Glyceraldehyde-3-phosphate dehydrogenase is largely unresponsive to low regulatory levels of hydrogen peroxide in Saccharomyces cerevisiae

BMC Biochemistry

Volumn 11, Issue 1, 2010, Pages

  Cyrne, Luísa ^a   Antunes, Fernando ^a   Sousa Lopes, Ana ^a   Diaz Bérrio, Joo ^a   Marinho, H Susana ^a  

^a UNIVERSITY OF LISBON   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HYDROGEN PEROXIDE; ISOENZYME; ENZYME INHIBITOR;

ARTICLE; CARBOHYDRATE SYNTHESIS; CELL DEATH; CELL SURVIVAL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME METABOLISM; INCUBATION TIME; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; STEADY STATE; TITRIMETRY; WILD TYPE; ANIMAL; CELL CYCLE; CYTOLOGY; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; METABOLISM; OXIDATION REDUCTION REACTION; UPREGULATION;

SACCHAROMYCES CEREVISIAE;

ANIMALS; CELL CYCLE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, FUNGAL; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE (PHOSPHORYLATING); HYDROGEN PEROXIDE; ISOENZYMES; OXIDATION-REDUCTION; SACCHAROMYCES CEREVISIAE; UP-REGULATION;

EID: 78650574149     PISSN: None     EISSN: 14712091     Source Type: Journal    
DOI: 10.1186/1471-2091-11-49     Document Type: Article

References (56)

1. Thiol chemistry and specificity in redox signaling. CC Winterbourn MB Hampton, Free Radic Biol Med 2008 45 549 561 10.1016/j.freeradbiomed.2008.05.004 18544350
2. Redox-based regulation of signal transduction: principles, pitfalls, and promises. YM Janssen-Heininger BT Mossman NH Heintz HJ Forman B Kalyanaraman T Finkel JS Stamler SG Rhee A van der Vliet, Free Radic Biol Med 2008 45 1 17 10.1016/j.freeradbiomed.2008.03.011 18423411
3. Protein-sulfenic acids: diverse roles for an unlikely player in enzyme catalysis and redox regulation. A Claiborne JI Yeh TC Mallett J Luba EJ Crane V Charrier D Parsonage, Biochemistry 1999 38 15407 15416 10.1021/bi992025k 10569923
4. Widespread sulfenic acid formation in tissues in response to hydrogen peroxide. AT Saurin H Neubert JP Brennan P Eaton, Proc Natl Acad Sci USA 2004 101 17982 17987 10.1073/pnas.0404762101 15604151
5. Sulfiredoxin, the cysteine sulfinic acid reductase specific to 2-Cys peroxiredoxin: its discovery, mechanism of action, and biological significance. SG Rhee W Jeong TS Chang HA Woo, Kidney Int Suppl 2007 3 S8 10.1038/sj.ki. 5002380 17653208
6. Amyloid-beta induces disulfide bonding and aggregation of GAPDH in Alzheimer's disease. RC Cumming D Schubert, FASEB J 2005 19 2060 2062 16186172
7. Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death. CM Haynes EA Titus AA Cooper, Mol Cell 2004 15 767 776 10.1016/j.molcel.2004.08.025 15350220
8. New nuclear functions of the glycolytic protein, glyceraldehyde-3- phosphate dehydrogenase, in mammalian cells. MA Sirover, J Cell Biochem 2005 95 45 52 10.1002/jcb.20399 15770658
9. Glyceraldehyde-3-phosphate dehydrogenase aggregate formation participates in oxidative stress-induced cell death. H Nakajima W Amano T Kubo A Fukuhara H Ihara YT Azuma H Tajima T Inui A Sawa T Takeuchi, J Biol Chem 2009 284 34331 34341 10.1074/jbc.M109.027698 19837666
10. Isolation and characterization of yeast strains carrying mutations in the glyceraldehyde-3-phosphate dehydrogenase genes. L McAlister MJ Holland, J Biol Chem 1985 260 15013 15018 2999100
11. Differential expression of the three yeast glyceraldehyde-3-phosphate dehydrogenase genes. L McAlister MJ Holland, J Biol Chem 1985 260 15019 15027 3905788
12. S-thiolation of glyceraldehyde-3-phosphate dehydrogenase induced by the phagocytosis-associated respiratory burst in blood monocytes. V Ravichandran T Seres T Moriguchi JA Thomas RB Johnston Jr, J Biol Chem 1994 269 25010 25015 7929187
13. S-thiolation of human endothelial cell glyceraldehyde-3-phosphate dehydrogenase after hydrogen peroxide treatment. I Schuppe-Koistinen P Moldeus T Bergman IA Cotgreave, Eur J Biochem 1994 221 1033 1037 10.1111/j.1432-1033. 1994.tb18821.x 8181459
14. Oxidative modifications of glyceraldehyde-3-phosphate dehydrogenase play a key role in its multiple cellular functions. NR Hwang SH Yim YM Kim J Jeong EJ Song Y Lee JH Lee S Choi KJ Lee, Biochem J 2009 423 253 264 10.1042/BJ20090854 19650766
15. Differential protein S-thiolation of glyceraldehyde-3-phosphate dehydrogenase isoenzymes influences sensitivity to oxidative stress. CM Grant KA Quinn IW Dawes, Mol Cell Biol 1999 19 2650 2656 10082531
16. Protein S-thiolation targets glycolysis and protein synthesis in response to oxidative stress in the yeast Saccharomyces cerevisiae. D Shenton CM Grant, Biochem J 2003 374 513 519 10.1042/BJ20030414 12755685
17. Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae. E Cabiscol E Piulats P Echave E Herrero J Ros, J Biol Chem 2000 275 27393 27398 10852912
18. Hydrogen peroxide-induced carbonylation of key metabolic enzymes in Saccharomyces cerevisiae: the involvement of the oxidative stress response regulators Yap1 and Skn7. VM Costa MA Amorim A Quintanilha P Moradas-Ferreira, Free Radic Biol Med 2002 33 1507 1515 10.1016/S0891-5849(02)01086-9 12446208
19. Proteomic analysis of carbonylated proteins in two-dimensional gel electrophoresis using avidin-fluorescein affinity staining. BS Yoo FE Regnier, Electrophoresis 2004 25 1334 1341 10.1002/elps.200405890 15174056
20. Regulation of protein S-thiolation by glutaredoxin 5 in the yeast Saccharomyces cerevisiae. D Shenton G Perrone KA Quinn IW Dawes CM Grant, J Biol Chem 2002 277 16853 16859 10.1074/jbc.M200559200 11882660
21. Role of hydrogen peroxide in NF-kappaB activation: from inducer to modulator. V Oliveira-Marques HS Marinho L Cyrne F Antunes, Antioxid Redox Signal 2009 11 2223 2243 10.1089/ars.2009.2601 19496701
22. Importance of catalase in the adaptive response to hydrogen peroxide: analysis of acatalasaemic Saccharomyces cerevisiae. S Izawa Y Inoue A Kimura, Biochem J 1996 320 61 67 8947468
23. Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J Lee C Godon G Lagniel D Spector J Garin J Labarre MB Toledano, J Biol Chem 1999 274 16040 16046 10.1074/jbc.274.23.16040 10347154
24. The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). MT Martinez-Pastor G Marchler C Schuller A Marchler-Bauer H Ruis F Estruch, EMBO J 1996 15 2227 2235 8641288
25. H2O2 sensing through oxidation of the Yap1 transcription factor. A Delaunay AD Isnard MB Toledano, EMBO J 2000 19 5157 5166 10.1093/emboj/19.19. 5157 11013218
26. H2O2 activates the nuclear localization of Msn2 and Maf1 through thioredoxins in Saccharomyces cerevisiae. S Boisnard G Lagniel C Garmendia-Torres M Molin E Boy-Marcotte M Jacquet MB Toledano J Labarre S Chedin, Eukaryot Cell 2009 8 1429 1438 10.1128/EC.00106-09 19581440
27. Decreased cellular permeability to H2O2 protects Saccharomyces cerevisiae cells in stationary phase against oxidative stress. A Sousa-Lopes F Antunes L Cyrne HS Marinho, FEBS Lett 2004 578 152 156 10.1016/j.febslet.2004.10.090 15581633
28. The Saccharomyces cerevisiae proteome of oxidized protein thiols: contrasted functions for the thioredoxin and glutathione pathways. N Le Moan G Clement S Le Maout F Tacnet MB Toledano, J Biol Chem 2006 281 10420 10430 10.1074/jbc.M513346200 16418165
29. Shotgun redox proteomics identifies specifically modified cysteines in key metabolic enzymes under oxidative stress in Saccharomyces cerevisiae. B McDonagh S Ogueta G Lasarte CA Padilla JA Barcena, J Proteomics 2009 72 677 689 10.1016/j.jprot.2009.01.023 19367685
30. Decrease of H2O2 plasma membrane permeability during adaptation to H2O2 in Saccharomyces cerevisiae. MR Branco HS Marinho L Cyrne F Antunes, J Biol Chem 2004 279 6501 6506 10.1074/jbc.M311818200 14645222
31. Two-dimensional electrophoretic separation of yeast proteins using a non-linear wide range (pH 3-10) immobilized pH gradient in the first dimension; reproducibility and evidence for isoelectric focusing of alkaline (pI > 7) proteins. J Norbeck A Blomberg, Yeast 1997 13 1519 1534 10.1002/(SICI)1097- 0061(199712)13:16<1519::AID-YEA211>3.0.CO;2-U 9509572
32. Differential synthesis of glyceraldehyde-3-phosphate dehydrogenase polypeptides in stressed yeast cells. H Boucherie N Bataille IT Fitch M Perrot MF Tuite, FEMS Microbiol Lett 1995 125 127 133 10.1111/j.1574-6968.1995.tb07348. x 7875559
33. The glyceraldehyde-3-phosphate dehydrogenase polypeptides encoded by the Saccharomyces cerevisiae TDH1, TDH2 and TDH3 genes are also cell wall proteins. ML Delgado JE O'Connor I Azorin J Renau-Piqueras ML Gil D Gozalbo, Microbiology 2001 147 411 417 11158358 (Pubitemid 32156817)
34. 2stimulon in Saccharomyces cerevisiae. C Godon G Lagniel J Lee J-M Buhler S Kieffer M Perrot H Boucherie MB Toledano J Labarre, J Biol Chem 1998 273 22480 22489 10.1074/jbc.273.35.22480 9712873
35. Genomic expression programs in the response of yeast cells to environmental changes. AP Gasch PT Spellman CM Kao O Carmel-Harel MB Eisen G Storz D Botstein PO Brown, Mol Biol Cell 2000 11 4241 4257 11102521
36. Hydrogen peroxide in the human body. B Halliwell MV Clement LH Long, FEBS Lett 2000 486 10 13 10.1016/S0014-5793(00)02197-9 11108833
37. Proteomic detection of hydrogen peroxide-sensitive thiol proteins in Jurkat cells. JW Baty MB Hampton CC Winterbourn, Biochem J 2005 389 785 795 10.1042/BJ20050337 15801906
38. Protein disulfide bond formation in the cytoplasm during oxidative stress. RC Cumming NL Andon PA Haynes M Park WH Fischer D Schubert, J Biol Chem 2004 279 21749 21758 10.1074/jbc.M312267200 15031298
39. 2induce apoptosis through Fenton chemistry independent of cellular thiol state. F Antunes E Cadenas, Free Radic Biol Med 2001 30 1008 1018 10.1016/S0891-5849(01)00493-2 11316581
40. Thioredoxins function as deglutathionylase enzymes in the yeast Saccharomyces cerevisiae. D Greetham J Vickerstaff D Shenton GG Perrone IW Dawes CM Grant, BMC Biochem 2010 11 3 10.1186/1471-2091-11-3 20074363
41. The yeast Saccharomyces cerevisiae contains two glutaredoxin genes that are required for protection against reactive oxygen species. S Luikenhuis G Perrone IW Dawes CM Grant, Mol Biol Cell 1998 9 1081 1091 9571241
42. Role of thioredoxins in the response of Saccharomyces cerevisiae to oxidative stress induced by hydroperoxides. EO Garrido CM Grant, Mol Microbiol 2002 43 993 1003 10.1046/j.1365-2958.2002.02795.x 11929546
43. NADH-reductive stress in Saccharomyces cerevisiae induces the expression of the minor isoform of glyceraldehyde-3-phosphate dehydrogenase (TDH1). H Valadi A Valadi R Ansell L Gustafsson L Adler J Norbeck A Blomberg, Curr Genet 2004 45 90 95 10.1007/s00294-003-0469-1 14652693
44. Glycolytic enzyme GAPDH promotes peroxide stress signaling through multistep phosphorelay to a MAPK cascade. S Morigasaki K Shimada A Ikner M Yanagida K Shiozaki, Mol Cell 2008 30 108 113 10.1016/j.molcel.2008.01.017 18406331
45. The Saccharomyces cerevisiae Sln1p-Ssk1p two-component system mediates response to oxidative stress and in an oxidant-specific fashion. KK Singh, Free Radic Biol Med 2000 29 1043 1050 10.1016/S0891-5849(00)00432-9 11084293
46. Rck1 and Rck2 MAPKAP kinases and the HOG pathway are required for oxidative stress resistance. E Bilsland C Molin S Swaminathan A Ramne P Sunnerhagen, Mol Microbiol 2004 53 1743 1756 10.1111/j.1365-2958.2004.04238.x 15341652
47. Metabolic reconfiguration is a regulated response to oxidative stress. CM Grant, J Biol 2008 7 1 10.1186/jbiol63 18226191
48. Dynamic rerouting of the carbohydrate flux is key to counteracting oxidative stress. M Ralser MM Wamelink A Kowald B Gerisch G Heeren EA Struys E Klipp C Jakobs M Breitenbach H Lehrach,, et al. J Biol 2007 6 10 10.1186/jbiol61 18154684
49. H2O2 induces rapid biophysical and permeability changes in the plasma membrane of Saccharomyces cerevisiae. V Folmer N Pedroso AC Matias SCDN Lopes F Antunes L Cyrne HS Marinho, Biochim Biophys Acta 2008 1778 1141 1147 10.1016/j.bbamem.2007.12.008 18187036
50. JR Johnston, Molecular Genetics of Yeast. A practical approach New York: IRL Press, Johnston JR, 1994 261 265
51. A simplification of the protein assay method of Lowry et al. which is more generally applicable. GL Peterson, Anal Biochem 1977 83 346 356 10.1016/0003-2697(77)90043-4 603028
52. Glyceraldehyde-3-Phosphate Dehydrogenase from Muscle. SF Velick, Methods Enzymol 1955 1 401 406 full-text
53. Catalase. HE Aebi, Methods of Enzymatic Analysis Weinheim: Verlag Chemie, Bergmeyer HU, 1984 273 284
54. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. UK Laemmli, Nature 1970 227 680 685 10.1038/227680a0 5432063
55. OJ Bjerrum C Schafer-Nielsen, Analytical Electrophoresis Weinheim: Verlag Chemie, Dunn MJ, 1986 315
56. ImageJ. WS Rasband, U. S. National Institutes of Health, Bethesda, Maryland, USA 1997