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Journal of Amino Acids
Volume 2011 (2011), Article ID 709404, 7 pages
http://dx.doi.org/10.4061/2011/709404
Review Article

Catalytic Site Cysteines of Thiol Enzyme: Sulfurtransferases

Department of Environmental Medicine, Nippon Medical School, 1-1-5 Sendagi Bunkyo-ku, Tokyo 113-8602, Japan

Received 23 September 2010; Accepted 9 November 2010

Academic Editor: Shandar Ahmad

Copyright © 2011 Noriyuki Nagahara. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. N. Nagahara, T. Matsumura, R. Okamoto, and Y. Kajihara, “Protein cysteine modifications: (1) medicinal chemistry for proteomics,” Current Medicinal Chemistry, vol. 16, no. 33, pp. 4419–4444, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. N. Nagahara, T. Matsumura, R. Okamoto, and Y. Kajihara, “Protein cysteine modifications: (2) reactivity specificity and topics of medicinal chemistry and protein engineering,” Current Medicinal Chemistry, vol. 16, no. 34, pp. 4490–4501, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. N. Nagahara, “Intermolecular disulfide bond to modulate protein function as a redox-sensing switch,” Amino Acids. In press. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. J. H. Quastel, C. P. Stewart, and H. E. Tunnicliffe, “On glutathione. IV. Constitution,” Biochemical Journal, vol. 17, pp. 586–592, 1923.
  5. A. Holmgren, “Glutathione-dependent synthesis of deoxyribonucleotides. Purification and characterization of glutaredoxin from Escherichia coli,” Journal of Biological Chemistry, vol. 254, no. 9, pp. 3664–3671, 1979. View at Scopus
  6. R. N. Perham and J. L. Harris, “Amino acid sequences around the reactive cysteine residues in glyceraldehyde-3-phosphate dehydrogenases,” Journal of Molecular Biology, vol. 7, pp. 316–320, 1963.
  7. S. Mohr, J. Stamler, and B. Brune, “Mechanism of covalent modification of glyceraldehyde-3- phosphate dehydrogenase at its active site thiol by nitric oxide, peroxynitrite and related nitrosating agents,” FEBS Letters, vol. 348, no. 3, pp. 223–227, 1994. View at Publisher · View at Google Scholar · View at Scopus
  8. T. Ishii, O. Sunami, H. Nakajima, H. Nishio, T. Takeuchi, and F. Hata, “Critical role of sulfenic acid formation of thiols in the inactivation of glyceraldehyde-3-phosphate dehydrogenase by nitric oxide,” Biochemical Pharmacology, vol. 58, no. 1, pp. 133–143, 1999. View at Publisher · View at Google Scholar · View at Scopus
  9. R. L. Levine, L. Mosoni, B. S. Berlett, and E. R. Stadtman, “Methionine residues as endogenous antioxidants in proteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 26, pp. 15036–15040, 1996. View at Publisher · View at Google Scholar · View at Scopus
  10. NA. E. Cheong, Y. O. Choi, and Y. O. Choi, “Molecular cloning, expression, and functional characterization of a 2Cys-peroxiredoxin in Chinese cabbage,” Plant Molecular Biology, vol. 40, no. 5, pp. 825–834, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. R. A. P. Stacy, E. Munthe, T. Steinum, B. Sharma, and R. B. Aalen, “A peroxiredoxin antioxidant is encoded by a dormancy-related gene, Per1, expressed during late development in the aleurone and embryo of barley grains,” Plant Molecular Biology, vol. 31, no. 6, pp. 1205–1216, 1996. View at Scopus
  12. K. S. Yang, S. W. Kang, H. A. Woo, S. C. Hwang, HO. Z. Chae, K. Kim, and S. G. Rhee, “Inactivation of human peroxiredoxin I during catalysis as the result of the oxidation of the catalytic site cysteine to cysteine-sulfinic acid,” Journal of Biological Chemistry, vol. 277, no. 41, pp. 38029–38036, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. B. Biteau, J. Labarre, and M. B. Toledano, “ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin,” Nature, vol. 425, no. 6961, pp. 980–984, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. M. D. Hatch and J. F. Turner, “A protein disulphide reductase from pea seeds,” The Biochemical journal, vol. 76, pp. 556–562, 1960. View at Scopus
  15. L. Zheng, R. H. White, V. L. Cash, and D. R. Dean, “Mechanism for the desulfurization of L-cysteine catalyzed by the NIFs gene product,” Biochemistry, vol. 33, no. 15, pp. 4714–4720, 1994. View at Scopus
  16. W. G. Dunphy and A. Kumagai, “The cdc25 protein contains an intrinsic phosphatase activity,” Cell, vol. 67, no. 1, pp. 189–196, 1991. View at Scopus
  17. P. A. Savitsky and T. Finkel, “Redox regulation of Cdc25C,” Journal of Biological Chemistry, vol. 277, no. 23, pp. 20535–20540, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  18. J. Sohn and J. Rudolph, “Catalytic and chemical competence of regulation of Cdc25 phosphatase by oxidation/reduction,” Biochemistry, vol. 42, no. 34, pp. 10060–10070, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. K. L. Guan and J. E. Dixon, “Evidence for protein-tyrosine-phosphatase catalysis proceeding via a cysteine-phosphate intermediate,” Journal of Biological Chemistry, vol. 266, no. 26, pp. 17026–17030, 1991. View at Scopus
  20. D. Heffetz, I. Bushkin, R. Dror, and Y. Zick, “The insulinomimetic agents H2O2 and vanadate stimulate protein tyrosine phosphorylation in intact cells,” Journal of Biological Chemistry, vol. 265, no. 5, pp. 2896–2902, 1990. View at Scopus
  21. R. Pallini, G. C. Guazzi, C. Cannella, and M. G. Cacace, “Cloning and sequence analysis of the human liver rhodanese: comparison with the bovine and chicken enzymes,” Biochemical and Biophysical Research Communications, vol. 180, no. 2, pp. 887–893, 1991. View at Publisher · View at Google Scholar · View at Scopus
  22. N. Nagahara and T. Nishino, “Role of amino acid residues in the active site of rat liver mercaptopyruvate sulfurtransferase: cDNA cloning, overexpression, and site- directed mutagenesis,” Journal of Biological Chemistry, vol. 271, no. 44, pp. 27395–27401, 1996. View at Publisher · View at Google Scholar · View at Scopus
  23. N. Nagahara and A. Katayama, “Post-translational regulation of mercaptopyruvate sulfurtransferase via a low redox potential cysteine-sulfenate in the maintenance of redox homeostasis,” Journal of Biological Chemistry, vol. 280, no. 41, pp. 34569–34576, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. B. H. Sörbo, “Crystalline rhodanese. II. The enzyme catalyzed reaction,” Acta Chemica Scandinavica, vol. 7, pp. 1137–1145, 1953.
  25. P. M. Horowitz and K. Falksen, “Oxidative inactivation of the enzyme rhodanese by reduced nicotinamide adenine dinucleotide,” Journal of Biological Chemistry, vol. 261, no. 36, pp. 16953–16956, 1986. View at Scopus
  26. P. M. Horowitz and S. Bowman, “Conformational changes accompany the oxidative inactivation of rhodanese by a variety of reagents,” Journal of Biological Chemistry, vol. 262, no. 18, pp. 8728–8733, 1987. View at Scopus
  27. E. N. Baker, “Structure of actinidin, after refinement at 1.7 θ resolution,” Journal of Molecular Biology, vol. 141, no. 4, pp. 441–484, 1980. View at Scopus
  28. R. M. Heinicke and R. Mori, “Effect of diisopropylfluorophosphate on sulfhydryl proteases,” Science, vol. 129, no. 3364, p. 1678, 1959. View at Scopus
  29. S. Ota, H. Umi, E. Muta, and Y. Okamoto, “Chemical modification of stem bromelain I-1 and fruit bromelain A with 2 hydroxy 5 nitrobenzyl bromide, tetranitromethane, and hydrogen peroxide,” Journal of Biochemistry, vol. 78, no. 3, pp. 627–635, 1975. View at Scopus
  30. T. Murachi, K. Tanaka, M. Hatanaka, and T. Murakami, “Intracellular Ca2+-dependent protease (CALPAIN) and its high-molecular-weight endogenous inhibitor (CALPASTATIN) Session VII Complex interactions and biologically active proteins,” in Advance in Enzyme Regulation 19, G. Weber, Ed., pp. 407–424, Pergamon Press, New York, NY, USA, 1981.
  31. A. Morelli, M. Grasso, and A. De Flora, “Oxidative inactivation of the calcium-stimulated neutral proteinase from human red blood cells by divicine and intracellular protection by reduced glutathione,” Archives of Biochemistry and Biophysics, vol. 251, no. 1, pp. 1–8, 1986. View at Scopus
  32. K. P. Wilson, J. A. F. Black, and J. A. F. Black, “Structure and mechanism of interleukin-1β converting enzyme,” Nature, vol. 370, no. 6487, pp. 270–275, 1994. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. V. Borutaite and G. C. Brown, “Caspases are reversibly inactivated by hydrogen peroxide,” FEBS Letters, vol. 500, no. 3, pp. 114–118, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. S. D. Elliott, “A proteolytic enzyme produced by group a streptococci with special reference to its effect on the type-specific m antigen,” The Journal of Experimental Medicine, vol. 81, pp. 573–592, 1945.
  35. M. C. Vissers and C. C. Winterbourn, “Myeloperoxidase-dependent oxidative inactivation of neutrophil neutral proteinases and microbicidal enzymes,” Biochemical Journal, vol. 245, no. 1, pp. 277–280, 1987. View at Scopus
  36. M. Ebata and K. T. Yasunobu, “Chymopapain. I. Isolation, crystallization, and preliminary characterization,” The Journal of Biological Chemistry, vol. 237, pp. 1086–1094, 1962. View at Scopus
  37. M. C. Vissers and C. C. Winterbourn, “Myeloperoxidase-dependent oxidative inactivation of neutrophil neutral proteinases and microbicidal enzymes,” Biochemical Journal, vol. 245, no. 1, pp. 277–280, 1987. View at Scopus
  38. R. M. Metrione, R. B. Johnston, and R. Seng, “Purification, partial characterization, and sequence around a reactive sulfhydryl of ficin,” Archives of Biochemistry and Biophysics, vol. 122, no. 1, pp. 137–143, 1967. View at Scopus
  39. T. Pechan, B. Jiang, D. Steckler, L. Ye, L. Lin, D. S. Luthe, and W. P. Williams, “Characterization of three distinct cDNA clones encoding cysteine proteinases from maize (Zea mays L.) callus,” Plant Molecular Biology, vol. 40, no. 1, pp. 111–119, 1999. View at Scopus
  40. S. D. Elliott, “A proteolytic enzyme produced by group a streptococci with special reference to its effect on the type-specific m antigen,” The Journal of Experimental Medicine, vol. 81, pp. 573–592, 1945.
  41. W. S. Lin, D. A. Armstrong, and G. M. Gaucher, “Formation and repair of papain sulfenic acid,” Canadian Journal of Biochemistry, vol. 53, no. 3, pp. 298–307, 1975. View at Scopus
  42. J. C. Edman, L. Ellis, R. W. Blacher, R. A. Roth, and W. J. Rutter, “Sequence of protein disulphide isomerase and implications of its relationship to thioredoxin,” Nature, vol. 317, no. 6034, pp. 267–270, 1985. View at Scopus
  43. C. Jacob, I. Knight, and P. G. Winyard, “Aspects of the biological redox chemistry of cysteine: from simple redox responses to sophisticated signalling pathways,” Biological Chemistry, vol. 387, no. 10-11, pp. 1385–1397, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. AL. Claiborne, J. I. Yeh, T. C. Mallett, J. Luba, E. J. Crane, V. Charrier, and D. Parsonage, “Protein-sulfenic acids: diverse roles for an unlikely player in enzyme catalysis and redox regulation,” Biochemistry, vol. 38, no. 47, pp. 15407–15416, 1999. View at Publisher · View at Google Scholar · View at Scopus
  45. L. B. Poole, P. A. Karplus, and AL. Claiborne, “Protein sulfenic acids in redox signaling,” Annual Review of Pharmacology and Toxicology, vol. 44, pp. 325–347, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. B. Hofmann, H. J. Hecht, and L. Flohé, “Peroxiredoxins,” Biological Chemistry, vol. 383, no. 3-4, pp. 347–364, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. A. Salmeen, J. N. Andersen, M. P. Myers, T. C. Meng, J. A. Hinks, N. K. Tonks, and D. Barford, “Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate,” Nature, vol. 423, no. 6941, pp. 769–773, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  48. R. L. M. Van Montfort, M. Congreve, D. Tisi, R. Carr, and H. Jhoti, “Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B,” Nature, vol. 423, no. 6941, pp. 773–777, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  49. K. Soda, A. Novogrodsky, and A. Meister, “Enzymatic desulfination of cysteine sulfinic acid,” Biochemistry, vol. 3, no. 10, pp. 1450–1454, 1964. View at Scopus
  50. H. Mihara, T. Kurihara, T. Yoshimura, K. Soda, and N. Esaki, “Cysteine sulfinate desulfinase, a NIFS-like protein of Escherichia coli with selenocysteine lyase and cysteine desulfurase activities. Gene cloning, purification, and characterization of a novel pyridoxal enzyme,” Journal of Biological Chemistry, vol. 272, no. 36, pp. 22417–22424, 1997. View at Publisher · View at Google Scholar · View at Scopus
  51. B. Biteau, J. Labarre, and M. B. Toledano, “ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin,” Nature, vol. 425, no. 6961, pp. 980–984, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  52. G. Georgiou and L. Masip, “An overoxidation journey with a return ticket,” Science, vol. 300, no. 5619, pp. 592–594, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  53. C. Jacob, A. L. Holme, and F. H. Fry, “The sulfinic acid switch in proteins,” Organic and Biomolecular Chemistry, vol. 2, no. 14, pp. 1953–1956, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  54. W. G. J. Hol, “The role of the α-helix dipole in protein function and structure,” Progress in Biophysics and Molecular Biology, vol. 45, no. 3, pp. 149–195, 1985. View at Scopus
  55. T. Kortemme and T. E. Creighton, “Ionisation of cysteine residues at the termini of model α-helical peptides. Relevance to unusual thiol pKa values in proteins of the thioredoxin family,” Journal of Molecular Biology, vol. 253, no. 5, pp. 799–812, 1995. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. N. Nagahara, “Molecular evolution of thioredoxin-dependent redox-sensing switch in mercaptopyruvate sulfurtransferase,” in Research Advances in Biological Chemistry, R. M. Mohan, Ed., vol. 1, pp. 19–26, Global Research Network, Kerala, India, 2007.
  57. M. S. Alphey, R. A. M. Williams, J. C. Mottram, G. H. Coombs, and W. N. Hunter, “The crystal structure of leishmania major 3-mercaptopyruvate sulfurtransferase. A three-domain architecture with a serine protease-like triad at the active site,” Journal of Biological Chemistry, vol. 278, no. 48, pp. 48219–48227, 2003. View at Publisher · View at Google Scholar · View at PubMed
  58. J. H. Ploegman, G. Drent, K. H. Kalk, and W. G. J. Hol, “Structure of bovine liver rhodanese. I. Structure determination at 2.5 Å resolution and a comparison of the conformation and sequence of its two domains,” Journal of Molecular Biology, vol. 123, no. 4, pp. 557–594, 1978.
  59. J. H. Ploegman, GÉ. Drent, K. H. Kalk, and W. G. J. Hol, “The structure of bovine liver rhodanese. II. The active site in the sulfur-substituted and the sulfur-free enzyme,” Journal of Molecular Biology, vol. 127, no. 2, pp. 149–162, 1979.
  60. J. H. Ploegman, G. Drent, and K. H. Kalk, “The covalent and tertiary structure of bovine liver rhodanese,” Nature, vol. 273, no. 5658, pp. 124–129, 1978.
  61. W. G. J. Hol, L. J. Lijk, and K. H. Kalk, “The high resolution three-dimensional structure of bovine liver rhodanese,” Fundamental and Applied Toxicology, vol. 3, no. 5, pp. 370–376, 1983.
  62. P. Schlesinger and J. Westley, “An expanded mechanism for rhodanese catalysis,” Journal of Biological Chemistry, vol. 249, no. 3, pp. 780–788, 1974.
  63. T. Fujii, M. Maeda, H. Mihara, T. Kurihara, N. Esaki, and Y. Hata, “Structure of a NifS homologue: X-ray structure analysis of CsdB, an Escherichia coli counterpart of mammalian selenocysteine lyase,” Biochemistry, vol. 39, no. 6, pp. 1263–1273, 2000. View at Publisher · View at Google Scholar
  64. D. Bordo, D. Deriu, R. Colnaghi, A. Carpen, S. Pagani, and M. Bolognesi, “The crystal structure of a sulfurtransferase from Azotobacter vinelandii highlights the evolutionary relationship between the rhodanese and phosphatase enzyme families,” Journal of Molecular Biology, vol. 298, no. 4, pp. 691–704, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  65. D. Bordo and P. Bork, “The rhodanese/Cdc25 phosphatase superfamily. Sequence-structure-function relations,” EMBO Reports, vol. 3, no. 8, pp. 741–746, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  66. R. A. Reynolds, A. W. Yem, C. L. Wolfe, M. R. Deibel, C. G. Chidester, and K. D. Watenpaugh, “Crystal structure of the catalytic subunit of Cdc25B required for G/M phase transition of the cell cycle,” Journal of Molecular Biology, vol. 293, no. 3, pp. 559–568, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  67. C. D. Lima, “Analysis of the E. coli NifS CsdB protein at 2.0 Å reveals the structural basis for perselenide and persulfide intermediate formation,” Journal of Molecular Biology, vol. 315, no. 5, pp. 1199–1208, 2002. View at Publisher · View at Google Scholar · View at PubMed
  68. D. L. Nandi, P. M. Horowitz, and J. Westley, “Rhodanese as a thioredoxin oxidase,” International Journal of Biochemistry and Cell Biology, vol. 32, no. 4, pp. 465–473, 2000. View at Publisher · View at Google Scholar
  69. E. Moutevelis and J. Warwicker, “Prediction of pKa and redox properties in the thioredoxin superfamily,” Protein Science, vol. 13, no. 10, pp. 2744–2752, 2004. View at Publisher · View at Google Scholar · View at PubMed
  70. N. Nagahara, T. Okazaki, and T. Nishino, “Cytosolic mercaptopyruvate sulfurtransferase is evolutionarily related to mitochondrial rhodanese. Striking similarity in active site amino acid sequence and the increase in the mercaptopyruvate sulfurtransferase activity of rhodanese by site-directed mutagenesis,” Journal of Biological Chemistry, vol. 270, no. 27, pp. 16230–16235, 1995. View at Publisher · View at Google Scholar
  71. T. Nakamura, Y. Yamaguchi, and H. Sano, “Plant mercaptopyruvate sulfurtransferases molecular cloning, subcellular localization and enzymatic activities,” European Journal of Biochemistry, vol. 267, no. 17, pp. 5621–5630, 2000. View at Publisher · View at Google Scholar
  72. C. de Duve, B. C. Pressman, R. Gianetto, R. Wattiaux, and F. Appehmans, “Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue,” The Biochemical journal, vol. 60, no. 4, pp. 604–617, 1955.
  73. A. Koj, J. Frendo, and L. Wojtczak, “Subcellular distribution and intramitochondrial localization of three sulfurtransferases in rat liver,” FEBS Letters, vol. 57, no. 1, pp. 42–46, 1975. View at Publisher · View at Google Scholar
  74. J. Papenbrock and A. Schmidt, “Characterization of a sulfurtransferase from Arabidopsis thaliana,” European Journal of Biochemistry, vol. 267, no. 1, pp. 145–154, 2000. View at Publisher · View at Google Scholar
  75. M. Elchebly, P. Payette, and P. Payette, “Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene,” Science, vol. 283, no. 5407, pp. 1544–1548, 1999. View at Publisher · View at Google Scholar
  76. L. D. Klaman, O. Boss, and O. Boss, “Increased energy expenditure, decreased adiposity, and tissue-specific insulin sensitivity in protein-tyrosine phosphatase 1B-deficient mice,” Molecular and Cellular Biology, vol. 20, no. 15, pp. 5479–5489, 2000. View at Publisher · View at Google Scholar
  77. B. G. Neel and N. K. Tonks, “Protein tyrosine phosphatases in signal transduction,” Current Opinion in Cell Biology, vol. 9, no. 2, pp. 193–204, 1997. View at Publisher · View at Google Scholar
  78. J. M. Denu and J. E. Dixon, “Protein tyrosine phosphatases: Mechanisms of catalysis and regulation,” Current Opinion in Chemical Biology, vol. 2, no. 5, pp. 633–641, 1998.
  79. S.-R. Lee, K.-S. Kwon, S.-R. Kim, and S. G. Rhee, “Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor,” Journal of Biological Chemistry, vol. 273, no. 25, pp. 15366–15372, 1998. View at Publisher · View at Google Scholar
  80. T. C. Meng, T. Fukada, and N. K. Tonks, “Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo,” Molecular Cell, vol. 9, no. 2, pp. 387–399, 2002. View at Publisher · View at Google Scholar
  81. L. O. Narhi, T. Arakawa, K. H. Aoki, R. Elmore, M. F. Rohde, T. Boone, and T. W. Strickland, “The effect of carbohydrate on the structure and stability of erythropoietin,” Journal of Biological Chemistry, vol. 266, no. 34, pp. 23022–23026, 1991.