Skip to main content
Springer Nature Link
Log in

Biochemical events in the activation and attenuation of the heat shock transcriptional response

  • Published:
Journal of Biosciences Aims and scope Submit manuscript

Abstract

The expression of heat shock proteins in response to cellular stress is mediated by a family of heat shock transcription factors (HSFs). The transcriptional activity of these HSFs is regulated by multiple redundant regulatory mechanisms which ensure the fine tuned expression of heat shock genes. These mechanisms include cis-regulatory domains and trans-acting proteins which modulate HSF activity and control the heat shock response. Heat shock gene expression is also regulated by selective use of various HSFs under distinct developmental and growth conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Abravaya K, Myers M P, Murphy S P and Morimoto R I 1992 The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression;Genes Dev. 6 1153–1164

    CAS  PubMed  Google Scholar 

  • Abravaya K, Phillips B and Morimoto R I 1991 Attenuation of the heat shock response in HeLa cells is mediated by the release of bound heat shock transcription factor and is modulated by changes in growth and in heat shock temperatures;Genes Dev. 5 2117–2127

    Article  CAS  Google Scholar 

  • Ananthan J, Goldberg A L and Voellmy R 1986 Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes;Science 232 522–524

    Article  CAS  Google Scholar 

  • Baler R, Dahl G and Voellmy R 1993 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

    Article  CAS  Google Scholar 

  • Baler R, Welch W J and Voellmy R 1992 Heat shock gene regulation by nascent polypeptides and denatured proteins: hsp70 as a potential autoregulatory factor;J. Cell Biol. 117 1151–1159

    CAS  PubMed  Google Scholar 

  • Brown S A and Kingston R E 1997 Disruption of downstream chromatin directed by a transcriptional activator;Genes Dev. 11 3116–3121

    Article  CAS  Google Scholar 

  • Clos J, Westwood J T, Becker P B, Wilson S, Lambert K and Wu C 1990 Molecular cloning and expression of a hexamericDrosophila heat shock factor subject to negative regulation;Cell 63 1085–1097

    Article  CAS  Google Scholar 

  • Clos J, Rabindran S, Wisniewski J and Wu C 1993 Induction temperature of human heat shock factor is reprogrammed in aDrosophila cell environment;Nature (London) 364 252–255

    Article  CAS  Google Scholar 

  • Cotto J J, Kline M and Morimoto R I 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

    Article  CAS  Google Scholar 

  • Cotto J, Fox S and Morimoto R 1997 HSF1 granules: a novel stress-induced nuclear compartment of human cells;J. Cell Sci. 110 2925–2934

    CAS  PubMed  Google Scholar 

  • Femandes M, Xiao H and Lis J T 1994 Fine structure analyses of theDrosophila andSaccharomyces heat shock factor-heat shock element interactions;Nucleic Acids Res. 22 167–173

    Article  Google Scholar 

  • Finley D, Ciechanover A and Varshavsky A 1984 Thermolability of ubiquitin-activating enzyme from the mammalian cell cycle mutant ts85;Cell 37 43–55

    Article  CAS  Google Scholar 

  • Gething M J and Sambrook J 1992 Protein folding in the cell;Nature (London) 355 33–45

    Article  CAS  Google Scholar 

  • Giardina C, Perez-Riba M and Lis J T 1992 Promoter melting and TFIID complexes onDrosophila genesin vivo;Genes Dev. 6 2190–2200

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Halladay J T and Craig E A 1995 A heat shock transcription factor with reduced activity suppresses a yeast HSP70 mutant;Mol. Cell Biol. 15 4890–4897

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hartl F U 1996 Molecular chaperones in cellular protein folding;Nature (London) 381 571–579

    Article  CAS  Google Scholar 

  • Hightower L E 1980 Cultured animal cells exposed to amino acid analogues or puromycin rapidly synthesize several polypeptides;J. Cell. Physiol. 102 407–427

    Article  CAS  Google Scholar 

  • Hiromi Y, Okamoto H, Gehring W J and Hotta Y 1986 Germline transformation withDrosophila mutant actin genes induces constitutive expression of heat shock genes;Cell 44 293–301

    Article  CAS  Google Scholar 

  • Jakobsen B K and Pelham H R 1988 Constitutive binding of yeast heat shock factor to DNAin vivo;Mol. Cell. Biol. 8 5040–5042

    Article  CAS  Google Scholar 

  • Jedlicka P, Mortin M A and Wu C 1997 Multiple functions ofDrosophila heat shock transcription factorin vivo;EMBO J. 16 2452–2462

    Article  CAS  Google Scholar 

  • Jolly C, Morimoto R, Robert-Nicoud M and Vourc'h C 1997 HSF1 transcription factor concentrates in nuclear foci during heat shock: relationship with transcription sites;J. Cell Sci. 110 2935–2941

    CAS  PubMed  Google Scholar 

  • Jurivich D A, Sistonen L, Kroes R A and Morimoto R I 1992 Effect of sodium salicylate on the human heat shock response;Science 255 1243–1245

    Article  CAS  Google Scholar 

  • Kanei-Ishii C, Yasukawa T, Morimoto R I and Ishii S 1994 c-Myb-induced trans-activation mediated by heat shock elements without sequence-specific DNA binding of c-Myb;J. Biol. Chem. 269 15768–15775

    CAS  PubMed  Google Scholar 

  • Kanei-Ishii C, Tanikawa J, Nakai A, Morimoto R I and Ishii S 1997 Activation of heat shock transcription factor 3 by c-Myb in the absence of cellular stress;Science 277 246–248

    Article  CAS  Google Scholar 

  • Kelley P M and Schlesinger M J 1978 The effect of amino acid analogues and heat shock on gene expression in chicken embryo fibroblasts;Cell 15 1277–1286

    Article  CAS  Google Scholar 

  • Kline M P and Morimoto R I 1997 Repression of the heat shock factor 1 transcriptional activation domain is modulated by constitutive phosphorylation;Mol. Cell Biol. 17 2107–2115

    Article  CAS  Google Scholar 

  • Knauf U, Newton E M, Kyriakis J and Kingston R E 1996 Repression of human heat shock factor 1 activity at control temperature by phosphorylation;Genes Dev. 10 2782–2793

    Article  CAS  Google Scholar 

  • Kroeger P E, Sarge K D and Morimoto R I 1993 Mouse heat shock transcription factors 1 and 2 prefer a trimeric binding site but interact differently with the HSP70 heat shock element;Mol. Cell Biol. 13 3370–3383

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Larson J S, Schuetz T J and Kingston R E 1988 Activationin vitro of sequence-specific DNA binding by a human regulatory factor;Nature (London) 335 372–375

    Article  CAS  Google Scholar 

  • Leppa S, Pirkkala L, Chow S C, Eriksson J E and Sistonen L 1997 Thioredoxin is transcriptionally induced upon activation of heat shock factor 2;J. Biol. Chem. 272 30400–30404

    Article  CAS  Google Scholar 

  • Lindquist S and Craig E A 1988 The heat-shock proteins;Annu. Rev. Genet. 22 631–677

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Mezger V, Renard J P, Christians E and Morange M 1994 Detection of heat shock element-binding activities by gel shift assay during mouse preimplantation development;Dev. Biol. 165 627–638

    Article  CAS  Google Scholar 

  • Morimoto R I 1993 Cells in stress: transcriptional activation of heat shock genes;Science 259 1409–1410

    Article  CAS  Google Scholar 

  • Mosser D D, Kotzbauer P T, Sarge K D and Morimoto R I 1990;In vitro activation of heat shock transcription factor DNA-binding by calcium and biochemical conditions that affect protein conformation;Proc. Natl. Acad. Sci. USA 87 3748–3752

    Article  CAS  Google Scholar 

  • Mosser D D, Duchaine J and Massie B 1993 The DNA-binding activity of the human heat shock transcription factor is regulatedin vivo by hsp70;Mol. Cell Biol. 13 5427–5438

    Article  CAS  Google Scholar 

  • Nakai A and Morimoto R I 1993 Characterization of a novel chicken heat shock transcription factor, heat shock factor 3, suggests a new regulatory pathway;Mol. Cell. Biol. 13 1983–1997

    Article  CAS  Google Scholar 

  • Nakai A, Kawazoe Y, Tanabe M, Nagata K and Morimoto R I 1995 The DNA-binding properties of two heat shock factors, HSF1 and HSF3, are induced in the avian erythroblast cell line HD6;Mol. Cell. Biol. 15 5268–5278

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Nover L, Scharf K D, Gagliardi D, Vergne P, Czarnecka-Verner E and Gurley W B 1996 The Hsf world: classification and properties of plant heat stress transcription factors;Cell Stress Chaperones 1 215–223

    Article  CAS  Google Scholar 

  • Orosz A, Wisniewski J and Wu C 1996 Regulation ofDrosophila heat shock factor trimerization: global sequence requirements and independence of nuclear localization;Mol. Cell. Biol. 16 7018–7030

    Article  CAS  Google Scholar 

  • Parker-Thornburg J and Bonner J J 1987 Mutations that induce the heat shock response ofDrosophila;Cell 51 763–772

    Article  CAS  Google Scholar 

  • Parsell D A and Sauer R T 1989 Induction of a heat shock-like response by unfolded protein inEscherichia coli: dependence on protein level not protein degradation;Genes Dev. 3 1226–1232

    Article  CAS  Google Scholar 

  • Pelham H R 1982 A regulatory upstream promoter element in theDrosophila hsp 70 heat-shock gene;Cell 30 517–528

    Article  CAS  Google Scholar 

  • Peteranderl R and Nelson H C 1992 Trimerization of the heat shock transcription factor by a triple-stranded alpha-helical coiled-coil;Biochemistry 31 12272–12276

    Article  CAS  Google Scholar 

  • Rabindran S K, Giorgi G, Clos J and Wu C 1991 Molecular cloning and expression of a human heat shock factor, HSF1.Proc. Natl. Acad. Sci. USA 88 6906–6910

    Article  CAS  Google Scholar 

  • Rabindran S K, Haroun R I, Clos J, Wisniewski J and Wu C 1993 Regulation of heat shock factor trimer formation: role of a conserved leucine zipper;Science 259 230–234

    Article  CAS  Google Scholar 

  • Rabindran S K, Wisniewski J, Li L, Li G C and Wu C 1994 Interaction between heat shock factor and hsp70 is insufficient to suppress induction of DNA-binding activityin vivo;Mol. Cell Biol. 14 6552–6560

    Article  CAS  Google Scholar 

  • Rallu M, Loones M, Lallemand Y, Morimoto R, Morange M and Mezger V 1997 Function and regulation of heat shock factor 2 during mouse embryogenesis;Proc. Natl. Acad. Sci. USA 94 2392–2397

    Article  CAS  Google Scholar 

  • Sarge K D, Zimarino V, Holm K, Wu C and Morimoto R I 1991 Cloning and characterization of two mouse heat shock factors with distinct inducible and constitutive DNA-binding ability;Genes Dev. 5 1902–1911

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sarge K D, Park-Sarge O K, Kirby J D, Mayo K E and Morimoto R I 1994 Expression of heat shock factor 2 in mouse testis: potential role as a regulator of heat-shock protein gene expression during spermatogenesis;Biol. Reprod. 50 1334–1343

    Article  CAS  Google Scholar 

  • Satyal S H, Chen D, Fox S G, Kramer J M and Morimoto R I 1998 Regulation of the heat shock transcriptional response by HSBP1;Genes Dev. (in press)

  • Schuetz T J, Gallo G J, Sheldon L, Tempst P and Kingston R E 1991 Isolation of a cDNA for HSF2: evidence for two heat shock factor genes in humans;Proc. Natl. Acad. Sci. USA 88 6911–6915

    Article  CAS  Google Scholar 

  • Shi Y, Kroeger P E and Morimoto R I 1995 The carboxyl-terminal transactivation domain of heat shock factor 1 is negatively regulated and stress responsive;Mol. Cell. Biol. 15 4309–4318

    Article  CAS  Google Scholar 

  • Shi Y, Mosser D D and Morimoto R I 1998 Molecular chaperones as HSF1-specific transcriptional repressors;Genes Dev. 12 654–666

    Article  CAS  Google Scholar 

  • Sistonen L, Sarge K D, Phillips B, Abravaya K and Morimoto R I 1992 Activation of heat shock factor 2 during hemin-induced differentiation of human erythroleukemia cells;Mol. Cell. Biol. 12 4104–4111

    Article  CAS  Google Scholar 

  • Sistonen L, Sarge K D and Morimoto R I 1994 Human heat shock factors 1 and 2 are differentially activated and can synergistically induce hsp70 gene transcription;Mol. Cell. Biol. 14 2087–2099

    Article  CAS  Google Scholar 

  • Sorger P K and Pelham H R 1988 Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation;Cell 54 855–864

    Article  CAS  Google Scholar 

  • Sorger P K and Nelson H C 1989 Trimerization of a yeast transcriptional activator via a coiled-coil motif;Cell 59 807–813

    Article  CAS  Google Scholar 

  • Sorger P K 1990 Yeast heat shock factor contains separable transient and sustained response transcriptional activators;Cell 62 793–805

    Article  CAS  Google Scholar 

  • Tanabe M, Kawazoe Y, Takeda S, Morimoto R I, Nagata K and Nakai A 1998 Disruption of the HSF3 gene results in the severe reduction of heat shock gene expression and loss of thermotolerance;EMBO J. 17 1750–1758

    Article  CAS  Google Scholar 

  • Tsukiyama T and Wu C 1995 Purification and properties of an ATP-dependent nucleosome remodeling factor;Cell 83 1011–1020

    Article  CAS  Google Scholar 

  • Vuister G W, Kim S J, Wu C and Bax A 1994 NMR evidence for similarities between the DNA-binding regions ofDrosophila melanogaster heat shock factor and the helix-tum-helix and HNF-3/forkhead families of transcription factors;Biochemistry 33 10–16

    Article  CAS  Google Scholar 

  • Wiederrecht G, Seto D and Parker C S 1988 Isolation of the gene encoding theS. cerevisiae heat shock transcription factor;Cell 54 841–853

    Article  CAS  Google Scholar 

  • Williams G T, McClanahan T K and Morimoto R I 1989 E1a transactivation of the human HSP70 promoter is mediated through the basal transcription complex;Mol. Cell. Biol. 9 2574–2587

    Article  CAS  Google Scholar 

  • Wisniewski J, Orosz A, Allada R and Wu C 1996 The C-terminal region ofDrosophila heat shock factor (HSF) contains a constitutively functional transactivation domain;Nucleic Acids Res. 24 367–374

    Article  CAS  Google Scholar 

  • Wu C 1984 Two protein-binding sites in chromatin are implicated in the activation of heat shock genes;Nature (London) 309 229–234

    Article  CAS  Google Scholar 

  • Wu C 1995 Heat shock transcription factors: structure and regulation;Annu. Rev. Cell Dev. Biol. 11 441–469

    Article  CAS  Google Scholar 

  • Xiao H, Perisic O and Lis J T 1991 Cooperative binding ofDrosophila heat shock factor to arrays of a conserved 5 bp unit;Cell 64 585–593

    Article  CAS  Google Scholar 

  • Zandi E, Tran T N, Chamberlain W and Parker C S 1997 Nuclear entry, oligomerization and DNA binding of theDrosophila heat shock transcription factor are regulated by a unique nuclear localization sequence;Genes Dev. 11 1299–1314

    Article  CAS  Google Scholar 

  • Zhong M and Wu C 1996 Proteolytic mapping of heat shock transcription factor domains;Protein Sci. 5 2592–2599

    Article  CAS  Google Scholar 

  • Zimarino V and Wu C 1987 Induction of sequence-specific binding ofDrosophila heat shock activator protein without protein synthesis;Nature (London) 327 727–730

    Article  CAS  Google Scholar 

  • Zimarino V, Wilson S and Wu C 1990 Antibody-mediated activation ofDrosophila heat shock factorin vitro;Science 249 546–549

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry, Molecular Biology and Cell Biology, Rice Institute for Biomedical Research, Northwestern University, 60208, Evanston, IL, USA

    Sanjeev H Satyal & Richard I Morimoto

Authors
  1. Sanjeev H Satyal
    View author publications

    Search author on:PubMed Google Scholar

  2. Richard I Morimoto
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Richard I Morimoto.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Satyal, S.H., Morimoto, R.I. Biochemical events in the activation and attenuation of the heat shock transcriptional response. J. Biosci. 23, 303–311 (1998). https://doi.org/10.1007/BF02936123

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02936123

Keywords