Summary
Heat shock protein gene expression is enhanced by proteotoxic stress, i.e., by conditions favoring protein unfolding. This upregulation of heat shock protein genes is mediated by heat shock transcription factor HSF1. A mechanism, the details of which are still elusive, senses adverse conditions and causes HSF1 to oligomerize and to acquire DNA-binding ability. The DNA-binding form of HSF1 then undergoes further conformational changes that render it transcriptionally competent. The current model in which heat shock protein 70 acts both as sensor of stress and as negative regulator of HSF1 oligomerization as well as alternative models involving additional protein factors are discussed.
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References
Abravaya, K., Philips, 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 temperature. Genes Dev. 5: 2117–2127.
Abravaya, K.A., Myers, M., Murphy, S.R 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.
Amin, J., Ananthan, J. and Voellmy, R. (1988) Key features of heat shock regulatory elements. Mol Cell. Biol. 8: 3761–3769.
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.
Baler, R. (1992) Ph. D. Thesis, University of Miami, Miami, FL.
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.
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 HSF 1. Mol. Cell. Biol. 13: 2486–2496.
Baler, R., Guettouche, T. and Voellmy, R. (1995) On the model of feedback regulation of heat shock gene expression by the shock proteins: Demonstration of heat shock protein 70-containing complexes of unactivated heat shock transcription factor 1. In: W.J. Whelan et al. (eds.): Miami Bio/Technology Short Reports, Vol 6. IRL Press at Oxford University Press, Oxford, p 35.
Beckmann, R.P., Mizzen, L. and Welch, W.J. (1990) Interaction of hsp70 with newly synthesized proteins: implications for protein folding and assembly. Science 248: 850–854.
Bole, D.G., Hendershot, L.M. and Kearney, J.F. (1986) Post-translational associations of immunoglobulin heavy chain binding protein with nascent heavy chains in non-secreting and secreting hybridomas. J. Cell. Biol. 102: 1558–1566.
Bonner, J.J., Heyward, S. and Fackenthal, D.L. (1992) Temperature-dependent regulation of a heterologous transcriptional activation domain fused to yeast heat shock transcription factor. Mol. Cell. Biol. 12: 1021–1030.
Brigelius, R. (1985) Mixed disulfides: biological functions and increase in oxidative stress. In: Oxidative Stress. Academic Press, Inc. London, pp 243–272.
Bruce, J.L., Price, B.D., Coleman, C.N. and Calderwood, S.K. (1993) Oxidative injury rapidly activates the heat shock transcription factor but fails to increase levels of heat shock proteins. Cancer Res. 53: 12–15.
Chen, Y., 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.
Choi, H.-S., Li, B., Lin, Z., Huang, L.E. and Liu, A.Y.-C. (1991) cAMP and cAMP-dependent protein kinase regulate the human heat shock protein 70 gene promoter activity. J. Biol. Chem. 266: 11858–11865.
Clos, J., Westwood, T., Becker, B., Wilson, S., Lambert, K. and Wu, C (1990) Molecular cloning and expression of a hexameric Drosophila heat shock factor subject to negative regulation. Cell 63: 1085–1097.
Collison, M.W., Beidler, D., Grimm, L.M. and Thomas, J. A. (1986) A comparison of protein S-thiolation (protein mixed-disulfide formation) in heart cells treated with t-butyl hydroperoxide or diamide. Biochim. Biophys. Acta 885: 58–67.
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.
Dreano, M., Brochot, J., Myers, A., Cheng-Meyer, C., Rungger, D., Voellmy, R. and Bromley, P. (1986) High-level, heat-regulated synthesis of proteins in eukaryotic cells. Gene 49: 1–8.
Freeman, M.L., Sierra-Rivera, E, Voorhees, G.J., Eisert, D.R. and Meredith, M.J. (1993) Synthesis of hsp70 is enhanced in glutathione-depleted Hep G2 cells. Radiat. Res. 135: 387–393.
Freeman, M.L., Sierra-Rivera, E., Meredith, M.J., Borelli, M.J. and Lepock, J.R. (1995) Formation of protein disulfides, generated by oxidative stress, represent a signal for induction of the stress response. J. Cell. Biochem. 19B: 197.
Goff, S.A. and Goldberg, A.L. (1985) Production of abnormal proteins in E. coli stimulates transcription of Ion and other heat shock genes. Cell 41: 587–595.
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.
Grimm, L.M., Collison, M.W., Fisher, R.A. and Thomas, J.A. (1985) Protein mixed-disulfides in cardiac cells. S-Thiolation of soluble proteins in response to diamide. Biophys. Biochem. Acta 844: 50–54.
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.
Hedge, R.S., Zuo, J., Voellmy, R. and Welch, W.J. (1995) Short-circuiting stress protein expression via a tyrosine kinase inhibitor, herbimycin A. J. Cell. Physiol 165: 186–200.
Hensold, J.O., Hunt, C.R., Calderwood, S.K., Housman, D.E. and Kingston, R.E. (1990) DNA binding of heat shock factor to the heat shock element is insufficient for transcriptional activation in murine erythroleukemia cells. Mol. Cell. Biol. 10: 1600–1608.
Hightower, L.E., Sadis, S.E. and Takenaka, J.M. (1994) Interactions of vertebrate hsc70 and hsp70 with unfolded proteins and peptides. In: R.I. Morimoto, A. Tissieres and C. Georgopoulos (eds): The Biology of Heat Shock Proteins and Molecular Chaperones. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y., pp 179–207.
Hodges, R.S., Sodeck, J., Smillie, L.B. and Jurasek, L. (1972) Tropomyosin: amino acid sequence and coiled-coil structure. Cold Spring Harb. Symp. Quant. Biol. 37: 299–310.
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.
Huang, L.E., Zhang, H., Bae, S.W. and Liu, A.Y.-C. (1994) Thiol reducing reagents inhibit the heat shock response. J. Biol. Chem. 269: 30718–30725.
Hutchison, K.A., Dittmar, K.D., Czar, M.J. and Pratt, W.B. (1994) Proof that hsp70 is required for assembly of the glucocorticoid receptor into a heterocomplex with hsp90. J. Biol. Chem. 269: 5043–5049.
Johnson, J.L. and Toft, D.O. (1995) binding of p23 and hsp90 during assembly with the progesterone receptor. Mol. Endocrin. 9: 670–678.
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.
Kosower, N.S. and Kosower, E.M. (1978) The glutathione status of cells. Internat. Rev. Cytol. 54: 109–160.
Levinson, W., Oppermann, H. and Jackson, J. (1980) Transition series metals and sulfhydryl reagents induce the synthesis of four proteins in eukaryotic cells. Biochim. Biophys. Acta 606: 170–180.
Lindquist, S. (1980) Varying patterns of protein synthesis in Drosophila during heat shock: implications for regulation. Dev. Biol. 77: 463–479.
McLachlan, A.D. and Stewart, M. (1975) Tropomyosin coiled-coil interactions: evidence for an unstaggered structure. J. Mol Biol. 98: 293–304.
Mitchell, J.B. and Russo, A. (1983) Thiols, thiol depletion, and thermosensitivity. Radiat. Res. 95: 471–485.
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.
Nadeau, K., Das, A. and Walsh, C.T. (1993) Hsp90 chaperonins possess ATPase activity and bind heat shock transcription factor and peptidyl prolyl isomerases. J. Biol. Chem. 268: 1479–1487.
Nelson, R.J., Ziegelhofer, T., Nicolet, C., Werner-Washburne, M. and Craig, E.A. (1992) The translation machinery and 70 kd heat shock protein cooperate in protein synthesis. Cell 71: 97–105.
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.
Palleros, D.R., Reid, K.L., Shi, L., Welch, W.J. and Fink, A.L. (1993) ATP-induced protein-hsp70 complex dissociation requires K+ and does not involve ATP hydrolysis. Nature 365: 664–666.
Parker, C.S. and Topol, J. (1984) A Drosophila RNA polymerase II transcription factor binds to the regulatory site of an hspl0 gene. Cell 37: 273–283.
Pratt, W.B. (1992) Control of steroid receptor function and cytoplasmic-nuclear transport by heat shock proteins. BioEssays 14: 841–848.
Price, B.D. and Calderwood, S.K. (1991) Ca2+ is essential for multistep activation of the heat shock factor in permeabilized cells. Mol. Cell. Biol. 11: 3365–3368.
Rabindran, S.K., Giorgi, G., Clos, J. and Wu, C. (1991) Molecular cloning and expression of a human heat shock transcription factor, HSF1. Proc. Natl. Acad. Sci. USA 88: 6906–6910.
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.
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 activity in vivo. Mol. Cell. Biol. 14: 6552–6560.
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.
Scherrer, L.C., Dalman, F.C., Massa, E., Meshinchi, S. and Pratt, W.B. (1990) Structural and functional reconstitution of the glucocorticoid-hsp90 complex. J. Biol. Chem. 265: 21397–21400.
Skibba, J.L., Stadnick, A., Kalbfleisch, J.H. and Powers, R.H. (1989) Effects of hyperthermia on xantine oxidase activity and glutathione levels in the perfused rat liver. J. Biochem. Toxicol. 4: 119–125.
Smith, D.F., Schowalter, D.B., Kost, S.L. and Toft, D.O. (1990) Reconstitution of progesterone receptor with heat shock proteins. Mol. Endocrinol 4: 1704–1711.
Smith, D.F., Stensgard, B.A., Welch, W.J. and Toft, D.O. (1992) Assembly of progesterone receptor with heat shock proteins and receptor activation are ATP-mediated events. J. Biol. Chem. 267: 1350–1356.
Smith, D. (1993) Dynamics of heat shock protein 90 - progesterone receptor binding and the disactivation loop model for steroid receptor complexes. Mol. Endocrinol 7: 1418–1429.
Smith, D.F. and Toft, D.O. (1993) Steroid receptors and their associated proteins. Mol. Endocrinol 7:4–11.
Smith, D.F., Whitesell, L., Nair, S.C., Chen, S., Prapapanich, V and Rimerman, R.A. (1995) Progesterone receptor structure and function altered by geldanamycin, an hsp90-binding agent; submitted.
Sorger, P.K., Lewis, M.J. and Pelham, H.R.B. (1987) Heat shock factor is regulated differently in yeast and HeLa cells. Nature 329: 81–84.
Sorger, P.K. and Nelson, H.C.M. (1989) Trimerization of a yeast transcriptional activator via a coiled-coil motif. Cell 59: 807–813.
Sorger, P. (1990) Yeast heat shock factor contains separable transient and sustained response transcriptional activators. Cell 62: 793–805.
Voellmy, R., Ahmed, A., Schiller, P., Bromley, P. and Rungger, D. (1985) Isolation and functional analysis of a human 70,000 dalton heat shock protein gene segment. Proc. Natl. Acad. Sci. USA 82: 4949–4953.
Voellmy, R. (1994) Transduction of the stress signal and mechanisms of transcriptional regulation of heat shock/stress protein gene expression in higher eukaryotes. Crit. Rev. Eukaryotic Gene Expression 4: 357–401.
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. Structural Biology 1: 605–614.
Welch, W.J. (1992) Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol. Rev. 72: 1063–1081.
Westwood, J.T., Clos, J. and Wu, C. (1991) Stress-induced oligomerization and chromosomal relocalization of heat-shock factor. Nature 353: 822–827.
Whitesell, L., Mimnaugh, E.G., DeCosta, B., Myers, C.E. and Neckers, L.M. (1994) Inhibition of heat shock protein hsp90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc. Natl. Acad. Sci. USA 91: 8324–8328.
Whitesell, L., Cook, PH. and Bagatell, R. (1995) Stable and specific binding of hsp90 by the benzoquinone ansamycins inhibits glucocorticoid receptor function. J. Cell Biochem. 19B: 206.
Wu, B.J., Hunt, C. and Morimoto, R.I. (1985) Structure and expression of the human gene encoding major heat shock protein hsp70. Mol. Cell. Biol. 5: 330–343.
Wu, C. (1984) Two protein-binding sites in chromatin implicated in the activation of heat shock genes. Nature 309: 229–234.
Xiao, H. and Lis, J.T. (1988) Germline transformation used to define key features of heat shock response elements. Science 239: 1139–1142.
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.
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.
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© 1996 Birkhäuser Verlag Basel/Switzerland
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Voellmy, R. (1996). Sensing stress and responding to stress. In: Feige, U., Yahara, I., Morimoto, R.I., Polla, B.S. (eds) Stress-Inducible Cellular Responses. EXS, vol 77. Birkhäuser Basel. https://doi.org/10.1007/978-3-0348-9088-5_9
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