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Plant methionine sulfoxide reductase A and B multigenic families

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Abstract

Methionine oxidation to methionine sulfoxide (MetSo), which results in modification of activity and conformation for many proteins, is reversed by an enzyme present in most organisms and termed as methionine sulfoxide reductase (MSR). On the basis of substrate stereospecificity, two types of MSR, A and B, that do not share any sequence similarity, have been identified. In the present review, we first compare the multigenic MSR families in the three plant species for which the genome is fully sequenced: Arabidopsis thaliana, Oryza sativa, and Populus trichocarpa. The MSR gene content is larger in A. thaliana (five MSRAs and nine MSRBs) compared to P. trichocarpa (five MSRAs and four MSRBs) and O. sativa (four MSRAs and three MSRBs). A complete classification based on gene structure, sequence identity, position of conserved reactive cysteines and predicted subcellular localization is proposed. On the basis of in silico and experimental data originating mainly from Arabidopsis, we report that some MSR genes display organ-specific expression patterns and that those encoding plastidic MSRs are highly expressed in photosynthetic organs. We also show that the expression of numerous MSR genes is enhanced by environmental conditions known to generate oxidative stress. Thioredoxins (TRXs) constitute very likely physiological electron donors to plant MSR proteins for the catalysis of MetSO reduction, but the specificity between the numerous TRXs and methionine sulfoxide reductases (MSRs) present in plants remains to be investigated. The essential role of plant MSRs in protection against oxidative damage has been recently demonstrated on transgenic Arabidopsis plants modified in the content of cytosolic or plastidic MSRA.

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References

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Bechtold U, Murphy DJ, Mullineaux PM (2004) Arabidopsis peptide methionine sulfoxide reductase2 prevents cellular oxidative damage in long nights. Plant Cell 16:908–919

    Article  PubMed  CAS  Google Scholar 

  • Bigelow DJ, Squier TC (2005) Redox modulation of cellular signalling and metabolism through reversible oxidation of methionine sensors in calcium regulatory proteins. Biochim Biophys Acta 1703:121–134

    PubMed  CAS  Google Scholar 

  • Boschi-Muller S, Olry A, Antoine M, Branlant G (2005) The enzymology and biochemistry of methionine sulfoxide reductases. Biochim Biophys Acta 1703:231–238

    PubMed  CAS  Google Scholar 

  • Brock JWC, Cotham WC, Ames JM, Thorpe SR, Baynes JW (2005) Proteomic method for the quantification of methionine sulfoxide. Ann NY Acad Sci 1043:284–289

    Article  PubMed  CAS  Google Scholar 

  • Broin M, Cuiné S, Peltier G, Rey P (2000) Involvement of CDSP32, a drought-induced thioredoxin, in the response to oxidative stress in potato plants. FEBS Lett 467:245–248

    Article  PubMed  CAS  Google Scholar 

  • Broin M, Cuiné S, Eymery F, Rey P (2002) The plastidic 2-cysteine peroxiredoxin is a target for a thioredoxin involved in the protection of the photosynthetic apparatus against oxidative damage. Plant Cell 14:1417–1432

    Article  PubMed  CAS  Google Scholar 

  • Broin M, Rey P (2003) Potato plants lacking the CDSP32 plastidic thioredoxin exhibit overoxidation of the BAS1 2-cysteine peroxiredoxin and increased lipid Peroxidation in thylakoids under photooxidative stress. Plant Physiol 132:1335–1343

    Article  PubMed  CAS  Google Scholar 

  • Brot N, Weissbach J, Werth J, Weissbach H (1981) Enzymatic reduction of protein-bound methionine sulfoxide. Proc Natl Acad Sci USA 78:2155–2158

    Article  PubMed  CAS  Google Scholar 

  • Davies MJ (2005) The oxidative environment and protein damage. Biochim Biophys Acta 1703:93–109

    PubMed  CAS  Google Scholar 

  • Ferguson DL, Burke JJ (1994) Methionyl sulfoxide content and protein-methionine-S-oxide reductase activity in response to water deficits or high temperature. Physiol Plant 90:253–258

    Article  CAS  Google Scholar 

  • Gabbita SP, Aksenov MY, Lovell MA, Markesbery WR (1999) Decrease in peptide methionine sulfoxide reductase in Alzheimer’s disease brain. J Neurochem 73:1660–1666

    Article  PubMed  CAS  Google Scholar 

  • Gao J, Yin DH, Yao Y, Sun H, Qin Z, Schoneich C, Williams TD, Squier TC (1998) Loss of conformational stability in calmodulin upon methionine oxidation. Biophys J 74:1115–1134

    Article  PubMed  CAS  Google Scholar 

  • Gelhaye E, Rouhier N, Jacquot J-P (2003) Evidence for a subgroup of thioredoxin h that requires GSH/Grx for its reduction. FEBS Lett 555:443–448

    Article  PubMed  CAS  Google Scholar 

  • Gelhaye E, Rouhier N, Navrot N, Jacquot JP (2005) The plant thioredoxin system. Cell Mol Life Sci 62:24–35

    Article  PubMed  CAS  Google Scholar 

  • Grimaud R, Ezraty B, Mitchell JK, Lafitte D, Bri C, Derrick PJ, Barras F (2001) Repair of oxidized proteins. Identification of a new methionine sulfoxide reductase. J Biol Chem 276:48915–48920

    Article  PubMed  CAS  Google Scholar 

  • Gustavsson N, Kokke B, Härndahl U, Silow M, Bechtold U, Poghosyan Z, Murphy D, Boelens W, Sundby C (2002) A peptide methionine sulfoxide reductase highly expressed in photosynthetic tissue in Arabidopsis thaliana can protect the chaperone-like activity of a chloroplast-localized small heat shock protein. Plant J 29:545–553

    Article  PubMed  CAS  Google Scholar 

  • Hansel A, Kuschel L, Hehl S, Lemke C, Agricola HJ, Hoshi T, Heinemann SH (2002) Mitochondrial targeting of the human peptide methionine sulfoxide reductase (MSRA), an enzyme involved in the repair of oxidized proteins. FASEB J 16:911–913

    PubMed  CAS  Google Scholar 

  • In O, Berberich T, Romdhane S, Feierabend J (2005) Changes in gene expression during dehardening of cold-hardened winter rye (Secale cereale L.) leaves and potential role of a peptide methionine sulfoxide reductase in cold-acclimation. Planta 220:941–950

    Article  PubMed  CAS  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  CAS  Google Scholar 

  • Kauffmann B, Aubry A, Favier F (2005) The three-dimensional structures of peptide methionine sulfoxide reductases: current knowledge and open questions. Biochim Biophys Acta 1703:249–260

    PubMed  CAS  Google Scholar 

  • Kim HY, Gladyshev VN (2004) Methionine sulfoxide reduction in mammals: characterization of methionine-R-sulfoxide reductases. Mol Biol Cell 15:1055–1064

    Article  PubMed  CAS  Google Scholar 

  • Koc A, Gasch AP, Rutherford JC, Kim HY, Gladyshev VN (2004) Methionine sulfoxide reductase regulation of yeast lifespan reveals reactive oxygen species-dependent and -independent components of aging. Proc Natl Acad Sci USA 101:7999–8004

    Article  PubMed  CAS  Google Scholar 

  • 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 USA 99:4245–4250

    Article  PubMed  CAS  Google Scholar 

  • Kumar RA, Koc A, Cerny RL, Gladyshev VN (2002) Reaction mechanism, evolutionary, and role of zinc in Drosophila methionine-R-sulfoxide reductase. J Biol Chem 277:37527–37535

    Article  PubMed  CAS  Google Scholar 

  • Lopez AP, Portales RB, López-Ráez JA, Medina-Escobar N, Blanco JM, Franco AR (2006) Characterization of a strawberry late-expressed and fruit-specific peptide methionine sulphoxide reductase. Physiol Plant 126:129–139

    Article  CAS  Google Scholar 

  • Marchand C, Le Marechal P, Meyer Y, Miginiac-Maslow M, Issakidis-Bourguet E, Decottignies P (2004) New targets of Arabidopsis thioredoxins revealed by proteomic analysis. Proteomics 4:2696–2706

    Article  PubMed  CAS  Google Scholar 

  • Meyer Y, Vignols F, Reichheld JP (2002) Classification of plant thioredoxins by sequence similarity and intron position. Methods Enzymol 347:394–402

    Article  PubMed  CAS  Google Scholar 

  • Meyer Y, Reichheld JP, Vignols F (2005) Thioredoxins in Arabidopsis and other plants. Photosynth Res 86:419–433

    Article  PubMed  CAS  Google Scholar 

  • 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 177:502–507

    PubMed  CAS  Google Scholar 

  • 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 94:9585–9589

    Article  PubMed  CAS  Google Scholar 

  • 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 95:14071–14075

    Article  PubMed  CAS  Google Scholar 

  • Mushegian AR, Koonin EV (1996) A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc Natl Acad Sci USA 93:10268–10273

    Article  PubMed  CAS  Google Scholar 

  • 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 21:3681–3693

    Article  PubMed  CAS  Google Scholar 

  • Oh JE, Hong SW, Lee Y, Koh EJ, Kim K, Seo YW, Chung N, Jeong M, Jang CS, Lee B, Kim KH, Lee H (2005) Modulation of gene expressions and enzyme activities of methionine sulfoxide reductases by cold, ABA or high salt treatments in Arabidopsis. Plant Sci 169:1030–1036

    Article  CAS  Google Scholar 

  • Rey P, Pruvot G, Becuwe N, Eymery F, Rumeau D, Peltier G (1998) A novel thioredoxin-like protein located in the chloroplast is induced by water deficit in Solanum tuberosum L. plants. Plant J 13:97–107

    Article  PubMed  CAS  Google Scholar 

  • Rey P, Cuiné S, Eymery F, Garin J, Court M, Jacquot J-P, Rouhier N, Broin M (2005) Analysis of the proteins targeted by CDSP32, a plastidic thioredoxin participating in oxidative stress responses. Plant J 41:31–42

    Article  PubMed  CAS  Google Scholar 

  • Rodrigo M-J, Moskovitz J, Salamini F, Bartels D (2002) Reverse genetic approaches in plants and yeast suggest a role for novel, evolutionarily conserved, selenoprotein-related genes in oxidative stress defense. Mol Genet Genomics 267:613–621

    Article  PubMed  CAS  Google Scholar 

  • 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 136:3784–3794

    Article  PubMed  CAS  Google Scholar 

  • Romero HM, Pell EJ, Tien M (2006) Expression profile analysis and biochemical properties of the peptide methionine sulfoxide reductase A (PMSRA) gene family in Arabidopsis. Plant Sci 170:705–714

    Article  CAS  Google Scholar 

  • Rouhier N, Gelhaye E, Jacquot J-P (2004) Plant glutaredoxins: still mysterious reducing systems. Cell Mol Life Sci 61:1266–1277

    Article  PubMed  CAS  Google Scholar 

  • Ruan H, Tang XD, Chen ML, Joiner ML, Sun G, Brot N, Weissbach H, Heinemann SH, Iverson L, Wu CF, Hoshi T (2002) High-quality life extension by the enzyme peptide methionine sulfoxide reductase. Proc Natl Acad Sci USA 99:2748–2753

    Article  PubMed  CAS  Google Scholar 

  • Sadanandom A, Piffanelli P, Knott K, Robinson C, Sharpe A, Lydiate D, Murphy D, Fairbairn DJ (1996) Identification of a peptide methionine sulphoxide reductase gene in an oleosin promoter from Brassica napus. Plant J 10:235–242

    Article  PubMed  CAS  Google Scholar 

  • Sadanandom A, Poghosyan Z, Fairbairn DJ, Murphy DJ (2000) Differential regulation of plastidial and cytosolic isoforms of peptide methionine sulfoxide reductase in Arabidopsis. Plant Physiol 123:255–264

    Article  PubMed  CAS  Google Scholar 

  • Sanchez J, Nikolau BJ, Stumpf PK (1983) Reduction of N-acetyl methionine sulfoxide in plants. Plant Physiol 73:619–623

    Article  PubMed  CAS  Google Scholar 

  • Stadtman ER, Moskowitz J, Berlett BS, Levine RL (2002) Cyclic oxidation and reduction of protein methionine residues is an important antioxidant mechanism. Mol Cell Biochem 234/235:3–9

    Article  CAS  Google Scholar 

  • Sundby C, Härndahl U, Gustavsson N, Ahrman E, Murphy DJ (2005) Conserved methionines in chloroplasts. Biochim Biophys Acta 1703:191–202

    PubMed  CAS  Google Scholar 

  • Toda T, Morisama T, Kobayashi S, Nomura K, Hatozaki S, Hirota M (2003) A proteomic approach to determination of the significance of protein oxidation in the ageing of mouse hippocampus. Appl Genomics Proteomics 2:43–50

    CAS  Google Scholar 

  • Vieira Dos Santos C, Cuiné S, Rouhier N, Rey P (2005) The Arabidopsis thaliana plastidic methionine sulfoxide reductase B proteins. Sequence and activity characteristics, comparison of the expression with plastidic methionine sulfoxide reductase A and induction by photooxidative stress. Plant Physiol 138:909–922

    Article  PubMed  CAS  Google Scholar 

  • Vieira Dos Santos C, Rey P (2006) Plant thioredoxins are key actors in oxidative stress response. Trends Plant Sci 11:329–334

    Article  PubMed  CAS  Google Scholar 

  • Weissbach H, Etienne F, Hoshi T, Heinemann SH, Lowther WT, Matthews B, St John G, Nathan C, Brot N (2002) Peptide methionine sulfoxide reductase: structure, mechanism of action, and biological function. Arch Biochem Biophys 397:172–178

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Neiers F, Boschi-Muller S, Branlant G (2005) The N-terminal domain of PILB from Neisseria meningitidis is a disulfide reductase that can recycle methionine sulfoxide reductases. J Biol Chem 280:12344–12350

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Pascal Rey.

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Rouhier, N., Santos, C.V.D., Tarrago, L. et al. Plant methionine sulfoxide reductase A and B multigenic families. Photosynth Res 89, 247–262 (2006). https://doi.org/10.1007/s11120-006-9097-1

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