Advertisement

Neurochemical Research

, Volume 44, Issue 1, pp 247–257 | Cite as

Methionine in Proteins: It’s Not Just for Protein Initiation Anymore

  • Jung Mi Lim
  • Geumsoo Kim
  • Rodney L. LevineEmail author
Original Paper

Abstract

Methionine in proteins is often thought to be a generic hydrophobic residue, functionally replaceable with another hydrophobic residue such as valine or leucine. This is not the case, and the reason is that methionine contains sulfur that confers special properties on methionine. The sulfur can be oxidized, converting methionine to methionine sulfoxide, and ubiquitous methionine sulfoxide reductases can reduce the sulfoxide back to methionine. This redox cycle enables methionine residues to provide a catalytically efficient antioxidant defense by reacting with oxidizing species. The cycle also constitutes a reversible post-translational covalent modification analogous to phosphorylation. As with phosphorylation, enzymatically-mediated oxidation and reduction of specific methionine residues functions as a regulatory process in the cell. Methionine residues also form bonds with aromatic residues that contribute significantly to protein stability. Given these important functions, alteration of the methionine–methionine sulfoxide balance in proteins has been correlated with disease processes, including cardiovascular and neurodegenerative diseases. Methionine isn’t just for protein initiation.

Keywords

Methionine Methionine sulfoxide Methionine sulfoxide reductase Oxidative defenses Protein structure Cellular regulation 

Abbreviations

Msr

Methionine sulfoxide reductase

MetO

Methionine sulfoxide

ROS

Reactive oxygen species

Notes

Acknowledgements

This research was supported by the Intramural Research Division of the National Heart, Lung, and Blood Institute (ZIA HL000225).

References

  1. 1.
    Levine RL, Mosoni L, Berlett BS, Stadtman ER (1996) Methionine residues as endogenous antioxidants in proteins. Proc Natl Acad Sci USA 93:15036–15040Google Scholar
  2. 2.
    Bender A, Hajieva P, Moosmann B (2008) Adaptive antioxidant methionine accumulation in respiratory chain complexes explains the use of a deviant genetic code in mitochondria. Proc Natl Acad Sci USA 105:16496–16501Google Scholar
  3. 3.
    Valley CC, Cembran A, Perlmutter JD, Lewis AK, Labello NP, Gao J, Sachs JN (2012) The methionine-aromatic motif plays a unique role in stabilizing protein structure. J Biol Chem 287:34979–34991Google Scholar
  4. 4.
    Lee BC, Peterfi Z, Hoffmann FW, Moore RE, Kaya A, Avanesov A, Tarrago L, Zhou Y, Weerapana E, Fomenko DE, Hoffmann PR, Gladyshev VN (2013) MsrB1 and MICALs regulate actin assembly and macrophage function via reversible stereoselective methionine oxidation. Mol Cell 51:397–404Google Scholar
  5. 5.
    Hung RJ, Spaeth CS, Yesilyurt HG, Terman JR (2013) SelR reverses Mical-mediated oxidation of actin to regulate F-actin dynamics. Nat Cell Biol 15:1445–1454Google Scholar
  6. 6.
    Hung R-J, Pak CW, Terman JR (2011) Direct redox regulation of F-actin assembly and disassembly by Mical. Science 334:1710–1713Google Scholar
  7. 7.
    Netzer N, Goodenbour JM, David A, Dittmar KA, Jones RB, Schneider JR, Boone D, Eves EM, Rosner MR, Gibbs JS, Embry A, Dolan B, Das S, Hickman HD, Berglund P, Bennink JR, Yewdell JW, Pan T (2009) Innate immune and chemically triggered oxidative stress modifies translational fidelity. Nature 462:522–526Google Scholar
  8. 8.
    Lee JY, Kim DG, Kim BG, Yang WS, Hong J, Kang T, Oh YS, Kim KR, Han BW, Hwang BJ, Kang BS, Kang MS, Kim MH, Kwon NH, Kim S (2014) Promiscuous methionyl-tRNA synthetase mediates adaptive mistranslation to protect cells against oxidative stress. J Cell Sci 127:4234–4245Google Scholar
  9. 9.
    Lavine TF (1947) The formation, resolution, and optical properties of the diasteriomeric sulfoxides derived from L-methionine. J Biol Chem 169:477–491Google Scholar
  10. 10.
    Vogt W (1995) Oxidation of methionine residues in proteins: tools, targets, and reversal. Free Radic Biol Med 18:93–105Google Scholar
  11. 11.
    Wood PM (1981) The redox potential for dimethyl sulphoxide reduction to dimethyl sulphide: evaluation and biochemical implications. FEBS Lett 124:11–14Google Scholar
  12. 12.
    Jocelyn PC (1967) The standard redox potential of cysteine-cystine from the thiol-disulphide exchange reaction with glutathione and lipoic acid. Eur J Biochem 2:327–331Google Scholar
  13. 13.
    Barton JP, Packer JE, Sims RJ (1973) Kinetics of reaction of hydrogen-peroxide with cysteine and cysteamine. J Chem Soc Perkin Trans 2:1547–1549Google Scholar
  14. 14.
    Peskin AV, Winterbourn CC (2001) Kinetics of the reactions of hypochlorous acid and amino acid chloramines with thiols, methionine, and ascorbate. Free Radic Biol Med 30:572–579Google Scholar
  15. 15.
    Winterbourn CC Comparative reactivities of various biological compounds with myeloperoxidase-hydrogen peroxide-chloride, and similarity of the oxidant to hypochlorite. Biochim Biophys Acta 840:204–210Google Scholar
  16. 16.
    Richardson DE, Regino CA, Yao H, Johnson JV (2003) Methionine oxidation by peroxymonocarbonate, a reactive oxygen species formed from CO2/bicarbonate and hydrogen peroxide. Free Radic Biol Med 35:1538–1550Google Scholar
  17. 17.
    Brot N, Weissbach H (1983) Biochemistry and physiological role of methionine sulfoxide reductase in proteins. Arch Biochem Biophys 223:271–281Google Scholar
  18. 18.
    Zhang XH, Weissbach H (2008) Origin and evolution of the protein-repairing enzymes methionine sulphoxide reductases. Biol Rev Camb Philos Soc 83:249–257Google Scholar
  19. 19.
    Toennies G, Kolb JJ (1939) Methionine studies. J Biol Chem 128:399–405Google Scholar
  20. 20.
    Weissbach H, Resnick L, Brot N (2005) Methionine sulfoxide reductases: history and cellular role in protecting against oxidative damage. Biochim Biophys Acta 1703:203–212Google Scholar
  21. 21.
    Lee BC, Dikiy A, Kim HY, Gladyshev VN (2009) Functions and evolution of selenoprotein methionine sulfoxide reductases. Biochim Biophys Acta 1790:1471–1477Google Scholar
  22. 22.
    Boschi-Muller S, Gand A, Branlant G (2008) The methionine sulfoxide reductases: catalysis and substrate specificities. Arch Biochem Biophys 474:266–273Google Scholar
  23. 23.
    Moskovitz J, Bar-Noy S, Williams WM, Requena J, Berlett BS, Stadtman ER (2001) Methionine sulfoxide reductase (MsrA) is a regulator of antioxidant defense and lifespan in mammals. Proc Natl Acad Sci USA 98:12920–12925Google Scholar
  24. 24.
    Moskovitz J, Berlett BS, Poston JM, Stadtman ER (1997) The yeast peptide-methionine sulfoxide reductase functions as an antioxidant in vivo. Proc Natl Acad Sci USA 94:9585–9589Google Scholar
  25. 25.
    Moskovitz J, Rahman MA, Strassman J, Yancey SO, Kushner SR, Brot N, Weissbach H (1995) Escherichia coli peptide methionine sulfoxide reductase gene: regulation of expression and role in protecting against oxidative damage. J Bacteriol 177:502–507Google Scholar
  26. 26.
    Douglas T, Daniel DS, Parida BK, Jagannath C, Dhandayuthapani S (2004) Methionine sulfoxide reductase A (MsrA) deficiency affects the survival of Mycobacterium smegmatis within macrophages. J Bacteriol 186:3590–3598Google Scholar
  27. 27.
    St John G, Brot N, Ruan J, Erdjument-Bromage H, Tempst P, Weissbach H, Nathan C (2001) Peptide methionine sulfoxide reductase from Escherichia coli and Mycobacterium tuberculosis protects bacteria against oxidative damage from reactive nitrogen intermediates. Proc Natl Acad Sci USA 98:9901–9906Google Scholar
  28. 28.
    Mahawar M, Tran V, Sharp JS, Maier RJ (2011) Synergistic roles of Helicobacter pylori methionine sulfoxide reductase and GroEL in repairing oxidant-damaged catalase. J Biol Chem 286:19159–19169Google Scholar
  29. 29.
    Ruan H, Tang XD, Chen ML, Joiner ML, Sun G, Brot N, Weissbach H, Heinemann SH, Iverson L, Wu CF, Hoshi T, Chen ML, Joiner MA, Heinemann SH (2002) High-quality life extension by the enzyme peptide methionine sulfoxide reductase. Proc Natl Acad Sci USA 99:2748–2753Google Scholar
  30. 30.
    Moskovitz J, Flescher E, Berlett BS, Azare J, Poston JM, Stadtman ER (1998) Overexpression of peptide-methionine sulfoxide reductase in Saccharomyces cerevisiae and human T cells provides them with high resistance to oxidative stress. Proc Natl Acad Sci USA 95:14071–14075Google Scholar
  31. 31.
    Romero HM, Berlett BS, Jensen PJ, Pell EJ, Tien M (2004) Investigations into the role of the plastidial peptide methionine sulfoxide reductase in response to oxidative stress in Arabidopsis. Plant Physiol 136:3784–3794Google Scholar
  32. 32.
    Yermolaieva O, Xu R, Schinstock C, Brot N, Weissbach H, Heinemann SH, Hoshi T (2004) Methionine sulfoxide reductase A protects neuronal cells against brief hypoxia/reoxygenation. Proc Natl Acad Sci USA 101:1159–1164Google Scholar
  33. 33.
    Fan H, Wu PF, Zhang L, Hu ZL, Wang W, Guan XL, Luo H, Ni M, Yang JW, Li MX, Chen JG, Wang F (2015) Methionine sulfoxide reductase A negatively controls microglia-mediated neuroinflammation via inhibiting ROS/MAPKs/NF-kappaB signaling pathways through a catalytic antioxidant function. Antioxid Redox Signal 22:832–847Google Scholar
  34. 34.
    Benoit SL, Maier RJ (2016) Helicobacter catalase devoid of catalytic activity protects the bacterium against oxidative stress. J Biol Chem 291:23366–23373Google Scholar
  35. 35.
    Chung H, Kim AK, Jung SA, Kim SW, Yu K, Lee JH (2010) The Drosophila homolog of methionine sulfoxide reductase A extends lifespan and increases nuclear localization of FOXO. FEBS Lett 584:3609–3614Google Scholar
  36. 36.
    Salmon AB, Kim G, Liu C, Wren JD, Georgescu C, Richardson A, Levine RL (2016) Effects of transgenic methionine sulfoxide reductase A (MsrA) expression on lifespan and age-dependent changes in metabolic function in mice. Redox Biol 10:251–256Google Scholar
  37. 37.
    Reddy VY, Pizzo SV, Weiss SJ (1989) Functional inactivation and structural disruption of human alpha 2-macroglobulin by neutrophils and eosinophils. J Biol Chem 264:13801–13809Google Scholar
  38. 38.
    Reddy VY, Desrochers PE, Pizzo SV, Gonias SL, Sahakian JA, Levine RL, Weiss SJ (1994) Oxidative dissociation of human alpha 2-macroglobulin tetramers into dysfunctional dimers. J Biol Chem 269:4683–4691Google Scholar
  39. 39.
    Almassy RJ, Janson CA, Hamlin R, Xuong NH, Eisenberg D (1986) Novel subunit-subunit interactions in the structure of glutamine synthetase. Nature 323:304–309Google Scholar
  40. 40.
    Levine RL (1983) Oxidative modification of glutamine synthetase. I. Inactivation is due to loss of one histidine residue. J Biol Chem 258:11823–11827Google Scholar
  41. 41.
    Garner B, Waldeck AR, Witting PK, Rye KA, Stocker R (1998) Oxidation of high density lipoproteins. II. Evidence for direct reduction of lipid hydroperoxides by methionine residues of apolipoproteins AI and AII. J Biol Chem 273:6088–6095Google Scholar
  42. 42.
    Sigalov AB, Stern LJ (1998) Enzymatic repair of oxidative damage to human apolipoprotein A-I. FEBS Lett 433:196–200Google Scholar
  43. 43.
    Cowie DB, Cohen GN, Bolton ET, De Robichon-Szulmajster H (1959) Amino acid analog incorporation into bacterial proteins. Biochim Biophys Acta 34:39–46Google Scholar
  44. 44.
    Barker DG, Bruton CJ (1979) The fate of norleucine as a replacement for methionine in protein synthesis. J Mol Biol 133:217–231Google Scholar
  45. 45.
    Luo S, Levine RL (2008) Testing the hypothesis that “methionine residues in proteins are antioxidants”. FASEB J 23:464–472Google Scholar
  46. 46.
    Wang X, Pan T (2016) Stress response and adaptation mediated by amino acid misincorporation during protein synthesis. Adv Nutr (Bethesda Md) 7:773s–779sGoogle Scholar
  47. 47.
    Aledo JC, Li Y, de Magalhaes JP, Ruiz-Camacho M, Perez-Claros JA (2011) Mitochondrially encoded methionine is inversely related to longevity in mammals. Aging Cell 10:198–207Google Scholar
  48. 48.
    Schindeldecker M, Moosmann B (2015) Protein-borne methionine residues as structural antioxidants in mitochondria. Amino Acids 47:1421–1432Google Scholar
  49. 49.
    Wehr NB, Levine RL (2012) Wanted and wanting: antibody against rnethionine sulfoxide. Free Radic Biol Med 53:1222–1225Google Scholar
  50. 50.
    Le DT, Liang X, Fomenko DE, Raza AS, Chong C-K, Carlson BA, Hatfield DL, Gladyshev VN (2008) Analysis of methionine/selenomethionine oxidation and methionine sulfoxide reductase function using methionine-rich proteins and antibodies against their oxidized forms. Biochemistry 47:6685–6694Google Scholar
  51. 51.
    Liang X, Zhang Y, Le DT, Gladyshev VN (2009) Characterization of peptide methionine oxidation and methionine sulfoxide reduction using methionine-rich proteins. FASEB J 23:855–858Google Scholar
  52. 52.
    Oien DB, Canello T, Gabizon R, Gasset M, Lundquist BL, Burns JM, Moskovitz J (2009) Detection of oxidized methionine in selected proteins, cellular extracts and blood serums by novel anti-methionine sulfoxide antibodies. Arch Biochem Biophys 485:35–40Google Scholar
  53. 53.
    Haigh CL, Drew SC (2015) Cavitation during the protein misfolding cyclic amplification (PMCA) method—the trigger for de novo prion generation? Biochem Biophys Res Commun 461:494–500Google Scholar
  54. 54.
    Fan H, Wu P-F, Zhang L, Hu Z-L, Wang W, Guan X-L, Luo H, Ni M, Yang J-W, Li M-X, Chen J-G, Wang F (2015) Methionine sulfoxide reductase A negatively controls microglia-mediated neuroinflammation via inhibiting ROS/MAPKs/NF-κB signaling pathways through a catalytic antioxidant function. Antioxid Redox Signal 22:832–847Google Scholar
  55. 55.
    Mochin MT, Underwood KF, Cooper B, McLenithan JC, Pierce AD, Nalvarte C, Arbiser J, Karlsson AI, Moise AR, Moskovitz J, Passaniti A (2015) Hyperglycemia and redox status regulate RUNX2 DNA-binding and an angiogenic phenotype in endothelial cells. Microvasc Res 97:55–64Google Scholar
  56. 56.
    Kim JS, Park HM, Chae S, Lee TH, Hwang DJ, Oh SD, Park JS, Song DG, Pan CH, Choi D, Kim YH, Nahm BH, Kim YK (2014) A pepper MSRB2 gene confers drought tolerance in rice through the protection of chloroplast-targeted genes. PLoS ONE 9:17Google Scholar
  57. 57.
    Moskovitz J, Du F, Bowman CF, Yan SS (2016) Methionine sulfoxide reductase A affects beta-amyloid solubility and mitochondrial function in a mouse model of Alzheimer’s disease. Am J Physiol Endocrinol Metab 310:E388–E393Google Scholar
  58. 58.
    Moskovitz J (2014) Detection and localization of methionine sulfoxide residues of specific proteins in brain tissue. Protein Pept Lett 21:52–55Google Scholar
  59. 59.
    Salama SA, Snapkai RM (2012) Amino acid chloramine damage to proliferating cell nuclear antigen in mammalian cells. In Vivo 26:501–517Google Scholar
  60. 60.
    Moskovitz J, Malik A, Hernandez A, Band M, Avivi A (2012) Methionine sulfoxide reductases and methionine sulfoxide in the subterranean mole rat (Spalax): characterization of expression under various oxygen conditions. Comp Biochem Physiol A Mol Integr Physiol 161:406–414Google Scholar
  61. 61.
    Ringman JM, Fithian AT, Gylys K, Cummings JL, Coppola G, Elashoff D, Pratico D, Moskovitz J, Bitan G (2012) Plasma methionine sulfoxide in persons with familial Alzheimer’s disease mutations. Dement Geriatr Cogn Disord 33:219–225Google Scholar
  62. 62.
    Oien DB, Osterhaus GL, Lundquist BL, Fowler SC, Moskovitz J (2010) Caloric restriction alleviates abnormal locomotor activity and dopamine levels in the brain of the methionine sulfoxide reductase A knockout mouse. Neurosci Lett 468:38–41Google Scholar
  63. 63.
    Day AM, Brown JD, Taylor SR, Rand JD, Morgan BA, Veal EA (2012) Inactivation of a peroxiredoxin by hydrogen peroxide is critical for thioredoxin-mediated repair of oxidized proteins and cell survival. Mol Cell 45:398–408Google Scholar
  64. 64.
    Hoshi T, Heinemann S (2001) Regulation of cell function by methionine oxidation and reduction. J Physiol 531:1–11Google Scholar
  65. 65.
    Bigelow DJ, Squier TC (2005) Redox modulation of cellular signaling and metabolism through reversible oxidation of methionine sensors in calcium regulatory proteins. Biochim Biophys Acta 1703:121–134Google Scholar
  66. 66.
    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 442:48–52Google Scholar
  67. 67.
    Sroussi HY, Berline J, Palefsky JM (2007) Oxidation of methionine 63 and 83 regulates the effect of S100A9 on the migration of neutrophils in vitro. J Leukoc Biol 81:818–824Google Scholar
  68. 68.
    Erickson JR, Joiner ML, Guan X, Kutschke W, Yang J, Oddis CV, Bartlett RK, Lowe JS, O’Donnell SE, Aykin-Burns N, Zimmerman MC, Zimmerman K, Ham AJ, Weiss RM, Spitz DR, Shea MA, Colbran RJ, Mohler PJ, Anderson ME (2008) A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 133:462–474Google Scholar
  69. 69.
    Godoy LC, Munoz-Pinedo C, Castro L, Cardaci S, Schonhoff CM, King M, Tortora V, Marin M, Miao Q, Jiang JF, Kapralov A, Jemmerson R, Silkstone GG, Patel JN, Evans JE, Wilson MT, Green DR, Kagan VE, Radi R, Mannick JB (2009) Disruption of the M80-Fe ligation stimulates the translocation of cytochrome c to the cytoplasm and nucleus in nonapoptotic cells. Proc Natl Acad Sci USA 106:2653–2658Google Scholar
  70. 70.
    Hardin SC, Larue CT, Oh MH, Jain V, Huber SC (2009) Coupling oxidative signals to protein phosphorylation via methionine oxidation in Arabidopsis. Biochem J 422:305–312Google Scholar
  71. 71.
    Fu X, Chen J, Gallagher R, Zheng Y, Chung DW, Lopez JA (2011) Shear stress-induced unfolding of VWF accelerates oxidation of key methionine residues in the A1A2A3 region. Blood 118:5283–5291Google Scholar
  72. 72.
    Hung RJ, Pak CW, Terman JR (2011) Direct redox regulation of F-actin assembly and disassembly by Mical. Science 334:1710–1713Google Scholar
  73. 73.
    Lim JC, Kim G, Levine RL (2013) Stereospecific oxidation of calmodulin by methionine sulfoxide reductase A. Free Radic Biol Med 61:257–264Google Scholar
  74. 74.
    Senn H, Wüthrich K (1985) Amino acid sequence, haem-iron co-ordination geometry and functional properties of mitochondrial and bacterial c-type cytochromes. Q Rev Biophys 18:111–134Google Scholar
  75. 75.
    Taylor KL, Pohl J, Kinkade JM (1992) Unique autolytic cleavage of human myeloperoxidase. Implications for the involvement of active site MET409. J Biol Chem 267:25282–25288Google Scholar
  76. 76.
    Kooter IM, Moguilevsky N, Bollen A, van der Veen LA, Otto C, Dekker HL, Wever R (1999) The sulfonium ion linkage in myeloperoxidase: direct spectroscopic detection by isotopic labeling and effect of mutation. J Biol Chem 274:26794–26802Google Scholar
  77. 77.
    Vanacore R, Ham AJ, Voehler M, Sanders CR, Conrads TP, Veenstra TD, Sharpless KB, Dawson PE, Hudson BG (2009) A sulfilimine bond identified in collagen IV. Science 325:1230–1234Google Scholar
  78. 78.
    Bhave G, Cummings CF, Vanacore RM, Kumagai-Cresse C, Ero-Tolliver IA, Rafi M, Kang JS, Pedchenko V, Fessler LI, Fessler JH, Hudson BG (2012) Peroxidasin forms sulfilimine chemical bonds using hypohalous acids in tissue genesis. Nat Chem Biol 8:784–790Google Scholar
  79. 79.
    Reid KSC, Lindley PF, Thornton JM (1985) Sulfur-aromatic interactions in proteins. FEBS Lett 190:209–213Google Scholar
  80. 80.
    Zauhar RJ, Colbert CL, Morgan RS, Welsh WJ (2000) Evidence for a strong sulfur-aromatic interaction derived from crystallographic data. Biopolymers 53:233–248Google Scholar
  81. 81.
    Lewis AK, Dunleavy KM, Senkow TL, Her C, Horn BT, Jersett MA, Mahling R, McCarthy MR, Perell GT, Valley CC, Karim CB, Gao J, Pomerantz WCK, Thomas DD, Cembran A, Hinderliter A, Sachs JN (2016) Oxidation increases the strength of the methionine-aromatic interaction. Nat Chem Biol 12:860–866Google Scholar
  82. 82.
    Chao CC, Ma YS, Stadtman ER (1997) Modification of protein surface hydrophobicity and methionine oxidation by oxidative systems. Proc Natl Acad Sci USA 94:2969–2974Google Scholar
  83. 83.
    García-Bermúdez M, López-Mejías R, González-Juanatey C, Castañeda S, Miranda-Filloy JA, Blanco R, Fernández-Gutiérrez B, Balsa A, González-Álvaro I, Gómez-Vaquero C, Llorca J, Martín J, González-Gay MA (2012) Association of the methionine sulfoxide reductase A rs10903323 gene polymorphism with cardiovascular disease in patients with rheumatoid arthritis. Scand J Rheumatol 41:350–353Google Scholar
  84. 84.
    Gu H, Chen W, Yin J, Chen S, Zhang J, Gong J (2013) Methionine sulfoxide reductase A rs10903323 G/A polymorphism is associated with increased risk of coronary artery disease in a Chinese population. Clin Biochem 46:1668–1672Google Scholar
  85. 85.
    Levy D, Ehret GB, Rice K, Verwoert GC, Launer LJ, Dehghan A, Glazer NL, Morrison AC, Johnson AD, Aspelund T, Aulchenko Y, Lumley T, Kottgen A, Vasan RS, Rivadeneira F, Eiriksdottir G, Guo X, Arking DE, Mitchell GF, Mattace-Raso FUS, Smith AV, Taylor K, Scharpf RB, Hwang S-J, Sijbrands EJG, Bis J, Harris TB, Ganesh SK, O’Donnell CJ, Hofman A, Rotter JI, Coresh J, Benjamin EJ, Uitterlinden AG, Heiss G, Fox CS, Witteman JCM, Boerwinkle E, Wang TJ, Gudnason V, Larson MG, Chakravarti A, Psaty BM, van Duijn CM (2009) Genome-wide association study of blood pressure and hypertension. Nat Genet 41:677–687Google Scholar
  86. 86.
    Xu YY, Du F, Meng B, Xie GH, Cao J, Fan D, Yu H (2015) Hepatic overexpression of methionine sulfoxide reductase A reduces atherosclerosis in apolipoprotein E-deficient mice. J Lipid Res 56:1891–1900Google Scholar
  87. 87.
    Zhao H, Sun J, Deschamps AM, Kim G, Liu C, Murphy E, Levine RL (2011) Myristoylated methionine sulfoxide reductase A protects the heart from ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 301:H1513–H1518Google Scholar
  88. 88.
    Larsson C (1978) Natural history and life expectancy in severe alpha1-antitrypsin deficiency, Pi Z. Acta Medica Scandinavica 204:345–351Google Scholar
  89. 89.
    Gadek JE, Fells GA, Crystal RG (1979) Cigarette smoking induces functional antiprotease deficiency in the lower respiratory tract of humans. Science 206:1315–1316Google Scholar
  90. 90.
    Carp H, Miller F, Hoidal JR, Janoff A (1982) Potential mechanism of emphysema: alpha 1-proteinase inhibitor recovered from lungs of cigarette smokers contains oxidized methionine and has decreased elastase inhibitory capacity. Proc Natl Acad Sci USA 79:2041–2045Google Scholar
  91. 91.
    McGuire WW, Spragg RG, Cohen AB, Cochrane CG (1982) Studies on the pathogenesis of the adult respiratory distress syndrome. J Clin Invest 69:543–553Google Scholar
  92. 92.
    Johnson D, Travis J (1979) The oxidative inactivation of human alpha-1-proteinase inhibitor. Further evidence for methionine at the reactive center. J Biol Chem 254:4022–4026Google Scholar
  93. 93.
    Taggart C, Cervantes-Laurean D, Kim G, McElvaney NG, Wehr N, Moss J, Levine RL (2000) Oxidation of either methionine 351 or methionine 358 in alpha 1-antitrypsin causes loss of anti-neutrophil elastase activity. J Biol Chem 275:27258–27265Google Scholar
  94. 94.
    Carp H, Janoff A, Abrams W, Weinbaum G, Drew RT, Weissbach H, Brot N (1983) Human methionine sulfoxide-peptide reductase, an enzyme capable of reactivating oxidized alpha-1-proteinase inhibitor in vitro. Am Rev Respir Dis 127:301–305Google Scholar
  95. 95.
    Cudic P, Joshi N, Sagher D, Williams BT, Stawikowski MJ, Weissbach H (2016) Identification of activators of methionine sulfoxide reductases A and B. Biochem Biophys Res Commun 469:863–867Google Scholar
  96. 96.
    Markesbery WR, Carney JM (1999) Oxidative alterations in Alzheimer’s disease. Brain Pathol (Zurich Switzerland) 9:133–146Google Scholar
  97. 97.
    Gabbita SP, Aksenov MY, Lovell MA, Markesbery WR (1999) Decrease in peptide methionine sulfoxide reductase in Alzheimer’s disease brain. J Neurochem 73:1660–1666Google Scholar
  98. 98.
    Hensley K, Hall N, Subramaniam R, Cole P, Harris M, Aksenov M, Aksenova M, Gabbita SP, Wu JF, Carney JM et al (1995) Brain regional correspondence between Alzheimer’s disease histopathology and biomarkers of protein oxidation. J Neurochem 65:2146–2156Google Scholar
  99. 99.
    Price DL, Borchelt DR, Walker LC, Sisodia SS (1992) Toxicity of synthetic aβ peptides and modeling of alzheimer’s disease. Neurobiol Aging 13:623–625Google Scholar
  100. 100.
    Wang C, Chen P, He X, Peng Z, Chen S, Zhang R, Cheng J, Liu Q (2017) Direct interaction between selenoprotein R and Aβ42. Biochem Biophys Res Commun 489:509–514Google Scholar
  101. 101.
    Varadarajan S, Yatin S, Aksenova M, Butterfield DA (2000) Review: Alzheimer’s amyloid beta-peptide-associated free radical oxidative stress and neurotoxicity. J Struct Biol 130:184–208Google Scholar
  102. 102.
    Butterfield DA (2014) The 2013 SFRBM discovery award: Selected discoveries from the butterfield laboratory of oxidative stress and its sequela in brain in cognitive disorders exemplified by Alzheimer disease and chemotherapy induced cognitive impairment. Free Radic Biol Med 74:157–174Google Scholar
  103. 103.
    Litvan I, Chesselet MF, Gasser T, Di Monte DA, Parker D Jr., Hagg T, Hardy J, Jenner P, Myers RH, Price D, Hallett M, Langston WJ, Lang AE, Halliday G, Rocca W, Duyckaerts C, Dickson DW, Ben-Shlomo Y, Goetz CG, Melamed E (2007) The etiopathogenesis of Parkinson disease and suggestions for future research. Part II. J Neuropathol Exp Neurol 66:329–336Google Scholar
  104. 104.
    Eriksen JL, Dawson TM, Dickson DW, Petrucelli L (2003) Caught in the act: alpha-synuclein is the culprit in Parkinson’s disease. Neuron 40:453–456Google Scholar
  105. 105.
    Liu F, Hindupur J, Nguyen JL, Ruf KJ, Zhu J, Schieler JL, Bonham CC, Wood KV, Davisson VJ, Rochet J-C (2008) Methionine sulfoxide reductase A protects dopaminergic cells from Parkinson’s disease-related insults. Free Radic Biol Med 45:242–255Google Scholar
  106. 106.
    Maltsev AS, Chen J, Levine RL, Bax A (2013) Site-specific interaction between alpha-synuclein and membranes probed by NMR-observed methionine oxidation rates. J Am Chem Soc 135:2943–2946Google Scholar
  107. 107.
    Feany MB, Bender WW (2000) A Drosophila model of Parkinson’s disease. Nature 404:394–398Google Scholar
  108. 108.
    Wassef R, Haenold R, Hansel A, Brot N, Heinemann SH, Hoshi T (2007) Methionine sulfoxide reductase A and a dietary supplement S-methyl-L-cysteine prevent Parkinson’s-like symptoms. J Neurosci 27:12808–12816Google Scholar
  109. 109.
    Lei KF, Wang YF, Zhu XQ, Lu PC, Sun BS, Jia HL, Ren N, Ye QH, Sun HC, Wang L, Tang ZY, Qin LX (2007) Identification of MSRA gene on chromosome 8p as a candidate metastasis suppressor for human hepatitis B virus-positive hepatocellular carcinoma. BMC Cancer 7:172Google Scholar
  110. 110.
    De Luca A, Sanna F, Sallese M, Ruggiero C, Grossi M, Sacchetta P, Rossi C, De Laurenzi V, Di Ilio C, Favaloro B (2010) Methionine sulfoxide reductase A down-regulation in human breast cancer cells results in a more aggressive phenotype. Proc Natl Acad Sci USA 107:18628–18633Google Scholar
  111. 111.
    Ahmed ZM, Yousaf R, Lee BC, Khan SN, Lee S, Lee K, Husnain T, Rehman AU, Bonneux S, Ansar M, Ahmad W, Leal SM, Gladyshev VN, Belyantseva IA, Van Camp G, Riazuddin S, Friedman TB, Riazuddin S (2011) Functional null mutations of MSRB3 encoding methionine sulfoxide reductase are associated with human deafness DFNB74. Am J Hum Genet 88:19–29Google Scholar
  112. 112.
    Shen X, Liu F, Wang Y, Wang H, Ma J, Xia W, Zhang J, Jiang N, Sun S, Wang X, Ma D (2015) Down-regulation of msrb3 and destruction of normal auditory system development through hair cell apoptosis in zebrafish. Int J Dev Biol 59:195–203Google Scholar
  113. 113.
    Kwon TJ, Cho HJ, Kim UK, Lee E, Oh SK, Bok J, Bae YC, Yi JK, Lee JW, Ryoo ZY, Lee SH, Lee KY, Kim HY (2014) Methionine sulfoxide reductase B3 deficiency causes hearing loss due to stereocilia degeneration and apoptotic cell death in cochlear hair cells. Hum Mol Genet 23:1591–1601Google Scholar
  114. 114.
    Ma X, Deng W, Liu X, Li M, Chen Z, He Z, Wang Y, Wang Q, Hu X, Collier DA, Li T (2011) A genome-wide association study for quantitative traits in schizophrenia in China. Genes Brain Behav 10:734–739Google Scholar
  115. 115.
    Ni P, Ma X, Lin Y, Lao G, Hao X, Guan L, Li X, Jiang Z, Liu Y, Ye B, Liu X, Wang Y, Zhao L, Cao L, Li T (2015) Methionine sulfoxide reductase A (MsrA) associated with bipolar I disorder and executive functions in A Han Chinese population. J Affect Disord 184:235–238Google Scholar
  116. 116.
    Lindgren CM, Heid IM, Randall JC, Lamina C, Steinthorsdottir V, Qi L, Speliotes EK, Thorleifsson G, Willer CJ, Herrera BM, Jackson AU, Lim N, Scheet P, Soranzo N, Amin N, Aulchenko YS, Chambers JC, Drong A, Luan J, Lyon HN, Rivadeneira F, Sanna S, Timpson NJ, Zillikens MC, Zhao JH, Almgren P, Bandinelli S, Bennett AJ, Bergman RN, Bonnycastle LL, Bumpstead SJ, Chanock SJ, Cherkas L, Chines P, Coin L, Cooper C, Crawford G, Doering A, Dominiczak A, Doney AS, Ebrahim S, Elliott P, Erdos MR, Estrada K, Ferrucci L, Fischer G, Forouhi NG, Gieger C, Grallert H, Groves CJ, Grundy S, Guiducci C, Hadley D, Hamsten A, Havulinna AS, Hofman A, Holle R, Holloway JW, Illig T, Isomaa B, Jacobs LC, Jameson K, Jousilahti P, Karpe F, Kuusisto J, Laitinen J, Lathrop GM, Lawlor DA, Mangino M, McArdle WL, Meitinger T, Morken MA, Morris AP, Munroe P, Narisu N, Nordstrom A, Nordstrom P, Oostra BA, Palmer CN, Payne F, Peden JF, Prokopenko I, Renstrom F, Ruokonen A, Salomaa V, Sandhu MS, Scott LJ, Scuteri A, Silander K, Song K, Yuan X, Stringham HM, Swift AJ, Tuomi T, Uda M, Vollenweider P, Waeber G, Wallace C, Walters GB, Weedon MN, Witteman JC, Zhang C, Zhang W, Caulfield MJ, Collins FS, Davey Smith G, Day IN, Franks PW, Hattersley AT, Hu FB, Jarvelin MR, Kong A, Kooner JS, Laakso M, Lakatta E, Mooser V, Morris AD, Peltonen L, Samani NJ, Spector TD, Strachan DP, Tanaka T, Tuomilehto J, Uitterlinden AG, van Duijn CM, Wareham NJ, Hugh W, Waterworth DM, Boehnke M, Deloukas P, Groop L, Hunter DJ, Thorsteinsdottir U, Schlessinger D, Wichmann HE, Frayling TM, Abecasis GR, Hirschhorn JN, Loos RJ, Stefansson K, Mohlke KL, Barroso I, McCarthy MI (2009) Genome-wide association scan meta-analysis identifies three Loci influencing adiposity and fat distribution. PLoS Genet 5:e1000508Google Scholar
  117. 117.
    Pillas D, Hoggart CJ, Evans DM, O’Reilly PF, Sipila K, Lahdesmaki R, Millwood IY, Kaakinen M, Netuveli G, Blane D, Charoen P, Sovio U, Pouta A, Freimer N, Hartikainen AL, Laitinen J, Vaara S, Glaser B, Crawford P, Timpson NJ, Ring SM, Deng G, Zhang W, McCarthy MI, Deloukas P, Peltonen L, Elliott P, Coin LJ, Smith GD, Jarvelin MR (2010) Genome-wide association study reveals multiple loci associated with primary tooth development during infancy. PLoS Genet 6:e1000856Google Scholar

Copyright information

© This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2018

Authors and Affiliations

  1. 1.Laboratory of BiochemistryNational Heart, Lung, and Blood InstituteBethesdaUSA
  2. 2.NIHBethesdaUSA

Personalised recommendations