Zinc starvation induces a stress response in Saccharomyces cerevisiae that is mediated by the Msn2p and Msn4p transcriptional activators

FEMS Yeast Research

Volumn 9, Issue 8, 2009, Pages 1187-1195

  Gauci, Victoria J ^a   Beckhouse, Anthony G ^b   Lyons, Victoria ^a   Beh, Eric J ^a   Rogers, Peter J ^c   Dawes, Ian W ^d   Higgins, Vincent J ^a  

^a UNIVERSITY OF WESTERN SYDNEY   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

^c Carlton and United Breweries   (Australia)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Fermentation; Msn2 4p; Saccharomyces cerevisiae; Zap1p; Zinc

Indexed keywords

BETA GALACTOSIDASE; ZINC;

AMINO ACID SEQUENCE; ARTICLE; FERMENTATION; FUNGAL GENE; GENE DELETION; GENE EXPRESSION; GENOME; MSN2 GENE; MSN4 GENE; NONHUMAN; PROMOTER REGION; PROTEIN ANALYSIS; SACCHAROMYCES CEREVISIAE; STRESS; ZINC DEFICIENCY;

BETA-GALACTOSIDASE; BINDING SITES; DNA, FUNGAL; DNA-BINDING PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; GENES, REPORTER; PROMOTER REGIONS, GENETIC; REGULON; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; ZINC;

SACCHAROMYCES CEREVISIAE;

EID: 70350538685     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2009.00557.x     Document Type: Article

References (48)

1. Alic N, Felder T, Temple MD, Gloeckner C, Higgins VJ, Briza P Dawes IW (2004) Genome-wide transcriptional responses to a lipid hydroperoxide: adaptation occurs without induction of oxidant defenses. Free Radical Bio Med 37 : 23 35.
2. Auld DS (2001) Zinc coordination sphere in biochemical zinc sites. Biometals 14 : 271 313.
3. Beckhouse AG, Grant CM, Rogers PJ, Dawes IW Higgins VJ (2008) The adaptive response of anaerobically grown Saccharomyces cerevisiae to hydrogen peroxide is mediated by the Yap1 and Skn7 transcription factors. FEMS Yeast Res 8 : 1214 1222.
4. Bilsland E, Molin C, Swaminathan S, Ramne A Sunnerhagen P (2004) Rck1 and Rck2 MAPKAP kinases and the HOG pathway are required for oxidative stress resistance. Mol Microbiol 53 : 1743 1756.
5. Bissinger PH, Wieser R, Hamilton B Ruis H (1989) Control of Saccharomyces cerevisiae catalase T gene (CTT1) expression by nutrient supply via RAS-Cyclic AMP pathway. Mol Cell Biol 9 : 1309 1315.
6. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72 : 248 254.
7. Bromberg SK, Bower PA, Duncombe GR, Fehring J, Gerber L, Lau VK Tata M (1997) Requirements for zinc, manganese, calcium, and magnesium in wort. J Am Soc Brew Chem 55 : 123 128.
8. Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, Jennings EG, Lee TI, Tru HL, Lander ES Lander RA (2001) Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12 : 323 337.
9. Del Vescovo V, Casagrande V, Bianchi MM et al 2008) Role of Hog1 and Yaf9 in the transcriptional response of Saccharomyces cerevisiae to cesium chloride. Physiol Genomics 33 : 110 120.
10. De Nicola R, Hazelwood LA, De Hulster EAF, Walsh MC, Knijnenburg TA, Reinders MJT, Walker GM, Pronk JT, Daran JM Daran-Lapujade P (2007) Physiological and transcriptional responses of Saccharomyces cerevisiae to zinc limitation in chemostat cultures. Appl Environ Microb 73 : 7680 7692.
11. Domitrovic T, Fernandes CM, Boy-Marcotte E Kurtenbach E (2006) High hydrostatic pressure activates gene expression through Msn2/4 stress transcription factors which are involved in the acquired tolerance by mild pressure precondition in Saccharomyces cerevisiae. FEBS Lett 580 : 6033 6038.
12. Eide D Guarente L (1992) Increased dosage of a transcriptional activator gene enhances iron-limited growth of Saccharomyces cerevisiae. J Gen Microbiol 138 : 347 354.
13. Francis SH, Colbran JL, McAllister-Lucas LM Corbin JD (1994) Zinc interactions and conserved motifs of the cGMP-binding cGMP-specific phosphodiesterase suggest that it is a zinc hydrolase. J Biol Chem 269 : 22477 22480.
14. Garmendia-Torres C, Goldbeter A Jacquet M (2007) Nucleocytoplasmic oscillations of the yeast transcription factor Msn2: evidence for periodic PKA activation. Curr Biol 17 : 1044 1049.
15. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11 : 4241 4257.
16. 2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Gene Dev 12 : 586 597.
17. Hahn JS Thiele DJ (2004) Activation of the Saccharomyces cerevisiae heat shock transcription factor under glucose starvation conditions by Snf1 protein kinase. J Biol Chem 279 : 5169 5176.
18. 2 response by the Msn2/4 transcription factors. Mol Microbiol 45 : 233 241.
19. Higgins VJ, Rogers PJ Dawes IW (2003) Application of genome-wide expression analysis to identify molecular markers useful in monitoring industrial fermentations. Appl Environ Microb 69 : 7535 7540.
20. Jacquet M, Renault G, Lallet S, De Mey J Goldbeter A (2003) Oscillatory nucleocytoplasmic shuttling of the general stress response transcriptional activators Msn2 and Msn4 in Saccharomyces cerevisiae. J Cell Biol 161 : 497 505.
21. Kaida D, Yashiroda H, Toh-e A Kikuchi Y (2002) Yeast Whi2 and Psr1-phosphatase form a complex and regulate STRE-mediated gene expression. Genes Cells 7 : 543 552.
22. Kenbaev B Sade B (2002) Response of field-grown barley cultivars grown on zinc-deficient soil to zinc application. Commun Soil Sci Plan 33 : 533 544.
23. Kobayashi N McEntee K (1993) Identification of cis and trans components of a novel heat shock stress regulatory pathway in Saccharomyces cerevisiae. Mol Cell Biol 13 : 248 256.
24. Lawrence CL, Botting CH, Antrobus R Coote PJ (2004) Evidence of a new role for the high-osmolarity glycerol mitogen-activated protein kinase pathway in yeast: regulating adaptation to citric acid. Mol Cell Biol 24 : 3307 3323.
25. Lenssen E, James N, Pedruzzi I et al 2005) The Ccr4-Not complex independently controls both Msn2-dependent transcriptional activation - via a newly identified Glc7/Bud14 type I protein phosphatase module - and TFIID promoter distribution. Mol Cell Biol 25 : 488 498.
26. Lyons TJ, Gasch AP, Gaither LA, Botstein D, Brown PO Eide DJ (2000) Genome-wide characterization of the Zap1p zinc-responsive regulon in yeast. P Natl Acad Sci USA 97 : 7957 7962.
27. Magonet E, Hayen P, Delforge D, Delaive E Remacle J (1992) Importance of the structural zinc atom for the stability of yeast alcohol dehydrogenase. Biochem J 287 : 361 365.
28. Marchler G, Schüller C, Adam G Ruis H (1993) A Saccharomyces cerevisiae UAS element controlled by protein kinase A activates transcription in response to a variety of stress conditions. EMBO J 12 : 1997 2003.
29. Martínez-Pastor MT, Marchler G, Schüller C, Marchler-Bauer A, Ruis H Estruch F (1996) The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress-response element (STRE). EMBO J 15 : 2227 2235.
30. Montgomery DC (2001) Design and Analysis of Experiments, pp. 96 99. Wiley, New York.
31. Ohtsu H Fukuzumi S (2001) Coordination of semiquinone and superoxide radical anions to the zinc ion in SOD model complexes that act as the key step in disproportionation of the radical anions. Chem Eur J 7 : 4947 4953.
32. Ohtsu H, Shimazaki Y, Odani A, Yamauchi O, Mori W, Itoh S Fukuzumi S (2000) Synthesis and characterization of imidazolate-bridged dinuclear complexes as active site models of Cu,Zn-SOD. J Am Chem Soc 122 : 5733 5741.
33. Rees EMR Stewart GG (1998) Strain specific response of Brewer's yeast strains to zinc concentrations in conventional and high gravity worts. J Inst Brew 104 : 221 228.
34. Rep M, Krantz M, Thevelein JM Hohmann S (2000) The transcriptional response of Saccharomyces cerevisiae to osmotic shock. Hot1p and Msn2p/Msn4p are required for the induction of subsets of high osmolarity glycerol pathway-dependent genes. J Biol Chem 275 : 8290 8300.
35. Rose M Botstein A (1983) Construction and use of gene fusions to lacZ (beta-galactosidase) that are expressed in yeast. Method Enzymol 101 : 167 180.
36. Schüller C, Brewster JL, Alexander MR, Gustin MC Ruis H (1994) The HOG pathway controls osmotic regulation of transcription via the stress response element (STRE) of the Saccharomyces cerevisiae CTT1 gene. EMBO J 13 : 4382 4389.
37. Schüller C, Mamnun YM, Mollapour M, Krapf G, Schuster M, Bauer BE, Piper PW Kuchler K (2004) Global phenotypic analysis and transcriptional profiling defines the weak acid response regulon in Saccharomyces cerevisiae. Mol Biol Cell 15 : 706 720.
38. Smith A, Ward MP Garrett S (1998) Yeast PKA represses Msn2p/Msn4p-dependent gene expression to regulate growth, stress response and glycogen accumulation. EMBO J 17 : 3556 3564.
39. Stehlik-Tomas V, Zetic VG, Stanzer D, Grba S Vahcic N (1994) Zinc, copper and manganese enrichment in yeast Saccharomyces cerevisiae. Food Technol Biotech 42 : 115 120.
40. Thorsen M, Di Y, Tängemo C et al 2006) The MAPK Hog1p modulates Fps1p-dependent arsenite uptake and tolerance in yeast. Mol Biol Cell 17 : 4400 4410.
41. Truong-Tran AQ, Carter J, Ruffin RE Zalewski PD (2001) The role of zinc in caspase activation and apoptotic cell death. Biometals 14 : 315 330.
42. Van Helden J, Andre B Collado-Vides J (1998) Extracting regulatory sites from the upstream region of yeast genes by computational analysis of oligonucleotide frequencies. J Mol Biol 281 : 827 842.
43. Vecseri-Hegyes B, Fodor P Hoschke À (2005) The role of zinc in beer production, I. Wort production. Acta Aliment Hung 34 : 17 24.
44. Vecseri-Hegyes B, Fodor P Hoschke À (2006) The role of zinc in beer production, II. Fermentation. Acta Aliment Hung 35 : 373 380.
45. Winkler A, Arkind C, Mattison CP, Burkholder A, Knoche K Ota I (2002) Heat stress activates the yeast high-osmolarity glycerol mitogen-activated protein kinase pathway, and protein tyrosine phosphatases are essential under heat stress. Eukaryot Cell 1 : 163 173.
46. Wu CY, Bird AJ, Chung LM, Newton MA, Winge DR Eide DJ (2008) Differential control of Zap1-regulated genes in response to zinc deficiency in Saccharomyces cerevisiae. BMC Genomics 9 : 370.
47. Zhao H Eide D (1997) Zap1p, a metalloregulatory protein involved in zinc-responsive transcriptional regulation in Saccharomyces cerevisiae. Mol Cell Biol 17 : 5044 5052.
48. Zhao H, Butler E, Rodgers J, Spizzo T, Duesterhoeff S Eide D (1998) Regulation of zinc homeostasis in yeast by binding of the ZAP1 transcriptional activator to zinc-responsive promoter elements. J Biol Chem 273 : 28713 28720.