Phosphorylation of the Yeast Heat Shock Transcription Factor Is Implicated in Gene-Specific Activation Dependent on the Architecture of the Heat Shock Element

Molecular and Cellular Biology

Volumn 24, Issue 9, 2004, Pages 3648-3659

  Hashikawa, Naoya ^a   Sakurai, Hiroshi ^a  

^a KANAZAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN;

ARTICLE; C TERMINAL MODULATOR; CONTROLLED STUDY; GENE ACTIVATION; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; STRESS; TRANSCRIPTION INITIATION; YEAST;

AMINO ACID SEQUENCE; DNA-BINDING PROTEINS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORYLATION; REGULATORY SEQUENCES, NUCLEIC ACID; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 1942518714     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.9.3648-3659.2004     Document Type: Article

References (64)

1. Ahn, S.-G., and D. J. Thiele. 2003. Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev. 17:516-528.
2. Ahn, S.-G., P. C. Liu, K. Klyachko, R. I. Morimoto, and D. J. Thiele. 2001. The loop domain of heat shock transcription factor 1 dictates DNA-binding specificity and responses to heat stress. Genes Dev. 15:2134-2145.
3. Amin, J., J. Ananthan, and R. Voellmy. 1988. Key features of heat shock regulatory elements. Mol. Cell. Biol. 8:3761-3769.
4. Boeke J. D., F. LaCroute, and G. R. Fink. 1983. A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197:345-346.
5. Bonner, J. J., S. Heyward, and D. L. Fackenthal. 1992. Temperature-dependent regulation of a heterologous transcriptional activation domain fused to yeast heat shock transcription factor. Mol. Cell. Biol. 12:1021-1030.
6. Bonner, J. J., T. Carlson, D. L. Fackenthal, D. Paddock, K. Storey, and K. Lea. 2000. Complex regulation of the yeast heat shock transcription factor. Mol. Biol. Cell 11:1739-1751.
7. 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.
8. Bulman, A. L., S. T. Hubl, and H. C. M. Nelson. 2001. The DNA-binding domain of yeast heat shock transcription factor independently regulates both the N- and C-terminal activation domains. J. Biol. Chem. 276:40254-40262.
9. Chen, T., and C. S. Parker. 2002. Dynamic association of transcriptional activation domains and regulatory regions in Saccharomyces cerevisiae heat shock factor. Proc. Natl. Acad. Sci. USA 99:1200-1205.
10. Chen, Y., N. A. Barlev, O. Westergaard, and B. K. Jakobsen. 1993. Identification of the C-terminal activator domain in yeast heat shock factor: independent control of transient and sustained transcriptional activity. EMBO J. 12:5007-5018.
11. Chu, B., F. Soncin, B. D. Price, M. A. Stevenson, and S. K. Calderwood. 1996. Sequential phosphorylation by mitogen-activated protein kinase and glycogen synthase kinase 3 represses transcriptional activation by heat shock factor-1. J. Biol. Chem. 271:30847-30857.
12. Chu, B., R. Zhong, F. Soncin, M. A. Stevenson, and S. K. Calderwood. 1998. Transcriptional activity of heat shock factor 1 at 37°C is repressed through phosphorylation on two distinct serine residues by glycogen synthase kinase 3 and protein kinases Cα and Cζ. J. Biol. Chem. 273:18640-18646.
13. Cotto, J. J., M. Kline, and R. I. Morimoto. 1996. Activation of heat shock factor 1 DNA binding precedes stress-induced serine phosphorylation: evidence for a multistep pathway of regulation. J. Biol. Chem. 271:3355-3358.
14. Dai, R., W. Frejtag, B. He, Y. Zhang, and N. F. Mivechi. 2000. c-Jun NH2-terminal kinase targeting and phosphorylation of heat shock factor-1 suppress its transcriptional activity. J. Biol. Chem. 275:18210-18218.
15. Drees, B. L., E. K. Grotkop, and H. C. M. Nelson. 1997. The GCN4 leucine zipper can functionally substitute for the heat shock transcription factor's trimerization domain. J. Mol. Biol. 273:61-74.
16. 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.
17. Feder, M. E., and G. E. Hofmann. 1999. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61:243-282.
18. Flick, K. E., L Gonzalez, Jr., C. J. Harrison, and H. C. Nelson. 1994. Yeast heat shock transcription factor contains a flexible linker between the DNA-binding and trimerization domains: implications for DNA binding by trimeric proteins. J. Biol. Chem. 269:12475-12481.
19. Gallo, G. J., H. Prentice, and R. E. Kingston. 1993. Heat shock factor is required for growth at normal temperatures in the fission yeast Schizosaccharomyces pombe. Mol. Cell. Biol. 13:749-761.
20. Giardina, C., and J. T. Lis. 1995. Dynamic protein-DNA architecture of a yeast heat shock promoter. Mol. Cell. Biol. 15:2737-2744.
21. 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.
22. He, B., Y.-H. Meng, and N. H. Mivechi. 1998. Glycogen synthase kinase 3β and extracellular signal-regulated protein kinase inactivate heat shock transcription factor 1 by facilitating the disappearance of transcriptionally active granules after heat shock. Mol. Cell. Biol. 18:6624-6633.
23. Høj, 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.
24. Holmberg, C. I., V. Hietakangas, A. Mikhailov, J. O. Rantanen, M. Kallio, A. Meinander, J. Hellman, N. Morrice, C. MacKintosh, R. I. Morimoto, J. E. Eriksson, and L. Sistonen. 2001. Phosphorylation of serine 230 promotes inducible transcriptional activity of heat shock factor 1. EMBO J. 20:3800-3810.
25. 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.
26. Jakobsen, B. K., and H. R. B. Pelham. 1991. A conserved heptapeptide restrains the activity of the yeast heat shock transcription factor. EMBO J. 10:369-376.
27. Kline, M. P., and R. I. Morimoto. 1997. Repression of the heat shock factor 1 transcriptional activation domain is modulated by constitutive phosphorylation. Mol. Cell. Biol. 17:2107-2115.
28. Knauf, U., E. M. Newton, J. Kyriakis, and R. E. Kingston. 1996. Repression of human heat shock factor 1 activity at control temperature by phosphorylation. Genes Dev. 10:2782-2793.
29. Kroeger, P. E., and R. I. Morimoto. 1994. Selection of new HSF1 and HSF2 DNA-binding sites reveals difference in trimer cooperativity. Mol. Cell. Biol. 14:7592-7603.
30. Lee, S., T. Carlson, N. Christian, K. Lea, J. Kedzie, J. P. Reilly, and J. J. Bonner. 2000. The yeast heat shock transcription factor changes conformation in response to superoxide and temperature. Mol. Biol. Cell 11:1753-1764.
31. Leung, D. W., E. Chen, and D. V. Goeddel. 1989. A method for random mutagenesis of a defined DNA segment using a modified polymerase chain reaction. Technique 1:11-15.
32. Littlefield, O., and H. C. Nelson. 1999. A new use for the 'wing' of the 'winged' helix-turn-helix motif in the HSF-DNA cocrystal. Nat. Struct. Biol. 6:464-470.
33. Liu, X.-D., and D. J. Thiele. 1996. Oxidative stress induces heat shock factor phosphorylation and HSF-dependent activation of yeast metallothionein gene transcription. Genes Dev. 10:592-603.
34. Liu, X.-D., P. C. C. Liu, N. Santoro, and D. J. Thiele. 1997. Conservation of a stress response: human heat shock transcription factors functionally substitute for yeast HSF. EMBO J. 16:6466-6477.
35. 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.
36. Nieto-Sotelo, J., G. Wiederrecht, A. Okuda, and C. S. Parker. 1990. The yeast heat shock transcription factor contains a transcriptional activation domain whose activity is repressed under nonshock conditions. Cell 62:807-817.
37. Pirkkala, L., P. Nykanen, and L. Sistonen. 2001. Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J. 15:1118-1131.
38. Sakurai, H., and T. Fukasawa. 1999. Activator-specific requirement for the general transcription factor IIE in yeast. Biochem. Biophys. Res. Commun. 261:734-739.
39. Sakurai, H., and T. Fukasawa. 2001. A novel domain of the yeast heat shock factor that regulates its activation function. Biochem. Biophys. Res. Commun. 285:696-701.
40. Sakurai, H., N. Hashikawa, H. Imazu, and T. Fukasawa. 2003. Carboxyterminal region of the yeast heat shock factor contains two domains that make transcription independent of the TFIIH protein kinase. Genes Cells 8:951-961.
41. Saltsman, K. A., H. L. Prentice, and R. E. Kingston. 1999. Mutations in the Schizosaccharomyces pombe heat shock factor that differentially affect responses to heat and cadmium stress. Mol. Gen. Genet. 261:161-169.
42. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
43. 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.
44. Sarge, K. D., S. P. Murphy, and R. I. Morimoto. 1993. Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress. Mol. Cell. Biol. 13:1392-1407. (Errata, 13:3122-3123 and 3838-3839.)
45. Sewell, A. K., F. Yokoya, W. Yu, T. Miyagawa, T. Murayama, and D. R. Winge. 1995. Mutated yeast heat shock transcription factor exhibits elevated basal transcriptional activation and confers metal resistance. J. Biol. Chem. 270:25079-25086.
46. Shi, Y., D. D. Mosser, and R. I. Morimoto. 1998. Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev. 12:654-666.
47. Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.
48. Silar, P., G. Butler, and D. J. Thiele. 1991. Heat shock transcription factor activates transcription of the yeast metallothionein gene. Mol. Cell. Biol. 11:1232-1238.
49. Sorger, P. K. 1990. Yeast heat shock factor contains separable transient and sustained response transcriptional activators. Cell 62:793-805.
50. 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.
51. Sorger, P. K., and H. C. M. Nelson. 1989. Trimerization of a yeast transcriptional activator via coiled-coil motif. Cell 59:807-814.
52. Sorger, P. K., and H. R. B. Pelham. 1988. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 54:855-864.
53. Tachibana, T., S. Astumi, R. Shioda, M. Ueno, M. Uritani, and T. Ushimaru. 2002. A novel non-conventional heat shock element regulates expression of MDJ1 encoding a DnaJ homolog in Saccharomyces cerevisiae. J. Biol. Chem. 277:22140-22146.
54. Tamai, K. T., X. Liu, P. Silar, T. Sosinowski, and D. J. Thiele. 1994. Heat shock transcription factor activates yeast metallothionein gene expression in response to heat and glucose starvation via distinct signalling pathways. Mol. Cell. Biol. 14:8155-8165.
55. Tanabe, M., N. Sasai, K. Nagata, X. D. Liu, P. C. C. Liu, D. J. Thiele, and A. Nakai. 1999. The mammalian HSF4 gene generates both an activator and a repressor of heat shock genes by alternative splicing. J. Biol. Chem. 274: 27845-27856.
56. Wei, R., H. Wilkinson, K. Pfeifer, C. Schneider, R. Young, and L. Guarente. 1986. Two or more copies of Drosophila heat shock consensus sequence serve to activate transcription in yeast. Nucleic Acids Res. 14:8183-8188.
57. Wiederrecht, G., D. Seto, and C. S. Parker. 1988. Isolation of the gene encoding the S. cerevisiae heat shock transcription factor. Cell 54:841-853.
58. Wu, C. 1995. Heat shock transcription factors: structure and regulation. Annu. Rev. Cell Dev. Biol. 11:441-469.
59. Xia, W., and R. Voellmy. 1997. Hyperphosphorylation of heat shock transcription factor 1 is correlated with transcriptional competence and slow dissociation of active factor trimers. J. Biol. Chem. 272:4094-4102.
60. 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.
61. Yang, W., W. Gahl, and D. Hamer. 1991. Role of heat shock transcription factor in yeast metallothionein gene expression. Mol. Cell. Biol. 11:3676-3681.
62. Young, M. R., and E. A. Craig. 1993. Saccharomyces cerevisiae HSP70 heat shock elements are functionally distinct. Mol. Cell. Biol. 13:5637-5646.
63. Zou, J., Y. Guo, T. Guettouche, D. F. Smith, and R. Voellmy. 1998. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94:471-480.
64. Zuo, J., D. Rungger, and R. Voellmy. 1995. Multiple layers of regulation of human heat shock transcription factor 1. Mol. Cell. Biol. 15:4319-4330.