Abstract
Major alterations in genetic activity have been observed in every organism after exposure to abnormally high temperatures. This phenomenon, called the heat shock response, was discovered in the fruit flyDrosophila. Studies with this organism led to the discovery of the heat shock proteins, whose genes were among the first eukaryotic genes to be cloned. Several of the most important aspects of the regulation of the heat shock response and of the functions of the heat shock proteins have been unraveled inDrosophila.
Similar content being viewed by others
Literatur
Amin, J., Mestril, R., Lawson, R., Klapper, H., and Voellmy, R., The heat shock consensus sequence is not sufficient for hsp70 gene expression inDrosophila melanogaster. Molec. cell Biol.5 (1985) 197–203.
Amin, J., Ananthan, J., and Voellmy R., Key features of heat shock regulatory elements. Molec. cell Biol.8 (1988) 3761–3769.
Arrigo, A.-P., Acetylation and methylation patterns of core histones are modified after heat or arsenite treatment ofDrosophila melanogaster tissue culture cells. Nucl. Acids Res.11 (1983) 1389–1404.
Arrigo, A.-P., Cellular localization of hsp23 duringDrosophila development and subsequent heat shock. Devl Biol.122 (1987) 39–48.
Arrigo, A.-P., Fakan, S., and Tissières, A., Localization of the heat shock induced proteins inDrosophila melanogaster tissue culture cells. Devl Biol.78 (1980) 86–103.
Ashburner, M., Patterns of puffing activity in the salivary gland chromosomes ofDrosophila V. Responses to environmental treatments. Chromosoma31 (1970) 356–376.
Beermann, W., Nuclear differentiation and functional morphology of chromosomes. Cold Spring Harbor Symp. Quant. Biol.21 (1956) 217–232.
Berger, E. M., Vitek, M. P., and Morganelli, C. M., Transcript length heterogeneity at the small heat shock genes ofDrosophila. J. molec Biol.186 (1985) 137–148.
Biessmann, H., Falkner, F.-G., Saumweber, H., and Walter, M. F., Disruption of vimentin cytoskeleton may play a role in heat shock response, in: Heat Shock: From Bacteria to Man, pp. 275–282. Eds M. Schlesinger, M. Ashburner and A. Tissières. Cold Spring Harbor Laboratory Press 1982.
Buzin, C. H., and Bournias-Vardiabasis, N., Teratogens induce a subset of small heat shock proteins inDrosophila primary embryonic cell cultures. Proc. natl Acad. Sci. USA81 (1984) 4075–4079.
Chomyn, A., and Mitchell, H. K., Synthesis of the 84,000 dalton protein in normal and heat shockedDrosophila melanogaster cells as detected by specific antibody. Insect Biochem.12 (1982) 105–114.
Clos, J., Westwood, J. T., Becker, P. B., Wilson, S., Lambert, K., and Wu, C., Molecular cloning and expression of a hexamericDrosophila heat shock factur subject to negative regulation. Cell63 (1990) 1085–1097.
Cohen, R. S., and Meselson, M., Inducible transcription and puffing inDrosophila melanogaster transformed with hsp70-phage λ hybrid heat shock genes. Proc. natl Acad. Sci. USA81 (1984) 5509–5513.
Cohen, R. S. and Meselson, M., Separate regulatory elements for the heat-inducible and ovarian expression of theDrosophila hsp26 gene. Cell43 (1985) 737–746.
Corces, V., Holmgren, R., Freund, R., Morimoto, R., and Meselson, M., Four heat shock proteins ofDrosophila melanogaster coded within a 12-kilobase region in chromosome, subdivision 67B. Proc. natl Acad. Sci. USA77 (1980) 5390–5393.
Craig, E. A., and McCarthy, B. J., FourDrosophila heat shock genes at 67B: characterization of recombinant plasmids. Nucl. Acids Res.8 (1980) 4441–4457.
DiDomenico, B. J., Bugaisky, G. E., and Lindquist, S., The heat shock response is self-regulated at both the transcriptional and post-transcriptional levels. Cell31 (1982) 593–603.
DiDomenico, B. J., Bugaisky, G. E., and Lindquist, S., Heat shock and recovery are mediated by different translation mechanisms. Proc. natl Acad. Sci. USA79 (1982) 6181–6185.
Dudler, R., and Travers, A. A., Upstream elements necessary for optimal function of the hsp70 promoter in transformed flies. Cell38 (1984) 391–398.
Ellgaard, E. G., and Clever, U., RNA metabolism during puff induction inDrosophila melanogaster. Chromosoma36 (1971) 60–78.
Ellis, R. J., and van der Vies, S. M., Molecular chaperones. A. Rev. Biochem.60 (1991) 321–347.
Glaser, R. L., Wolfner, M. F., and Lis, J. T., Spatial and temporal pattern of hsp26 expression during normal development. EMBO J.5 (1986) 747–754.
Glaser, R. L., and Lis, J. T., Multiple, compensatory regulatory elements specify spermatocyte-specific expression of theDrosophila melanogaster hsp26 gene. Molec. cell Biol.10 (1990) 131–137.
Gloor, H., Phanokopie-Versuche mit Äther anDrosophila. Rev. Suisse Zool.54 (1947) 637–712.
Glover, C. V. C., Heat-shock effects on protein phosphorylation inDrosophila, in: Heat Shock: From Bacteria to Man, pp. 227–234. Eds M. J. Schlesinger, M. Ashburner and A. Tissières. Cold Spring Harbor Laboratory Press 1982.
Goldschmidt, R., Gen und Ausseneigenschaft. 1. (Untersuchung anDrosophila). Z. Indukt. Abstammungs Vererbungsl.69 (1935) 38–131.
Grunstein, M., Histone function in transcription. A. Rev. Cell Biol.6 (1990) 643–678.
Hackett, R. W., and Lis, J. T., DNA sequence analysis reveals extensive homologies of regions preceding, hsp70 and αβ heat shock genes inDrosophila melanogaster. Proc. natl Acad. Sci. USA78 (1981) 6196–6200.
Hackett, R. W., and Lis, J. T., Localization of the hsp83 RNA within 3292 nucleotide sequence from the 63B heat shock locus ofD. melanogaster. Nucl. Acids Res.11 (1983) 7011–7030.
Hightower, L. E., Heat shock, stress proteins, chaperones and proteotoxicity. Cell66 (1991) 191–197.
Hiromi, Y., Okamoto, H., Gehring, W. J., and Hotta, Y., Gremline transformation withDrosophila mutant actin genes induces constitutive expression of heat shock genes. Cell44 (1986) 293–301.
Hoffman, E. P., Gerring, S. L., and Corces, V. G., The ovarian, ecdysterone, and heat-shock-responsive promoters of theDrosophila melanogaster hsp27 gene react very differently to perturbations of DNA sequence. Molec. cell Biol.7 (1987) 973–981.
Holmgren, R., Livak, K., Morimoto, R., Freund, R., and Meselson, M., Studies of cloned sequences from fourDrosophila heat shock loci. Cell18 (1979) 1359–1370.
Holmgren, R., Corces, V., Morimoto, R., Blackman, R., and Meselson M., Sequence homologies in the 5′ regions of fourDrosophila heat-shock genes. Proc. natl Acad. Sci. USA78 (1981) 3775–3778.
Hultmark, D., Klemenz, R., and Gehring, W., Translational and transcriptional control elements in the untranslated leader of the heat-shock gene hsp22. Cell44 (1986) 429–438.
Ingolia, T. D., and Craig, E. A., Four smallDrosophila heat shock proteins are related to each other and to mammalian α-crystallin. Proc. natl Acad. Sci. USA79 (1982) 2360–2364.
Ireland, R. C., Berger, E., Sirotkin, K., Yund, M. A., Osterbur, D., and Fristrom, J., Ecdysterone induces the transcription of four heatshock genes inDrosophila S3 cells and imaginal discs. Devl Biol.93 (1982) 498–507.
Karch, F., Török, I., and Tissières A., Extensive regions of homology in front of the two hsp70 heat shock variant genes inDrosophila melanogaster. J. molec. Biol.148 (1981) 219–230.
Kellum, R., and Schedl, P., A position-effect assay for boundaries of higher order chromosomal domains. Cell64 (1991) 941–950.
Klemenz, R., Hultmark, D., and Gehring, W. J., Selective translation of heat shock mRNA inDrosophila melanogaster depends on sequence information in the leader. EMBO J.4 (1985) 2053–2060.
Kruger, C., and Benecke, B.-J., In vitro translation ofDrosophila heat shock and non-heat shock mRNAs in heterologous and homologous cell-free system. Cell23 (1981) 595–603.
Levinger, L., and Varshavsky, A., Selective arrangement of ubiquitinated and D1 protein-containing nucleosomes within theDrosophila genome. Cell.28 (1982) 375–385.
Lewis, M., Helmsing, P.J., and Ashburner, M., Parallel changes in puffing activity and patterns of protein synthesis in salivary glands ofDrosophila. Proc. natl Acad. Sci. USA72 (1975) 3604–3608.
Lindquist, S., Varying patterns of protein synthesis inDrosophila during heat shock: implications for regulation. Devl Biol.77 (1980) 463–479.
Lindquist, S., and Craig, E. A., The heat-shock proteins. A. Rev. Genet.22 (1988) 631–677.
Livak, K. T., Freund, R., Schweber, M., Wensink, P. C., and Meselson, M., Sequence organization and transcription of two heat shock loci inDrosophila. Proc. natl Acad. Sci. USA75 (1978) 5613–5617.
Maroto, F.G., and Sierra, J. M., Translational control in heatshockedDrosophila embryos. J. biol. Chem.263 (1988) 15720–15725.
Mason, P. J., Hall, L. M. C., and Gausz, J., The expression of heat shock genes during normal development inDrosophila melanogaster (heat shock/abundant transcripts/developmental regulation). Molec. gen. Genet.194 (1984) 73–78.
McGarry, T. J., and Lindquist, S., The preferential translation ofDrosophila hsp70 mRNA requires sequences in the untranslated leader. Cell42 (1985) 903–911.
McKenzie, S. L., Henikoff, S., and Meselson M., Localization of RNA from heat-induced polysomes at puff sites inDrosophila melanogaster. Proc. natl Acad. Sci. USA72 (1975) 1117–1121.
McKenzie, S. L., and Meselson, M., Translation in vitro ofDrosophila heat-shock messages. J. molec. Biol.117 (1977) 279–283.
Mestril, R., Schiller, P., Amin, J., Klapper, H., Jayakumar, A., and Voellmy, R., Heat shock and ecdysterone activation ofDrosophila melanogaster hsp23 gene: a sequence element implied in development regulation. EMBO J.5 (1986) 1667–1673.
Mirault, M.-E., Goldschmidt-Clermont, M., Moran, L., Arrigo, A.-P., and Tissières, A., The effect of heat shock on gene expression inDrosophila melanogaster. Cold Spring Harbor Symp. Quant. Biol.42 (1978) 819–827.
Mirault, M.-E., Southgate, R., and Delwart, E., Regulation of heat shock genes: a DNA sequence upstream ofDrosophila hsp 70 genes is essential for their induction in monkey cells. EMBO J.1 (1982) 1279–1285.
Miron, T., Vancompernolle, K., Vanderkerckhove, J., Wilchek, M., and Geiger, B., A 25-kD inhibitor of actin polymerization is a low molecular mass heat shock protein. J. Cell Biol.114 (1991) 255–261.
Mitchell, H. K., and Lipps, L. S., Heat shock and phenocopy induction inDrosophila. Cell15 (1978) 907–918.
Mitchell, H. K., and Petersen, N. S., Rapid changes in gene expression in differentiating tissues ofDrosophila. Devl Biol.85 (1981) 233–242.
Mitchell, H. K., and Moller, G., Petersen, N. S., and Lipps-Sarmiento, L., Specific protection from phenocopy induction by heat shock. Dev. Genet.1 (1979) 181–192.
Morimoto, R. I., Tissières, A., and Georgopoulos, G., (Eds) Stress Proteins in Biology and Medicine. Cold Spring Harbor Laboratory Press. 1990.
Nolan, N. L., and Kidwell, W.R., Effect of heat shock on poly(ADP-ribose) synthetase and DNA repair inDrosophila cells. Radiat. Res.90 (1982) 187–203.
O'Connor, D., and Lis, J. T., Two closely linked transcription units within the 63B heat shock puff ofD. melanogaster display strikingly different regulation. Nucl. Acids Res.9 (1981) 5075–5092.
Parker, C. S., and Topol, J., ADrosophila RNA polymerase II transcription factor binds to the regulatory site of an hsp70 gene. Cell37 (1984) 273–283.
Pauli, D., Spierer, A., and Tissières, A. Several hundred base pairs upstream ofDrosophila hsp23 and 26 genes are required for their heat induction in transformed flies. EMBO J.5 (1986) 755–761.
Pauli, D., and Tonka, C.-H., ADrosophila heat shock gene from locus 67B is expressed during embryogenesis and pupation. J. molec. Biol.198 (1987) 235–240.
Pauli, D., Tonka, C.-H., Tissières, A., and Arrigo, A.-P., Tissuespecific expression of the heat shock protein hsp27 duringDrosophila melanogaster development. J. Cell Biol.111 (1990) 817–828.
Pelham, H. R. B., A regulatory upstream promoter element in theDrosophila hsp heat-shock gene. Cell30 (1982) 517–528.
Pelham, H. R. B., Hsp 70 accelerates the recovery of nucleolar morphology after heat shock. EMBO J.3 (1984) 3095–3100.
Pelham, H. R. B., Speculations on the functions of the major heat shock and glucose regulated proteins. Cell46 (1986) 959–961.
Perisic, O., Xiao, H., and Lis, J., Stable binding ofDrosophila heat shock factor to head-to-tail and tail-to-tail repeats of a conserved 5 bp recognition unit. Cell59 (1989) 797–806.
Perkins, L. A., Doctor, J. S. K., Stinson, L., Perrimon, N., and Craig, E. A., Molecular and development characterization of the heat shock cognate 4 gene ofDrosophila melanogaster. Molec. cell. Biol.10 (1990) 3232–3238.
Petersen, N. S., and Mitchell, H. K., Recovery of protein synthesis after heat shock: prior heat treatment affects the ability of cells to translate mRNA. Proc. natl Acad. Sci. USA78 (1981) 1708–1711.
Petersen, R., and Lindquist, S., TheDrosophila hsp70 message is rapidly degraded at normal temperatures and stabilized by heat shock. Gene72 (1988) 161–168.
Petersen, R., and Lindquist, S., Regulation of hsp70 synthesis by messenger RNA degradation. Cell Reg.1 (1989) 135–149.
Riddihough, G., and Pelham, H. R. B., An ecdysone response element in theDrosophila hsp27 promoter. EMBO J.6 (1987) 3729–3734.
Ritossa, F., A new puffing pattern induced by temperature shock and DNP inDrosophila. Experientia13 (1962) 571–573.
Ritossa, F., New puffs induced by temperature shock, DNP and salicylate in salivary chromosomes ofD. melanogaster. Drosophila Inf. Service37 (1963) 122–123.
Ritossa, F., Experimental activation of specific loci in polytene chromosomes ofDrosophila. Exp. Cell Res.35 (1964) 602–607.
Ritossa, F., Behaviour of RNA and DNA synthesis at the puff level in salivary gland chromosomes ofDrosophila. Exp. Cell Res.36 (1964) 515–523.
Rubin, G. M., and Hogness, D. S., Effect of heat shock on the synthesis of low molecular weight RNAs inDrosophila: accumulation of a novel form of 5S RNA. Cell6 (1975) 207–213.
Sanders, M. M., Triemer, D. F., and Olsen, A. S., Regulation of protein synthesis in heat-shockedDrosophila cells: soluble factors control translation in vitro. J. biol. Chem.261 (1986) 2189–2196.
Schedl, P. S., Artavanis-Tsakonas, S., Steward, R., Gehring, W.J., Mirault, M.-E., Goldschmidt-Clermont, M., Moran, L., and Tissières, A., Two hybrid plasmids withDrosophila melanogaster DNA sequences complementary to mRNA coding for the major heat shock proteins Cell14 (1978) 921–929.
Simard, R., and Bernhard, W., A heat-sensitive cellular function located in the nucleolus. J. Cell Biol.34 (1967) 61–76.
Simon, J. A., Sutton, C. A., Lobell, R. B., Glaser, R. L., and Lis, J. T., Determinants of heat shock-induced chromosome puffing. Cell40 (1985) 805–817.
Sirotkin, K., and Davidson, N., Developmentally regulated transcription fromDrosophila melanogaster, chromosomal site 67B. Devl Biol.89 (1982) 196–210.
Sorger, P. K., Heat shock factor and the heat shock response. Cell65 (1991) 363–366.
Sorger, P. K., and Pelham, H. R. B., Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature dependent phosphorylation. Cell54 (1988) 855–864.
Sorger, P. K., and Nelson, H. C. M., Trimerization of a yeast transcriptional activator via a coiled-coil motif. Cell59 (1989) 807–813.
Spradling, A. C., Pardue, M. L., and Penman, S., Messenger RNA in heat-shockedDrosophila cells. J. molec. Biol.109 (1977) 559–587.
Storti, R. V., Scott, M. P., Rich, A., and Pardue, M. L., Translational control of protein synthesis in response to heat shock inD. melanogaster cells. Cell22 (1980) 825–834.
Thomas, S. R., and Lengyel, J. A., Ecdysteroid-regulated heat-shock gene expression duringDrosophila melanogaster development. Devl Biol.115 (1986) 434–438.
Tissières, A., Mitchell, H. K., and Tracy, V. M., Protein synthesis in salivary glands ofDrosophila melanogaster: relation to chromosome puffs. J. molec. Biol.84 (1974) 389–398.
Velazquez, J. M., and Lindquist, S., Hsp70: nuclear concentration during environmental stress and cytoplasmic storage during recovery. Cell36 (1984) 655–662.
Voellmy, R., Goldschmidt-Clermont, M., Southgate, R., Tissières, A., Levis, R., and Gehring, W., A DNA segment isolated from chromosomal site 67B inD. melanogaster contains four closely linked heat-shock genes. Cell23 (1981) 261–270.
Webster, W. S., Germain, M. A., and Edwards, M. J., The induction of microphthalmia, encephalocele, and other heat defects following hyperthermia during the gastrulation process in the rat. Teratology31 (1985) 73–82.
Westwood, J. T., Clos, J., and Wu, C., Stress-induced oligomerization and chromosomal relocalization of heat-shock factor. Nature353 (1991) 822–827.
Wiederrecht G., Seto, D., and Parker, C. S., Isolation of the gene encoding theS. cerevisiae heat shock transcription factor. Cell54 (1988) 841–853.
Wu, C., Activating protein factor binds in vitro to upstream control sequences in heat shock gene chromatin. Nature311 (1984) 81–84.
Wu, C., Wilson, S., Walker, B., Dawid, I., Paisley, T., Zimarino, V., and Ueda, H., Purification and properties ofDrosophila heat shock activator protein. Science238 (1987) 1247–1253.
Xiao, H., and Lis, J.T., Germ line transformation used to define key features of heat-shock response elements. Science239 (1988) 1139–1142.
Xiao, H., and Lis, J. T., Heat shock and developmental regulation of theDrosophila melanogaster hsp83 gene. Molec. cell Biol.9 (1989) 1746–1753.
Xiao, H., Perisic, O., and Lis, J. T., Cooperative binding ofDrosophila heat shock factor to arrays of a conserved 5 bp unit. Cell64 (1991) 585–593.
Yost, H. J., and Lindquist, S., RNA splicing is interrupted by heat shock and is rescued by heat shock protein synthesis. Cell45 (1986) 185–193.
Yost, H. J., and Lindquist, S., Translation of unspliced transcripts after heat shock. Science242 (1988) 1544–1548.
Yost, H. J., Petersen, R. B., and Lindquist, S., Posttranscriptional regulation of heat shock protein synthesis inDrosophila, in: Stress Proteins in Biology and Medicine, pp. 379–409. Eds R. I. Morimoto, A. Tissières and G. Georgopoulos. Cold Spring Harbor Laboratory Press 1990.
Zimarino, V., and Wu, C., Induction of sequence specific binding ofDrosophila heat shock activator protein without protein synthesis. Nature327 (1987) 727–730.
Zimmerman, J. L., Petri, W., and Meselson, M., Accumulation of a specific subset ofD. melanogaster heat shock mRNAs in normal development without heat shock. Cell32 (1983) 1161–1170.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Pauli, D., Arrigo, A.P. & Tissières, A. Heat shock response in Drosophila. Experientia 48, 623–629 (1992). https://doi.org/10.1007/BF02118306
Published:
Issue Date:
DOI: https://doi.org/10.1007/BF02118306