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Heat stress response and heat stress transcription factors

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Abstract

Expression of heat shock protein (HSP)-coding genes is controlled by heat stress transcription factors (Hsfs). They are structurally and functionally conserved throughout the eukaryotic kingdom. In addition to the DNA-binding domain with the helix-turn-helix motif essential for DNA recognition, three functional parts in the C-terminal activator domain were characterized: (i) the HR-A/B region is responsible for oligomerization and activity control, (ii) the nuclear localizing signal (NLS) formed by a cluster of basic amino acid residues which is required and sufficient for nuclear import and (iii) short C-terminal peptide motifs with a central Trp residue (AHA elements). These three parts are indispensible for the activator function. A peculiaritiy of plants is the heat shock-inducible new synthesis of Hsfs. In tomato HsfA1 is constitutively expressed, whereas Hsfs A2 and B1 are heat shock-inducible proteins themselves. We used Hsf knock-out strains of yeast and transient reporter assays in tobacco protoplasts for functional analysis of Hsf-coding cDNA clones and mutants derived from them. HsfA2, which in tomato cell cultures is expressed only after heat shock induction, tends to form large cytoplasmic aggregates together with other HSPs (heat stress granules). In the transient expression assay its relatively low activator potential is evidently due to the inefficient nuclear import. However, the intramolecular shielding of the NLS can be released either by deletion of a short C-terminal fragment or by coexpression with HsfA1, which forms hetero-oligomers with HsfA2.

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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

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Ashburner M and Bonner J J 1979 The induction of gene activity inDrosophila by heat shock;Cell 17 241–254

    Article  CAS  PubMed  Google Scholar 

  • Baler R, Dahl G and Voellmy R 1993 Activation of human heat shock-genes is accompanied by oligomerisation, modification and rapid translocation of heat shock transcription factor;Mol. Cell. Biol. 13 2486–2496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baler R, Welch W J and Voellmy R 1992 Heat shock gene regulation by nascent polypeptides and denatured proteins—Hsp 70 as a potential autoregulatory factor;J. Cell Biol. 117 1151–1159

    Article  CAS  PubMed  Google Scholar 

  • Baler R, Zou J and Voellmy R 1996 Evidence for a role of Hsp70 in the regulation of the heat shock response in mammalian cells;Cell Stress Chap. 1 33–39

    Article  CAS  Google Scholar 

  • Beckmann R P, Lovett M and Welch W J 1992 Examining the function and regulation of hsp70 in cells subjected to metabolic stress;J. Cell Biol. 117 1137–1150

    Article  CAS  PubMed  Google Scholar 

  • Bensaude O, Pinto M, Dubois M-F, Trung N V and Morange M 1990 Protein denaturation during heat shock and related stress; inStress proteins (eds) M J Schlesinger, G Santoro and E Garaci (Berlin: Springer) Chapter 8, pp 89–99

    Chapter  Google Scholar 

  • Bharadwaj S, Hnatov A, Ali A and Ovsenek N 1998 Induction of the DNA-binding and transcriptional activities of heat shock factor 1 is uncoupled inXenopus oocytes;BBA Mol. Cell Res. 1402 79–85

    CAS  Google Scholar 

  • Bienz M and Pelham H R B 1987 Mechanisms of heat-shock gene activation in higher eukaryotes;Adv. Genet. 24 31–72

    Article  CAS  PubMed  Google Scholar 

  • Boorstein W R and Craig E A 1990 Transcriptional regulation of SSA3, and HSP70 gene fromSaccharomyces cerevisiae;Mol. Cell. Biol. 10 3262–3267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boscheinen O, Lyck R, Queitsch C, Treuter E, Zimarino V and Scharf K-D 1997 Heat stress transcription factors from tomato can functionally replace HSF1 in the yeastSaccharomyces cerevisiae;Mol. Gen. Genet. 255, 322–331

    Article  CAS  PubMed  Google Scholar 

  • Brown J L, North S and Bussey H 1993 SKN7, a yeast multicopy suppressor of a mutation affecting cell wall beta-glucan assembly, encodes a product with domains homologous to prokaryotic 2-component regulators and to heat shock transcription factors;J. Bacteriol. 175 6908–6915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bukau B 1993 Regulation of theEscherichia coli heat-shock response;Mol. Microbiol. 9 671–680

    Article  CAS  PubMed  Google Scholar 

  • Bush K T, Goldberg A L and Nigam S K 1997 Proteasome inhibition leads to a heat-shock response, induction of endoplasmic reticulum chaperones and thermotelerance;J. Biol. Chem. 272 9086–9092

    Article  CAS  PubMed  Google Scholar 

  • Chen Y Q, Barlev N A, Westergaard O and Jakobsen B K (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chu B, Soncin F, Price B D, Stevenson M A and Calderwood S K 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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;J. Biol. Chem. 271 3335–3358

    Article  Google Scholar 

  • Cox J S and Walter P 1996 A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response;Cell 87 391–404

    Article  CAS  PubMed  Google Scholar 

  • Crick F H C 1953 The packaging of α-helices: simple coiled-coils;Acta Crystallogr. 6 689–697

    Article  CAS  Google Scholar 

  • Czarnecka-Verner E, Yuan C-X, Fox P C and Gurley W B 1995 Isolation and characterization of six heat shock transcription factor cDNA clones from soybean;Plant Mol. Biol. 29 37–51

    Article  CAS  PubMed  Google Scholar 

  • Czarnecka-Verner E, Yuan C-X, Nover L, Scharf K-D, Englich G and Gurley W B 1998 Plant heat shock transcription factors: positive and negative aspects of regulation;Acta Physiol. Plant (in press)

  • Damberger F F, Pelton J G, Harrison C J, Nelson H C M and Wemmer D E 1994 Solution structure of the DNA-binding domain of the heat shock transcription factor determined by multidimensional heteronuclear magnetic resonance spectroscopy;Protein Sci. 3 1806–1821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Danese P N and Silhavy T J 1997 The sigma(E) and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes inEscherichia coli;Genes Dev. 11 1183–1193

    Article  CAS  PubMed  Google Scholar 

  • DeLasPenas A, Connolly L and Gross C A 1997 The sigma(E)-mediated response to extracytoplasmic stress inEscherichia coli is transduced by RseA and RseB, two negative regulators of sigma(E);Mol. Microbiol. 24 373–385

    Article  CAS  Google Scholar 

  • DiDomenico B J, Bugaisky G E and Lindquist S 1982 The heat shock response is self-regulated at both the transcriptional and posttranscriptional levels;Cell 31 593–603

    Article  CAS  PubMed  Google Scholar 

  • Dingwall C and Laskey R A 1991 Nuclear targeting sequences—a consensus?;Trends Biochem. Sci. 16 478–481

    Article  CAS  PubMed  Google Scholar 

  • Drysdale C M, Jackson B M, McVeigh R, Klebanow E R, Bai Y, Kokubo T, Swanson M, Nakatani Y, Weil P A and Hinnebusch A G 1998 The Gcn4p activation domain interacts specificallyin vitro with RNA polymerase II holoenzyme, TFIID and the Adap-Gcn5p coactivator complex;Mol. Cell. Biol. 18 1711–1724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubois M F, Hovanessian A G and Bensaude O 1991 Heat-shock-induced denaturation of proteins characterization of the insolubilization of the interferon-induced p68 kinase;J. Biol. Chem. 266 9707–9711

    CAS  PubMed  Google Scholar 

  • Farkas T, Kutskova Y A and Zimarino V 1998 Intramolecular repression of mouse heat shock factor 1;Mol. Cell Biol. 18 906–918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fiorenza M T, Farkas T, Dissing M, Kolding D and Zimarino V 1995 Complex expression of murine heat shock transcription factors;Nucleic Acids Res. 23 467–474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forreiter C and Nover L 1998 Heat induced stress proteins and the concept of molecular chaparones;J. Biosci. 23 287–302

    Article  CAS  Google Scholar 

  • Frankel A D and Kim P S 1991 Modular structure of transcription factors: Implications for gene regulation;Cell 65 717–719

    Article  CAS  PubMed  Google Scholar 

  • Gagliardi D, Breton C, Chaboud A, Vergne P and Dumas C 1995 Expression of heat shock factor and heat shock protein 70 genes during maize pollen development;Plant Mol. Biol. 29 841–856

    Article  CAS  PubMed  Google Scholar 

  • Gallo G J, Prentice H and Kingston R E 1993 Heat shock factor is required for growth at normal temperatures in the fission yeastSchizosaccharomyces pombe;Mol. Cell. Biol. 13 749–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gamer J, Multhaup G, Tomoyasu T, McCarthy J S, Rüdiger S, Schönfeld H J, Schirra C, Bujard H and Bukau B 1996 A cycle of binding and release of the DnaK, DnaJ and GrpE chaperones regulates the activity of theEscherichia coli heat shock transcription factor sigma 32;EMBO J. 15 607–617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goff S A and Goldberg A L 1987 An increased content of protease La, the lon gene product, increases protein degradation and blocks growth inEscherichia coli;J. Biol. Chem. 262 4508–4515

    CAS  PubMed  Google Scholar 

  • Goodson M L and Sarge K D 1995 Regulated expression of heat shock factor 1 isoforms with distinct leucine zipper arrays via tissue-dependent alternative splicing;Biochem. Biophys. Res. Commun. 211 943–949

    Article  CAS  PubMed  Google Scholar 

  • Goodson M L, Park-Sarge O K and Sarge K D 1995 Tissue-dependent expression of heat shock factor 2 isoforms with distinct transcriptional activities;Mol. Cell. Biol. 15 5288–5293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Görlich D and Mattaj I W 1996 Nucleocytoplasmic transport;Science 2271 1513–1518

    Article  Google Scholar 

  • Grant C M, Firoozan M and Tuite M F 1989 Mistranslation induces the heat-shock response in the yeastSaccharomyces cerevisiae;Mol. Microbiol. 3 215–220

    Article  CAS  PubMed  Google Scholar 

  • Green M, Schuetz T J, Sullivan E K and Kingston R E 1995 The heat shock-responsive domain of human HSF1 that regulates transcription activation domain function;Mol. Cell. Biol. 15 3354–3362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison C J, Bohm A A and Nelson H C M 1994 Crystal structure of the DNA binding domain of the heat shock transcription factor;Science 263 224–227

    Article  CAS  PubMed  Google Scholar 

  • Hegde R S, Zuo J, Voellmy R and Welch W J 1995 Short circuiting stress protein expression via a tyrosine kinase inhibitor, herbimycin;Am. J. Cell Physiol. 165 186–200

    Article  CAS  Google Scholar 

  • Hendrick J P, Langer T, Davis T A, Hartl F U and Wiedmann M 1993 Control of folding and membrane translocation by binding of the chaperone DnaJ to nascent polypeptides;Proc. Natl. Acad. Sci. USA 90 10216–10220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hightower L E and White F P 1981 Cellular response to stress: Comparison of a family of 71–73 kilodalton proteins rapidly synthesized in rat tissue slices and canavanine-treated cells in culture;J. Cell. Physiol. 108 261–275

    Article  CAS  PubMed  Google Scholar 

  • Hiromi Y and Hotta Y 1985 Actin gene mutations inDrosophila; Heat shock activation in the direct flight muscles;EMBO J. 4 1681–1687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoj A and Jakobsen B K 1994 A short element required for turning off heat shock transcription factor: Evidence that phosphorylation enhances deactivation;EMBO J. 13 2617–2624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hübel A and Schöffl F 1994 Arabidopsis heat shock factor: Isolation and characterization of the gene and the recombinant protein;Plant Mol. Biol. 26 353–362

    Article  PubMed  Google Scholar 

  • Hübel A, Lee J H, Wu C and Schöffl F 1995Arabidopsis heat shock factor is constitutively active inDrosophila and human cells;Mol. Gen. Genet. 248 136–141

    Article  PubMed  Google Scholar 

  • Hurt E C 1996 Importins/karyopherins meet nucleoporins;Cell 84 509–515

    Article  CAS  PubMed  Google Scholar 

  • Imamoto N, Matsuoka Y, Kurihara T, Kohno K, Miyagi M, Sakiyama F, Okada Y, Tsunasawa S and Yoneda Y 1992 Antibodies against 70-kD heat shock cognate protein inhibit mediated nuclear import of karyophilic proteins;J. Cell Biol. 119 1047–1061

    Article  CAS  PubMed  Google Scholar 

  • Jakobsen B K and Pelham H R B 1991 A conserved heptapeptide restrains the activity of the yeast heat shock transcription factor;EMBO J. 10 369–375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jurivich D H, 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  PubMed  Google Scholar 

  • Kadonaga J T 1998 Eukaryotic transcription: An interlaced network of transcription factors and chromatin-modifying machines;Cell 92 307–313

    Article  CAS  PubMed  Google Scholar 

  • Kamano H and Klempnauer K H 1997 c-Myb and cyclin d1 mediate heat shock element dependent activation of the human hsp70 promoter;Oncogene 14 1223–1229

    Article  CAS  PubMed  Google Scholar 

  • Kampinga H H 1993 Thermotolerance in mammalian cells—Protein denaturation and aggregation and stress proteins;J. Cell Sci. 104 11–17

    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  PubMed  Google Scholar 

  • Kanemori M, Nishihara K, Yanagi H and Yura T 1997 Synergistic roles of HslVU and other ATP-dependent proteases in controlling in vivo turnover of sigma 32 and abnormal proteins inEscherichia coli;J. Bacteriol. 179 7219–7225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawahara T, Yanagi H, Yura T and Mori K 1997 Endoplasmic reticulum stress-induced mRNA splicing permits synthesis of transcription factor Hac1p/Ern4p that activates the unfolded protein response;Mol. Cell. Biol. 8 1845–1862

    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  PubMed  Google Scholar 

  • Kim D, Ouyang H and Li G C 1995 Heat shock protein hsp70 accelerates the recovery of heat-shocked mammalian cells through its modulation of heat shock transcription factor HSF1;Proc. Natl. Acad. Sci. USA 92 2126–2130

    Article  CAS  PubMed  PubMed Central  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  PubMed  PubMed Central  Google Scholar 

  • Knauf U, Newton E M, Kyriakis J and Kingston R E 1996 Repression of human heat shock factor1 activity at control temperature by phosphorylation;Genes Dev. 10 2782–2793

    Article  CAS  PubMed  Google Scholar 

  • Krems B, Charizanis C and Entian K-D 1995 Mutants ofSaccharomyces cerevisiae sensitive to oxidative and osmotic stress;Curr. Genet. 27 427–434

    Article  CAS  PubMed  Google Scholar 

  • Langer T, Lu C, Echols H, Flanagan J, Hayer M K and Hartl F-U 1992 Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone-mediated protein folding;Nature (London) 356 683–689

    Article  CAS  Google Scholar 

  • Lee D H and Goldberg A L 1998 Proteasome inhibitors cause induction of heat shock proteins and trehalose, which together confer thermotolerance inSaccharomyces cerevisiae;Mol. Cell. Biol. 18 30–38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee J H, Hubel A and Schöffl F 1995 Derepression of the activity of genetically engineered heat shock factor causes constitutive synthesis of heat shock proteins and increased thermotolerance in transgenicArabidopsis;Plant J. 8 603–612

    Article  CAS  PubMed  Google Scholar 

  • Lee K-J and Hahn G M 1988 Abnormal protein as the trigger for the induction of stress responses: Heat, diamide and sodium arsenite;J. Cell. Physiol. 136 411–420

    Article  CAS  PubMed  Google Scholar 

  • Lee T I and Young R A 1998 Regulation of gene expression by TBP-associated proteins;Genes Dev. 12 1398–1408

    Article  CAS  PubMed  Google Scholar 

  • Lee Y L and Dewey W C 1987 Effect of cycloheximide or puromycin on induction of thermotolerance by sodium arsenite in Chinese hamster ovary cells: Involvement of heat shock proteins;J. Cell. Physiol. 132 41–48

    Article  CAS  PubMed  Google Scholar 

  • Leppa S, Pirkkala L, Saarento H, Sarge K D and Sistonen L 1997 Overexpression of HSF2-beta inhibits hemin-induced heat shock gene expression and erythroid differentiation in K562 cells;J. Biol. Chem. 272 15293–15298

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Liu X D, Liu P C 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  PubMed  PubMed Central  Google Scholar 

  • Lovejoy B, Choe S, Cascio D, McRorie D K, DeGrado W F and Eisenberg D 1993 Crystal structure of a synthetic triple-stranded α-helical bundle;Science 259 1288–1293

    Article  CAS  PubMed  Google Scholar 

  • Lyck R, Harmening U, Höhfeld I, Treuter E Scharf K-D and Nover L 1997 Intracellular distribution and identification of the nuclear localization signals of two plant heat-stress transcription factors;Planta 202 117–125

    Article  CAS  PubMed  Google Scholar 

  • McDuffee A T, Senisterra G Huntley S, Lepock J R, Sekhar K R, Meredith M J, Borrelli M J, Morrow J D and Freeman M L 1997 Proteins containing non-native disulfide bonds generated by oxidative stress can act as signals for the induction of the heat shock response;J. Cell. Physiol. 171 143–151

    Article  CAS  PubMed  Google Scholar 

  • McKenzie S L and Meselson M 1977 Translationin vitro ofDrosophila heat shock messages;J. Mol. Biol. 117 279–283

    Article  CAS  PubMed  Google Scholar 

  • McMillan D R, Xiao X Z, Shao L, Graves K and Benjamin I J 1998 Targeted disruption of heat shock transcription factor 1 abolishes thermotolerance and protection against heat-inducible apoptosis;J. Biol. Chem. 273 7523–7528

    Article  CAS  PubMed  Google Scholar 

  • Mercier P A, Foksa J, Ovsenek N and Westwood J T 1997 Xenopus heat shock factor 1 is a nuclear protein before heat stress;J. Biol. Chem. 272 14147–14151

    Article  CAS  PubMed  Google Scholar 

  • Mifflin L C and Cohen R E 1994a Characterization of denatured protein inducers of the heat shock (stress) response inXenopus laevis oocytes;J. Biol. Chem. 269 15710–15717

    CAS  PubMed  Google Scholar 

  • Mifflin L C and Cohen R E 1994b Hsc70 moderates the heat shock (stress) response inXenopus laevis oocytes and binds to denatured protein inducers;J. Biol. Chem. 269 15718–15723

    CAS  PubMed  Google Scholar 

  • Milarski K L and Morimoto R I 1986 Expression of human HSP70 during the synthetic phase of the cell cycle;Proc. Natl. Acad. Sci. USA 83 9517–9522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Missiakas D, Mayer M P, Lemaire M, Georgopoulos C and Raina S 1997 Modulation of theEscherichia coli sigma(E) (RpoE) heat-shock transcription-factor activity by the RseA, RseB and RseC proteins;Mol. Microbiol. 24 355–371

    Article  CAS  PubMed  Google Scholar 

  • Missiakas D and Raina S 1997a Protein folding in the bacterial periplasm;J. Bacteriol. 179 2465–2471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Missiakas D and Raina S 1997b Signal transduction pathways in response to protein misfolding in the extracytoplasmic compartments ofE. coli: role of two new phsophoprotein phosphatases PrpA and PrpB;EMBO J. 16 1670–1685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morgan B A, Banks G R, Toone W M, Raitt D, Kuge S and Johnson L H 1997 The Skn7 response regulator controls gene expression in the oxidative stress response of the budding yeastSaccharomyces cerevisiae, EMBO J 16 1035–1044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mori K, Sant A, Kohno K, Normington K, Gething M J and Sambrook J F 1992 A 22 bp cis-acting element is necessary and sufficient for the induction of the yeast KAR2 (BiP) gene by unfolded proteins;EMBO J. 11 2583–2593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murphy S P, Gorzowski J J, Sarge K D and Phillips B 1994 Characterization of constitutive HSF2 DNA-binding activity in mouse embryonal carcinoma cells;Mol. Cell. Biol. 14 5309–5317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nair S C, Toran E J, Rimerman R A, Hyermstad S, Smithgall T E and Smith D F 1996 A pathway of multi-chaperone interactions common to diverse regulatory proteins: estrogen receptor, Fes tyrosine kinase, heat shock transcription factor Hsf 1 and the aryl hydrocarbon receptor;Cell Stress Chap. 1 237–250

    Article  CAS  Google Scholar 

  • Nakahigashi K, Kanemori M, Morita M, Yanagi H and T Yura 1998 Conserved function and regulation ofσ 32 homologues in Gram-negative bacteria;J. Biosci. 23 407–414

    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  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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  PubMed  PubMed Central  Google Scholar 

  • Newton E M, Knauf U, Green M and Kingston R E 1996 The regulatory domain of human heat shock factor 1 is sufficient to sense heat stress;Mol. Cell. Biol. 16 839–846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen V T and Bensaude O 1994 Increased thermal aggregation of proteins in ATP-depleted mammalian cells;Eur. J. Biochem. 220 239–246

    Article  CAS  PubMed  Google Scholar 

  • Nieto-Sotelo J, Wiederrecht G, Okuda A and Parker C S 1990 The yeast heat shock transcription factor contains a transcriptional activation domain whose activity is repressed under nonshock conditions;Cell 62 807–817

    Article  CAS  PubMed  Google Scholar 

  • Nikawa J Sugiyama M, Hayashi K and Nakashima A 1997 Suppression of theSaccharomyces cerevisiae hacl/ire15 mutation by yeast genes and human cDNAs;Gene 201 5–10

    Article  CAS  PubMed  Google Scholar 

  • Nover L 1987 Expression of heat shock genes in homologous and heterologous systems;Enzyme Microb. Technol. 9 130–144

    Article  CAS  Google Scholar 

  • Nover L (ed.) 1991Heat shock response (Boca Raton: CRC Press)

    Google Scholar 

  • Nover L, Neumann D and Scharf K-D 1990Heat Shock and other Stress Response Systems of Plants Res Problems Cell Diff. (Berlin: Springer)

    Google Scholar 

  • Nover L and Scharf K-D 1997 Heat stress proteins and transcription factors;Cell. Mol. Life Sci. 53 80–103

    Article  CAS  PubMed  Google Scholar 

  • Nover L, Scharf K-D, Gagliardi D, Vergne P, Czamecka-Verner E and Gurley WB 1996 The Hsf world: Classification and properties of plant heat stress transcription factors;Cell Stress Chap. 1 215–223

    Article  CAS  Google Scholar 

  • Nover L, Scharf K-D and Neumann D 1989 Cytoplasmic heat shock granules are formed from precursor particles and are associated with a specific set of mRNAs;Mol. Cell. Biol. 9 1298–1308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nunes S L and Calderwood S K 1995 Heat shock factor-1 and the heat shock cognate 70 protein associate in high molecular weight complexes in the cytoplasm of NIH-3T3 cells;Biochem. Biophys. Res. Commun. 213 1–6.

    Article  CAS  PubMed  Google Scholar 

  • Ohno M, Fornerod M and Mattaj I W 1998 Nucleocytoplasmic transport: The last 200 nanometers;Cell 92 327–336

    Article  CAS  PubMed  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  PubMed  PubMed Central  Google Scholar 

  • Palleros D R, Welch W J and Fink A L 1991 Interactions of Hsp70 with unfolded proteins: Effects of temperature and nucleotides on the kinetics of binding;Proc. Natl. Acad. Sci. USA 88 5719–5723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pelham H R B and Bienz M 1982 A synthetic heat-shock promoter element confers heat-inducibility on the Herpes simplex virus thymidine kinase gene;EMBO J. 1 1473–1477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pinto M, Morange M and Bensaude O 1991 Denaturation of proteins during heat shock—In vivo recovery of solubility and activity of reporter enzymes;J. Biol. Chem. 266 13941–13946

    CAS  PubMed  Google Scholar 

  • Pogliano J, Lynch A S, Belin D, Lin E C C and Beckwith J 1997 Regulation ofEscherichia coli cell envelope proteins involved in protein folding and degradation by the Cpx two-component system;Genes Dev. 11 1169–1182

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  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 DNBA-binding activity in vivo;Mol. Cell. Biol. 14 6552–6560

    Article  CAS  PubMed  PubMed Central  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  PubMed  PubMed Central  Google Scholar 

  • Ritossa F 1962 A new puffing pattern induced by temperature shock and DNP inDrosophila;Experientia 18 571–573

    Article  CAS  Google Scholar 

  • Sandaltzopoulos R and Becker P B 1998 Heat shock factor increases the reinitiation rate from potentiated chromatin templates;Mol. Cell. Biol. 18 361–367

    Article  CAS  PubMed  PubMed Central  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  PubMed  PubMed Central  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  PubMed  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  PubMed  Google Scholar 

  • Scharf K-D, Heider H, Höhfeld I, Lyck R, Schmidt E and Nover L 1998 The tomato Hsf system: HsfA2 needs interaction with HsfA1 for efficient nuclear import and may be localized in cytoplasmic heat stress granules;Mol. Cell. Biol. 18 2240–2251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scharf K-D, Materna T, Treuter E and Nover L 1994 Heat stress promoters and transcription factors; inPlant promoters and transcription factors (ed.) L Nover (Berlin: Springer Verlag) pp 121–158

    Google Scholar 

  • Scharf K-D, Rose S, Thierfelder J and Nover L 1993 Two cDNAs for tomato heat stress transcription factors;Plant Physiol. 102 1355–1356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scharf K-D, Rose S, Zott W, Schoeffl F and Nover L 1990 Three tomato genes code for heat stress transcription factors with a region of remarkable homology to the DNA-binding domain of the yeast HSF;EMBO J. 9 4495–4501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schlesinger M J, Ashburner M and Tissieres A (eds) 1982Heat shock from bacteria to man (New York: Cold Spring Harbor Lab Press)

    Google Scholar 

  • Schröder H, Langer T, Hartl F-U and Bukau B 1993 DnaK, DnaJ and GrpE form a cellular chaperone machinery capable of repairing heat-induced protein damage;EMBO J. 12 4137–4144

    Article  PubMed  PubMed Central  Google Scholar 

  • 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  PubMed  PubMed Central  Google Scholar 

  • Schultheiss J, Kunert O, Gase U, Scharf K-D, Nover L and Rüterjans H 1996 Solution structure of the DNA-binding domain of the tomato heat stress transcription factor HSF24;Eur. J. Biochem. 236 911–921

    Article  CAS  PubMed  Google Scholar 

  • Sheldon L A and Kingston R E 1993 Hydrophobic coiled-coil domains regulate the subcellular localization of human heat shock factor-2;Genes Dev. 7 1549–1558

    Article  CAS  PubMed  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  PubMed  PubMed Central  Google Scholar 

  • Shi Y G and Thomas J O 1992 The transport of proteins into the nucleus requires the 70 kilodalton heat shock protein or its cytosolic cognate;Mol. Cell. Biol. 12 2186–2192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shulga N, Roberts P, Gu Z Y, Spitz L, Tabb M M, Nomura M and Goldfarb D S 1996 In vivo nuclear transport kinetics inSaccharomyces cerevisiae—a role for heat shock protein 70 during targeting and translocation;J. Cell. Biol. 135 329–339

    Article  CAS  PubMed  Google Scholar 

  • Sidrauski C, Cox J S and Walter P 1996 tRNA ligase is required for regulated tRNA splicing in the unfolded protein response;Cell 87 405–413

    Article  CAS  PubMed  Google Scholar 

  • Sidrauski C and Walter P 1997 The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response;Cell 90 1031–1039

    Article  CAS  PubMed  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  PubMed  PubMed Central  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 erythreoleukemia cells;Mol. Cell. Biol. 12 4104–4111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Stege G J J, Li G C, Li L, Kampinga H H and Konings A W T 1994 On the role of Hsp72 in heat-induced intranuclear protein aggregation;Int. J. Hyperthermia 10 659–674

    Article  CAS  PubMed  Google Scholar 

  • Stone D E and Craig E A 1990 Self-regulation of 70-kilodalton heat shock proteins inSaccharomyces cerevisiae;Mol. Cell. Biol. 10 1622–1632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Struhl K 1996 Chromatin structure and RNA polymerase II connection—Implications for transcription;Cell 84 179–182

    Article  CAS  PubMed  Google Scholar 

  • Struhl K and Moqtaderi Z 1998 The TAFs in the HAT;Cell 94 1–4

    Article  CAS  PubMed  Google Scholar 

  • Stump D G, Landsberger N and Wolffe A P 1995 The cDNA encodingXenopus laevis heat-shock factor 1 (XHsf1)—nucleotide and deduced amino-acid sequences and properties of the encoded protein;Gene 160 207–211

    Article  CAS  PubMed  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  PubMed  PubMed Central  Google Scholar 

  • Tanabe M, Nakai A, Kawazoe Y and Nagata K 1997 Different thresholds in the responses of two heat shock transcription factors, HSF1 and HSF3;J. Biol. Chem. 272 15389–15395

    Article  CAS  PubMed  Google Scholar 

  • Thomas G P and Mathews M B 1984 Alterations of transcription and translation in HeLa cells exposed to amino acid analogs;Mol. Cell. Biol. 4 1063–1072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tissieres A, Mitchell H K and Tracy U M 1974 Protein synthesis in salivary glands of D melanogaster Relation to chromosome puffs;J Mol. Biol. 84 389–398

    Article  CAS  PubMed  Google Scholar 

  • Treuter E, Nover L, Ohme K and Scharf K-D 1993 Promoter specificity and deletion analysis of three heat stress transcription factors of tomato;Mol. Gen. Genet. 240 113–125

    Article  CAS  PubMed  Google Scholar 

  • Uesugi M, Nyanguile O, Lu H, Levine A J and Verdine G L 1997 Induced alpha helix in the VP16 activation domain upon binding to a human TAF;Science 277 1310–1313

    Article  CAS  PubMed  Google Scholar 

  • Vuister G W, Kim S-J, Orosz A, Marquardt J, Wu C and Bax A 1994 Solution structure of the DNA-binding domain ofDrosophila heat shock transcription factor;Nature Struct Biol 1 605–614

    Article  CAS  PubMed  Google Scholar 

  • Werner-Washburne M, Becker J, Kosic-Smithers J and Craig E A 1989 Yeast Hsp70 RNA levels vary in response to the physiological status of the cell;J. Bacteriol. 171 2680–2688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Westwood J T and Wu C 1993 Activation ofDrosophila heat shock factor—Conformational change associated with a monomer-to-trimer transition;Mol. Cell. Biol. 13 3481–3486

    Article  CAS  PubMed  PubMed Central  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  PubMed  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  PubMed  PubMed Central  Google Scholar 

  • Wu C 1995 Heat stress transcription factors;Annu. Rev. Cell Biol,11, 441–469

    Article  CAS  Google Scholar 

  • Xia W L and Voellmy R 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

    Article  CAS  PubMed  Google Scholar 

  • Xiao H, Friesen J D and Lis J T 1994 A highly conserved domain of RNA polymerase II shares a functional element with acidic activation domains of upstream transcription factors;Mol. Cell. Biol. 14 7507–7516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao N Q and DeFranco D B 1997 Overexpression of unliganded steroid receptors activates endogenous heat shock factor;Mol. Endocrinol. 11 1365–1374

    Article  CAS  PubMed  Google Scholar 

  • Yang J and Defranco D B 1994 Differential roles of heat shock protein 70 in thein vitro nuclear import of glucocorticoid receptor and simian virus 40 large tumor antigen;Mol. Cell. Biol. 14 5088–5098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan C-X, Czarnecka-Verner E and Gurley W B 1997 Expression of human heat shock transcription factors 1 and 2 in HeLa cells and yeast;Cell Stress Chap. 2 263–275

    Article  CAS  Google Scholar 

  • Yura T 1996 Regulation and conservation of the heat-shock transcription factor sigma 32;Genes Cells 1 277–284

    Article  CAS  PubMed  Google Scholar 

  • Zandi E, Tran T N T, 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  PubMed  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  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Scharf, KD., Höhfeld, I. & Nover, L. Heat stress response and heat stress transcription factors. J. Biosci. 23, 313–329 (1998). https://doi.org/10.1007/BF02936124

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