An approach to the hypoxic and oxidative stress responses in Kluyveromyces lactis by analysis of mRNA levels

FEMS Yeast Research

Volumn 7, Issue 5, 2007, Pages 702-714

  Blanco, Moisés ^a   Núñez, Laura ^a   Tarrío, Nuria ^a   Canto, Elena ^a   Becerra, Manuel ^a   González Siso, M Isabel ^a   Cerdán, M Esperanza ^a  

^a UNIVERSITY OF A CORUÑA   (Spain)

Author keywords

DNA arrays; Hypoxia; Kluyveromyces lactis; Oxidative stress; Transcriptome

Indexed keywords

GLUCOSE 6 PHOSPHATE ISOMERASE; HYDROGEN PEROXIDE; MESSENGER RNA; RAG2 PROTEIN;

AEROBIC METABOLISM; CONFERENCE PAPER; CONTROLLED STUDY; DNA MICROARRAY; FUNGAL STRAIN; GLYCOLYSIS; HYPOXIA; KLUYVEROMYCES; NONHUMAN; OXIDATIVE STRESS; SACCHAROMYCES CEREVISIAE; WILD TYPE; YEAST;

ANOXIA; CULTURE MEDIA; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; HEAT-SHOCK RESPONSE; KLUYVEROMYCES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; PROTEOME; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

CANDIDA ALBICANS; KLUYVEROMYCES LACTIS; SACCHAROMYCES CEREVISIAE;

EID: 34447315910     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2007.00233.x     Document Type: Conference Paper

References (56)

1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105 : 121 126.
2. Becerra M, Lombardía-Ferreira LJ, Hauser NC, Hoheisel JD, Tizón B Cerdán ME (2002) The yeast transcriptome in aerobic and hypoxic conditions: effects of hap1 rox1 rox3 and srb10 deletions. Mol Microbiol 43 : 545 555. Erratum in Mol Microbiol 45: 265.
3. Becerra M, Tarrío N, González-Siso MI Cerdán ME (2004) Genome-wide analysis of Kluyveromyces lactis in wild type and rag2 mutant strains. Genome 47 : 970 978.
4. Betina S, Gavurnikova G, Haviernik P, Sabova L Kolarov J (1995) Expression of the AAC2 gene encoding the major mitochondrial ADP/ATP carrier in Saccharomyces cerevisiae is controlled at the transcriptional level by oxygen heme and HAP2 factor. Eur J Biochem 229 : 651 657.
5. Billard P, Dumond H Bolotin-Fukuhara M (1997) Characterization of an AP-1-like transcription factor that mediates an oxidative stress response in Kluyveromyces lactis. Mol Gen Genet 257 : 62 70.
6. Blanco M, Becerra M, González-Siso MI Cerdán ME (2005) Functional characterization of KlHEM13, a hypoxic gene of Kluyveromyces lactis. Can J Microbiol 51 : 241 249. Erratum in Can J Microbiol 51: 431.
7. Bolotin-Fukuhara M, Casaregola S Aigle M (2006) Genome evolution: lessons from Genolevures. Topics Curr Genet 15 : 165 196.
8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein - dye binding. Anal Biochem 72 : 248 254.
9. Bussereau F, Casaregola S, Lafay JF Bolotin-Fukuhara M (2006) The Kluyveromyces lactis repertoire of transcriptional regulators. FEMS Yeast Res 6 : 325 335.
10. Chomczynski P Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162 : 156 159.
11. Deckert J, Khalaf RA, Hwang SM Zitomer RS (1999) Characterization of the DNA binding and bending HMG domain of the yeast hypoxic repressor Rox1. Nucleic Acids Res 27 : 3518 3526.
12. Delaunay A, Pflieger D, Barrault MB, Vinh J Toledano MB (2002) A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111 : 471 481.
13. Demasi AP, Pereira GA Netto LE (2001) Cytosolic thioredoxin peroxidase I is essential for the antioxidant defense of yeast with dysfunctional mitochondria. FEBS Lett 509 : 430 434.
14. Dirmeier R, O'Brien KM, Engle M, Dodd A, Spears E Poyton RO (2002) Exposure of yeast cells to anoxia induces transient oxidative stress. Implications for the induction of hypoxic genes. J Biol Chem 277 : 34 773 34 778.
15. Dumond H, Danielou N, Pinto M Bolotin-Fukuhara M (2000) A large-scale study of Yap1p-dependent genes in normal aerobic and H2O2-stress conditions: the role of Yap1p in cell proliferation control in yeast. Mol Microbiol 36 : 830 845.
16. Fontanesi F, Viola AM Ferrero I (2006) Heterologous complementation of the Klaac null mutation of Kluyveromyces lactis by the Saccharomyces cerevisiae AAC3 gene encoding the ADP/ATP carrier. FEMS Yeast Res 6 : 414 420.
17. Garrido EO Grant CM (2002) Role of thioredoxins in the response of Saccharomyces cerevisiae to oxidative stress induced by hydroperoxides. Mol Microbiol 43 : 993 1003.
18. Gavurniková G, Sabová L, Kissova I, Haviernik P Kolarov J (1996) Transcription of the AAC1 gene encoding an isoform of mitochondrial ADP/ATP carrier in Saccharomyces cerevisiae is regulated by oxygen in a heme-independent manner. Eur J Biochem 239 : 759 763.
19. Goffrini P, Wesolowski-Louvel M Ferrero I (1991) A phosphoglucose isomerase gene is involved in the Rag phenotype of the yeast Kluyveromyces lactis. Mol Gen Genet 228 : 401 409.
20. González-Domínguez M, Mendez-Carro C Cerdán ME (1997) Isolation and characterization of the KlHEM1 gene in Kluyveromyces lactis. Yeast 13 : 961 971.
21. González-Domínguez M, Freire-Picos MA, Ramil E, Guiard B Cerdán ME (2000) Heme-mediated transcriptional control in Kluyveromyces lactis. Curr Genet 38 : 171 177.
22. González-Siso MI, Freire-Picos MA Cerdán ME (1996a) Reoxidation of the NADPH produced by the pentose phosphate pathway is necessary for the utilization of glucose by Kluyveromyces lactis rag2 mutants. FEBS Lett 387 : 7 10.
23. González-Siso MI, Ramil E, Cerdán ME Freire-Picos MA (1996b) Respirofermentative metabolism in Kluyveromyces lactis: ethanol production and the Crabtree effect. Enzyme Microb Technol 18 : 585 591.
24. González-Siso MI, Freire-Picos MA, Ramil E, González- Domínguez M, Rodríguez Torres A Cerdán ME (2000) Respirofermentative metabolism in Kluyveromyces lactis: insights and perspectives. Enzyme Microb Technol 26 : 699 705.
25. Hansen JM, Zhang H Jones DP (2006) Differential oxidation of thioredoxin-1, thioredoxin-2 and glutathione by metal ions. Free Radic Biol Med 40 : 138 145.
26. Hauser NC, Vingron M, Scheideler M, Krems B, Hellmuth K, Entian KD Hoheisel JD (1998) Transcriptional profiling on all open reading frames of Saccharomyces cerevisiae. Yeast 14 : 1209 1221.
27. He XJ Fassler JS (2005) Identification of novel Yap1p and Skn7p binding sites involved in the oxidative stress response of Saccharomyces cerevisiae. Mol Microbiol 58 : 1454 1467.
28. Hodge MR, Kim G, Singh K Cumsky MG (1989) Inverse regulation of the yeast COX5 genes by oxygen and heme. Mol Cell Biol 9 : 1958 1964.
29. Holmgren A Björnstedt M (1995) Thioredoxin and thioredoxin reductase. Methods Enzymol 252 : 199 208.
30. Ihmels J, Bergmann S, Gerami-Nejad M, Yanai I, McClellan M, Berman J Barkai N (2005) Rewiring of the yeast transcriptional network through the evolution of motif usage. Science 309 : 938 940.
31. Kaiser C, Michaelis S Mitchell A (1994) Methods in Yeast Genetics, A Cold Spring Harbor Laboratory Course Manual. Cold Spring Harbor, New York.
32. Kang HA, Schwelberger HG Hershey JW (1992) The two genes encoding protein synthesis initiation factor eIF-5A in Saccharomyces cerevisiae are members of a duplicated gene cluster. Mol Gen Genet 233 : 487 490.
33. Kellis M, Birren BW Lander ES (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428 : 617 624.
34. Keng T (1992) HAP1 and ROX1 form a regulatory pathway in the repression of HEM13 transcription in Saccharomyces cerevisiae. Mol Cell Biol 12 : 2616 2623.
35. Kiers J, Zeeman AM, Luttik M, Thiele C, Castrillo JI, Steensma HY, van Dijken JP Pronk JT (1998) Regulation of alcoholic fermentation in batch and chemostat cultures of Kluyveromyces lactis CBS 2359. Yeast 14 : 459 469.
36. Klinkenberg LG, Mennella TA, Luetkenhaus K Zitomer RS (2005) Combinatorial repression of the hypoxic genes of Saccharomyces cerevisiae by DNA binding proteins Rox1 and Mot3. Eukaryot Cell 4 : 649 660.
37. Kwon M, Chong S, Han S Kim K (2003) Oxidative stresses elevate the expression of cytochrome c peroxidase in Saccharomyces cerevisiae. Biochim Biophys Acta 1623 : 1 5.
38. Laz TM, Pietras DF Sherman F (1984) Differential regulation of the duplicated isocytochrome c genes in yeast. Proc Natl Acad Sci USA 81 : 4475 4479.
39. Mennella TA, Klinkenberg LG Zitomer RS (2003) Recruitment of Tup1-Ssn6 by yeast hypoxic genes and chromatin-independent exclusion of TATA binding protein. Eukaryot Cell 2 : 1288 1303.
40. Sabová L, Zeman I, Supek F Kolarov J (1993) Transcriptional control of AAC3 gene encoding mitochondrial ADP/ATP translocator in Saccharomyces cerevisiae by oxygen heme and ROX1 factor. Eur J Biochem 213 : 547 553.
41. Sambrook J, Fritsch EF Maniatis T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Press, New York.
42. Sertil O, Kapoor R, Cohen BD, Abramova N Lowry CV (2003) Synergistic repression of anaerobic genes by Mot3 and Rox1 in Saccharomyces cerevisiae. Nucleic Acids Res 31 : 5831 5837.
43. Sherman D, Durrens P, Beyne E, Nikolski M Souciet JL (2004) Genolevures Consortium Genolevures: comparative genomics and molecular evolution of hemiascomycetous yeasts. Nucleic Acids Res 32 : D315 D318.
44. Snoek IS Steensma HY (2006) Why does Kluyveromyces lactis not grow under anaerobic conditions? Comparison of essential anaerobic genes of Saccharomyces cerevisiae with the Kluyveromyces lactis genome. FEMS Yeast Res 6 : 393 403.
45. Tarrío N, Díaz Prado S, Cerdán ME González Siso MI (2004) Isolation and characterization of two nuclear genes encoding glutathione and thioredoxin reductases from the yeast Kluyveromyces lactis. Biochim Biophys Acta 1678 : 170 175.
46. Tarrío N, Díaz-Prado S, Cerdán ME González Siso MI (2005) The nuclear genes encoding the internal (KlNDI1) and external (KlNDE1) alternative NAD(P)H: ubiquinone oxidoreductases of mitochondria from Kluyveromyces lactis. Biochim Biophys Acta 1707 : 199 210.
47. Tarrío N, Becerra M, Cerdán ME González Siso MI (2006a) Reoxidation of cytosolic NADPH in Kluyveromyces lactis. FEMS Yeast Res 6 : 371 380.
48. Tarrío N, Cerdán ME González- Siso MI (2006b) Characterization of the second external alternative dehydrogenase from mitochondria of the respiratory yeast Kluyveromyces lactis. Biochim Biophys Acta 1757 : 1476 1484.
49. Ter Linde JJ, Liang H, Davis RW, Steensma HY, van Dijken JP Pronk JT (1999) Genome-wide transcriptional analysis of aerobic and anaerobic chemostat cultures of Saccharomyces cerevisiae. J Bacteriol 181 : 7409 7413.
50. Verdiere J, Gaisne M Labbe-Bois R (1991) CYP1 (HAP1) is a determinant effector of alternative expression of heme-dependent transcribed genes in yeast. Mol Gen Genet 228 : 300 306. Erratum in Mol Gen Genet 229: 324.
51. Wolfe KH Shields DC (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387 : 708 713.
52. Wong S, Butler G Wolfe KH (2002) Gene order evolution and paleopolyploidy in hemiascomycete yeasts. Proc Natl Acad Sci USA 99 : 9272 9277.
53. Zagorec M Labbe-Bois R (1986) Negative control of yeast coproporphyrinogen oxidase synthesis by heme and oxygen. J Biol Chem 261 : 2506 2509.
54. Zhang L Hach A (1999) Molecular mechanism of heme signalling in yeast: the transcriptional activator Hap1 serves as the key mediator. Cell Mol Life Sci 56 : 415 426.
55. Zitomer RS Hall BD (1976) Yeast cytochrome c messenger RNA. In vitro translation and specific immunoprecipitation of the CYC1 gene product. J Biol Chem 251 : 6320 6326.
56. Zitomer RS Lowry CV (1992) Regulation of gene expression by oxygen in Saccharomyces cerevisiae. Microbiol Rev 56 : 1 11.