Abstract
The cellular response to a heat shock treatment was originally observed in Drosophila by the appearance of specific puffs on polytene chromosomes (Ritossa 1962). These puffs are characterised by a high level of transcriptional activity. Concomitant with this physical manifestation is the strong induction of a restricted number of specific polypeptides thereby named Heat Shock Proteins (HSP). In Drosophila melanogaster, the major HSP were first identified through 35S-labelling experiments on Drosophila tissue culture cells and salivary glands (Tissières et al. 1974) and have been commonly divided into three subfamilies based on their apparent molecular weight on SDS-PAGE. The Hsp83 and Hsp60 species are each sole members of their class, while many different genes encode for the highly conserved members of the Hsp70 subfamily. The small heat shock proteins (sHSP) group includes four polypeptides encoded by identified genes (hsp22, hsp23, hsp26 and hsp27) which are all found within the same locus on chromosome 3 (67B). However, additional genes carrying open reading frames (ORF) which could potentially encode for proteins carrying the α-crystallin domain, hallmark domain of the sHSP family, have been readily identified both within (hsp67a, hsp67b and hsp67c—formerly known as gene1, gene2 and gene3) and outside (l(2)efl) the 67B locus.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Amin J, Mestril R, Voellmy R (1991) Genes for Drosophila small heat shock proteins are regulated differently by ecdysterone. Mol Cell Biol 11:5937–5944
Arrigo AP, Ahmed-Zadeh C (1981) Immunofluorescence localization of a small heat shock protein (Hsp23) in salivary gland cells of Drosophila melanogaster. Mol Gen Genet 184:73–79
Arrigo AP, Landry J (1994) Expression and function of the low-molecular-weight heat shock proteins. In: Morimoto RI, Tissières A, Georgopoulos C (eds) The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory Press, New York, pp 335–337.
Arrigo AP, Pauli D (1988) Characterization of Hsp27 and three immunologically related polypeptides during Drosophila development. Exp Cell Res 175:169–183
Arrigo AP, Tanguay RM (1991) Expression of heat shock proteins during development in Drosophila. In: Hightower L, Nover L (eds) Heat shock and development. Springer, Berlin Heidelberg New York, pp 106–111.
Arrigo A-P, Darlix J-L, Khandjian EW, Simon M, Spahr PF (1985) Characterization of the prosome from Drosophila and its similarity to the cytoplasmic structures formed by the low molecular weight heat-shock proteins. EMBO J 4:399–406
Ayme A, Tissières A (1985) Locus 67B of Drosophila melanogaster contains seven, not four, closely related heat shock proteins. EMBO J 4:2949–2954
Beaulieu JF, Arrigo AP, Tanguay RM (1989) Interaction of Drosophila 27,000 Mr heat-shock protein with the nucleus of heat-shock ed and ecdysone-stimulated culture cells. J Cell Sci 92: 29–36
Berger EM (1984) The regulation and function of small heat-shock protein synthesis. Dev Genet 4:255–265
Berger EM, Woodward MP (1983) Small heat shock proteins in Drosophila may confer thermal tolerance. Exp Cell Res 147:437–442
Bournias-Vardiabasis N, Buzin C, Flores J (1990) Differential expression of heat shock protein in Drosophila embryonic cells following metal ion exposure. Exp Cell Res 189:177–182
Buzin CH, Bournias-Vardiabasis N (1984) Teratogens induce a subset of small heat shock proteins in Drosophila primary embryonic cell cultures. Proc Natl Acad Sci USA 81:4075–4079
Cheney CM, Shearn A (1983) Developmental regulation of Drosophila imaginai disc proteins: synthesis of a heat-shock protein under non-heat-shock conditions. Dev Biol 95:325–330
Cohen RS, Meselson M (1985) Separate regulatory elements for the heat-inducible and ovarian expression of the Drosophila hsp26 gene. Cell 43:737–746
Corees V, Holmgren R, Freund R, Morimoto R, Meselson M (1980) Four heat shock proteins of Drosophila melanogaster coded within a 12-kilobase region in chromosome subdivision 67B. Proc Natl Acad Sci USA 77:5390–5393
Courgeon A-M, Rollet E, Becker J, Maisonhaute C, Best-Belpomme M (1988) Hydrogen peroxide (H202) induces actin and some heat-shock proteins in Drosophila cells. Eur Biochem 171: 163–170
Cryderman DE, Tang H, Bell C, Gilmour DS, Wallrath LL (1999) Heterochromatic silencing of Drosophila heat shock genes acts at the level of promoter potentiation. Nucleic Acids Res 27: 3364–3370
De Sa CM, Rollet E, de SA M-F, Tanguay RM, Best-Belpomme M, Scherrer K (1989) Prosomes and heat shock complexes in Drosophila melanogaster cells. Mol Cell Biol 9:2672–2681
Desterro JMP, Rodriguez MS, Hay RT (1998) SUMO-1 modification of IKBoc inhibits NF-κB activation. Mol Cell 2:233–239
Dobens L, Rudolph K, Berger EM (1991) Ecdysterone regulatory elements functions as both transcriptional activators and repressors. Mol Cell Biol 11:1846–1853
Duband JL, Lettre F, Arrigo AP, Tanguay RM (1986) Expression and localization of Hsp23 in unstressed and heat-shock ed Drosophila cultured cells. Can J Genet Cytol 28:1088–1092
Dubrovsky EB, Dretzen G, Bellard M (1994) The Drosophila broad-complex regulates developmental changes in transcription and chromatin structure of the 67B heat-shock gene cluster. J Mol Biol 241:353–362
Dubrovsky EB, Dretzen G, Berger EM (1996) The broad-complex gene is a tissue-specific modulator of the ecdysone response of the Drosophila hsp23 gene. Mol Cell Biol 16:6542–6552
Dura J-M (1981) Stage dependent synthesis of heat shock induced proteins in early embryos of Drosophila melanogaster. Mol Gen Genet 184:381–385
Eissenberg JC, Elgin SCR (1987) Hsp28stl: a P-element insertion mutation that alters the expression of a heat shock gene in Drosophila melanogaster. Genetics 115:333–340
Fink AL (1999) Chaperone-mediated protein folding. Physiol Rev 79:425–449
Frank LH, Cheung H-K, Cohen RS (1992) Identification and characterization of Drosophila female germ line transcriptional control elements. Development 114:481–491
Frydenberg J, Pierpaoli M, Loeschcke V (1999) Drosophila melanogaster is polymorphic for a specific repeated (CATA) sequence in the regulatory region of hsp23. Gene 236:243–250
Gilmour DS, Thomas GH, Elgin SCR (1989) Drosophila nuclear proteins bind to regions of alternating C and T residues in gene promoters. Science 245:1487–1490
Glaser RL, Lis JT (1990) Multiple, compensatory regulatory elements specify spermatocytespecific expression of the Drosophila melanogaster hsp26 gene. Mol Cell Biol 10:131–137
Glaser RL, Thomas GH, Siegfried E, Elgin SC, Lis JT (1990) Optimal heat-induced expression of the Drosophila hsp26 gene requires a promoter sequence containing (CT)n.(GA)n repeats. J Mol Biol 211:751–761
Gostissa M, Hengstermann A, Fogal V, Sandy P, Schwarz SE, Scheffner M, Del Sal G (1999) Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1. EMBO J 18:6462–6471
Haass C, Klein U, Kloetzel P-M (1990) Developmental expression of Drosophila melanogaster small heat-shock proteins. J Cell Sci 96:413–418
Haass C, Kloetzel P-M (1990) Molecular analysis of N-ecdysone induced 16 S complexes in Drosophila Schneider’s S3 cells. Biochem Biophys Res Comm 168:314–319
Henrich VC, Szekely AA, Kim SJ, Brown NE, Antoniewski C, Hayden MA, Lepesant JA, Gilbert LI (1994) Expression and function of the ultraspiracle (usp) gene during development of Drosophila melanogaster. Dev Biol 165:38–52
Hoffman E, Corces V (1986) Sequences involved in temperature and ecdysterone-induced transcription are located in separate regions of a Drosophila melanogaster heat shock gene. Mol Cell Biol 6:663–673
Hoffman EP, Gerring SL, Corees VG (1987) The ovarian, ecdysterone, and heat-shock-response promoters of the Drosophila melanogaster hsp27 gene react very differently to perturbations of DNA sequence. Mol Cell Biol 7:973–981
Hultmark D, Klemenz R, Gehring WJ (1986) Translational and transcriptional control elements in the untranslated leader of the heat-shock gene hsp22. Cell 44:429–438
Ingolia TD, Craig EA (1982) Four small Drosophila heat-shock proteins are related to each other and to mammalian N-crystallin. Proc Natl Acad Sci USA 79:2360–2364
Ireland RC, Berger EM (1982) Synthesis of low molecular weight heat shock peptides stimulated by ecdysterone in a cultured Drosophila cell line. Proc Natl Acad Sci USA 79:855–859
Ireland RC, Berger E, Sirotkin K, Yund MA, Osterbur D, Fristrom J (1982) Ecdysterone induces the transcription of four heat-shock genes in Drosophila S3 cells and imaginai discs. Dev Biol 93:498–507
Joanisse DR, Inaguma Y, Tanguay RM (1998a) Cloning and developmental expression of a nuclear ubiquitin-conjugating enzyme (DmUbc9) that interacts with small heat shock proteins in Drosophila melanogaster. Biochem Biophys Res Commun 244:102–109
Joanisse DR, Michaud S, Inaguma I, Tanguay RM (1998b) Small heat shock proteins of Drosophila: Developmental expression and functions. J Biosci 23:369–376
Kelly SE, Cartwright IL (1989) Perturbation of chromatin architecture on ecdysterone induction of Drosophila melanogaster small heat shock protein genes. Mol Cell Biol 9:332–335
King V, Tower J (1999) Aging-specific expression of Drosophila Hsp22. Dev Biol 207:107–118
Klemenz R, Gehring WJ (1986) Sequence requirement for expression of the Drosophila melanogaster heat shock protein hsp22 gene during heat shock and normal development. Mol Cell Biol 6:2011–2019
Kloetzel P-M, Bautz EKF (1983) Heat-shock proteins are associated with hnRNA in Drosophila melanogaster tissue culture cells. EMBO J 2:705–710
Kretz-Remy C, Tanguay RM (1999) SUMO/sentrin: protein modifiers regulating important cellular functions. Biochem Cell Biol 77:299–309
Kurapati R, Brar Passananti H, Rose MR, Tower J (2000) Increased hsp22 RNA levels in Drosophila lines genetically selected for increased longevity. J Gerontol 55A:B552–B559
Kurzik-Dumke U, Lohman E (1995) Sequence of the new Drosophila melanogaster small heat-shock-related gene, lethal (2) essential for life [1 (2) efl], at locus 59F4,5. Gene 154:171–175
Leemans R, Egger B, Loop T, Kammermeier L, He H, Hartmann B, Certa U, Hirth F, Reichert H, Sanjay TW (2000) Quantitative transcript imaging in normal and heat-shock ed Drosophila embryos by using high-density oligonucleotide arrays. Proc Natl Acad Sci USA 97:12138–12143
Leicht BG, Bonner JJ (1988) Genetic analysis of chromosomal region 67A-D of Drosophila melanogaster. Genetics 119:579–593
Lu Q, Wallrath LL, Allan BD, Glaser RL, Lis JT, Elgin SC (1992) Promoter sequence containing (CT)n.(GA)n repeats is critical for the formation of the DNase I hypersensitive sites in the Drosophila hsp26 gene. J Mol Biol 225:985–998
Lu Q, Wallrath LL, Granok H, Elgin SCR (1993) (CT)n.(GA)n repeats and heat shock elements have distinct roles in chromatin structure and transcriptional activation of the Drosophila hsp26 gene. Mol Cell Biol 13:2802–2814
Lu Q, Wallrath LL, Elgin SCR (1995) The role of a positioned nucleosome at the Drosophila melanogaster hsp26 promoter. EMBO J 14:4738–4746
Luo Y, Amin J, Voellmy R (1991) Ecdysterone receptor is a sequence-specific transcription factor involved in the developmental regulation of heat shock genes. Mol Cell Biol 11:3660–3675
Marin R, Tanguay RM (1996) Stage-specific localization of the small heat shock protein Hsp27 during oogenesis in Drosophila melanogaster. Chromosoma 105:142–149
Marin R, Valet JP, Tanguay RM (1993) hsp23 and hsp26 exhibit distinct spatial and temporal patterns of constitutive expression in Drosophila adults. Dev Genet 14:69–77
Marin R, Demers M, Tanguay R (1996a) Cell-specific heat-shock induction of Hsp23 in the eye of Drosophila melanogaster. Cell Stress Chaperones 1:40–46
Marin R, Landry J, Tanguay RM (1996b) Tissue-specific post-translational modification of the small heat shock protein Hsp27 in Drosophila. Exp Cell Res 223:1–8
Mehlen P, Preville X, Chareyron P, Briolay J, Klemenz R, Arrigo AP (1995) Constitutive expression of human Hsp27, Drosophila Hsp27 or human αB-crystallin confers resistance to TNF.N-and oxidative stress-induced cytotoxicity in stably transfected murine L929 fibroblasts. J Immunol 154:363–374
Mehlen P, Kretz-Remy C, Préville X, Arrigo AP (1996a) Human Hsp27, Drosophila Hsp27 and human αB-crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNFa-induced cell death. EMBO J 15:2695–2706
Mehlen P, Schulze-Osthoff K, Arrigo AP (1996b) Small stress proteins as novel regulators of apoptosis. J Biol Chem 271:16510–16514
Mestril R, Rungger D, Schiller P, Voellmy R (1985) Identification of a sequence element in the promoter of the Drosophila melanogaster hsp23 gene that is required for its heat activation. EMBO J 4:2971–2976
Mestril R, Schiller P, Amin J, Klapper H, Ananthan J, Voellmy R (1986) Heat shock and ecdysterone activation of the Drosophila melanogaster hsp23 gene; a sequence element implied in developmental regulation. EMBO J 5:1667–1673
Michaud S, Marin R, Tanguay RM (1997a) Regulation of heat shock gene induction and expression during Drosophila development. Cell Mol Life Sci 53:104–113
Michaud S, Marin R, Westwood JT, Tanguay RM (1997b) Cell-specific expression and heat-shock induction of Hsps during spermatogenesis in Drosophila melanogaster. J Cell Sci 110: 1989–1997
Montell DJ, Rorth P, Spradling AC (1992) Slow border cells, a locus required for a developmentally regulated cell migration during oogenesis, encodes Drosophila C/EBR Cell 71:51–62
Morrow G, Inaguma Y, Kato K, Tanguay RM (2000) The small heat-shock protein Hsp22 of Drosophila melanogaster is a mitochondrial protein displaying oligomeric organization. J Biol Chem 275:31204–31210
Müller S, Berger M, Lehembre F, Seeler J-S, Haupt Y, Dejean A (2000) c-Jun and p53 activity is modulated by SUMO-1 modification. J Biol Chem 275:13321–13329
Nakai K, Kanehisa M (1992) A knowledge base for predicting protein localisation sites in eukaryotic cells. Genomics 14:897–911
Neupert W (1997) Protein import into mitochondria. Annu Rev Biochem 66:863–917
Nightingale KP, Wellinger RE, Sogo JM, Becker PB (1998) Histone acetylation facilitates RNA polymerase II transcription of the Drosophila hsp26 gene in chromatin. EMBO J 17:2865–2876
O’Brien T, Lis JT (1993) Rapid changes in Drosophila transcription after an instantaneous heat shock. Mol Cell Biol 13:3456–3463
Pauli D, Tissières A (1990) Developmental expression of the heat shock genes in Drosophila melanogaster. In: Morimoto R, Tissières A, Georgopoulos C (eds) Stress proteins in biology and medicine. Cold Spring Harbour Laboratory Press, New York, pp 361–437.
Pauli D, Tonka CH (1987) A Drosophila heat shock gene from locus 67B is expressed during embryogenesis and pupation. J Mol Biol 198:235–240
Pauli D, Tonka CH, Ayme-Southgate A (1988) An unusual split Drosophila heat shock gene expressed during embryogenesis, pupation and in testes. J Mol Biol 200:47–53
Pauli D, Tonka CH, Tissieres A, Arrigo AP (1990) Tissue-specific expression of the heat shock protein Hsp27 during Drosophila melanogaster development. J Cell Biol 111:817–828
Poukka H, Aarnisalo P, Karvonen U, Palvimo JJ, Jänne OA (1999) Ubc9 interacts with the androgen receptor and activates receptor-dependent transcription. J Biol Chem 274:19441–19446
Quivy J-P, Becker PB (1996) The architecture of the heat-inducible Drosophila hsp27 promoter in nuclei. J Mol Biol 256:249–263
Riddihough G, Pelham HRB (1986) Activation of the Drosophila hsp27 promoter by heat shock and by ecdysone involves independent and remote regulatory sequences. EMBO J 5:1653–1658
Riddihough G, Pelham HRB (1987) An ecdysone response element in the Drosophila hsp27 promoter. EMBO J 6:3729–3734
Ritossa F (1962) A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia 18:571–573
Rodriguez MS, Desterro JMP, Lain S, Midgley CA, Lane DP, Hay RT (1999) SUMO-1 modification activates the transcriptional response of p53. EMBO J 18:6455–6461
Rollet E, Best-Belpomme M (1986) Hsp 26 and 27 are phosphorylated in response to heat shock and ecdysterone in Drosophila melanogaster cells. Biochem Biophys Res Commun 141: 426–433
Rollet E, Lavoie JN, Landry J, Tanguay RM (1992) Expression of Drosophila’s 27kDa heat shock protein into rodent cells confers thermal resistance. Biochem Biophys Res Commun 185: 116–120
Ropp M, Courgeon A-M, Calvayrac R, Best-Belpomme M (1983) The possible role of the superoxyde ion in the induction of heat-shock and specific proteins in aerobic Drosophila cells during return to normoxia after a period of anaerobiosis. Can J Biochem Cell Biol 61:456–461
Rorth P (1996) A modular misexpression screen in Drosophila detecting tissue-specific phenotypes. Proc Natl Acad Sci USA 93:12418–12422
Rorth P, Szabo K, Bailey A, Laverty T, Rehm J, Rubin GM, Weigmann K, Milán M, Benes B, Ansorge W, Cohen SM (1998) Systematic gain-of-function genetics in Drosophila. Development 125: 1049–1057
Rorth P, Szabo K, Texido G (2000) The level of C/EBP protein is critical for cell migration during Drosophila oogenesis and is tightly controlled by regulated degradation. Mol Cell 6:23–30
Saltzman A, Searfoss G, Marcireau C, Stone M, Ressner R, Munro R, Franks C, D’Alonzo J, Tocque B, Jaye M, Ivaschenko Y (1998) hUBC9 associates with MEKKI and type I TNFκ receptor and stimulates NFKB activity. FEBS Letters 425:431–435
Schubiger M, Truman JW (2000) The RXR ortholog USP suppresses early metamorphic processes in Drosophila in the absence of ecdysteroids. Development 127:1151–1159
Schuldt C, Kloetzel P-M (1985) Analysis of cytoplasmic 19 S ring-type particles in Drosophila which contain Hsp 23 at normal growth temperature. Dev Biol 110:65–74
Shopland LS, Lis JT (1996) HSF recruitment and loss at most Drosophila heat shock loci is coordinated and depends on proximal promoter sequence. Chromosoma 105:158–171
Sirotkin K, Bartley N, Perry III WL, Briggs D, Grell EH, Morganelli C, Berger EM, Bonner JJ, Leicht B (1986) Deletion polymorphism in a Drosophila melanogaster heat shock gene. Mol Gen Genet 204:266–272
Southgate R, Ayme A, Voellmy R (1983) Nucleotide sequence analysis of the Drosophila small heat shock gene cluster at locus 67B. J Mol Biol 165:35–57
Tanguay RM, Joanisse DR, Inaguma Y, Michaud S (1999) Small heat shock proteins: in search of functions in vivo. In: Storey KB (ed) Environmental stress and gene regulation. BIOS Scientific Publishers Ltd, Oxford, pp 125-13.
Thomas GH, Elgin SCR (1988) Protein/DNA architecture of the DNase I hypersensitive region of the Drosophila hsp26 promoter. EMBO J 7:2191–2201
Tissières A, Mitchell HK, Tracy UM (1974) Protein synthesis in salivary glands of Drosophila melanogaster. relation to chromosome puffs. J Mol Biol 84:389–398
Vazquez J (1991) Response to heat shock of gene 1, a Drosophila melanogaster small heat shock gene, is developmentally regulated. Mol Gen Genet 226:393–400
Vazquez J, Pauli D, Tissières A (1993) Transcriptional regulation in Drosophila during heat shock: a nuclear run-on analysis. Chromosoma 102:233–248
Vincent M, Tanguay RM (1982) Different intracellular distributions of heat-shock and arseniteinduced proteins in Drosophila Kc cells. J Mol Biol 162:365–378
Vitek MP, Berger EM (1984) Steroid and high-temperature induction of the small heat-shock protein genes in Drosophila. J Mol Biol 178:173–189
Wall G, Varga-Weisz PD, Sandaltzopoulos R, Becker PB (1995) Chromatin remodeling by GAGA factor and heat shock factor at the hypersensitive Drosophila hsp26 promoter in vitro. EMBO J 14:1727–1736
Westwood JT, Clos J, Wu C (1991) Stress-induced oligomerization and chromosomal relocalization of heat-shock factor. Nature 353:822–827
Wheeler JC, Bieschke ET, Tower J (1995) Muscle-specific expression of Drosophila Hsp70 in response to aging and oxidative stress. Proc Natl Acad Sci USA 92:10408–10412
Yeh ETH, Gong L, Kamitani T (2000) Ubiquitin-like proteins: new wines in new bottles. Gene 248: 1–14
Zimmerman JL, Petri W, Meselson M (1983) Accumulation of a specific subset of D. melanogaster heat shock mRNAs in normal development without heat shock. Cell 32:1161–1170
Zou S, Meadows S, Sharp L, Jan LY, Nung Jan Y (2000) Genome-wide study of aging and oxydative stress response in Drosophila melanogaster. Proc Natl Acad Sci USA 97:13726–13731
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2002 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Michaud, S., Morrow, G., Marchand, J., Tanguay, R.M. (2002). Drosophila Small Heat Shock Proteins: Cell and Organelle-Specific Chaperones?. In: Arrigo, AP., Müller, W.E.G. (eds) Small Stress Proteins. Progress in Molecular and Subcellular Biology, vol 28. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-56348-5_5
Download citation
DOI: https://doi.org/10.1007/978-3-642-56348-5_5
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-62708-8
Online ISBN: 978-3-642-56348-5
eBook Packages: Springer Book Archive