Proteome alteration in oxidative stress-sensitive methionine sulfoxide reductase-silenced HEK293 cells

Free Radical Biology and Medicine

Volumn 65, Issue , 2013, Pages 1023-1036

  Ugarte, Nicolas ^a   Ladouce, Romain ^a   Radjei, Sabrina ^a   Gareil, Monique ^a   Friguet, Bertrand ^a   Petropoulos, Isabelle ^a  

^a SORBONNE UNIVERSITÉ   (France)

Author keywords

Adaptive response; Free radicals; Methionine sulfoxide reductases; Oxidative stress; Oxidized protein repair; Proteomics; RNA silencing

Indexed keywords

METHIONINE SULFOXIDE REDUCTASE; METHIONINE SULFOXIDE REDUCTASE A; METHIONINE SULFOXIDE REDUCTASE B; METHIONINE SULFOXIDE REDUCTASE B1; METHIONINE SULFOXIDE REDUCTASE B2; PROTEOME; RNA; UNCLASSIFIED DRUG; N-CHLOROTAURINE; OXIDIZING AGENT; TAURINE;

AGING; AMINO ACID SEQUENCE; ARTICLE; CELL STRAIN HEK293; CELL VIABILITY; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; MASS SPECTROMETRY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; ANALOGS AND DERIVATIVES; GENE SILENCING; GENETICS; HEK293 CELL LINE; METABOLISM; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE;

MAMMALIA;

GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; METHIONINE SULFOXIDE REDUCTASES; OXIDANTS; OXIDATIVE STRESS; PROTEIN INTERACTION MAPS; PROTEOME; RNA INTERFERENCE; TAURINE;

EID: 84884529090     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.08.008     Document Type: Article

References (63)

1. B.S. Berlett, and E.R. Stadtman Protein oxidation in aging, disease, and oxidative stress J. Biol. Chem. 272 1997 20313 20316 (Pubitemid 27355575)
2. N. Brot, and H. Weissbach Peptide methionine sulfoxide reductase: biochemistry and physiological role Biopolymers 55 2000 288 296 (Pubitemid 32224089)
3. A. Hansel, S.H. Heinemann, and T. Hoshi Heterogeneity and function of mammalian MSRs: enzymes for repair, protection and regulation Biochim. Biophys. Acta 1703 2005 239 247 (Pubitemid 40170447)
4. S. Vougier, J. Mary, N. Dautin, J. Vinh, B. Friguet, and D. Ladant Essential role of methionine residues in calmodulin binding to Bordetella pertussis adenylate cyclase, as probed by selective oxidation and repair by the peptide methionine sulfoxide reductases J. Biol. Chem 279 2004 30210 30218 (Pubitemid 38937946)
5. C.R. Picot, M. Perichon, J.C. Cintrat, B. Friguet, and I. Petropoulos The peptide methionine sulfoxide reductases, MsrA and MsrB (hCBS-1), are downregulated during replicative senescence of human WI-38 fibroblasts FEBS Lett. 558 2004 74 78 (Pubitemid 38167413)
6. O. Yermolaieva, R. Xu, C. Schinstock, N. Brot, H. Weissbach, S.H. Heinemann, and T. Hoshi Methionine sulfoxide reductase A protects neuronal cells against brief hypoxia/reoxygenation Proc. Natl. Acad. Sci. USA 101 2004 1159 1164 (Pubitemid 38182659)
7. 2-mediated oxidative stress Free Radic. Biol. Med. 39 2005 1332 1341 (Pubitemid 41540088)
8. F. Cabreiro, C.R. Picot, M. Perichon, J. Castel, B. Friguet, and I. Petropoulos Overexpression of mitochondrial methionine sulfoxide reductase B2 protects leukemia cells from oxidative stress-induced cell death and protein damage J. Biol. Chem. 283 2008 16673 16681
9. F. Cabreiro, C.R. Picot, M. Perichon, B. Friguet, and I. Petropoulos Overexpression of methionine sulfoxide reductases A and B2 protects MOLT-4 cells against zinc-induced oxidative stress Antioxid. Redox Signaling 11 2009 215 225
10. R.L. Levine, L. Mosoni, B.S. Berlett, and E.R. Stadtman Methionine residues as endogenous antioxidants in proteins Proc. Natl. Acad. Sci. USA 93 1996 15036 15040 (Pubitemid 27009547)
11. I. Petropoulos, J. Mary, M. Perichon, and B. Friguet Rat peptide methionine sulphoxide reductase: cloning of the cDNA, and down-regulation of gene expression and enzyme activity during aging Biochem. J. 355 2001 819 825 (Pubitemid 32434101)
12. S.V. Novoselov, H.Y. Kim, D. Hua, B.C. Lee, C.M. Astle, D.E. Harrison, B. Friguet, M.M. Moustafa, B.A. Carlson, D.L. Hatfield, and V. Gladyshev Regulation of selenoproteins and methionine sulfoxide reductases A and B1 by age, calorie restriction, and dietary selenium in mice Antioxid. Redox Signaling 12 2010 829 838
13. E.K. Ahmed, A. Rogowska-Wrzesinska, P. Roepstorff, A.L. Bulteau, and B. Friguet Protein modification and replicative senescence of WI-38 human embryonic fibroblasts Aging Cell 9 2010 252 272
14. H. Ruan, X.D. Tang, M.L. Chen, M.L. Joiner, G. Sun, N. Brot, H. Weissbach, S.H. Heinemann, L. Iverson, C.F. Wu, T. Hoshi, and M.A. Joiner High-quality life extension by the enzyme peptide methionine sulfoxide reductase Proc. Natl. Acad. Sci. USA 99 2002 2748 2753 (Pubitemid 34240532)
15. A. Koc, A.P. Gasch, J.C. Rutherford, H.Y. Kim, and V.N. Gladyshev Methionine sulfoxide reductase regulation of yeast lifespan reveals reactive oxygen species-dependent and -independent components of aging Proc. Natl. Acad. Sci. USA 101 2004 7999 8004 (Pubitemid 38698043)
16. A.N. Minniti, R. Cataldo, C. Trigo, L. Vasquez, P. Mujica, F. Leighton, N.C. Inestrosa, and R. Aldunate Methionine sulfoxide reductase A expression is regulated by the DAF-16/FOXO pathway in Caenorhabditis elegans Aging Cell 8 2009 690 705
17. D.H. Lim, J.Y. Han, J.R. Kim, Y.S. Lee, and H.Y. Kim Methionine sulfoxide reductase B in the endoplasmic reticulum is critical for stress resistance and aging in Drosophila Biochem. Biophys. Res. Commun. 419 2012 20 26
18. A.B. Salmon, V.I. Perez, A. Bokov, A. Jernigan, G. Kim, H. Zhao, R.L. Levine, and A. Richardson Lack of methionine sulfoxide reductase A in mice increases sensitivity to oxidative stress but does not diminish life span FASEB J 23 2009 3601 3608
19. S.P. Gabbita, M.Y. Aksenov, M.A. Lovell, and W.R. Markesbery Decrease in peptide methionine sulfoxide reductase in Alzheimer′s disease brain J. Neurochem. 73 1999 1660 1666 (Pubitemid 29440169)
20. R. Wassef, R. Haenold, A. Hansel, N. Brot, S.H. Heinemann, and T. Hoshi Methionine sulfoxide reductase A and a dietary supplement S-methyl-L-cysteine prevent Parkinson′s-like symptoms J. Neurosci. 27 2007 12808 12816 (Pubitemid 350159591)
21. B. Garner, P.K. Witting, A.R. Waldeck, J.K. Christison, M. Raftery, and R. Stocker Oxidation of high density lipoproteins. I. Formation of methionine sulfoxide in apolipoproteins AI and AII is an early event that accompanies lipid peroxidation and can be enhanced by alpha-tocopherol J. Biol. Chem. 273:6080-6087 1998
22. B. Ezraty, R. Grimaud, M. El Hassouni, D. Moinier, and F. Barras Methionine sulfoxide reductases protect Ffh from oxidative damages in Escherichia coli EMBO J. 23 2004 1868 1877 (Pubitemid 38649649)
23. J.R. Erickson, M.L. Joiner, X. Guan, W. Kutschke, J. Yang, C.V. Oddis, R.K. Bartlett, J.S. Lowe, S.E. O′Donnell, N. Aykin-Burns, M.C. Zimmerman, K. Zimmerman, A.J. Ham, R.M. Weiss, D.R. Spitz, M.A. Shea, R.J. Colbran, P.J. Mohler, and M.E. Anderson A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation Cell 133 2008 462 474 (Pubitemid 351608692)
24. L.A. Brennan, W. Lee, T. Cowell, F. Giblin, and M. Kantorow Deletion of mouse MsrA results in HBO-induced cataract: MsrA repairs mitochondrial cytochrome c Mol. Vision 15 2009 985 999
25. M. Mahawar, V. Tran, J.S. Sharp, and R.J. Maier Synergistic roles of Helicobacter pylori methionine sulfoxide reductase and GroEL in repairing oxidant-damaged catalase J. Biol. Chem. 286 2011 19159 19169
26. F. Cabreiro, C.R. Picot, M. Perichon, J. Mary, B. Friguet, and I. Petropoulos Identification of proteins undergoing expression level modifications in WI-38 SV40 fibroblasts overexpressing methionine sulfoxide reductase A Biochimie 89 2007 1388 1395 (Pubitemid 47570066)
27. B. Ghesquière, V. Jonckheere, N. Colaert, J. Van Durme, E. Timmerman, M. Goethals, J. Schymkowitz, F. Rousseau, J. Vandekerckhove, and K. Gevaert Redox proteomics of protein-bound methionine oxidation Mol. Cell. Proteomics 10 M110 2011 006866
28. J. Vandesompele, K. De Preter, F. Pattyn, B. Poppe, N. Van Roy, A. De Paepe, and F. Speleman Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes Genome Biol. 3 2002 (RESEARCH0034)
29. N. Brot, J. Werth, D. Koster, and H. Weissbach Reduction of N-acetyl methionine sulfoxide: a simple assay for peptide methionine sulfoxide reductase Anal. Biochem. 122 1982 291 294 (Pubitemid 12053351)
30. A. Shevchenko, M. Wilm, O. Vorm, and M. Mann Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels Anal. Chem. 68 1996 850 858
31. G. Bussone, H. Dib, J.D. Dimitrov, L. Camoin, C. Broussard, N. Tamas, L. Guillevin, S.V. Kaveri, and L. Mouthon Identification of target antigens of self-reactive IgG in intravenous immunoglobulin preparations Proteomics 9 2009 2253 2262
32. D. van der Vlies, E.H. Pap, J.A. Post, J.E. Celis, and K.W. Wirtz Endoplasmic reticulum resident proteins of normal human dermal fibroblasts are the major targets for oxidative stress induced by hydrogen peroxide Biochem. J. 366 2002 825 830
33. A.V. Peskin, and C.C. Winterbourn Kinetics of the reactions of hypochlorous acid and amino acid chloramines with thiols, methionine, and ascorbate Free Radic. Biol. Med. 30 2001 572 579 (Pubitemid 32162964)
34. M.A. Marchetti, G.O. Pizarro, D. Sagher, C. Deamicis, N. Brot, J.F. Hejtmancik, H. Weissbach, and M. Kantorow Methionine sulfoxide reductases B1, B2, and B3 are present in the human lens and confer oxidative stress resistance to lens cells Invest. Ophthalmol. Visual Sci. 46 2005 2107 2112
35. M.A. Baraibar, J. Hyzewicz, A. Rogowska-Wrzesinska, R. Ladouce, P. Roepstorff, V. Mouly, and B. Friguet Oxidative stress-induced proteome alterations target different cellular pathways in human myoblasts Free Radic. Biol. Med. 51 2011 1522 1532
36. M. Ning, D.A. Sarracino, A.T. Kho, S. Guo, S.R. Lee, B. Krastins, F.S. Buonanno, J.A. Vizcaino, S. Orchard, D. McMullin, X. Wang, and E.H. Lo Proteomic temporal profile of human brain endothelium after oxidative stress Stroke 42 2011 37 43
37. T. Kinumi, Y. Ogawa, J. Kimata, Y. Saito, Y. Yoshida, and E. Niki Proteomic characterization of oxidative dysfunction in human umbilical vein endothelial cells (HUVEC) induced by exposure to oxidized LDL Free Radic. Res. 39 2005 1335 1344 (Pubitemid 43023798)
38. Z. Liu, H. Lu, H. Shi, Y. Du, J. Yu, S. Gu, X. Chen, K.J. Liu, and C.A. Hu PUMA overexpression induces reactive oxygen species generation and proteasome-mediated stathmin degradation in colorectal cancer cells Cancer Res. 65 2005 1647 1654 (Pubitemid 40478588)
39. Y. Gao, J.O. Thomas, R.L. Chow, G.H. Lee, and N.J. Cowan A cytoplasmic chaperonin that catalyzes beta-actin folding Cell 69 1992 1043 1050
40. M.B. Yaffe, G.W. Farr, D. Miklos, A.L. Horwich, M.L. Sternlicht, and H. Sternlicht TCP1 complex is a molecular chaperone in tubulin biogenesis Nature 358 1992 245 248
41. E.J. Jung, N.K. Avliyakulov, P. Boontheung, J.A. Loo, A.E. Nel, and DEP Pro-oxidative chemicals induce heat shock proteins and an unfolding protein response in a bronchial epithelial cell line as determined by DIGE analysis Proteomics 7 2007 3906 3918 (Pubitemid 350100007)
42. J.P. Conway, and M. Kinter Proteomic and transcriptomic analyses of macrophages with an increased resistance to oxidized low density lipoprotein (oxLDL)-induced cytotoxicity generated by chronic exposure to oxLDL Mol. Cell. Proteomics 4 2005 1522 1540 (Pubitemid 41555477)
43. R.J. Hung, C.W. Pak, and J.R. Terman Direct redox regulation of F-actin assembly and disassembly by Mical Science 334 2011 1710 1713
44. X. Wang, S. Ling, D. Zhao, Q. Sun, Q. Li, F. Wu, J. Nie, L. Qu, B. Wang, X. Shen, Y. Bai, Y. Li, and Y. Li Redox regulation of actin by thioredoxin-1 is mediated by the interaction of the proteins via cysteine 62 Antioxid. Redox Signaling 13 2010 565 573
45. Y. Qu, J. Wang, P.S. Ray, H. Guo, J. Huang, M. Shin-Sim, B.A. Bukoye, B. Liu, A.V. Lee, X. Lin, P. Huang, J.W. Martens, A.E. Giuliano, N. Zhang, N.H. Cheng, and X. Cui Thioredoxin-like 2 regulates human cancer cell growth and metastasis via redox homeostasis and NF-kappaB signaling J. Clin. Invest. 121 2011 212 225
46. S. Goto, M. Kawakatsu, S. Izumi, Y. Urata, K. Kageyama, Y. Ihara, T. Koji, T. Kondo, and Glutathione S-transferase pi localizes in mitochondria and protects against oxidative stress Free Radic. Biol. Med. 46 2009 1392 1403
47. L.H. Butterfield, A. Merino, S.H. Golub, and H. Shau From cytoprotection to tumor suppression: the multifactorial role of peroxiredoxins Antioxid. Redox Signaling 1 1999 385 402 (Pubitemid 129628306)
48. M.M. Stacey, A.V. Peskin, M.C. Vissers, and C.C. Winterbourn Chloramines and hypochlorous acid oxidize erythrocyte peroxiredoxin 2 Free Radic. Biol. Med. 47 2009 1468 1476
49. P. Csermely, T. Schnaider, C. Soti, Z. Prohaszka, and G. Nardai The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review Pharmacol. Ther. 79 1998 129 168 (Pubitemid 28380440)
50. D.A. Bota, and K.J. Davies Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism Nat. Cell Biol. 4 2002 674 680 (Pubitemid 34993703)
51. H. Sarioglu, S. Brandner, M. Haberger, C. Jacobsen, J. Lichtmannegger, M. Wormke, and U. Andrae Analysis of 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced proteome changes in 5 L rat hepatoma cells reveals novel targets of dioxin action including the mitochondrial apoptosis regulator VDAC2 Mol. Cell. Proteomics 7 2008 394 410 (Pubitemid 351298451)
52. M. Jain, D.A. Brenner, L. Cui, C.C. Lim, B. Wang, D.R. Pimentel, S. Koh, D.B. Sawyer, J.A. Leopold, D.E. Handy, J. Loscalzo, C.S. Apstein, and R. Liao Glucose-6-phosphate dehydrogenase modulates cytosolic redox status and contractile phenotype in adult cardiomyocytes Circ. Res. 93 2003 e9 16
53. S. Filosa, A. Fico, F. Paglialunga, M. Balestrieri, A. Crooke, P. Verde, P. Abrescia, J.M. Bautista, and G. Martini Failure to increase glucose consumption through the pentose-phosphate pathway results in the death of glucose-6-phosphate dehydrogenase gene-deleted mouse embryonic stem cells subjected to oxidative stress Biochem. J. 370 2003 935 943 (Pubitemid 36399086)
54. S.K. Legan, I. Rebrin, R.J. Mockett, S.N. Radyuk, V.I. Klichko, R.S. Sohal, and W.C. Orr Overexpression of glucose-6-phosphate dehydrogenase extends the life span of Drosophila melanogaster J. Biol. Chem. 283 2008 32492 32499
55. M.L. Cheng, H.Y. Ho, Y.H. Wu, and D.T. Chiu Glucose-6-phosphate dehydrogenase-deficient cells show an increased propensity for oxidant-induced senescence Free Radic. Biol. Med. 36 2004 580 591 (Pubitemid 38230175)
56. S.Y. Kim, H.T. Kang, H.R. Choi, and S.C. Park Biliverdin reductase A in the prevention of cellular senescence against oxidative stress Exp. Mol. Med. 43 2011 15 23
57. Y.R. Chen, C.L. Chen, L. Zhang, K.B. Green-Church, and J.L. Zweier Superoxide generation from mitochondrial NADH dehydrogenase induces self-inactivation with specific protein radical formation J. Biol. Chem. 280 2005 37339 37348 (Pubitemid 41642339)
58. Starr, J. M.; Shiels, P. G.; Harris, S. E.; Pattie, A.; Pearce, M. S.; Relton, C. L.; Deary, I. J. Oxidative stress, telomere length and biomarkers of physical aging in a cohort aged 79 years from the 1932 Scottish Mental Survey. Mech. Ageing Dev. 129:745-751; 2008.
59. C. Grillo, C. D′Ambrosio, A. Scaloni, M. Maceroni, S. Merluzzi, C. Turano, and F. Altieri Cooperative activity of Ref-1/APE and ERp57 in reductive activation of transcription factors Free Radic. Biol. Med. 41 2006 1113 1123 (Pubitemid 44331573)
60. T.J. Cohen, A.W. Hwang, T. Unger, J.Q. Trojanowski, and V.M. Lee Redox signalling directly regulates TDP-43 via cysteine oxidation and disulphide cross-linking EMBO J. 31 2011 1241 1252
61. C. Colombrita, E. Zennaro, C. Fallini, M. Weber, A. Sommacal, E. Buratti, V. Silani, and A. Ratti TDP-43 is recruited to stress granules in conditions of oxidative insult J. Neurochem. 111 2009 1051 1061
62. H. Hayakawa, A. Fujikane, R. Ito, M. Matsumoto, K.I. Nakayama, and M. Sekiguchi Human proteins that specifically bind to 8-oxoguanine-containing RNA and their responses to oxidative stress Biochem. Biophys. Res. Commun. 403 2010 220 224
63. S. Arguelles, M. Cano, A. Machado, and A. Ayala Effect of aging and oxidative stress on elongation factor-2 in hypothalamus and hypophysis Mech. Ageing Dev. 132 2011 55 64