Proteomic analysis of the oxidative stress response in kluyveromyces lactis and effect of glutathione reductase depletion

Journal of Proteome Research

Volumn 9, Issue 5, 2010, Pages 2358-2376

  Garcia Leiro A ^a   Cerdan M E ^a   Gonzalez Siso M I ^a  

^a UNIVERSITY OF A CORUÑA   (Spain)

Author keywords

Glutathione reductase; Kluyveromyces; Oxidative stress; Proteomics; Yeast

Indexed keywords

GLUTATHIONE REDUCTASE; GLYCOLYTIC ENZYME; HYDROGEN PEROXIDE; OXIDOREDUCTASE;

AMINO ACID METABOLISM; ARTICLE; CARBOHYDRATE METABOLISM; CITRIC ACID CYCLE; DOWN REGULATION; ENERGY YIELD; ENZYME ACTIVITY; FUNGAL STRAIN; FUNGUS GROWTH; KLUYVEROMYCES; MASS SPECTROMETRY; MOLECULAR WEIGHT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEOMICS; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION;

AMINO ACIDS; CARBOHYDRATE METABOLISM; CLUSTER ANALYSIS; FUNGAL PROTEINS; GLUTATHIONE REDUCTASE; HYDROGEN PEROXIDE; ISOELECTRIC POINT; KLUYVEROMYCES; MOLECULAR WEIGHT; MULTIVARIATE ANALYSIS; MUTATION; OXIDATIVE STRESS; PROTEOME; PROTEOMICS; REPRODUCIBILITY OF RESULTS;

KLUYVEROMYCES; KLUYVEROMYCES LACTIS; PROTISTA; SACCHAROMYCES CEREVISIAE;

EID: 77952045719     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr901086w     Document Type: Article

References (54)

1. Weeks, M. E.; Sinclair, J.; Butt, A.; Chung, Y. L.; Worthington, J. L.; Wilkinson, C. R.; Griffiths, J.; Jones, N.; Waterfield, M. D.; Timms, J. A parallel proteomic and metabolomic analysis of the hydrogen peroxide- and Sty1p-dependent stress response in Schizosaccharomyces pombe Proteomics 2006, 6 (9) 2772-2796
2. González-Siso, M. I.; García-Leiro, A.; Tarrío, N.; Cerdán, M. E. Sugar metabolism, redox balance and oxidative stress response in the respiratory yeast Kluyveromyces lactis Microb. Cell Fact. 2009, 8, 46
3. González-Siso, M. I.; Freire-Picos, M. A.; Ramil, E.; González-Domínguez, M.; Rodríguez Torres, A.; Cerdán, M. E. Respirofermentative metabolism in Kluyveromyces lactis: Insights and perspectives Enzyme Microb. Technol. 2000, 26 (9-10) 699-705
4. Ocampo, A.; Barrientos, A. From the bakery to the brain business: developing inducible yeast models of human neurodegenerative disorders Biotechniques 2008, 45 (4) 7-14
5. Sherman, D.; Durrens, P.; Beyne, E.; Nikolski, M.; Souciet, J. L. Génolevures Consortium. Genolevures: comparative genomics and molecular evolution of hemiascomycetous yeasts Nucleic Acids Res. 2004, 32 (S1) D315-D318
6. Buckholz, R. G.; Gleeson, M. A. Yeast systems for the commercial production of heterologous proteins Biotechnology (N.Y.) 1991, 9 (11) 1067-1072
7. Oktyabrsky, O. N.; Smirnova, G. V. Redox regulation of cellular functions Biochemistry (Moscow) 2007, 72 (2) 132-145
8. Gasch, A. P.; Spellman, P. T.; Kao, C. M.; Carmel-Harel, O.; Eisen, M. B.; Storz, G.; Botstein, D.; Brown, P. O. Genomic expression programs in the response of yeast cells to environmental changes Mol. Biol. Cell 2000, 11 (12) 4241-4257
9. Koerkamp, M. G.; Rep, M.; Bussemaker, H. J.; Hardy, G. P.; Mul, A.; Piekarska, K.; Szigyarto, C. A.; De Mattos, J. M.; Tabak, H. F. Dissection of transient oxidative stress response in Saccharomyces cerevisiae by using DNA microarrays Mol. Biol. Cell 2002, 13 (8) 2783-2794
10. Molina-Navarro, M. M.; Castells-Roca, L.; Bellí, G.; García-Martínez, J.; Marín-Navarro, J.; Moreno, J.; Pérez-Ortín, J. E.; Herrero, E. Comprehensive transcriptional analysis of the oxidative response in yeast J. Biol. Chem. 2008, 283 (26) 17908-17918
11. Kelley, R.; Ideker, T. Genome-wide fitness and expression profiling implicate Mga2 in adaptation to hydrogen peroxide PLoS Genet. 2009, 5 (5 e1000488
12. 2 stimulon in Saccharomyces cerevisiae J. Biol. Chem. 1998, 273 (35) 22480-22489
13. Shanmuganathan, A.; Avery, S. V.; Willetts, S. A.; Houghton, J. E. Copper-induced oxidative stress in Saccharomyces cerevisiae targets enzymes of the glycolytic pathway FEBS Lett. 2004, 556 (1-3) 253-259
14. 2 challenge J. Proteome Res. 2006, 5 (10) 2539-2546
15. Kim, I.; Yun, H.; Jin, I. Comparative proteomic analyses of the yeast Saccharomyces cerevisiae KNU5377 strain against menadione-induced oxidative stress J. Microbiol. Biotechnol. 2007, 17 (2) 207-217
16. 2 Proteomics 2007, 7 (9) 1434-1445
17. Mascarenhas, C.; Edwards-Ingram, L. C.; Zeef, L.; Shenton, D.; Ashe, M. P.; Grant, C. M. Gcn4 is required for the response to peroxide stress in the yeast Saccharomyces cerevisiae Mol. Biol. Cell 2008, 19 (7) 2995-3007
18. Braconi, D.; Bernardini, G.; Possenti, S.; Laschi, M.; Arena, S.; Scaloni, A.; Geminiani, M.; Sotgiu, M.; Santucci, A. Proteomics and redox-proteomics of the effects of herbicides on a wild-type wine Saccharomyces cerevisiae strain J. Proteome Res. 2009, 8 (1) 257-267
19. De Groot, M. J. L.; Daran-Lapujade, P.; van Breukelen, B.; Knijnenburg, T. A.; de Hulster, E. A.; Reinders, M. J.; Pronk, J. T.; Heck, A. J.; Slijper, M. Quantitative proteomics and transcriptomics of anaerobic and aerobic yeast cultures reveals post-transcriptional regulation of key cellular processes Microbiology 2007, 153 (11) 3864-3878
20. Díaz Prado, S.; Tarrío, N.; Cerdan, M. E.; González-Siso, M. I. Cloning genes from a library using a clustering strategy and PCR Mol. Biotechnol. 2004, 26 (1) 35-38
21. Tarrío, N.; Díaz Prado, S.; Cerdán, M. E.; González-Siso, M. I. Isolation and characterization of two nuclear genes encoding glutahione and thioredoxin reductases from the yeast Kluyveromyces lactis Biochim. Biophys. Acta 2004, 1678 (2-3) 170-175
22. Blanco, M.; Núñez, L.; Tarrío, N.; Canto, E.; Becerra, M.; Cerdán, M. E.; González-Siso, M. I. An approach to the hypoxic and oxidative stress responses in Kluyveromyces lactis by analysis of mRNA FEMS Yeast Res. 2007, 7 (5) 702-714
23. Tarrío, N.; García-Leiro, A.; Cerdán, M. E.; González-Siso, M. I. The role of glutathione reductase in the interplay between oxidative stress response and turnover of cytosolic NADPH in Kluyveromyces lactis FEMS Yeast Res. 2008, 8 (4) 597-606
24. Grant, C. M.; Collinson, L. P.; Roe, J. H.; Dawes, I. W. Yeast glutathione reductase is required for protection against oxidative stress and is a target gene for yAP-1 transcriptional regulation Mol. Microbiol. 1996, 21 (1) 171-179
25. García-Leiro, A.; Cerdán, M. E.; González-Siso, M. I. A functional analysis of Kluyveromyces lactis glutathione reductase. Yeast, in press. DOI: 10.1002/yea.1760.
26. Zitomer, R. S.; Hall, B. D. Yeast cytochrome c messenger RNA. In vitro translation and specific inmunoprecipitation of the CYC1 gene product J. Biol. Chem. 1976, 251 (20) 6320-6326
27. Ruíz-Romero, C.; López-Armada, M. J.; Blanco, F. J. Mitochondrial proteomic characterization of human normal articular chondrocytes Osteoarthritis Cartilage 2006, 14 (6) 507-518
28. Ruíz-Romero, C.; Calamia, V.; Mateos, J.; Carreira, V.; Martínez-Gomariz, M.; Fernández, M.; Blanco, F. J. Mitochondrial dysregulation of osteoarthritic human articular chondrocytes analyzed by proteomics Mol. Cell. Proteomics 2009, 8 (1) 172-189
29. Chang, Q.; Griest, T. A.; Harter, T. M.; Petrash, J. M. Functional studies of aldo-keto reductases in Saccharomyces cerevisiae Biochim. Biophys. Acta 2007, 1773 (3) 321-329
30. 2 receptor and redox-transducer in gene activation Cell 2002, 111 (4) 471-481
31. Kusch, H.; Engelmann, S.; Albrecht, D.; Morschhäuser, J.; Hecker, M. Proteomic analysis of the oxidative stress response in Candida albicans Proteomics 2007, 7 (5) 686-697
32. Tarrío, N.; Becerra, M.; Cerdán, M. E.; González-Siso, M. I. Reoxidation of cytosolic NADPH in Kluyveromyces lactis FEMS Yeast Res. 2006, 6 (3) 371-380
33. Díaz Prado, S.; Cerdán, M. E.; González-Siso, M. I. Isolation and transcriptional regulation of the Kluyveromyces lactis FBA1 (fructose-1,6-bisphosphate aldolase) gene Can. J. Microbiol. 2004, 50 (8) 645-652
34. Grant, C. M. Metabolic reconfiguration is a regulated response to oxidative stress J. Biol. 2008, 7 (1) 1
35. Jacoby, J.; Hollenberg, C. P.; Heinisch, J. J. Transaldolase mutants in the yeast Kluyveromyces lactis provide evidence that glucose can be metabolized through the pentose phosphate pathway Mol. Microbiol. 1993, 10 (4) 867-876
36. Blank, L. M.; Lehmbeck, F.; Saber, U. Metabolic-flux and network analysis in fourteen hemiascomycetous yeasts FEMS Yeast Res. 2005, 5 (6-7) 545-558
37. Becerra, M.; Tarrío, N.; González-Siso, M. I.; Cerdán, M. E. Genome-wide analysis of Kluyveromyces lactis in wild-type and rag2 mutant strains Genome 2004, 47 (5) 970-978
38. Saliola, M.; Scappucci, G.; De Maria, I.; Lodi, T.; Mancini, P.; Falcone, C. Deletion of the glucose-6-phosphate dehydrogenase gene KlZWF1 affects both fermentative and respiratory metabolism in Kluyveromyces lactis Eukaryot. Cell. 2007, 6 (1) 19-27
39. Bucciarelli, T.; Saliola, M.; Brisdelli, F.; Bozzi, A.; Falcone, C.; Di Ilio, C.; Martin, F. Oxidation of Cys278 of ADH I isozyme from Kluyveromyces lactis by naturally occurring disulfides causes its reversible inactivation Biochim. Biophys. Acta 2009, 1794 (3) 563-568
40. Wang, X.; Mann, C. J.; Bai, Y.; Ni, L.; Weiner, H. Molecular cloning, characterization, and potential roles of cytosolic and mitochondrial aldehyde dehydrogenases in ethanol metabolism in Saccharomyces cerevisiae J. Bacteriol. 1998, 180 (4) 822-830
41. Saliola, M.; Sponziello, M.; DAmici, S.; Lodi, T.; Falcone, C. Characterization of KlGUT2, a gene of the glycerol-3-phosphate shuttle, in Kluyveromyces lactis FEMS Yeast Res. 2008, 8 (5) 697-705
42. Tarrío, N.; Díaz Prado, S.; Cerdán, M. E.; González-Siso, M. I. The nuclear genes encoding the internal (KlNDI1) and external (KlNDE1) alternative NAD(P)H:ubiquinone oxidoreductases of mitochondria from Kluyveromyces lactis Biochim. Biophys. Acta 2005, 1707 (2-3) 199-210
43. Tarrío, N.; Cerdán, M. E.; González-Siso, M. I. Characterization of the second external alternative dehydrogenase from mitochondria of the respiratory yeast Kluyveromyces lactis Biochim. Biophys. Acta 2006, 1757 (11) 1476-1484
44. Shenton, D.; Grant, C. M. Protein S-thiolation targets glycolysis and protein synthesis in response to oxidative stress in the yeast Saccharomyces cerevisiae Biochem. J. 2003, 374 (2) 513-519
45. Bao, R.; Zhang, Y.; Lou, X.; Zhou, C. Z.; Chen, Y. Structural and kinetic analysis of Saccharomyces cerevisiae thioredoxin Trx1: implications for the catalytic mechanism of GSSG reduced by the thioredoxin system Biochim. Biophys. Acta 2009, 1794 (8) 1218-1223
46. Stoltzman, C. A.; Peterson, C. W.; Breen, K. T.; Muoio, D. M.; Billin, A. N.; Ayer, D. E. Glucose sensing by MondoA:Mlx complexes: a role for hexokinases and direct regulation of thioredoxin-interacting protein expression Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (19) 6912-6917
47. Verho, R.; Richard, P.; Jonson, P. H.; Sundqvist, L.; Londesborough, J.; Penttilä, M. Identification of the first fungal NADP-GAPDH from Kluyveromyces lactis Biochemistry 2002, 41 (46) 13833-13838
48. Boucherié, H.; Bataille, N.; Fitch, I. T.; Perrot, M.; Tuite, M. F. Differential synthesis of glyceraldehyde-3-phosphate dehydrogenase polypeptides in stressed yeast cells FEMS Microbiol. Lett. 1995, 125 (2-3) 127-133
49. Saliola, M.; De Maria, I.; Lodi, T.; Fiori, A.; Falcone, C. KlADH3, a gene encoding a mitochondrial alcohol dehydrogenase, affects respiratory metabolism and cytochrome content in Kluyveromyces lactis FEMS Yeast Res. 2006, 6 (8) 1184-1192
50. Hartl, F. U.; Hayer-Hartl, M. Molecular chaperones in the cytosol: from nascent chain to folded protein Science 2002, 295 (5561) 1852-1858
51. Picard, D. Heat-shock protein 90, a chaperone for folding and regulation Cell. Mol. Life Sci. 2002, 59 (10) 1640-1648
52. Lamas-Maceiras, M.; Núñez, L.; Rodríguez-Belmonte, E.; González-Siso, M. I.; Cerdán, M. E. Functional characterization of KlHAP1: a model to foresee different mechanisms of transcriptional regulation by Hap1p in yeasts Gene 2007, 405 (1-2) 96-107
53. Coleman, S. T.; Fang, T. K.; Rovinsky, S. A.; Turano, F. J.; Moye-Rowley, W. S. Expression of a glutamate decarboxylase homologue is required for normal oxidative stress tolerance in Saccharomyces cerevisiae J. Biol. Chem. 2001, 276 (1) 244-250
54. Minard, K. I.; McAlister-Henn, L. Sources of NADPH in yeast vary with carbon source J. Biol. Chem. 2005, 280 (48) 39890-39896