Mutational analysis of human heat-shock transcription factor 1 reveals a regulatory role for oligomerization in DNA-binding specificity

Biochemical Journal

Volumn 424, Issue 2, 2009, Pages 253-261

  Takemori, Yukiko ^a   Enoki, Yasuaki ^a   Yamamoto, Noritaka ^a   Fukai, Yo ^a   Adachi, Kaori ^a   Sakurai, Hiroshi ^a  

^a KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

Author keywords

Heat shock element (HSE); Heat shock protein (HSP); Heat shock response; Heat shock transcription factor (HSF); Protein DNA interaction

Indexed keywords

AMINO ACID SUBSTITUTION; CELLULAR PROCESS; CONFORMATIONAL CHANGE; DNA-BINDING DOMAIN; DNA-BINDING SPECIFICITY; HEAT-SHOCK; HEAT-SHOCK PROTEIN; HELA CELL; IN-VITRO; INVERTED REPEAT; MUTATIONAL ANALYSIS; PROTEIN-DNA INTERACTION; PROTEIN-DNA INTERACTIONS; REGULATORY SEQUENCES; TARGET GENES; TEMPERATURE-SENSITIVE GROWTH; YEAST CELL;

AMINES; AMINO ACIDS; BIOACTIVITY; DNA; GENES; NUCLEIC ACIDS; OLIGOMERIZATION; ORGANIC ACIDS; TRANSCRIPTION FACTORS; YEAST;

TRANSCRIPTION;

HEAT SHOCK TRANSCRIPTION FACTOR 1;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CELL FUNCTION; CELL ISOLATION; CONTROLLED STUDY; DNA BINDING; DNA CONFORMATION; ENZYME SPECIFICITY; GENE EXPRESSION REGULATION; GENE REPRESSION; GENETIC TRANSCRIPTION; GROWTH DISORDER; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; INVERTED REPEAT; MUTATIONAL ANALYSIS; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY SEQUENCE; SACCHAROMYCES CEREVISIAE; TEMPERATURE; YEAST;

AMINO ACID SEQUENCE; DNA; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; SACCHAROMYCES CEREVISIAE; SUBSTRATE SPECIFICITY; TRANSCRIPTION FACTORS;

EID: 70450209178     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20090922     Document Type: Article

References (52)

1. Young, J. C., Agashe, V. R., Siegers, K. and Hartl, F. U. (2004) Pathways of chaperone-mediated protein folding in the cytosol. Nat. Rev. Mol. Cell Biol. 5, 781-791
2. Morimoto, R. I. (2008) Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev. 22, 1427-1438
3. 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
4. Pirkkala, L., Nykanen, P. and Sistonen, L. (2001) Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J. 15, 1118-1131
5. Amin, J., Ananthan, J. and Voellmy, R. (1988) Key features of heat shock regulatory elements. Mol. Cell. Biol. 8, 3761-3769
6. Tamai, K. T., Liu, X., Silar, P., Sosinowski, T. and Thiele, D. J. (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, 8155-81654
7. Yamamoto, A., Mizukami, Y. and Sakurai, H. (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
8. Sakurai, H. and Takemori, Y. (2007) Interaction between heat shock transcription factors (HSFs) and divergent binding sequences: binding specificities of yeast HSFs and human HSF1. J. Biol. Chem. 282, 13334-13341
9. Akerfelt, M., Trouillet, D., Mezger, V. and Sistonen, L. (2007) Heat shock factors at a crossroad between stress and development. Ann. N.Y. Acad. Sci. 1113, 15-27
10. Sarge, K. D., Murphy, S. P. and Morimoto, R. I. (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
11. a Erratum (1993) Mol. Cell. Biol. 13, 3838-3839
12. Zuo, J., Rungger, D. and Voellmy, R. (1995) Multiple layers of regulation of human heat shock transcription factor 1. Mol. Cell. Biol. 15, 4319-4330
13. Zou, J., Guo, Y., Guettouche, T., Smith, D. F. and Voellmy, R. (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
14. Shi, Y., Mosser, D. D. and Morimoto, R. I. (1998) Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev. 12, 654-666
15. Voellmy, R. (2004) On mechanisms that control heat shock transcription factor activity in metazoan cells. Cell Stress Chaperones 9, 122-133
16. Holmberg, C. I., Tran, S. E., Eriksson, J. E. and Sistonen, L. (2002) Multisite phosphorylation provides sophisticated regulation of transcription factors. Trends Biochem. Sci. 27, 619-627
17. Hietakangas, V., Ahlskog, J. K., Jakobsson, A. M., Hellesuo, M., Sahlberg, N. M., Holmberg, C. I., Mikhailov, A., Palvimo, J. J., Pirkkala, L. and Sistonen, L. (2003) Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1. Mol. Cell. Biol. 23, 2953-2968
18. Westerheide, S. D., Anckar, J., Stevens, Jr, S. M., Sistonen, L. and Morimoto, R. I. (2009) Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 323, 1063-1066
19. Yamamoto, N., Takemori, Y., Sakurai, M., Sugiyama, K. and Sakurai, H. (2009) Differential recognition of heat shock elements by members of the heat shock transcription factor family. FEBS J. 276, 1962-1974
20. Cunniff, N. F. and Morgan, W. D. (1993) Analysis of heat shock element recognition by saturation mutagenesis of the human HSP70.1 gene promoter. J. Biol. Chem. 268, 8317-8324
21. Kroeger, P. E. and Morimoto, R. I. (1994) Selection of new HSF1 and HSF2 DNA-binding sites reveals difference in trimer cooperativity. Mol. Cell. Biol. 14, 7592-7603
22. Trinklein, N. D., Murray, J. I., Hartman, S. J., Botstein, D. and Myers, R. M. (2004) The role of heat shock transcription factor 1 in the genome-wide regulation of the mammalian heat shock response. Mol. Biol. Cell 15, 1254-1261
23. Liu, X. D., Liu, P. C., Santoro, N. and Thiele, D. J. (1997) Conservation of a stress response: human heat shock transcription factors functionally substitute for yeast HSF. EMBO J. 16, 6466-6477
24. Liu, P. C. and Thiele, D. J. (1999) Modulation of human heat shock factor trimerization by the linker domain. J. Biol. Chem. 274, 17219-17225
25. Ahn, S. G., Liu, P. C., Klyachko, K., Morimoto, R. I. and Thiele, D. J. (2001) The loop domain of heat shock transcription factor 1 dictates DNA-binding specificity and responses to heat stress. Genes Dev. 15, 2134-2145
26. Imazu H., and Sakurai H. (2005) Saccharomyces cerevisiae heat shock transcription factor regulates cell wall remodeling in response to heat shock. Eukaryotic Cell 4, 1050-1056
27. Takemori, Y., Sakaguchi, A., Matsuda, S., Mizukami, Y. and Sakurai, H. (2005) Stress-induced transcription of the endoplasmic reticulum oxidoreductin gene ERO1 in the yeast Saccharomyces cerevisiae. Mol. Genet. Genomics 275, 89-96
28. Leung, D. W., Chen, E. and Goeddel, D. V. (1989) A method for random mutagenesis of a defined DNA segment using a modified polymerase chain reaction. Technique 1, 11-15
29. Belli, G., Gari, E., Aldea, M. and Herrero, E. (1998) Functional analysis of yeast essential genes using a promoter-substitution cassette and the tetracycline-regulatable dual expression system. Yeast 14, 1127-1138
30. Ahn, S. G. and Thiele, D. J. (2003) Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev. 17, 516-528
31. Lu, M., Kim, H. E., Li, C. R., Kim, S., Kwak, I. J., Lee, Y. J., Kim, S. S., Moon, J. Y., Kim, C. H., Kim, D. K. et al. (2008) Two distinct disulfide bonds formed in human heat shock transcription factor 1 act in opposition to regulate its DNA binding activity. Biochemistry 47, 6007-6015
32. Zuo, J., Baler, R., Dahl, G. and Voellmy, R. (1994) Activation of the DNA-binding ability of human heat shock transcription factor 1 may involve the transition from an intramolecular to an intermolecular triple-stranded coiled-coil structure. Mol. Cell. Biol. 14, 7557-7568
33. Green, M., Schuetz, T. J., Sullivan, E. K. and Kingston, R. E. (1995) A heat shock-responsive domain of human HSF1 that regulates transcription activation domain function. Mol. Cell. Biol. 15, 3354-3362
34. Nakai, A., Tanabe, M., Kawazoe, Y., Inazawa, J., Morimoto, R. I. and Nagata, K. (1997) HSF4, a new member of the human heat shock factor family which lacks properties of a transcriptional activator. Mol. Cell. Biol. 17, 469-481
35. Hashikawa, N., Yamamoto, N. and Sakurai, H. (2007) Different mechanisms are involved in the transcriptional activation by yeast heat shock transcription factor through two different types of heat shock elements. J. Biol. Chem. 282, 10333-10340
36. Dai, C., Whitesell, L., Rogers, A. B. and Lindquist, S. (2007) Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 130, 1005-1018
37. Reinke, H., Saini, C., Fleury-Olela, F., Dibner, C., Benjamin, I. J. and Schibler, U. (2008) Differential display of DNA-binding proteins reveals heat-shock factor 1 as a circadian transcription factor. Genes Dev. 22, 331-345
38. Xiao, X., Zuo, X., Davis, A. A., McMillan, D. R., Curry, B. B., Richardson, J. A. and Benjamin, I. J. (1999) HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. EMBO J. 18, 5943-5952
39. Santos, S. D. and Saraiva, M. J. (2004) Enlarged ventricles, astrogliosis and neurodegeneration in heat shock factor 1 null mouse brain. Neuroscience 126, 657-663
40. Inouye, S., Izu, H., Takaki, E., Suzuki, H., Shirai, M., Yokota, Y., Ichikawa, H., Fujimoto, M. and Nakai, A. (2004) Impaired IgG production in mice deficient for heat shock transcription factor 1. J. Biol. Chem. 279, 38701-38709
41. Takaki, E., Fujimoto, M., Nakahari, T., Yonemura, S., Miyata, Y., Hayashida, N., Yamamoto, K., Vallee, R. B., Mikuriya, T., Sugahara, K. et al. (2007) Heat shock transcription factor 1 is required for maintenance of ciliary beating in mice. J. Biol. Chem. 282, 37285-37292
42. Harrison, C. J., Bohm, A. A. and Nelson, H. C. (1994) Crystal structure of the DNA binding domain of the heat shock transcription factor. Science 263, 224-227
43. Vuister, G. W., Kim, S. J., Orosz, A., Marquardt, J., Wu, C. and Bax, A. (1994) Solution structure of the DNA-binding domain of Drosophila heat shock transcription factor. Nat. Struct. Biol. 1, 605-614
44. Littlefield, O. and Nelson, H. C. (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
45. Lu, M., Lee, Y. J., Park, S. M., Kang, H. S., Kang, S. W., Kim, S. and Park, J. S. (2009) Aromatic-participant interactions are essential for disulfide-bond-based trimerization in human heat shock transcription factor 1. Biochemistry 48, 3795-3797
46. McClellan, A. J., Xia, Y., Deutschbauer, A. M., Davis, R. W., Gerstein, M. and Frydman, J. (2007) Diverse cellular functions of the Hsp90 molecular chaperone uncovered using systems approaches. Cell 131, 121-135
47. Walsh, P., Bursa, D., Law, Y. C., Cyr, D. and Lithgow, T. (2004) The J-protein family: modulating protein assembly, disassembly and translocation. EMBO Rep. 5, 567-571
48. Nathan, D. F., Vos, M. H. and Lindquist, S. (1997) In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc. Natl. Acad. Sci. U.S.A. 94, 12949-12956
49. Glover, J. R. and Lindquist, S. (1998) Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94, 73-82
50. Zarzov, P., Boucherie, H. and Mann, C. (1997) A yeast heat shock transcription factor (Hsf1) mutant is defective in both Hsc82/Hsp82 synthesis and spindle pole body duplication. J. Cell Sci. 110, 1879-1891
51. Morano, K. A., Santoro, N., Koch, K. A. and Thiele, D. J. (1999) A trans-activation domain in yeast heat shock transcription factor is essential for cell cycle progression during stress. Mol. Cell. Biol. 19, 402-411
52. Xiao, H., Perisic, O. and Lis, J. Y. (1991) Cooperative binding of Drosophila heat shock factor to arrays of a conserved 5 bp unit. Cell 64, 585-593