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Evolution of Structural and Coordination Features Within the Methionine Sulfoxide Reductase B Family

  • Elena Shumilina
  • Olena Dobrovolska
  • Alexander DikiyEmail author
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 39)

Summary

In this review, we summarize the evolution, sequence, structural and coordination peculiarities of proteins belonging to the Methionine Sulfoxide Reductase B family (MsrBs). These proteins represent important redox proteins. MsrBs are found in all kingdoms of life. Whereas prokaryotes have only one type of MsrB, mammals possess three, MsrB1, MsrB2 and MsrB3, distributed in different cellular compartments, and regulated by alternative splicing and specific targeting signals. Structural analysis of mammalian and bacterial MsrBs revealed a well-conserved β-core, and dramatic variability in C-and N-terminus. Mostly, MsrBs contain structural zinc ions coordinated by four cysteines. However, some of MsrBs lack coordinating cysteines and, therefore may not contain zinc ion.

Keywords

Adenylate Kinase Meet Residue Methionine Sulfoxide Methionine Sulfoxide Reductase Zinc Binding Site 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations:

Met

– Methionine

Msr

– Methionine sulfoxide reductase

MsrB

– Methionine sulfoxide reductase B

ROS

– Reactive oxygen species

Notes

Acknowledgements

AD acknowledges the support from NT Faculty, NTNU. ES acknowledges the NT Faculty, NTNU, for financial support through a post-doctoral fellowship. OD acknowledges the NT Faculty, NTNU, for financial support through a PhD fellowship.

References

  1. Aachmann FL, Sal LS, Kim HY, Marino SM, Gladyshev VN, Dikiy A (2010) Insights into function, catalytic mechanism, and fold evolution of selenoprotein methionine sulfoxide reductase B1 through structural analysis. J Biol Chem 285:33315–33323PubMedCentralPubMedCrossRefGoogle Scholar
  2. Aachmann FL, Kwak GH, Del Conte R, Kim HY, Gladyshev VN, Dikiy A (2011) Structural and biochemical analysis of mammalian methionine sulfoxide reductase B2. Proteins 79:3123–3131PubMedCentralPubMedCrossRefGoogle Scholar
  3. Andreini C, Bertini I, Cavallaro G, Holliday GL, Thornton JM (2008) Metal ions in biological catalysis: from enzyme databases to general principles. J Biol Inorg Chem 13:1205–1218PubMedCrossRefGoogle Scholar
  4. Auld DS (2001a) Zinc coordination sphere in biochemical zinc sites. Biometals 14:271–313PubMedCrossRefGoogle Scholar
  5. Auld DS (2001b) Zinc sites in metalloenzymes and related proteins. In: Bertini I, Sigel A, Sigel H (eds) Handbook on metalloproteins. Marcel Dekker, New York, pp 881–959Google Scholar
  6. Bar-Noy S, Moskovitz J (2002) Mouse methionine sulfoxide reductase B: effect of selenocysteine incorporation on its activity and expression of the seleno-containing enzyme in bacterial and mammalian cells. Biochem Biophys Res Commun 297:956–961PubMedCrossRefGoogle Scholar
  7. Bell IM, Fisher ML, Wu ZP, Hilvert D (1993) Kinetic studies on the peroxidase activity of selenosubtilisin. Biochemistry 32:3754–3762PubMedCrossRefGoogle Scholar
  8. Berry MB, Phillips GN Jr (1998) Crystal structures of Bacillus stearothermophilus adenylate kinase with bound Ap5A, Mg2+ Ap5A, and Mn2+ Ap5A reveal an intermediate lid position and six coordinate octahedral geometry for bound Mg2+ and Mn2+. Proteins 32:276–288PubMedCrossRefGoogle Scholar
  9. Bertini I, Sigel A, Sigel H (2001) Handbook on metalloproteins. Marcel Dekker, New YorkGoogle Scholar
  10. Bock A, Forchhammer K, Heider J, Baron C (1991) Selenoprotein synthesis: an expansion of the genetic code. Trends Biochem Sci 16:463–467PubMedCrossRefGoogle Scholar
  11. Boschi-Muller S, Azza S, Sanglier-Cianferani S, Talfournier F, Van Dorsselear A, Branlant G (2000) A sulfenic acid enzyme intermediate is involved in the catalytic mechanism of peptide methionine sulfoxide reductase from Escherichia coli. J Biol Chem 275:35908–35913PubMedCrossRefGoogle Scholar
  12. Boschi-Muller S, Olry A, Antoine M, Branlant G (2005) The enzymology and biochemistry of methionine sulfoxide reductases. Biochim Biophys Acta 1703:231–238PubMedCrossRefGoogle Scholar
  13. Boschi-Muller S, Gand A, Branlant G (2008) The methionine sulfoxide reductases: catalysis and substrate specificities. Arch Biochem Biophys 474:266–273PubMedCrossRefGoogle Scholar
  14. Brot N, Weissbach H (1983) Biochemistry and physiological role of methionine sulfoxide residues in proteins. Arch Biochem Biophys 223:271–281PubMedCrossRefGoogle Scholar
  15. Brot N, Weissbach H (2000) Peptide methionine sulfoxide reductase: biochemistry and physiological role. Biopolymers 55:288–296PubMedCrossRefGoogle Scholar
  16. Brot N, Weissbach L, Werth J, Weissbach H (1981) Enzymatic reduction of protein-bound methionine sulfoxide. Proc Natl Acad Sci U S A 78:2155–2158PubMedCentralPubMedCrossRefGoogle Scholar
  17. Caldwell P, Luk DC, Weissbach H, Brot N (1978) Oxidation of the methionine residues of Escherichia coli ribosomal protein L12 decreases the protein’s biological activity. Proc Natl Acad Sci U S A 75:5349–5352PubMedCentralPubMedCrossRefGoogle Scholar
  18. Carfi A, Pares S, Duee E, Galleni M, Duez C, Frere JM, Dideberg O (1995) The 3-D structure of a zinc metallo-beta-lactamase from Bacillus cereus reveals a new type of protein fold. EMBO J 14:4914–4921PubMedCentralPubMedGoogle Scholar
  19. Ciorba MA, Heinemann SH, Weissbach H, Brot N, Hoshi T (1997) Modulation of potassium channel function by methionine oxidation and reduction. Proc Natl Acad Sci U S A 94:9932–9937PubMedCentralPubMedCrossRefGoogle Scholar
  20. Ciorba MA, Heinemann SH, Weissbach H, Brot N, Hoshi T (1999) Regulation of voltage-dependent K + channels by methionine oxidation: effect of nitric oxide and vitamin C. FEBS Lett 442:48–52PubMedCrossRefGoogle Scholar
  21. Dobrovolska O, Rychkov G, Shumilina E, Nerinovski K, Schmidt A, Shabalin K, Yakimov A, Dikiy A (2012) Structural insights into interaction between mammalian methionine sulfoxide reductase B1 and thioredoxin. J Biomed Biotechnol 2012:586539PubMedCentralPubMedCrossRefGoogle Scholar
  22. Ezraty B, Aussel L, Barras F (2005) Methionine sulfoxide reductases in prokaryotes. Biochim Biophys Acta 1703:221–229PubMedCrossRefGoogle Scholar
  23. Fabiane SM, Sohi MK, Wan T, Payne DJ, Bateson JH, Mitchell T, Sutton BJ (1998) Crystal structure of the zinc-dependent beta-lactamase from Bacillus cereus at 1.9 A resolution: binuclear active site with features of a mononuclear enzyme. Biochemistry 37:12404–12411PubMedCrossRefGoogle Scholar
  24. Fomenko DE, Xing W, Adair BM, Thomas DJ, Gladyshev VN (2007) High-throughput identification of catalytic redox-active cysteine residues. Science 315:387–389PubMedCrossRefGoogle Scholar
  25. Gerdts CJ, Elliott M, Lovell S, Mixon MB, Napuli AJ, Staker BL, Nollert P, Stewart L (2008) The plug-based nanovolume Microcapillary Protein Crystallization System (MPCS). Acta Crystallogr Sect D 64:1116–1122CrossRefGoogle Scholar
  26. Gladyshev VN, Jeang KT, Stadtman TC (1996) Selenocysteine, identified as the penultimate C-terminal residue in human T-cell thioredoxin reductase, corresponds to TGA in the human placental gene. Proc Natl Acad Sci U S A 93:6146–6151PubMedCentralPubMedCrossRefGoogle Scholar
  27. Go YM, Jones DP (2008) Redox compartmentalization in eukaryotic cells. Biochim Biophys Acta 1780:1273–1290PubMedCentralPubMedCrossRefGoogle Scholar
  28. Gromer S, Johansson L, Bauer H, Arscott LD, Rauch S, Ballou DP, Williams CH Jr, Schirmer RH, Arner ES (2003) Active sites of thioredoxin reductases: why selenoproteins? Proc Natl Acad Sci U S A 100:12618–12623PubMedCentralPubMedCrossRefGoogle Scholar
  29. Hansel A, Jung S, Hoshi T, Heinemann SH (2003) A second human methionine sulfoxide reductase (hMSRB2) reducing methionine-R-sulfoxide displays a tissue expression pattern distinct from hMSRB1. Redox Rep 8:384–388PubMedCrossRefGoogle Scholar
  30. Hansel A, Heinemann SH, Hoshi T (2005) Heterogeneity and function of mammalian MSRs: enzymes for repair, protection and regulation. Biochim Biophys Acta 1703:239–247PubMedCrossRefGoogle Scholar
  31. Hatfield DL, Gladyshev VN (2002) How selenium has altered our understanding of the genetic code. Mol Cell Biol 22:3565–3576PubMedCentralPubMedCrossRefGoogle Scholar
  32. Hondal RJ, Nilsson BL, Raines RT (2001) Selenocysteine in native chemical ligation and expressed protein ligation. J Am Chem Soc 123:5140–5141PubMedCrossRefGoogle Scholar
  33. Huang W, Escribano J, Sarfarazi M, Coca-Prados M (1999) Identification, expression and chromosome localization of a human gene encoding a novel protein with similarity to the pilB family of transcriptional factors (pilin) and to bacterial peptide methionine sulfoxide reductases. Gene 233:233–240PubMedCrossRefGoogle Scholar
  34. Huber RE, Criddle RS (1967) Comparison of the chemical properties of selenocysteine and selenocystine with their sulfur analogs. Arch Biochem Biophys 122:164–173PubMedCrossRefGoogle Scholar
  35. Jung S, Hansel A, Kasperczyk H, Hoshi T, Heinemann SH (2002) Activity, tissue distribution and site-directed mutagenesis of a human peptide methionine sulfoxide reductase of type B: hCBS1. FEBS Lett 527:91–94PubMedCrossRefGoogle Scholar
  36. Kauffmann B, Favier F, Olry A, Boschi-Muller S, Carpentier P, Branlant G, Aubry A (2002) Crystallization and preliminary X-ray diffraction studies of the peptide methionine sulfoxide reductase B domain of Neisseria meningitidis PILB. Acta Crystallogr D Biol Crystallogr 58:1467–1469PubMedCrossRefGoogle Scholar
  37. Kim HY, Gladyshev VN (2004a) Characterization of mouse endoplasmic reticulum methionine-R-sulfoxide reductase. Biochem Biophys Res Commun 320:1277–1283PubMedCrossRefGoogle Scholar
  38. Kim HY, Gladyshev VN (2004b) Methionine sulfoxide reduction in mammals: characterization of methionine-R-sulfoxide reductases. Mol Biol Cell 15:1055–1064PubMedCentralPubMedCrossRefGoogle Scholar
  39. Kim HY, Gladyshev VN (2005) Different catalytic mechanisms in mammalian selenocysteine- and cysteine-containing methionine-R-sulfoxide reductases. PLoS Biol 3:e375PubMedCentralPubMedCrossRefGoogle Scholar
  40. Kim HY, Gladyshev VN (2006) Alternative first exon splicing regulates subcellular distribution of methionine sulfoxide reductases. BMC Mol Biol 7:11PubMedCentralPubMedCrossRefGoogle Scholar
  41. Kim HY, Gladyshev VN (2007) Methionine sulfoxide reductases: selenoprotein forms and roles in antioxidant protein repair in mammals. Biochem J 407:321–329PubMedCrossRefGoogle Scholar
  42. Kim HY, Kim JR (2008) Thioredoxin as a reducing agent for mammalian methionine sulfoxide reductases B lacking resolving cysteine. Biochem Biophys Res Commun 371:490–494PubMedCrossRefGoogle Scholar
  43. Kim HY, Fomenko DE, Yoon YE, Gladyshev VN (2006) Catalytic advantages provided by selenocysteine in methionine-S-sulfoxide reductases. Biochemistry 45:13697–13704PubMedCentralPubMedCrossRefGoogle Scholar
  44. Kim YK, Shin YJ, Lee WH, Kim HY, Hwang KY (2009) Structural and kinetic analysis of an MsrA-MsrB fusion protein from Streptococcus pneumoniae. Mol Microbiol 72:699–709PubMedCentralPubMedCrossRefGoogle Scholar
  45. Korndorfer IP, Fessner WD, Matthews BW (2000) The structure of rhamnose isomerase from Escherichia coli and its relation with xylose isomerase illustrates a change between inter and intra-subunit complementation during evolution. J Mol Biol 300:917–933PubMedCrossRefGoogle Scholar
  46. Kryukov GV, Kumar RA, Koc A, Sun Z, Gladyshev VN (2002) Selenoprotein R is a zinc-containing stereo-specific methionine sulfoxide reductase. Proc Natl Acad Sci U S A 99:4245–4250PubMedCentralPubMedCrossRefGoogle Scholar
  47. Kumar RA, Koc A, Cerny RL, Gladyshev VN (2002) Reaction mechanism, evolutionary analysis, and role of zinc in Drosophila methionine-R-sulfoxide reductase. J Biol Chem 277:37527–37535PubMedCrossRefGoogle Scholar
  48. Kuschel L, Hansel A, Schonherr R, Weissbach H, Brot N, Hoshi T, Heinemann SH (1999) Molecular cloning and functional expression of a human peptide methionine sulfoxide reductase (hMsrA). FEBS Lett 456:17–21PubMedCrossRefGoogle Scholar
  49. Lange OF, Rossi P, Sgourakis NG, Song Y, Lee HW, Aramini JM, Ertekin A, Xiao R, Acton TB, Montelione GT, Baker D (2012) Determination of solution structures of proteins up to 40 kDa using CS-Rosetta with sparse NMR data from deuterated samples. Proc Natl Acad Sci U S A 109:10873–10878PubMedCentralPubMedCrossRefGoogle Scholar
  50. Lee TH, Kim HY (2008) An anaerobic bacterial MsrB model reveals catalytic mechanisms, advantages, and disadvantages provided by selenocysteine and cysteine in reduction of methionine-R-sulfoxide. Arch Biochem Biophys 478:175–180PubMedCrossRefGoogle Scholar
  51. Lee BC, Lee YK, Lee HJ, Stadtman ER, Lee KH, Chung N (2005) Cloning and characterization of antioxidant enzyme methionine sulfoxide-S-reductase from Caenorhabditis elegans. Arch Biochem Biophys 434:275–281PubMedCrossRefGoogle Scholar
  52. Lee BC, Dikiy A, Kim HY, Gladyshev VN (2009) Functions and evolution of selenoprotein methionine sulfoxide reductases. Biochim Biophys Acta 1790:1471–1477PubMedCentralPubMedCrossRefGoogle Scholar
  53. Lemire BD, Fankhauser C, Baker A, Schatz G (1989) The mitochondrial targeting function of randomly generated peptide sequences correlates with predicted helical amphiphilicity. J Biol Chem 264:20206–20215PubMedGoogle Scholar
  54. Levine RL, Mosoni L, Berlett BS, Stadtman ER (1996) Methionine residues as endogenous antioxidants in proteins. Proc Natl Acad Sci U S A 93:15036–15040PubMedCentralPubMedCrossRefGoogle Scholar
  55. Levine RL, Berlett BS, Moskovitz J, Mosoni L, Stadtman ER (1999) Methionine residues may protect proteins from critical oxidative damage. Mech Ageing Dev 107:323–332PubMedCrossRefGoogle Scholar
  56. Lin TY (1999) G33D mutant thioredoxin primarily affects the kinetics of reaction with thioredoxin reductase. Probing the structure of the mutant protein. Biochemistry 38:15508–15513PubMedCrossRefGoogle Scholar
  57. Lippard SJ, Berg JM (1994) Principles of bioinorganic chemistry. University Science, Mill ValleyGoogle Scholar
  58. Lowther WT, Brot N, Weissbach H, Matthews BW (2000) Structure and mechanism of peptide methionine sulfoxide reductase, an “anti-oxidation” enzyme. Biochemistry 39:13307–13312PubMedCrossRefGoogle Scholar
  59. Lowther WT, Weissbach H, Etienne F, Brot N, Matthews BW (2002) The mirrored methionine sulfoxide reductases of Neisseria gonorrhoeae pilB. Nat Struct Biol 9:348–352PubMedGoogle Scholar
  60. Makarova KS, Ponomarev VA, Koonin EV (2001) Two C or not two C: recurrent disruption of Zn-ribbons, gene duplication, lineage-specific gene loss, and horizontal gene transfer in evolution of bacterial ribosomal proteins. Genome Biol 2 (9):research0033.1–0033.14Google Scholar
  61. Metanis N, Keinan E, Dawson PE (2006) Synthetic seleno-glutaredoxin 3 analogues are highly reducing oxidoreductases with enhanced catalytic efficiency. J Am Chem Soc 128:16684–16691PubMedCentralPubMedCrossRefGoogle Scholar
  62. Moskovitz J, Weissbach H, Brot N (1996) Cloning the expression of a mammalian gene involved in the reduction of methionine sulfoxide residues in proteins. Proc Natl Acad Sci U S A 93:2095–2099PubMedCentralPubMedCrossRefGoogle Scholar
  63. Moskovitz J, Poston JM, Berlett BS, Nosworthy NJ, Szczepanowski R, Stadtman ER (2000) Identification and characterization of a putative active site for peptide methionine sulfoxide reductase (MsrA) and its substrate stereospecificity. J Biol Chem 275:14167–14172PubMedCrossRefGoogle Scholar
  64. Mulkidjanian AY, Galperin MY (2009) On the origin of life in the zinc world. 2. Validation of the hypothesis on the photosynthesizing zinc sulfide edifices as cradles of life on Earth. Biol Direct 4:27PubMedCentralPubMedCrossRefGoogle Scholar
  65. Muttenthaler M, Alewood PF (2008) Selenopeptide chemistry. J Pept Sci 14:1223–1239PubMedCrossRefGoogle Scholar
  66. Neupert W (1997) Protein import into mitochondria. Annu Rev Biochem 66:863–917PubMedCrossRefGoogle Scholar
  67. Novoselov SV, Rao M, Onoshko NV, Zhi H, Kryukov GV, Xiang Y, Weeks DP, Hatfield DL, Gladyshev VN (2002) Selenoproteins and selenocysteine insertion system in the model plant cell system, Chlamydomonas reinhardtii. EMBO J 21:3681–3693PubMedCentralPubMedCrossRefGoogle Scholar
  68. Ohno S (1970) Evolution by gene duplication. Springer, BerlinCrossRefGoogle Scholar
  69. Olry A, Boschi-Muller S, Marraud M, Sanglier-Cianferani S, Van Dorsselear A, Branlant G (2002) Characterization of the methionine sulfoxide reductase activities of PILB, a probable virulence factor from Neisseria meningitidis. J Biol Chem 277:12016–12022PubMedCrossRefGoogle Scholar
  70. Olry A, Boschi-Muller S, Branlant G (2004) Kinetic characterization of the catalytic mechanism of methionine sulfoxide reductase B from Neisseria meningitidis. Biochemistry 43:11616–11622PubMedCrossRefGoogle Scholar
  71. Olry A, Boschi-Muller S, Yu H, Burnel D, Branlant G (2005) Insights into the role of the metal binding site in methionine-R-sulfoxide reductases B. Protein Sci 14:2828–2837PubMedCentralPubMedCrossRefGoogle Scholar
  72. Panina EM, Mironov AA, Gelfand MS (2003) Comparative genomics of bacterial zinc regulons: enhanced ion transport, pathogenesis, and rearrangement of ribosomal proteins. Proc Natl Acad Sci U S A 100:9912–9917PubMedCentralPubMedCrossRefGoogle Scholar
  73. Pearson RG, Sobel H, Songstad J (1968) Nucleophilic reactivity constants toward methyl iodide and trans-[Pt(Py)2cl2]. J Am Chem Soc 90:319CrossRefGoogle Scholar
  74. Perrier V, Surewicz WK, Glaser P, Martineau L, Craescu CT, Fabian H, Mantsch HH, Barzu O, Gilles AM (1994) Zinc chelation and structural stability of adenylate kinase from Bacillus subtilis. Biochemistry 33:9960–9967PubMedCrossRefGoogle Scholar
  75. Ranaivoson FM, Neiers F, Kauffmann B, Boschi-Muller S, Branlant G, Favier F (2009) Methionine sulfoxide reductase B displays a high level of flexibility. J Mol Biol 394:83–93PubMedCrossRefGoogle Scholar
  76. Roise D, Schatz G (1988) Mitochondrial presequences. J Biol Chem 263:4509–4511PubMedGoogle Scholar
  77. Russel M, Model P (1986) The role of thioredoxin in filamentous phage assembly. Construction, isolation, and characterization of mutant thioredoxins. J Biol Chem 261:14997–15005PubMedGoogle Scholar
  78. Sharov VS, Ferrington DA, Squier TC, Schoneich C (1999) Diastereoselective reduction of protein-bound methionine sulfoxide by methionine sulfoxide reductase. FEBS Lett 455:247–250PubMedCrossRefGoogle Scholar
  79. Shechter Y (1986) Selective oxidation and reduction of methionine residues in peptides and proteins by oxygen exchange between sulfoxide and sulfide. J Biol Chem 261:66–70PubMedGoogle Scholar
  80. Shumilina E, Dobrovolska O, Del Conte R, Holen HW, Dikiy A (2014) Competitive cobalt for zinc substitution in mammalian methionine sulfoxide reductase B1 overexpressed in E.coli: structural and functional insight. J Biol Inorg Chem 19(1):85–95PubMedCentralPubMedCrossRefGoogle Scholar
  81. Singh VK, Moskovitz J (2003) Multiple methionine sulfoxide reductase genes in Staphylococcus aureus: expression of activity and roles in tolerance of oxidative stress. Microbiology 149:2739–2747PubMedCrossRefGoogle Scholar
  82. Stadtman TC (1996) Selenocysteine. Annu Rev Biochem 65:83–100PubMedCrossRefGoogle Scholar
  83. Sun H, Gao J, Ferrington DA, Biesiada H, Williams TD, Squier TC (1999) Repair of oxidized calmodulin by methionine sulfoxide reductase restores ability to activate the plasma membrane Ca-ATPase. Biochemistry 38:105–112PubMedCrossRefGoogle Scholar
  84. Truscott KN, Pfanner N, Voos W (2001) Transport of proteins into mitochondria. Rev Physiol Biochem Pharmacol 143:81–136PubMedCrossRefGoogle Scholar
  85. Vallee BL, Auld DS (1990) Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 29:5647–5659PubMedCrossRefGoogle Scholar
  86. Vogt W (1995) Oxidation of methionyl residues in proteins: tools, targets, and reversal. Free Radic Biol Med 18:93–105PubMedCrossRefGoogle Scholar
  87. von Heijne G (1986a) Mitochondrial targeting sequences may form amphiphilic helices. EMBO J 5:1335–1342Google Scholar
  88. von Heijne G (1986b) Towards a comparative anatomy of N-terminal topogenic protein sequences. J Mol Biol 189:239–242CrossRefGoogle Scholar
  89. von Heijne G (1990) Protein targeting signals. Curr Opin Cell Biol 2:604–608CrossRefGoogle Scholar
  90. Vougier S, Mary J, Friguet B (2003) Subcellular localization of methionine sulphoxide reductase A (MsrA): evidence for mitochondrial and cytosolic isoforms in rat liver cells. Biochem J 373:531–537PubMedCentralPubMedCrossRefGoogle Scholar
  91. Whitlow M, Howard AJ, Finzel BC, Poulos TL, Winborne E, Gilliland GL (1991) A metal-mediated hydride shift mechanism for xylose isomerase based on the 1.6 A Streptomyces rubiginosus structures with xylitol and D-xylose. Proteins 9:153–173PubMedCrossRefGoogle Scholar
  92. Yao Y, Yin D, Jas GS, Kuczer K, Williams TD, Schoneich C, Squier TC (1996) Oxidative modification of a carboxyl-terminal vicinal methionine in calmodulin by hydrogen peroxide inhibits calmodulin-dependent activation of the plasma membrane Ca-ATPase. Biochemistry 35:2767–2787PubMedCrossRefGoogle Scholar
  93. Yu HJ, Liu JQ, Bock A, Li J, Luo GM, Shen JC (2005) Engineering glutathione transferase to a novel glutathione peroxidase mimic with high catalytic efficiency. Incorporation of selenocysteine into a glutathione-binding scaffold using an auxotrophic expression system. J Biol Chem 280:11930–11935PubMedCrossRefGoogle Scholar
  94. Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298CrossRefGoogle Scholar
  95. Zhang J (2012) Genetic redundancies and their evolutionary maintenance. In: Soyer OS (ed) Evolutionary systems biology, vol 751, Advances in experimental medicine and biology. Springer, New York, pp 279–300CrossRefGoogle Scholar
  96. Zhang Y, Gladyshev VN (2011) Comparative genomics of trace element dependence in biology. J Biol Chem 286:23623–23629PubMedCentralPubMedCrossRefGoogle Scholar
  97. Zhang XH, Weissbach H (2008) Origin and evolution of the protein-repairing enzymes methionine sulphoxide reductases. Biol Rev Camb Philos Soc 83:249–257PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2014

Authors and Affiliations

  • Elena Shumilina
    • 1
  • Olena Dobrovolska
    • 1
  • Alexander Dikiy
    • 1
    Email author
  1. 1.Department of BiotechnologyNorwegian University of Science and TechnologyTrondheimNorway

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