Different requirements of the SWI/SNF complex for robust nucleosome displacement at promoters of heat shock factor and Msn2- and Msn4-regulated heat shock genes

Molecular and Cellular Biology

Volumn 28, Issue 4, 2008, Pages 1207-1217

  Erkina, Tamara Y ^a   Tschetter, Paul A ^a   Erkine, Alexandre M ^a  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; HEAT SHOCK PROTEIN; HISTONE; PROTEIN; PROTEIN MSN2; PROTEIN MSN4; PROTEIN SWI; RNA POLYMERASE II; TRANSCRIPTION FACTOR SNF; UNCLASSIFIED DRUG;

ARTICLE; GENE; GENE DELETION; HEAT SHOCK; HPS82 GENE; HSP12 GENE; MSN2 GENE; MSN4 GENE; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; SSA4 GENE;

CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA-BINDING PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; KINETICS; NUCLEOSOMES; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 38949161446     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01069-07     Document Type: Article

References (65)

1. Adkins, M. W., and J. K. Tyler. 2006. Transcriptional activators are dispensable for transcription in the absence of Spt6-mediated chromatin reassembly of promoter regions. Mol. Cell 21:405-416.
2. Amin, J., J. Ananthan, and R. Voellmy. 1988. Key features of heat shock regulatory elements. Mol. Cell. Biol. 8:3761-3769.
3. Amoros, M., and F. Estruch. 2001. Hsf1p and Msn2/4p cooperate in the expression of Saccharomyces cerevisiae genes HSP26 and HSP104 in a gene-and stress type-dependent manner. Mol. Microbiol. 39:1523-1532.
4. Becker, P. B., and W. Horz. 2002. ATP-dependent nucleosome remodeling. Annu. Rev. Biochem. 71:247-273.
5. Boorstein, W. R., and E. A. Craig. 1990. Structure and regulation of the SSA4 HSP70 gene of Saccharomyces cerevisiae. J. Biol. Chem. 265:18912-18921.
6. Bose, S., J. A. Dutko, and R. S. Zitomer. 2005. Genetic factors that regulate the attenuation of the general stress response of yeast. Genetics 169:1215-1226.
7. Boy-Marcotte, E., G. Lagniel, M. Perrot, F. Bussereau, A. Boudsocq, M. Jacquet, and J. Labarre. 1999. The heat shock response in yeast: differential regulations and contributions of the Msn2p/Msn4p and Hsf1p regulons. Mol. Microbiol. 33:274-283.
8. Cairns, B. R., Y. J. Kim, M. H. Sayre, B. C. Laurent, and R. D. Romberg. 1994. A multisubunit complex containing the SWI1/ADR6, SWI2/SNF2, SWI3, SNF5, and SNF6 gene products isolated from yeast. Proc. Natl. Acad. Sci. USA 91:1950-1954.
9. Chi, Y., M. J. Huddleston, X. Zhang, R. A. Young, R. S. Annan, S. A. Carr, and R. J. Deshaies. 2001. Negative regulation of Gcn4 and Msn2 transcription factors by Srb10 cyclin-dependent kinase. Genes Dev. 15:1078-1092.
10. Collins, G. A., and W. P. Tansey. 2006. The proteasome: a utility tool for transcription? Curr. Opin. Genet. Dev. 16:197-202.
11. Cote, J., J. Quinn, J. L. Workman, and C. L. Peterson. 1994. Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. Science 265:53-60.
12. Dhasarathy, A., and M. P. Kladde. 2005. Promoter occupancy is a major determinant of chromatin remodeling enzyme requirements. Mol. Cell. Biol. 25:2698-2707.
13. Dobi, K. C., and F. Winston. 2007. Analysis of transcriptional activation at a distance in Saccharomyces cerevisiae. Mol. Cell. Biol. 27:5575-5586.
14. Erkina, T. Y., and A. M. Erkine. 2006. Displacement of histones at promoters of Saccharomyces cerevisiae heat shock genes is differentially associated with histone H3 acetylation. Mol. Cell. Biol. 26:7587-7600.
15. Erkine, A. M., C. C. Adams, T. Diken, and D. S. Gross. 1996. Heat shock factor gains access to the yeast HSC82 promoter independently of other sequence-specific factors and antagonizes nucleosomal repression of basal and induced transcription. Mol. Cell. Biol. 16:7004-7017.
16. Erkine, A. M., and D. S. Gross. 2003. Dynamic chromatin alterations triggered by natural and synthetic activation domains. J. Biol. Chem. 278:7755-7764.
17. Erkine, A. M., S. F. Magrogan, E. A. Sekinger, and D. S. Gross. 1999. Cooperative binding of heat shock factor to the yeast HSP82 promoter in vivo and in vitro. Mol. Cell. Biol. 19:1627-1639.
18. Erkine, A. M., C. Sient-Gyorgyi, S. F. Simmons, and D. S. Gross. 1995. The upstream sequences of the HSP82 and HSC82 genes of Saccharomyces cerevisiae: regulatory elements and nucleosome positioning motifs. Yeast 11:573-580.
19. Estruch, F. 2000. Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol. Rev. 24:469-486.
20. Gangaraju, V. K., and B. Bartholomew. 2007. Mechanisms of ATP dependent chromatin remodeling. Mutat. Res. 618:3-17.
21. Carreau, H., R. N. Hasan, G. Renault, F. Estruch, E. Boy-Marcotte, and M. Jacquet. 2000. Hyperphosphorylation of Msn2p and Msn4p in response to heat shock and the diauxic shift is inhibited by cAMP in Saccharomyces cerevisiae. Microbiology 146:2113-2120.
22. Gasch, A. P., P. T. Spellman, C. M. Kao, O. Carmel-Harel, M. B. Eisen, G. Storz, D. Botstein, and P. O. Brown. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11:4241-4257.
23. Giardina, C., and J. T. Lis. 1995. Dynamic protein-DNA architecture of a yeast heat shock promoter. Mol. Cell. Biol. 15:2737-2744.
24. Gorner, W., E. Durchschlag, M. T. Martinez-Pastor, F. Estruch, G. Ammerer, B. Hamilton, H. Ruis, and C. Schuller. 1998. Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev. 12:586-597.
25. Gorner, W., E. Durchschlag, J. Wolf, E. L. Brown, G. Ammerer, H. Ruis, and C. Schuller. 2002. Acute glucose starvation activates the nuclear localization signal of a stress-specific yeast transcription factor. EMBO J. 21:135-144.
26. Gross, D. S., K. E. English, K. W. Collins, and S. W. Lee. 1990. Genomic footprinting of the yeast HSP82 promoter reveals marked distortion of the DNA helix and constitutive occupancy of heat shock and TATA elements. J. Mol. Biol. 216:611-631.
27. Guidener, U., S. Heck, T. Fielder, J. Beinhauer, and J. H. Hegemann. 1996. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 24:2519-2524.
28. Gutierrez, J. L., M. Chandy, M. J. Carrozza, and J. L. Workman. 2007. Activation domains drive nucleosome eviction by SWI/SNF. EMBO J. 26:730-740.
29. Hahn, J. S., Z. Hu, D. J. Thiele, and V. R. Iyer. 2004. Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol. Cell. Biol. 24:5249-5256.
30. Hashikawa, N., and H. Sakurai. 2004. Phosphorylation of the yeast heat shock transcription factor is implicated in gene-specific activation dependent on the architecture of the heat shock element. Mol. Cell. Biol. 24:3648-3659.
31. Hoj, A., and B. K. Jakobsen. 1994. A short element required for turning off heat shock transcription factor: evidence that phosphorylation enhances deactivation. EMBO J. 13:2617-2624.
32. Jacquet, M., G. Renault, S. Lallet, J. De Mey, and A. Goldbeter. 2003. Oscillatory nucleocytoplasmic shuttling of the general stress response transcriptional activators Msn2 and Msn4 in Saccharomyces cerevisiae. J. Cell Biol. 161:497-505.
33. Jakobsen, B. K., and H. R. Pelham. 1988. Constitutive binding of yeast heat shock factor to DNA in vivo. Mol. Cell. Biol. 8:5040-5042.
34. Kristjuhan, A., and J. Q. Svejstrup. 2004. Evidence for distinct mechanisms facilitating transcript elongation through chromatin in vivo. EMBO J. 23:4243-4252.
35. Kundu, S., P. J. Horn, and C. L. Peterson. 2007. SWI/SNF is required for transcriptional memory at the yeast GAL gene cluster. Genes Dev. 21:997-1004.
36. Kwon, H., A. N. Imbalzano, P. A. Khavari, R. E. Kingston, and M. R. Green. 1994. Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex. Nature 370:477-481.
37. Lallet, S., H. Garreau, C. Garmendia-Torres, D. Szestakowska, E. Boy-Marcotte, S. Quevillon-Cheruel, and M. Jacquet. 2006. Role of Gal11, a component of the RNA polymerase II mediator in stress-induced hyperphosphorylation of Msn2 in Saccharomyces cerevisiae. Mol. Microbiol. 62:438-452.
38. Lallet, S., H. Garreau, C. Poisier, E. Boy-Marcotte, and M. Jacquet. 2004. Heat shock-induced degradation of Msn2p, a Saccharomyces cerevisiae transcription factor, occurs in the nucleus. Mol. Genet. Genomics 272:353-362.
39. Lee, C. K., Y. Shibata, B. Rao, B. D. Strahl, and J. D. Lieb. 2004. Evidence for nucleosome depletion at active regulatory regions genome-wide. Nat. Genet. 36:900-905.
40. Lee, K. K., P. Prochasson, L. Florens, S. K. Swanson, M. P. Washburn, and J. L. Workman. 2004. Proteomic analysis of chromatin-modifying complexes in Saccharomyces cerevisiae identifies novel subunits. Biochem. Soc. Trans. 32:899-903.
41. Lindstrom, K. C., J. C. Vary, Jr., M. R. Parthun, J. Delrow, and T. Tsukiyama. 2006. Isw1 functions in parallel with the NuA4 and Swr1 complexes in stress-induced gene repression. Mol. Cell. Biol. 26:6117-6129.
42. Martens, J. A., and F. Winston. 2003. Recent advances in understanding chromatin remodeling by Swi/Snf complexes. Curr. Opin. Genet. Dev. 13:136-142.
43. Martens, J. A., P. Y. Wu, and F. Winston. 2005. Regulation of an intergenic transcript controls adjacent gene transcription in Saccharomyces cerevisiae. Genes Dev. 19:2695-2704.
44. Martinez-Pastor, M. T., G. Marchler, C. Schuller, A. Marchler-Bauer, H. Ruis, and F. Estruch. 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.
45. Morimoto, R. I. 1998. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12:3788-3796.
46. Moskvina, E., C. Schuller, C. T. Maurer, W. H. Mager, and H. Ruis. 1998. A search in the genome of Saccharomyces cerevisiae for genes regulated via stress response elements. Yeast 14:1041-1050.
47. Owen-Hughes, T., and J. L. Workman. 1996. Remodeling the chromatin structure of a nucleosome array by transcription factor-targeted trans-displacement of histones. EMBO J. 15:4702-4712.
48. Perisic, O., H. Xiao, and J. T. Lis. 1989. Stable binding of Drosophila heat shock factor to head-to-head and tail-to-tail repeats of a conserved 5 bp recognition unit. Cell 59:797-806.
49. Ramos, P. C., J. Hockendorff, E. S. Johnson, A. Varshavsky, and R. J. Dohmen. 1998. Ump1p is required for proper maturation of the 20S proteasome and becomes its substrate upon completion of the assembly. Cell 92:489-499.
50. Santoro, N., N. Johansson, and D. J. Thiele. 1998. Heat shock element architecture is an important determinant in the temperature and transactivation domain requirements for heat shock transcription factor. Mol. Cell. Biol. 18:6340-6352.
51. Singh, H., A. M. Erkine, S. B. Kremer, H. M. Duttweiler, D. A. Davis, J. Iqbal, R. R. Gross, and D. S. Gross. 2006. A functional module of yeast mediator that governs the dynamic range of heat-shock gene expression. Genetics 172:2169-2184.
52. Smith, C. L., R. Horowitz-Scherer, J. F. Flanagan, C. L. Woodcock, and C. L. Peterson. 2003. Structural analysis of the yeast SWI/SNF chromatin remodeling complex. Nat. Struct. Biol 10:141-145.
53. Sorger, P. K., M. J. Lewis, and H. R. Pelham. 1987. Heat shock factor is regulated differently in yeast and HeLa cells. Nature 329:81-84.
54. Sorger, P. K., and H. R. Pelham. 1988. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 54:855-864.
55. Tansey, W. P. 2001. Transcriptional activation: risky business. Genes Dev. 15:1045-1050.
56. Taylor, I. C., J. L. Workman, T. J. Schuetz, and R. E. Kingston. 1991. Facilitated binding of GAL4 and heat shock factor to nucleosomal templates: differential function of DNA-binding domains. Genes Dev. 5:1285-1298.
57. Treger, J. M., A. P. Schmitt, J. R. Simon, and K. McEntee. 1998. Transcriptional factor mutations reveal regulatory complexities of heat shock and newly identified stress genes in Saccharomyces cerevisiae. J. Biol. Chem. 273:26875-26879.
58. Uffenbeck, S. R., and J. E. Krebs. 2006. The role of chromatin structure in regulating stress-induced transcription in Saccharomyces cerevisiae. Biochem. Cell Biol. 84:477-489.
59. Utley, R. T., J. Cote, T. Owen-Hughes, and J. L. Workman. 1997. SWI/SNF stimulates the formation of disparate activator-nucleosome complexes but is partially redundant with cooperative binding. J. Biol. Chem. 272:12642-12649.
60. Voellmy, R. 2004. On mechanisms that control heat shock transcription factor activity in metazoan cells. Cell Stress Chaperones 9:122-133.
61. Wu, C. 1995. Heat shock transcription factors: structure and regulation. Annu. Rev. Cell Dev. Biol. 11:441-469.
62. Xiao, H., and J. T. Lis. 1988. Germline transformation used to define key features of heat-shock response elements. Science 239:1139-1142.
63. Xiao, H., O. Perisic, and J. T. Lis. 1991. Cooperative binding of Drosophila heat shock factor to arrays of a conserved 5 bp unit. Cell 64:585-593.
64. Yamamoto, A., Y. Mizukami, and H. Sakurai. 2005. Identification of a novel class of target genes and a novel type of binding sequence of heat shock transcription factor in Saccharomyces cerevisiae. J. Biol. Chem. 280:11911-11919.
65. Zhao, J., J. Herrera-Diaz, and D. S. Gross. 2005. Domain-wide displacement of histones by activated heat shock factor occurs independently of Swi/Snf and is not correlated with RNA polymerase II density. Mol. Cell. Biol. 25:8985-8999.