Structure of human heat-shock transcription factor 1 in complex with DNA

Nature Structural and Molecular Biology

Volumn 23, Issue 2, 2016, Pages 140-146

  Neudegger, Tobias ^a   Verghese, Jacob ^a   Hayer Hartl, Manajit ^a   Hartl, F Ulrich ^a   Bracher, Andreas ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; DNA; HEAT SHOCK TRANSCRIPTION FACTOR 1; MEMBRANE PROTEIN; SKN7 PROTEIN; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; HEAT SHOCK TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR;

ARTICLE; CHAETOMIUM; CHAETOMIUM THERMOPHILUM; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA BINDING; DNA SEQUENCE; MOLECULAR INTERACTION; NONHUMAN; OLIGOMERIZATION; PARALOGY; PRIORITY JOURNAL; PROTEIN STRUCTURE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; NUCLEOTIDE SEQUENCE; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

BASE SEQUENCE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DNA; DNA-BINDING PROTEINS; HUMANS; MODELS, MOLECULAR; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION FACTORS;

EID: 84956730115     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3149     Document Type: Article

References (81)

1. Balch, W.E., Morimoto, R.I., Dillin, A., & Kelly, J.W. Adapting proteostasis for disease intervention. Science 319, 916-919 (2008
2. Kim, Y.E., Hipp, M.S., Bracher, A., Hayer-Hartl, M., & Hartl, F.U. Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem. 82, 323-355 (2013
3. Åkerfelt, M., Morimoto, R.I., & Sistonen, L. Heat shock factors: integrators of cell stress, development and lifespan. Nat. Rev. Mol. Cell Biol. 11, 545-555 (2010
4. Vabulas, R.M., Raychaudhuri, S., Hayer-Hartl, M., & Hartl, F.U. Protein folding in the cytoplasm and the heat shock response. Cold Spring Harb. Perspect. Biol. 2, a004390 (2010
5. Anckar, J., & Sistonen, L. Regulation of HSF1 function in the heat stress response: implications in aging and disease. Annu. Rev. Biochem. 80, 1089-1115 (2011
6. Morimoto, R.I. The heat shock response: systems biology of proteotoxic stress in aging and disease. Cold Spring Harb. Symp. Quant. Biol. 76, 91-99 (2011
7. Pelham, H.R. A regulatory upstream promoter element in the Drosophila hsp 70 heat-shock gene. Cell 30, 517-528 (1982
8. Amin, J., Ananthan, J., & Voellmy, R. Key features of heat shock regulatory elements. Mol. Cell. Biol. 8, 3761-3769 (1988
9. Xiao, H., & Lis, J.T. Germline transformation used to define key features of heat-shock response elements. Science 239, 1139-1142 (1988
10. Wu, C. Heat shock transcription factors: structure and regulation. Annu. Rev. Cell Dev. Biol. 11, 441-469 (1995
11. Pattaramanon, N., Sangha, N., & Gafni, A. The carboxy-terminal domain of heat-shock factor 1 is largely unfolded but can be induced to collapse into a compact, partially structured state. Biochemistry 46, 3405-3415 (2007
12. Harrison, C.J., Bohm, A.A., & Nelson, H.C. Crystal structure of the DNA binding domain of the heat shock transcription factor. Science 263, 224-227 (1994
13. Vuister, G.W., et al. Solution structure of the DNA-binding domain of Drosophila heat shock transcription factor. Nat. Struct. Biol. 1, 605-614 (1994
14. Liu, G., et al. Solution NMR structure of heat shock factor protein 1 DNA binding domain from Homo sapiens, Northeast Structural Genomics Consortium Target HR3023C (2011
15. Littlefield, O., & Nelson, H.C. A new use for the wing of the winged helix-turn-helix motif in the HSF-DNA cocrystal. Nat. Struct. Biol. 6, 464-470 (1999
16. Baler, R., Dahl, G., & Voellmy, R. Activation of human heat shock genes is accompanied by oligomerization, modification, and rapid translocation of heat shock transcription factor HSF1. Mol. Cell. Biol. 13, 2486-2496 (1993
17. Sarge, K.D., Murphy, S.P., & Morimoto, R.I. 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 (1993
18. Xiao, X., et al. HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. EMBO J. 18, 5943-5952 (1999
19. Mendillo, M.L., et al. HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell 150, 549-562 (2012
20. Santagata, S., et al. Tight coordination of protein translation and HSF1 activation supports the anabolic malignant state. Science 341, 1238303 (2013
21. Dai, C., Whitesell, L., Rogers, A.B., & Lindquist, S. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 130, 1005-1018 (2007
22. Scherz-Shouval, R., et al. The reprogramming of tumor stroma by HSF1 is a potent enabler of malignancy. Cell 158, 564-578 (2014
23. Mercier, P.A., Winegarden, N.A., & Westwood, J.T. Human heat shock factor 1 is predominantly a nuclear protein before and after heat stress. J. Cell Sci. 112, 2765-2774 (1999
24. Rabindran, S.K., Haroun, R.I., Clos, J., Wisniewski, J., & Wu, C. Regulation of heat shock factor trimer formation: role of a conserved leucine zipper. Science 259, 230-234 (1993
25. Zuo, J., Baler, R., Dahl, G., & Voellmy, R. 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 (1994
26. Neef, D.W., Jaeger, A.M., & Thiele, D.J. Genetic selection for constitutively trimerized human HSF1 mutants identifies a role for coiled-coil motifs in DNA binding. G3 (Bethesda) 3, 1315-1324 (2013
27. Abravaya, K., Myers, M.P., Murphy, S.P., & Morimoto, R.I. The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression. Genes Dev. 6, 1153-1164 (1992
28. Nadeau, K., Das, A., & Walsh, C.T. Hsp90 chaperonins possess ATPase activity and bind heat shock transcription factors and peptidyl prolyl isomerases. J. Biol. Chem. 268, 1479-1487 (1993
29. Zou, J., Guo, Y., Guettouche, T., Smith, D.F., & Voellmy, R. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94, 471-480 (1998
30. Neef, D.W., et al. A direct regulatory interaction between chaperonin TRiC and stress-responsive transcription factor HSF1. Cell Rep. 9, 955-966 (2014
31. Shi, Y., Mosser, D.D., & Morimoto, R.I. Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev. 12, 654-666 (1998
32. Morimoto, R.I. Dynamic remodeling of transcription complexes by molecular chaperones. Cell 110, 281-284 (2002
33. Larson, J.S., Schuetz, T.J., & Kingston, R.E. In vitro activation of purified human heat shock factor by heat. Biochemistry 34, 1902-1911 (1995
34. Kline, M.P., & Morimoto, R.I. Repression of the heat shock factor 1 transcriptional activation domain is modulated by constitutive phosphorylation. Mol. Cell. Biol. 17, 2107-2115 (1997
35. Hietakangas, V., et al. Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1. Mol. Cell. Biol. 23, 2953-2968 (2003
36. Westerheide, S.D., Anckar, J., Stevens, S.M. Jr., Sistonen, L., & Morimoto, R.I. Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 323, 1063-1066 (2009
37. Raychaudhuri, S., et al. Interplay of acetyltransferase EP300 and the proteasome system in regulating heat shock transcription factor 1. Cell 156, 975-985 (2014
38. Grady, D.L., et al. Highly conserved repetitive DNA sequences are present at human centromeres. Proc. Natl. Acad. Sci. USA. 89, 1695-1699 (1992
39. Denegri, M., et al. Human chromosomes 9, 12, and 15 contain the nucleation sites of stress-induced nuclear bodies. Mol. Biol. Cell 13, 2069-2079 (2002
40. Jolly, C., et al. In vivo binding of active heat shock transcription factor 1 to human chromosome 9 heterochromatin during stress. J. Cell Biol. 156, 775-781 (2002
41. Jolly, C., et al. Stress-induced transcription of satellite III repeats. J. Cell Biol. 164, 25-33 (2004
42. Metz, A., Soret, J., Vourch, C., Tazi, J., & Jolly, C. A key role for stress-induced satellite III transcripts in the relocalization of splicing factors into nuclear stress granules. J. Cell Sci. 117, 4551-4558 (2004
43. Flick, K.E., Gonzalez, L. Jr., Harrison, C.J., & Nelson, H.C. 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 (1994
44. Zelin, E., Zhang, Y., Toogun, O.A., Zhong, S., & Freeman, B.C. The p23 molecular chaperone and GCN5 acetylase jointly modulate protein-DNA dynamics and open chromatin status. Mol. Cell 48, 459-470 (2012
45. Ahn, S.G., & Thiele, D.J. Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev. 17, 516-528 (2003
46. Lu, M., et al. 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 (2008
47. Xiao, H., Perisic, O., & Lis, J.T. Cooperative binding of Drosophila heat shock factor to arrays of a conserved 5 bp unit. Cell 64, 585-593 (1991
48. Sorger, P.K., & Pelham, H.R. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 54, 855-864 (1988
49. Wiederrecht, G., Seto, D., & Parker, C.S. Isolation of the gene encoding the S. cerevisiae heat shock transcription factor. Cell 54, 841-853 (1988
50. Fassler, J.S., & West, A.H. Fungal Skn7 stress responses and their relationship to virulence. Eukaryot. Cell 10, 156-167 (2011
51. Li, S., et al. The yeast histidine protein kinase, Sln1p, mediates phosphotransfer to two response regulators, Ssk1p and Skn7p. EMBO J. 17, 6952-6962 (1998
52. Morgan, B.A., et al. The Skn7 response regulator controls gene expression in the oxidative stress response of the budding yeast Saccharomyces cerevisiae. EMBO J. 16, 1035-1044 (1997
53. Li, S., et al. The eukaryotic two-component histidine kinase Sln1p regulates OCH1 via the transcription factor, Skn7p. Mol. Biol. Cell 13, 412-424 (2002
54. Peteranderl, R., & Nelson, H.C. Trimerization of the heat shock transcription factor by a triple-stranded alpha-helical coiled-coil. Biochemistry 31, 12272-12276 (1992
55. Sandqvist, A., et al. Heterotrimerization of heat-shock factors 1 and 2 provides a transcriptional switch in response to distinct stimuli. Mol. Biol. Cell 20, 1340-1347 (2009
56. Neef, D.W., Jaeger, A.M., & Thiele, D.J. Heat shock transcription factor 1 as a therapeutic target in neurodegenerative diseases. Nat. Rev. Drug Discov. 10, 930-944 (2011
57. Alarcon, S.V., et al. Tumor-intrinsic and tumor-extrinsic factors impacting hsp90- targeted therapy. Curr. Mol. Med. 12, 1125-1141 (2012
58. Calamini, B., & Morimoto, R.I. Protein homeostasis as a therapeutic target for diseases of protein conformation. Curr. Top. Med. Chem. 12, 2623-2640 (2012
59. Treisman, J., Gänczy, P., Vashishtha, M., Harris, E., & Desplan, C. A single amino acid can determine the DNA binding specificity of homeodomain proteins. Cell 59, 553-562 (1989
60. Tucker-Kellogg, L., et al. Engrailed (Gln50Lys) homeodomain-DNA complex at 1.9 Å resolution: structural basis for enhanced affinity and altered specificity. Structure 5, 1047-1054 (1997
61. Catanzariti, A.M., Soboleva, T.A., Jans, D.A., Board, P.G., & Baker, R.T. An efficient system for high-level expression and easy purification of authentic recombinant proteins. Protein Sci. 13, 1331-1339 (2004
62. Jaeger, A.M., Makley, L.N., Gestwicki, J.E., & Thiele, D.J. Genomic heat shock element sequences drive cooperative human heat shock factor 1 DNA binding and selectivity. J. Biol. Chem. 289, 30459-30469 (2014
63. Wyatt, P.J. Light scattering and the absolute characterization of macromolecules. Anal. Chim. Acta 272, 1-40 (1993
64. Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010
65. Evans, P. Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62, 72-82 (2006
66. Evans, P.R. Scala. Joint CCP4 ESF-EACBM Newsl. 33, 22-24 (1997
67. Evans, P.R., & Murshudov, G.N. How good are my data and what is the resolution?. Acta Crystallogr. D Biol. Crystallogr. 69, 1204-1214 (2013
68. French, G., & Wilson, K. On the treatment of negative intensity observations. Acta Crystallogr. A 34, 517-525 (1978
69. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994
70. Pape, T., & Schneider, T.R. HKL2MAP: a graphical user interface for phasing with SHELX programs. J. Appl. Crystallogr. 37, 843-844 (2004
71. Sheldrick, G.M. Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr. D Biol. Crystallogr. 66, 479-485 (2010
72. Langer, G., Cohen, S.X., Lamzin, V.S., & Perrakis, A. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc. 3, 1171-1179 (2008
73. Vagin, A.A., & Isupov, M.N. Spherically averaged phased translation function and its application to the search for molecules and fragments in electron-density maps. Acta Crystallogr. D Biol. Crystallogr. 57, 1451-1456 (2001
74. Emsley, P., & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004
75. Murshudov, G.N., Vagin, A.A., & Dodson, E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997
76. Kleywegt, G.T., & Jones, T.A. A super position. Joint CCP4 ESF-EACBM Newsl. 31, 9-14 (1994
77. Sali, A., & Blundell, T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815 (1993
78. Fiser, A., Do, R.K., & Sali, A. Modeling of loops in protein structures. Protein Sci. 9, 1753-1773 (2000
79. Fiser, A., & Sali, A. ModLoop: automated modeling of loops in protein structures. Bioinformatics 19, 2500-2501 (2003
80. Pettersen, E.F., et al. UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004
81. Gouet, P., Courcelle, E., Stuart, D.I., & Métoz, F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308 (1999