Genome-wide Analysis Reveals New Roles for the Activation Domains of the Saccharomyces Cerevisiae Heat Shock Transcription Factor (Hsf1) During the Transient Heat Shock Response

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2006 Aug 24

PMID 16926161

Citations 41

Authors

Dawn L Eastmond

Hillary C M Nelson

Affiliations

Soon will be listed here.

Abstract

In response to elevated temperatures, cells from many organisms rapidly transcribe a number of mRNAs. In Saccharomyces cerevisiae, this protective response involves two regulatory systems: the heat shock transcription factor (Hsf1) and the Msn2 and Msn4 (Msn2/4) transcription factors. Both systems modulate the induction of specific heat shock genes. However, the contribution of Hsf1, independent of Msn2/4, is only beginning to emerge. To address this question, we constructed an msn2/4 double mutant and used microarrays to elucidate the genome-wide expression program of Hsf1. The data showed that 7.6% of the genome was heat-induced. The up-regulated genes belong to a wide range of functional categories, with a significant increase in the chaperone and metabolism genes. We then focused on the contribution of the activation domains of Hsf1 to the expression profile and extended our analysis to include msn2/4Delta strains deleted for the N-terminal or C-terminal activation domain of Hsf1. Cluster analysis of the heat-induced genes revealed activation domain-specific patterns of expression, with each cluster also showing distinct preferences for functional categories. Computational analysis of the promoters of the induced genes affected by the loss of an activation domain showed a distinct preference for positioning and topology of the Hsf1 binding site. This study provides insight into the important role that both activation domains play for the Hsf1 regulatory system to rapidly and effectively transcribe its regulon in response to heat shock.

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References

Estruch F . Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev. 2000; 24(4):469-86. DOI: 10.1111/j.1574-6976.2000.tb00551.x. View

Mai B, Breeden L . Xbp1, a stress-induced transcriptional repressor of the Saccharomyces cerevisiae Swi4/Mbp1 family. Mol Cell Biol. 1997; 17(11):6491-501. PMC: 232502. DOI: 10.1128/MCB.17.11.6491. View

Hahn J, Hu Z, Thiele D, Iyer V . Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol Cell Biol. 2004; 24(12):5249-56. PMC: 419887. DOI: 10.1128/MCB.24.12.5249-5256.2004. View

Heyer L, Kruglyak S, Yooseph S . Exploring expression data: identification and analysis of coexpressed genes. Genome Res. 1999; 9(11):1106-15. PMC: 310826. DOI: 10.1101/gr.9.11.1106. View

Bonner J, Heyward S, Fackenthal D . Temperature-dependent regulation of a heterologous transcriptional activation domain fused to yeast heat shock transcription factor. Mol Cell Biol. 1992; 12(3):1021-30. PMC: 369534. DOI: 10.1128/mcb.12.3.1021-1030.1992. View

Rowley A, Johnston G, Butler B, Werner-Washburne M, Singer R . Heat shock-mediated cell cycle blockage and G1 cyclin expression in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1993; 13(2):1034-41. PMC: 358988. DOI: 10.1128/mcb.13.2.1034-1041.1993. View

Tachibana T, Astumi S, Shioda R, Ueno M, Uritani M, Ushimaru T . A novel non-conventional heat shock element regulates expression of MDJ1 encoding a DnaJ homolog in Saccharomyces cerevisiae. J Biol Chem. 2002; 277(25):22140-6. DOI: 10.1074/jbc.M201267200. View

Wiederrecht G, Seto D, Parker C . Isolation of the gene encoding the S. cerevisiae heat shock transcription factor. Cell. 1988; 54(6):841-53. DOI: 10.1016/s0092-8674(88)91197-x. View

Hahn J, Thiele D . Activation of the Saccharomyces cerevisiae heat shock transcription factor under glucose starvation conditions by Snf1 protein kinase. J Biol Chem. 2003; 279(7):5169-76. DOI: 10.1074/jbc.M311005200. View

10.

Jedlicka P, Mortin M, Wu C . Multiple functions of Drosophila heat shock transcription factor in vivo. EMBO J. 1997; 16(9):2452-62. PMC: 1169845. DOI: 10.1093/emboj/16.9.2452. View

11.

Gallo G, Prentice H, Kingston R . Heat shock factor is required for growth at normal temperatures in the fission yeast Schizosaccharomyces pombe. Mol Cell Biol. 1993; 13(2):749-61. PMC: 358957. DOI: 10.1128/mcb.13.2.749-761.1993. View

12.

Lee T, Rinaldi N, Robert F, Odom D, Bar-Joseph Z, Gerber G . Transcriptional regulatory networks in Saccharomyces cerevisiae. Science. 2002; 298(5594):799-804. DOI: 10.1126/science.1075090. View

13.

Travers K, Patil C, Wodicka L, Lockhart D, Weissman J, Walter P . Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell. 2000; 101(3):249-58. DOI: 10.1016/s0092-8674(00)80835-1. View

14.

Peteranderl R, NELSON H . Trimerization of the heat shock transcription factor by a triple-stranded alpha-helical coiled-coil. Biochemistry. 1992; 31(48):12272-6. DOI: 10.1021/bi00163a042. View

15.

Sakurai H, Hashikawa N, Imazu H, Fukasawa T . Carboxy-terminal region of the yeast heat shock factor contains two domains that make transcription independent of the TFIIH protein kinase. Genes Cells. 2004; 8(12):951-61. DOI: 10.1046/j.1356-9597.2003.00689.x. View

16.

Bulman A, HUBL S, NELSON H . The DNA-binding domain of yeast heat shock transcription factor independently regulates both the N- and C-terminal activation domains. J Biol Chem. 2001; 276(43):40254-62. DOI: 10.1074/jbc.M106301200. View

17.

Sakurai H, Fukasawa T . A novel domain of the yeast heat shock factor that regulates its activation function. Biochem Biophys Res Commun. 2001; 285(3):696-701. DOI: 10.1006/bbrc.2001.5234. View

18.

Pirkkala L, Nykanen P, Sistonen L . Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J. 2001; 15(7):1118-31. DOI: 10.1096/fj00-0294rev. View

19.

Morimoto R, Kline M, Bimston D, Cotto J . The heat-shock response: regulation and function of heat-shock proteins and molecular chaperones. Essays Biochem. 1997; 32:17-29. View

20.

Gorner W, Durchschlag E, Estruch F, Ammerer G, Hamilton B, Ruis H . Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev. 1998; 12(4):586-97. PMC: 316529. DOI: 10.1101/gad.12.4.586. View