Novel aspects of heat shock factors: DNA recognition, chromatin modulation and gene expression

FEBS Journal

Volumn 277, Issue 20, 2010, Pages 4140-4149

  Sakurai, Hiroshi ^a   Enoki, Yasuaki ^a  

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

Author keywords

chromatin; heat shock element; heat shock transcription factor; histone; protein DNA interactions

Indexed keywords

HEAT SHOCK PROTEIN; HEAT SHOCK TRANSCRIPTION FACTOR 1; HEAT SHOCK TRANSCRIPTION FACTOR 2; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; CHROMATIN; DNA;

BINDING AFFINITY; CELLULAR STRESS RESPONSE; CHROMATIN; DNA DETERMINATION; DNA REPLICATION; DROSOPHILA; GENE EXPRESSION; HEAT SHOCK; HUMAN; MAMMAL CELL; MODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN FUNCTION; SACCHAROMYCES; SHORT SURVEY; TRANSCRIPTION REGULATION; YEAST; ANIMAL; GENETICS; METABOLISM;

MAMMALIA;

ANIMALS; CHROMATIN; DNA; GENE EXPRESSION; HEAT-SHOCK PROTEINS; HUMANS; YEASTS;

EID: 77957270749     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07829.x     Document Type: Short Survey

References (78)

1. Fujimoto M Nakai A (2010) The heat shock factor family and adaptation to proteotoxic stress. FEBS J 277, 4112 4125.
2. Björk JK Sistonen L (2010) Regulation of the members of the mammalian heat shock factor family. FEBS J 277, 4126 4139.
3. Abane R Mezger V (2010) Roles of heat shock factors in gametogenesis and development. FEBS J 277, 4150 4172. (Pubitemid 350015004)
4. Pirkkala L, Nykanen P Sistonen L (2001) Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J 15, 1118 1131. (Pubitemid 32436297)
5. Harrison CJ, Bohm AA Nelson HC (1994) Crystal structure of the DNA binding domain of the heat shock transcription factor. Science 263, 224 227. (Pubitemid 24067928)
6. Vuister GW, Kim SJ, Orosz A, Marquardt J, Wu C Bax A (1994) Solution structure of the DNA-binding domain of Drosophila heat shock transcription factor. Nat Struct Biol 1, 605 614. (Pubitemid 2122339)
7. Peteranderl R, Rabenstein M, Shin YK, Liu CW, Wemmer DE, King DS Nelson HC (1999) Biochemical and biophysical characterization of the trimerization domain from the heat shock transcription factor. Biochemistry 38, 3559 3569. (Pubitemid 129514610)
8. Zhong M, Orosz A Wu C (1998) Direct sensing of heat and oxidation by Drosophila heat shock transcription factor. Mol Cell 2, 101 108. (Pubitemid 128378971)
9. Ahn SG Thiele DJ (2003) Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev 17, 516 528.
10. Rabindran SK, Haroun RI, Clos J, Wisniewski J Wu C (1993) Regulation of heat shock factor trimer formation: role of the conserved leucine zipper. Science 259, 230 234. (Pubitemid 23041800)
11. Zuo J, Baler R, Dahl G 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. (Pubitemid 24326422)
12. Farkas T, Kutskova YA Zimarino V (1998) Intramolecular repression of mouse heat shock factor 1. Mol Cell Biol 18, 906 918. (Pubitemid 28063424)
13. Newton EM, Knauf U, Green M Kingston RE (1996) The regulatory domain of human heat shock factor 1 is sufficient to sense heat stress. Mol Cell Biol 16, 839 846. (Pubitemid 26061653)
14. Perisic O, Xiao H Lis JT (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. (Pubitemid 20022370)
15. Littlefield O Nelson HC (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. (Pubitemid 29218017)
16. Cunniff NF Morgan WD (1993) Analysis of heat shock element recognition by saturation mutagenesis of the human HSP70.1 gene promoter. J Biol Chem 268, 8317 8324.
17. Fernandes M, Xiao H Lis JT (1994) Fine structure analyses of the Drosophila and Saccharomyces heat shock factor-heat shock element interactions. Nucleic Acids Res 22, 167 173. (Pubitemid 24160931)
18. Kroeger PE Morimoto RI (1994) Selection of new HSF1 and HSF2 DNA-binding sites reveals difference in trimer cooperativity. Mol Cell Biol 14, 7592 7603.
19. Xiao H, Perisic O Lis JT (1991) Cooperative binding of Drosophila heat shock factor to arrays of a conserved 5 bp unit. Cell 64, 585 593. (Pubitemid 121002974)
20. Hashikawa N, Mizukami Y, Imazu H Sakurai H (2006) Mutated yeast heat shock transcription factor activates transcription independently of hyperphosphorylation. J Biol Chem 281, 3936 3942. (Pubitemid 43847817)
21. Yamamoto N, Takemori Y, Sakurai M, Sugiyama K Sakurai H (2009) Differential recognition of heat shock elements by members of the heat shock transcription factor family. FEBS J 276, 1962 1974.
22. Cicero MP, Hubl ST, Harrison CJ, Littlefield O, Hardy JA Nelson HC (2001) The wing in yeast heat shock transcription factor (HSF) DNA-binding domain is required for full activity. Nucleic Acids Res 29, 1715 1723. (Pubitemid 32427852)
23. Ahn SG, Liu PC, Klyachko K, Morimoto RI Thiele DJ (2001) The loop domain of heat shock transcription factor 1 dictates DNA-binding specificity and responses to heat stress. Genes Dev 15, 2134 2145. (Pubitemid 32762056)
24. Lu M, Lee YJ, Park SM, Kang HS, Kang SW, Kim S Park JS (2009) Aromatic-participant interactions are essential for disulfide-bond-based trimerization in human heat shock transcription factor 1. Biochemistry 48, 3795 3797.
25. Liu PC Thiele DJ (1999) Modulation of human heat shock factor trimerization by the linker domain. J Biol Chem 274, 17219 17225. (Pubitemid 129519057)
26. Trott A Morano KA (2003) The yeast response to heat shock. In Yeast Stress Responses (Hohmann S Mager PWH eds pp 71 119. Springer-Verlag
27. Hahn JS, Hu Z, Thiele DJ Iyer VR (2004) Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol Cell Biol 24, 5249 5256. (Pubitemid 38738160)
28. Yamamoto A, Mizukami Y 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. (Pubitemid 40418506)
29. Yamamoto A, Ueda J, Yamamoto N, Hashikawa N Sakurai H (2007) Role of heat shock transcription factor in Saccharomyces cerevisiae oxidative stress response. Eukaryot Cell 6, 1373 1379. (Pubitemid 47257706)
30. Sorger PK (1990) Yeast heat shock factor contains separable transient and sustained response transcriptional activators. Cell 62, 793 805. (Pubitemid 20275718)
31. Chou S, Chatterjee S, Lee M Struhl K (1999) Transcriptional activation in yeast cells lacking transcription factor IIA. Genetics 153, 1573 1581.
32. Lee D Lis JT (1998) Transcriptional activation independent of TFIIH kinase and the RNA polymerase II mediator in vivo. Nature 393, 389 392. (Pubitemid 28269715)
33. Apone LM, Virbasius CA, Holstege FC, Wang J, Young RA Green MR (1998) Broad, but not universal, transcriptional requirement for yTAFII17, a histone H3-like TAFII present in TFIID and SAGA. Mol Cell 2, 653 661. (Pubitemid 128379090)
34. Moqtaderi Z, Keaveney M Struhl K (1998) The histone H3-like TAF is broadly required for transcription in yeast. Mol Cell 2, 675 682. (Pubitemid 128379092)
35. Silar P, Butler G Thiele DJ (1991) Heat shock transcription factor activates transcription of the yeast metallothionein gene. Mol Cell Biol 11, 1232 1238. (Pubitemid 21895479)
36. Hashikawa N, Yamamoto N 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. (Pubitemid 47093400)
37. Sakurai H 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. (Pubitemid 47100495)
38. Xiao X, Zuo X, Davis AA, McMillan DR, Curry BB, Richardson JA Benjamin IJ (1999) HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. EMBO J 18, 5943 5952. (Pubitemid 29515671)
39. Sistonen L, Sarge KD Morimoto RI (1994) Human heat shock factors 1 and 2 are differentially activated and can synergistically induce hsp70 gene transcription. Mol Cell Biol 14, 2087 2099. (Pubitemid 24074606)
40. Nakai A, Tanabe M, Kawazoe Y, Inazawa J, Morimoto RI 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. (Pubitemid 26425637)
41. Fujimoto M, Hayashida N, Katoh T, Oshima K, Shinkawa T, Prakasam R, Tan K, Inouye S, Takii R Nakai A (2010) A novel mouse HSF3 has the potential to activate non-classical heat shock genes during heat shock. Mol Biol Cell 21, 106 116.
42. Trinklein ND, Murray JI, Hartman SJ, Botstein D Myers RM (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. (Pubitemid 38316232)
43. Fujimoto M, Oshima K, Shinkawa T, Wang BB, Inouye S, Hayashida N, Takii R Nakai A (2008) Analysis of HSF4 binding regions reveals its necessity for gene regulation during development and heat shock response in mouse lenses. J Biol Chem 283, 29961 29970.
44. Chang Y, Ostling P, Akerfelt M, Trouillet D, Rallu M, Gitton Y, El Fatimy R, Fardeau V, Le Crom S, Morange M et al. (2006) Role of heat-shock factor 2 in cerebral cortex formation and as a regulator of p35 expression. Genes Dev 20, 836 847.
45. Takemori Y, Enoki Y, Yamamoto N, Fukai Y, Adachi K Sakurai H (2009) Mutational analysis of human heat-shock transcription factor 1 reveals a regulatory role for oligomerization in DNA-binding specificity. Biochem J 424, 253 261.
46. Pan Y, Tsai CJ, Ma B Nussinov R (2010) Mechanisms of transcription factor selectivity. Trends Genet 26, 75 83.
47. Loison F, Debure L, Nizard P, Le Goff P, Michel D Le Drean Y (2006) Up-regulation of the clusterin gene after proteotoxic stress: implication of HSF1-HSF2 heterocomplexes. Biochem J 395, 223 231.
48. Ostling P, Björk JK, Roos-Mattjus P, Mezger V Sistonen L (2007) Heat shock factor 2 (HSF2) contributes to inducible expression of hsp genes through interplay with HSF1. J Biol Chem 282, 7077 7086. (Pubitemid 47093630)
49. Sandqvist A, Björk JK, Akerfelt M, Chitikova Z, Grichine A, Vourc'h C, Jolly C, Salminen TA, Nymalm Y Sistonen L (2009) Heterotrimerization of heat-shock factors 1 and 2 provides a transcriptional switch in response to distinct stimuli. Mol Biol Cell 20, 1340 1347.
50. Taylor IC, Workman JL, Schuetz TJ Kingston RE (1991) Facilitated binding of GAL4 and heat shock factor to nucleosomal templates: differential function of DNA-binding domains. Genes Dev 5, 1285 1298.
51. Li B, Carey M Workman JL (2007) The role of chromatin during transcription. Cell 128, 707 719. (Pubitemid 46273570)
52. Zanton SJ Pugh BF (2006) Full and partial genome-wide assembly and disassembly of the yeast transcription machinery in response to heat. Genes Dev 20, 2250 2265. (Pubitemid 44244526)
53. Schwabish MA Struhl K (2006) Asf1 mediates histone eviction and deposition during elongation by RNA polymerase II. Mol Cell 22, 415 422.
54. Shivaswamy S Iyer VR (2008) Stress-dependent dynamics of global chromatin remodeling in yeast: dual role for SWISNF in the heat shock stress response. Mol Cell Biol 28, 2221 2234. (Pubitemid 351429969)
55. Zhao J, Herrera-Diaz J Gross DS (2005) Domain-wide displacement of histones by activated heat shock factor occurs independently of SwiSnf and is not correlated with RNA polymerase II density. Mol Cell Biol 25, 8985 8999. (Pubitemid 41429088)
56. Erkina TY, Tschetter PA Erkine AM (2008) Different requirements of the SWISNF complex for robust nucleosome displacement at promoters of heat shock factor and Msn2- and Msn4-regulated heat shock genes. Mol Cell Biol 28, 1207 1217.
57. Erkina TY, Zou Y, Freeling S, Vorobyev VI Erkine AM (2009) Functional interplay between chromatin remodeling complexes RSC, SWISNF and ISWI in regulation of yeast heat shock genes. Nucleic Acids Res 38, 1441 1449.
58. Kremer SB Gross DS (2009) The SAGA and Rpd3 chromatin modification complexes dynamically regulate heat shock gene structure and expression. J Biol Chem 284, 32914 32931.
59. Venturi CB, Erkine AM Gross DS (2000) Cell cycle-dependent binding of yeast heat shock factor to nucleosomes. Mol Cell Biol 20, 6435 6448. (Pubitemid 30650231)
60. Petesch SJ Lis JT (2008) Rapid, transcription-independent loss of nucleosomes over a large chromatin domain at Hsp70 loci. Cell 134, 74 84.
61. Jensen MM, Christensen MS, Bonven B Jensen TH (2008) Requirements for chromatin reassembly during transcriptional downregulation of a heat shock gene in Saccharomyces cerevisiae. FEBS J 275, 2956 2964. (Pubitemid 351678682)
62. Core LJ Lis JT (2008) Transcription regulation through promoter-proximal pausing of RNA polymerase II. Science 319, 1791 1792. (Pubitemid 351451556)
63. Price DH (2008) Poised polymerases: on your mark.get set.go Mol Cell 30, 7 10.
64. Gilmour DS (2009) Promoter proximal pausing on genes in metazoans. Chromosoma 118, 1 10.
65. Bevilacqua A, Fiorenza MT Mangia F (2000) A developmentally regulated GAGA box-binding factor and Sp1 are required for transcription of the hsp70.1 gene at the onset of mouse zygotic genome activation. Development 127, 1541 1551. (Pubitemid 30232604)
66. Xing H, Wilkerson DC, Mayhew CN, Lubert EJ, Skaggs HS, Goodson ML, Hong Y, Park-Sarge OK Sarge KD (2005) Mechanism of hsp70i gene bookmarking. Science 307, 421 423. (Pubitemid 40139986)
67. Xing H, Vanderford NL Sarge KD (2008) The TBP-PP2A mitotic complex bookmarks genes by preventing condensin action. Nat Cell Biol 10, 1318 1323.
68. Sarge KD Park-Sarge OK (2009) Mitotic bookmarking of formerly active genes: keeping epigenetic memories from fading. Cell Cycle 8, 818 823.
69. Inouye S, Fujimoto M, Nakamura T, Takaki E, Hayashida N, Hai T Nakai A (2007) Heat shock transcription factor 1 opens chromatin structure of interleukin-6 promoter to facilitate binding of an activator or a repressor. J Biol Chem 282, 33210 33217. (Pubitemid 350159268)
70. Corey LL, Weirich CS, Benjamin IJ Kingston RE (2003) Localized recruitment of a chromatin-remodeling activity by an activator in vivo drives transcriptional elongation. Genes Dev 17, 1392 1401.
71. Xu D, Zalmas LP La Thangue NB (2008) A transcription cofactor required for the heat-shock response. EMBO Rep 9, 662 669. (Pubitemid 351927687)
72. Thomson S, Hollis A, Hazzalin CA Mahadevan LC (2004) Distinct stimulus-specific histone modifications at hsp70 chromatin targeted by the transcription factor heat shock factor-1. Mol Cell 15, 585 594. (Pubitemid 39141785)
73. Gómez AV, Galleguillos D, Maass JC, Battaglioli E, Kukuljan M Andrés ME (2008) CoREST represses the heat shock response mediated by HSF1. Mol Cell 31, 222 231.
74. Espinoza CA, Allen TA, Hieb AR, Kugel JF Goodrich JA (2004) B2 RNA binds directly to RNA polymerase II to repress transcript synthesis. Nat Struct Mol Biol 11, 822 829.
75. Mariner PD, Walters RD, Espinoza CA, Drullinger LF, Wagner SD, Kugel JF Goodrich JA (2008) Human Alu RNA is a modular transacting repressor of mRNA transcription during heat shock. Mol Cell 29, 499 509.
76. Shamovsky I, Ivannikov M, Kandel ES, Gershon D Nudler E (2006) RNA-mediated response to heat shock in mammalian cells. Nature 440, 556 560.
77. Fritah S, Col E, Boyault C, Govin J, Sadoul K, Chiocca S, Christians E, Khochbin S, Jolly C Vourc'h C (2009) Heat-shock factor 1 controls genome-wide acetylation in heat-shocked cells. Mol Biol Cell 20, 4976 4984.
78. Khaleque MA, Bharti A, Gong J, Gray PJ, Sachdev V, Ciocca DR, Stati A, Fanelli M Calderwood SK (2008) Heat shock factor 1 represses estrogen-dependent transcription through association with MTA1. Oncogene 27, 1886 1893. (Pubitemid 351430827)