Chem. 286, 10515-10529
28. Brantley, R. E., Jr., Smerdon, S. J., Wilkinson, A. J., Singleton, E. W., and Olson, J. S. (1993) The mechanism of autoxidation of myoglobin. J. Biol. Chem. 268, 6995-7010
29. Shikama, K. (1998) The molecular mechanism of autoxidation for myoglobin and hemoglobin: A venerable puzzle. Chem. Rev. 98, 1357-1374
30. Stadtman, E. R., and Levine, R. L. (2000) Protein oxidation. Ann. N.Y. Acad. Sci. 899, 191-208
31. Kowalik-Jankowska, T., Rajewska, A., Jankowska, E., Wiśniewska, K., and Grzonka, Z. (2006) Products of Cu(II)-catalyzed oxidation of the N-terminal fragments ofα-synuclein in the presence of hydrogen peroxide. J. Inorg. Biochem. 100, 1623-1631
32. Berglund, G. I., Carlsson, G. H., Smith, A. T., Szöke, H., Henriksen, A., and Hajdu, J. (2002) The catalytic pathway of horseradish peroxidase at high resolution. Nature 417, 463-468
33. Yi, J., Thomas, L. M., and Richter-Addo, G. B. (2011) Structure of human R-state aquomethemoglobin at 2.0 Å resolution. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 67, 647-651
34. Hersleth, H. P., Dalhus, B., Görbitz, C. H., and Andersson, K. K. (2002) An iron hydroxide moiety in the 1.35 Å resolution structure of hydrogen peroxide derived myoglobin compound II at pH 5.2. J. Biol. Inorg. Chem. 7, 299-304
35. Buehler, P. W., and Alayash, A. I. (2007) Oxidation of hemoglobin: mechanisms of control in vitro and in vivo. Transfusion Alternatives in Transfusion Medicine 9, 204-212
36. Butt, O. I., Buehler, P. W., and D'Agnillo, F. (2011) Blood-brain barrier disruption and oxidative stress in guinea pig after systemic exposure to modified cell-free hemoglobin. Am. J. Pathol. 178, 1316-1328
37. Cooper, C. E., Schaer, D. J., Buehler, P. W., Wilson, M. T., Reeder, B. J., Silkstone, G., Svistunenko, D. A., Bulow, L., and Alayash, A. I. (2013) Haptoglobin binding stabilizes hemoglobin ferryl iron and the globin radical on tyrosine145. Antioxid. Redox Signal. 18, 2264-2273
38. Bonaventura, C., Henkens, R., Alayash, A. I., Banerjee, S., and Crumbliss, A. L. (2013) Molecular controls of the oxygenation and redox reactions of hemoglobin. Antioxid. Redox Signal. 18, 2298-2313
39. Jia, Y., Wood, F., Menu, P., Faivre, B., Caron, A., and Alayash, A. I. (2004) Oxygen binding and oxidation reactions of human hemoglobin conjugated to carboxylate dextran. Biochim. Biophys. Acta 1672, 164-173
40. Reeder, B. J. (2010) The redox activity of hemoglobins: from physiologic functions to pathologic mechanisms. Antioxid. Redox Signal. 13, 1087-1123
41. Reeder, B. J., Grey, M., Silaghi-Dumitrescu, R.-L., Svistunenko, D. A., Bülow, L., Cooper, C. E., and Wilson, M. T. (2008) Tyrosine residues as redox cofactors in human hemoglobin. J. Biol. Chem. 283, 30780-30787
42. Reeder, B. J., Svistunenko, D. A., Cooper, C. E., and Wilson, M. T. (2012) Engineering tyrosine-based electron flow pathways in proteins: the case of aplysia myoglobin. J. Am. Chem. Soc. 134, 7741-7749
43. Bates, D. K., Winters, R. T., and Sell, B. A. (1986) Intramolecular capture of pummerer rearrangement intermediates. 1. Synthesis of pyrrolo[2,1-C][1,4]benzothiazines. J. Heterocyclic Chem. 23, 695-699
44. Bates, D. K., Winters, R. T., and Picard, J. A. (1992) Intramolecular capture of pummerer rearrangement intermediates. 3. Interrupted pummerer rearrangement-capture of tricoordinate sulfur species generated under pummerer rearrangement conditions. J. Org. Chem. 57, 3094-3097
45. Guengerich, F. P. (2007) Mechanisms of cytochrome P450 substrate oxidation: MiniReview. J. Biochem. Mol. Toxicol. 21, 163-168
46. Cooper, C. E., Jurd, M., Nicholls, P., Wankasi, M. M., Svistunenko, D. A., and Wilson, M. T. (2005)Onthe formation, nature, stability and biological relevance of the primary reaction intermediates of myoglobins with hydrogen peroxide. Antioxid. Redox Signal. 21, 3483-3488
47. Reisberg, P. I., and Olson, J. S. (1980) Rates of isonitrile binding to the isolated α and α subunits of human hemoglobin. J. Biol. Chem. 255, 4151-4158
48. Hargrove, M. S., Whitaker, T., Olson, J. S., Vali, R. J., and Mathews, A. J. (1997) Quaternary structure regulates hemin dissociation from human hemoglobin. J. Biol. Chem. 272, 17385-17389