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Drosophila Small Heat Shock Proteins: An Update on Their Features and Functions

  • Chapter
The Big Book on Small Heat Shock Proteins

Part of the book series: Heat Shock Proteins ((HESP,volume 8))

Abstract

Small heat shock proteins (sHsps) are present in varying numbers in all organisms. In Drosophila melanogaster there are 12 sHsps, which have distinctive developmental expression patterns, intracellular localizations and substrate specificities. Even if most of Drosophila sHsps do not have a known mammalian ortholog, they share their involvement in multiple cellular processes such as cytoskeleton modulation, apoptosis and autophagy. New data on Drosophila sHsps have arisen from high-throughput genomic and proteomic studies as well as from deletion experiments. In addition to showing the complexity of this family, these experiments suggest the involvement of sHsps in new cellular processes such as the involvement of Hsp27 in piRNA biosynthesis. The goal of this review is to summarize the new findings on each Drosophila sHsp and to highlight its similarity to other sHsps as well as its distinctive features.

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References

  • Accili D, Arden KC (2004) FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 117(4):421–426

    CAS  PubMed  Google Scholar 

  • Apidianakis Y, Mindrinos MN, Xiao W, Lau GW, Baldini RL, Davis RW, Rahme LG (2005) Profiling early infection responses: pseudomonas aeruginosa eludes host defenses by suppressing antimicrobial peptide gene expression. Proc Natl Acad Sci U S A 102(7):2573–2578

    CAS  PubMed Central  PubMed  Google Scholar 

  • Arias E, Cuervo AM (2011) Chaperone-mediated autophagy in protein quality control. Curr Opin Cell Biol 23(2):184–189. doi:10.1016/j.ceb.2010.10.009

    CAS  PubMed Central  PubMed  Google Scholar 

  • Arndt V, Dick N, Tawo R, Dreiseidler M, Wenzel D, Hesse M, Fürst DO, Saftig P, Saint R, Fleischmann BK, Hoch M, Höhfeld J (2010) Chaperone-assisted selective autophagy is essential for muscle maintenance. Curr Biol 20:143–148. doi:10.1016/j.cub.2009.11.022

    CAS  PubMed  Google Scholar 

  • Artero R, Furlong EE, Beckett K, Scott MP, Baylies M (2003) Notch and Ras signaling pathway effector genes expressed in fusion competent and founder cells during Drosophila myogenesis. Development 130(25):6257–6272

    CAS  PubMed  Google Scholar 

  • Awofala AA, Davies JA, Jones S (2012) Functional roles for redox genes in ethanol sensitivity in Drosophila. Funct Integr Genomics 12(2):305–315

    CAS  PubMed  Google Scholar 

  • Ayme A, Tissieres A (1985) Locus 67B of Drosophila melanogaster contains seven, not four, closely related heat shock genes. EMBO J 4(11):2949–2954

    CAS  PubMed Central  PubMed  Google Scholar 

  • Azad P, Zhou D, Russo E, Haddad GG (2009) Distinct mechanisms underlying tolerance to intermittent and constant hypoxia in Drosophila melanogaster. PLoS One 4(4):e5371

    PubMed Central  PubMed  Google Scholar 

  • Baird NA, Turnbull DW, Johnson EA (2006) Induction of the heat shock pathway during hypoxia requires regulation of heat shock factor by hypoxia-inducible factor-1. J Biol Chem 281(50):38675–38681

    CAS  PubMed  Google Scholar 

  • Basha E, O’Neill H, Vierling E (2012) Small heat shock proteins and alpha-crystallins: dynamic proteins with flexible functions. Trends Biochem Sci 37(3):106–117

    CAS  PubMed Central  PubMed  Google Scholar 

  • Basha E, Jones C, Blackwell AE, Cheng G, Waters ER, Samsel KA, Siddique M, Pett V, Wysocki V, Vierling E (2013) An unusual dimeric small heat shock protein provides insight into the mechanism of this class of chaperones. J Mol Biol 425(10):1683–1696

    CAS  PubMed Central  PubMed  Google Scholar 

  • Beaulieu JF, Arrigo AP, Tanguay RM (1989) Interaction of Drosophila 27,000 Mr heat-shock protein with the nucleus of heat-shocked and ecdysone-stimulated culture cells. J Cell Sci 92(Pt 1):29–36

    PubMed  Google Scholar 

  • Bhole D, Allikian MJ, Tower J (2004) Doxycycline-regulated over-expression of hsp22 has negative effects on stress resistance and life span in adult Drosophila melanogaster. Mech Ageing Dev 125(9):651–663

    CAS  PubMed  Google Scholar 

  • Bilak A, Su TT (2009) Regulation of Drosophila melanogaster pro-apoptotic gene hid. Apoptosis 14(8):943–949

    PubMed Central  PubMed  Google Scholar 

  • Bilen J, Bonini NM (2007) Genome-wide screen for modifiers of ataxin-3 neurodegeneration in Drosophila. PLoS Genet 3(10):1950–1964

    CAS  PubMed  Google Scholar 

  • Birch-Machin I, Gao S, Huen D, McGirr R, White RA, Russell S (2005) Genomic analysis of heat-shock factor targets in Drosophila. Genome Biol 6(7):R63

    PubMed Central  PubMed  Google Scholar 

  • Blum T, Briesemeister S, Kohlbacher O (2009) MultiLoc2: integrating phylogeny and gene ontology terms improves subcellular protein localization prediction. BMC Bioinformatics 10:274

    PubMed Central  PubMed  Google Scholar 

  • Bodenmiller B, Mueller LN, Pedrioli PG, Pflieger D, Junger MA, Eng JK, Aebersold R, Tao WA (2007) An integrated chemical, mass spectrometric and computational strategy for (quantitative) phosphoproteomics: application to Drosophila melanogaster Kc167 cells. Mol Biosyst 3(4):275–286

    CAS  PubMed  Google Scholar 

  • Boelens WC, Croes Y, de Jong WW (2001) Interaction between alphaB-crystallin and the human 20S proteasomal subunit C8/alpha7. Biochim Biophys Acta 1544(1–2):311–319

    CAS  PubMed  Google Scholar 

  • Boncoraglio A, Minoia M, Carra S (2012) The family of mammalian small heat shock proteins (HSPBs): implications in protein deposit diseases and motor neuropathies. Int J Biochem Cell Biol 44(10):1657–1669

    CAS  PubMed  Google Scholar 

  • Boyd O, Weng P, Sun X, Alberico T, Laslo M, Obenland DM, Kern B, Zou S (2011) Nectarine promotes longevity in Drosophila melanogaster. Free Radic Biol Med 50(11):1669–1678

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brandt T, Corces VG (2008) The Lawc protein is required for proper transcription by RNA polymerase II in Drosophila. Mol Genet Genomics 280(5):385–396

    CAS  PubMed Central  PubMed  Google Scholar 

  • Briesemeister S, Blum T, Brady S, Lam Y, Kohlbacher O, Shatkay H (2009) SherLoc2: a high-accuracy hybrid method for predicting subcellular localization of proteins. J Proteome Res 8(11):5363–5366

    CAS  PubMed  Google Scholar 

  • Bryantsev AL, Kurchashova SY, Golyshev SA, Polyakov VY, Wunderink HF, Kanon B, Budagova KR, Kabakov AE, Kampinga HH (2007) Regulation of stress-induced intracellular sorting and chaperone function of Hsp27 (HspB1) in mammalian cells. Biochem J 407(3):407–417

    CAS  PubMed Central  PubMed  Google Scholar 

  • Carra S, Brunsting JF, Lambert H, Landry J, Kampinga HH (2009) HspB8 participates in protein quality control by a non-chaperone-like mechanism that requires eIF2{alpha} phosphorylation. J Biol Chem 284(9):5523–5532

    CAS  PubMed  Google Scholar 

  • Carra S, Boncoraglio A, Kanon B, Brunsting JF, Minoia M, Rana A, Vos MJ, Seidel K, Sibon OC, Kampinga HH (2010) Identification of the Drosophila ortholog of HSPB8: implication of HSPB8 loss of function in protein folding diseases. J Biol Chem 285(48):37811–37822

    CAS  PubMed Central  PubMed  Google Scholar 

  • Carra S, Rusmini P, Crippa V, Giorgetti E, Boncoraglio A, Cristofani R, Naujock M, Meister M, Minoia M, Kampinga HH, Poletti A (2013) Different anti-aggregation and pro-degradative functions of the members of the mammalian sHSP family in neurological disorders. Philos Trans R Soc Lond B Biol Sci 368(1617):20110409

    PubMed Central  PubMed  Google Scholar 

  • Catalan A, Hutter S, Parsch J (2012) Population and sex differences in Drosophila melanogaster brain gene expression. BMC Genomics 13:654

    CAS  PubMed Central  PubMed  Google Scholar 

  • Celniker SE, Dillon LA, Gerstein MB, Gunsalus KC, Henikoff S, Karpen GH, Kellis M, Lai EC, Lieb JD, MacAlpine DM, Micklem G, Piano F, Snyder M, Stein L, White KP, Waterston RH, mod EC (2009) Unlocking the secrets of the genome. Nature 459(7249):927–930

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ceriani MF, Hogenesch JB, Yanovsky M, Panda S, Straume M, Kay SA (2002) Genome-wide expression analysis in Drosophila reveals genes controlling circadian behavior. J Neurosci 22(21):9305–9319

    CAS  PubMed  Google Scholar 

  • Cernilogar FM, Onorati MC, Kothe GO, Burroughs AM, Parsi KM, Breiling A, Lo Sardo F, Saxena A, Miyoshi K, Siomi H, Siomi MC, Carninci P, Gilmour DS, Corona DF, Orlando V (2011) Chromatin-associated RNA interference components contribute to transcriptional regulation in Drosophila. Nature 480(7377):391–395

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cervantes-Gomez F, Nimmanapalli R, Gandhi V (2009) Transcription inhibition of heat shock proteins: a strategy for combination of 17-allylamino-17-demethoxygeldanamycin and actinomycin d. Cancer Res 69(9):3947–3954

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chahine S, O’Donnell MJ (2010) Effects of acute or chronic exposure to dietary organic anions on secretion of methotrexate and salicylate by Malpighian tubules of Drosophila melanogaster larvae. Arch Insect Biochem Physiol 73(3):128–147

    CAS  PubMed  Google Scholar 

  • Chakrabarti S, Liehl P, Buchon N, Lemaitre B (2012) Infection-induced host translational blockage inhibits immune responses and epithelial renewal in the Drosophila gut. Cell Host Microbe 12(1):60–70

    CAS  PubMed  Google Scholar 

  • Chan WM, Tsoi H, Wu CC, Wong CH, Cheng TC, Li HY, Lau KF, Shaw PC, Perrimon N, Chan HY (2011) Expanded polyglutamine domain possesses nuclear export activity which modulates subcellular localization and toxicity of polyQ disease protein via exportin-1. Hum Mol Genet 20(9):1738–1750

    CAS  PubMed  Google Scholar 

  • Chen J, Shi X, Padmanabhan R, Wang Q, Wu Z, Stevenson SC, Hild M, Garza D, Li H (2008) Identification of novel modulators of mitochondrial function by a genome-wide RNAi screen in Drosophila melanogaster. Genome Res 18(1):123–136

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen J, Xie C, Tian L, Hong L, Wu X, Han J (2010) Participation of the p38 pathway in Drosophila host defense against pathogenic bacteria and fungi. Proc Natl Acad Sci U S A 107(48):20774–20779

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen SF, Kang ML, Chen YC, Tang HW, Huang CW, Li WH, Lin CP, Wang CY, Wang PY, Chen GC, Wang HD (2012) Autophagy-related gene 7 is downstream of heat shock protein 27 in the regulation of eye morphology, polyglutamine toxicity, and lifespan in Drosophila. J Biomed Sci 19:52

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chevenet F, Brun C, Banuls AL, Jacq B, Christen R (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 7:439

    PubMed Central  PubMed  Google Scholar 

  • Chintapalli VR, Wang J, Dow JA (2007) Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet 39(6):715–720

    CAS  PubMed  Google Scholar 

  • Chou KC, Shen HB (2010) A new method for predicting the subcellular localization of eukaryotic proteins with both single and multiple sites: Euk-mPLoc 2.0. PLoS One 5(4):e9931

    PubMed Central  PubMed  Google Scholar 

  • Chou AH, Yeh TH, Ouyang P, Chen YL, Chen SY, Wang HL (2008) Polyglutamine-expanded ataxin-3 causes cerebellar dysfunction of SCA3 transgenic mice by inducing transcriptional dysregulation. Neurobiol Dis 31(1):89–101

    CAS  PubMed  Google Scholar 

  • Colinet H, Lee SF, Hoffmann A (2010a) Knocking down expression of Hsp22 and Hsp23 by RNA interference affects recovery from chill coma in Drosophila melanogaster. J Exp Biol 213(Pt 24):4146–4150

    CAS  PubMed  Google Scholar 

  • Colinet H, Lee SF, Hoffmann A (2010b) Temporal expression of heat shock genes during cold stress and recovery from chill coma in adult Drosophila melanogaster. FEBS J 277(1):174–185

    CAS  PubMed  Google Scholar 

  • Colinet H, Siaussat D, Bozzolan F, Bowler K (2013) Rapid decline of cold tolerance at young age is associated with expression of stress genes in Drosophila melanogaster. J Exp Biol 216(Pt 2):253–259

    CAS  PubMed  Google Scholar 

  • Craig EA, McCarthy BJ (1980) Four Drosophila heat shock genes at 67B: characterization of recombinant plasmids. Nucleic Acids Res 8(19):4441–4457

    CAS  PubMed Central  PubMed  Google Scholar 

  • Creagh EM, Brumatti G, Sheridan C, Duriez PJ, Taylor RC, Cullen SP, Adrain C, Martin SJ (2009) Bicaudal is a conserved substrate for Drosophila and mammalian caspases and is essential for cell survival. PLoS One 4(3):e5055

    PubMed Central  PubMed  Google Scholar 

  • Curtis C, Landis GN, Folk D, Wehr NB, Hoe N, Waskar M, Abdueva D, Skvortsov D, Ford D, Luu A, Badrinath A, Levine RL, Bradley TJ, Tavare S, Tower J (2007) Transcriptional profiling of MnSOD-mediated lifespan extension in Drosophila reveals a species-general network of aging and metabolic genes. Genome Biol 8(12):R262

    PubMed Central  PubMed  Google Scholar 

  • Delbecq SP, Klevit RE (2013) One size does not fit all: the oligomeric states of alphaB crystallin. FEBS Lett 587(8):1073–1080

    CAS  PubMed  Google Scholar 

  • den Engelsman J, van de Schootbrugge C, Yong J, Pruijn GJ, Boelens WC (2013) Pseudophosphorylated alphaB-crystallin is a nuclear chaperone imported into the nucleus with help of the SMN complex. PLoS One 8(9):e73489

    Google Scholar 

  • Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36(Web Server issue):W465–W469

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dereeper A, Audic S, Claverie JM, Blanc G (2010) BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol Biol 10:8

    PubMed Central  PubMed  Google Scholar 

  • Eleftherianos I, Castillo JC (2012) Molecular mechanisms of aging and immune system regulation in Drosophila. Int J Mol Sci 13(8):9826–9844

    CAS  PubMed Central  PubMed  Google Scholar 

  • Estrada B, Choe SE, Gisselbrecht SS, Michaud S, Raj L, Busser BW, Halfon MS, Church GM, Michelson AM (2006) An integrated strategy for analyzing the unique developmental programs of different myoblast subtypes. PLoS Genet 2(2):e16

    PubMed Central  PubMed  Google Scholar 

  • Fernandez-Ayala DJ, Chen S, Kemppainen E, O’Dell KM, Jacobs HT (2010) Gene expression in a Drosophila model of mitochondrial disease. PLoS One 5(1):e8549

    PubMed Central  PubMed  Google Scholar 

  • Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Res 42(Database issue):D222–D230

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fisher KH, Deane CM, Wakefield JG (2008) The functional domain grouping of microtubule associated proteins. Commun Integr Biol 1(1):47–50

    CAS  PubMed Central  PubMed  Google Scholar 

  • Franco M, Seyfried NT, Brand AH, Peng J, Mayor U (2011) A novel strategy to isolate ubiquitin conjugates reveals wide role for ubiquitination during neural development. Mol Cell Proteomics 10(5):M110 002188

    PubMed Central  PubMed  Google Scholar 

  • Fu X (2014) Chaperone function and mechanism of small heat-shock proteins. Acta Biochim Biophys Sin (Shanghai) 46(5):347–356

    Google Scholar 

  • Garrido C, Paul C, Seigneuric R, Kampinga HH (2012) The small heat shock proteins family: the long forgotten chaperones. Int J Biochem Cell Biol 44(10):1588–1592

    CAS  PubMed  Google Scholar 

  • Geiger-Thornsberry GL, Mackay TF (2004) Quantitative trait loci affecting natural variation in Drosophila longevity. Mech Ageing Dev 125(3):179–189

    CAS  PubMed  Google Scholar 

  • Giannakou ME, Partridge L (2007) Role of insulin-like signalling in Drosophila lifespan. Trends Biochem Sci 32(4):180–188

    CAS  PubMed  Google Scholar 

  • Girardot F, Lasbleiz C, Monnier V, Tricoire H (2006) Specific age-related signatures in Drosophila body parts transcriptome. BMC Genomics 7:69

    PubMed Central  PubMed  Google Scholar 

  • Goldstein LS, Gunawardena S (2000) Flying through the drosophila cytoskeletal genome. J Cell Biol 150(2):F63–F68

    CAS  PubMed  Google Scholar 

  • Gong L, Puri M, Unlu M, Young M, Robertson K, Viswanathan S, Krishnaswamy A, Dowd SR, Minden JS (2004) Drosophila ventral furrow morphogenesis: a proteomic analysis. Development 131(3):643–656

    CAS  PubMed  Google Scholar 

  • Graham AM, Merrill JD, McGaugh SE, Noor MA (2012) Geographic selection in the small heat shock gene complex differentiating populations of Drosophila pseudoobscura. J Hered 103(3):400–407

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gregory JM, Barros TP, Meehan S, Dobson CM, Luheshi LM (2012) The aggregation and neurotoxicity of TDP-43 and its ALS-associated 25 kDa fragment are differentially affected by molecular chaperones in Drosophila. PLoS One 7(2):e31899

    CAS  PubMed Central  PubMed  Google Scholar 

  • Grover D, Yang J, Ford D, Tavare S, Tower J (2009) Simultaneous tracking of movement and gene expression in multiple Drosophila melanogaster flies using GFP and DsRED fluorescent reporter transgenes. BMC Res Notes 2:58

    PubMed Central  PubMed  Google Scholar 

  • Gruenewald C, Botella JA, Bayersdorfer F, Navarro JA, Schneuwly S (2009) Hyperoxia-induced neurodegeneration as a tool to identify neuroprotective genes in Drosophila melanogaster. Free Radic Biol Med 46(12):1668–1676

    CAS  PubMed  Google Scholar 

  • Habermann K, Mirgorodskaya E, Gobom J, Lehmann V, Muller H, Blumlein K, Deery MJ, Czogiel I, Erdmann C, Ralser M, von Kries JP, Lange BM (2012) Functional analysis of centrosomal kinase substrates in Drosophila melanogaster reveals a new function of the nuclear envelope component otefin in cell cycle progression. Mol Cell Biol 32(17):3554–3569

    CAS  PubMed Central  PubMed  Google Scholar 

  • Handler D, Olivieri D, Novatchkova M, Gruber FS, Meixner K, Mechtler K, Stark A, Sachidanandam R, Brennecke J (2011) A systematic analysis of Drosophila TUDOR domain-containing proteins identifies Vreteno and the Tdrd12 family as essential primary piRNA pathway factors. EMBO J 30(19):3977–3993

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hands S, Sinadinos C, Wyttenbach A (2008) Polyglutamine gene function and dysfunction in the ageing brain. Biochim Biophys Acta 1779(8):507–521

    CAS  PubMed  Google Scholar 

  • Hao X, Zhang S, Timakov B, Zhang P (2007) The Hsp27 gene is not required for Drosophila development but its activity is associated with starvation resistance. Cell Stress Chaperones 12(4):364–372

    CAS  PubMed Central  PubMed  Google Scholar 

  • Harvey KF, Mattila J, Sofer A, Bennett FC, Ramsey MR, Ellisen LW, Puig O, Hariharan IK (2008) FOXO-regulated transcription restricts overgrowth of Tsc mutant organs. J Cell Biol 180(4):691–696

    CAS  PubMed Central  PubMed  Google Scholar 

  • Head MW, Goldman JE (2000) Small heat shock proteins, the cytoskeleton, and inclusion body formation. Neuropathol Appl Neurobiol 26(4):304–312

    CAS  PubMed  Google Scholar 

  • Herranz R, Larkin OJ, Dijkstra CE, Hill RJ, Anthony P, Davey MR, Eaves L, van Loon JJ, Medina FJ, Marco R (2012) Microgravity simulation by diamagnetic levitation: effects of a strong gradient magnetic field on the transcriptional profile of Drosophila melanogaster. BMC Genomics 13:52

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hirano Y, Kuriyama Y, Miyashita T, Horiuchi J, Saitoe M (2012) Reactive oxygen species are not involved in the onset of age-related memory impairment in Drosophila. Genes Brain Behav 11(1):79–86

    CAS  PubMed  Google Scholar 

  • Houtkooper RH, Mouchiroud L, Ryu D, Moullan N, Katsyuba E, Knott G, Williams RW, Auwerx J (2013) Mitonuclear protein imbalance as a conserved longevity mechanism. Nature 497(7450):451–457

    CAS  PubMed  Google Scholar 

  • Hsu AL, Murphy CT, Kenyon C (2003) Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 300(5622):1142–1145

    CAS  PubMed  Google Scholar 

  • Huen NY, Chan HY (2005) Dynamic regulation of molecular chaperone gene expression in polyglutamine disease. Biochem Biophys Res Commun 334(4):1074–1084

    CAS  PubMed  Google Scholar 

  • Hughes JR, Meireles AM, Fisher KH, Garcia A, Antrobus PR, Wainman A, Zitzmann N, Deane C, Ohkura H, Wakefield JG (2008) A microtubule interactome: complexes with roles in cell cycle and mitosis. PLoS Biol 6(4):e98

    PubMed Central  PubMed  Google Scholar 

  • Hull-Thompson J, Muffat J, Sanchez D, Walker DW, Benzer S, Ganfornina MD, Jasper H (2009) Control of metabolic homeostasis by stress signaling is mediated by the lipocalin NLaz. PLoS Genet 5(4):e1000460

    PubMed Central  PubMed  Google Scholar 

  • Jensen HR, Scott IM, Sims SR, Trudeau VL, Arnason JT (2006) The effect of a synergistic concentration of a Piper nigrum extract used in conjunction with pyrethrum upon gene expression in Drosophila melanogaster. Insect Mol Biol 15(3):329–339

    CAS  PubMed  Google Scholar 

  • Jin JK, Whittaker R, Glassy MS, Barlow SB, Gottlieb RA, Glembotski CC (2008) Localization of phosphorylated alphaB-crystallin to heart mitochondria during ischemia-reperfusion. Am J Physiol Heart Circ Physiol 294(1):H337–H344

    CAS  PubMed  Google Scholar 

  • Joanisse DR, Inaguma Y, Tanguay RM (1998) 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(1):102–109

    CAS  PubMed  Google Scholar 

  • Kallappagoudar S, Varma P, Pathak RU, Senthilkumar R, Mishra RK (2010) Nuclear matrix proteome analysis of Drosophila melanogaster. Mol Cell Proteomics 9(9):2005–2018

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kampinga HH, Garrido C (2012) HSPBs: small proteins with big implications in human disease. Int J Biochem Cell Biol 44(10):1706–1710

    CAS  PubMed  Google Scholar 

  • Kapelnikov A, Zelinger E, Gottlieb Y, Rhrissorrakrai K, Gunsalus KC, Heifetz Y (2008) Mating induces an immune response and developmental switch in the Drosophila oviduct. Proc Natl Acad Sci U S A 105(37):13912–13917

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kim H, Morrow G, Westwood TJ, Michaud S, Tanguay RM (2010) Gene expression profiling implicates OXPHOS complexes in aging and lifespan extension in flies overexpressing a small mitochondrial chaperone, Hsp22. J Exp Gerontol 45(7–8):611–620

    CAS  Google Scholar 

  • King V, Tower J (1999) Aging-specific expression of Drosophila hsp22. Dev Biol 207(1):107–118

    CAS  PubMed  Google Scholar 

  • Kingsolver MB, Huang Z, Hardy RW (2013) Insect antiviral innate immunity: pathways, effectors, and connections. J Mol Biol 425(24):4921–4936

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kurapati R, Passananti HB, Rose MR, Tower J (2000) Increased hsp22 RNA levels in Drosophila lines genetically selected for increased longevity. J Gerontol A Biol Sci Med Sci 55(11):B552–B559

    CAS  PubMed  Google Scholar 

  • Laayouni H, Garcia-Franco F, Chavez-Sandoval BE, Trotta V, Beltran S, Corominas M, Santos M (2007) Thermal evolution of gene expression profiles in Drosophila subobscura. BMC Evol Biol 7:42

    PubMed Central  PubMed  Google Scholar 

  • Landis GN, Abdueva D, Skvortsov D, Yang J, Rabin BE, Carrick J, Tavare S, Tower J (2004) Similar gene expression patterns characterize aging and oxidative stress in Drosophila melanogaster. Proc Natl Acad Sci U S A 101(20):7663–7668

    CAS  PubMed Central  PubMed  Google Scholar 

  • Landis G, Shen J, Tower J (2012) Gene expression changes in response to aging compared to heat stress, oxidative stress and ionizing radiation in Drosophila melanogaster. Aging (Albany NY) 4(11):768–789

    CAS  Google Scholar 

  • Lee KS, Choi JS, Hong SY, Son TH, Yu K (2008) Mobile phone electromagnetic radiation activates MAPK signaling and regulates viability in Drosophila. Bioelectromagnetics 29(5):371–379

    CAS  PubMed  Google Scholar 

  • Leemans R, Egger B, Loop T, Kammermeier L, He H, Hartmann B, Certa U, Hirth F, Reichert H (2000) Quantitative transcript imaging in normal and heat-shocked Drosophila embryos by using high-density oligonucleotide arrays. Proc Natl Acad Sci U S A 97(22):12138–12143

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li SS, Zhang ZY, Yang CJ, Lian HY, Cai P (2013) Gene expression and reproductive abilities of male Drosophila melanogaster subjected to ELF-EMF exposure. Mutat Res 758(1–2):95–103

    CAS  PubMed  Google Scholar 

  • Liao PC, Lin HY, Yuh CH, Yu LK, Wang HD (2008) The effect of neuronal expression of heat shock proteins 26 and 27 on lifespan, neurodegeneration, and apoptosis in Drosophila. Biochem Biophys Res Commun 376(4):637–641

    CAS  PubMed  Google Scholar 

  • Liu R, Woolner S, Johndrow JE, Metzger D, Flores A, Parkhurst SM (2008) Sisyphus, the Drosophila myosin XV homolog, traffics within filopodia transporting key sensory and adhesion cargos. Development 135(1):53–63

    CAS  PubMed  Google Scholar 

  • Loop T, Leemans R, Stiefel U, Hermida L, Egger B, Xie F, Primig M, Certa U, Fischbach KF, Reichert H, Hirth F (2004) Transcriptional signature of an adult brain tumor in Drosophila. BMC Genomics 5(1):24

    PubMed Central  PubMed  Google Scholar 

  • Ma W, Teng Y, Hua H, Hou J, Luo T, Jiang Y (2013) Upregulation of heat shock protein 27 confers resistance to actinomycin D-induced apoptosis in cancer cells. FEBS J 280(18):4612–4624

    CAS  PubMed  Google Scholar 

  • Maaroufi H, Tanguay RM (2013) Analysis and phylogeny of small heat shock proteins from marine viruses and their cyanobacteria host. PLoS One 8(11):e81207

    CAS  PubMed Central  PubMed  Google Scholar 

  • Marin R, Tanguay RM (1996) Stage-specific localization of the small heat shock protein Hsp27 during oogenesis in Drosophila melanogaster. Chromosoma 105(3):142–149

    CAS  PubMed  Google Scholar 

  • 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(1):69–77

    CAS  PubMed  Google Scholar 

  • Marin R, Landry J, Tanguay RM (1996) Tissue-specific posttranslational modification of the small heat shock protein HSP27 in Drosophila. Exp Cell Res 223(1):1–8

    CAS  PubMed  Google Scholar 

  • Marunouchi T, Abe Y, Murata M, Inomata S, Sanbe A, Takagi N, Tanonaka K (2013) Changes in small heat shock proteins HSPB1, HSPB5 and HSPB8 in mitochondria of the failing heart following myocardial infarction in rats. Biol Pharm Bull 36(4):529–539

    CAS  PubMed  Google Scholar 

  • Matsuda S, Vert JP, Saigo H, Ueda N, Toh H, Akutsu T (2005) A novel representation of protein sequences for prediction of subcellular location using support vector machines. Protein Sci 14(11):2804–2813

    CAS  PubMed Central  PubMed  Google Scholar 

  • McGraw LA, Clark AG, Wolfner MF (2008) Post-mating gene expression profiles of female Drosophila melanogaster in response to time and to four male accessory gland proteins. Genetics 179(3):1395–1408

    CAS  PubMed Central  PubMed  Google Scholar 

  • Michaud S, Tanguay RM (2003) Expression of the Hsp23 chaperone during Drosophila embryogenesis: association to distinct neural and glial lineages. BMC Dev Biol 3:9

    PubMed Central  PubMed  Google Scholar 

  • Michaud S, Morrow G, Marchand J, Tanguay RM (2002) Drosophila small heat shock proteins: cell and organelle-specific chaperones? Prog Mol Subcell Biol 28:79–101

    CAS  PubMed  Google Scholar 

  • Michaud S, Lavoie S, Guimond MO, Tanguay RM (2008) The nuclear localization of Drosophila Hsp27 is dependent on a monopartite arginine-rich NLS and is uncoupled from its association to nuclear speckles. Biochim Biophys Acta 1783(6):1200–1210

    CAS  PubMed  Google Scholar 

  • Mileva-Seitz V, Xiao C, Seroude L, Robertson RM (2008) Tissue-specific targeting of Hsp26 has no effect on heat resistance of neural function in larval Drosophila. Cell Stress Chaperones 13(1):85–95

    CAS  PubMed Central  PubMed  Google Scholar 

  • Morozova TV, Anholt RR, Mackay TF (2006) Transcriptional response to alcohol exposure in Drosophila melanogaster. Genome Biol 7(10):R95

    PubMed Central  PubMed  Google Scholar 

  • 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(40):31204–31210

    CAS  PubMed  Google Scholar 

  • Morrow G, Battistini S, Zhang P, Tanguay RM (2004a) Decreased lifespan in the absence of expression of the mitochondrial small heat shock protein Hsp22 in Drosophila. J Biol Chem 279(42):43382–43385

    CAS  PubMed  Google Scholar 

  • Morrow G, Samson M, Michaud S, Tanguay RM (2004b) Overexpression of the small mitochondrial Hsp22 extends Drosophila life span and increases resistance to oxidative stress. FASEB J 18(3):598–599

    CAS  PubMed  Google Scholar 

  • Morrow G, Heikkila JJ, Tanguay RM (2006) Differences in the chaperone-like activities of the four main small heat shock proteins of Drosophila melanogaster. Cell Stress Chaperones 11(1):51–60

    CAS  PubMed Central  PubMed  Google Scholar 

  • Moskalev A, Shaposhnikov M, Turysheva E (2009) Life span alteration after irradiation in Drosophila melanogaster strains with mutations of Hsf and Hsps. Biogerontology 10(1):3–11

    CAS  PubMed  Google Scholar 

  • Muller L, Hutter S, Stamboliyska R, Saminadin-Peter SS, Stephan W, Parsch J (2011) Population transcriptomics of Drosophila melanogaster females. BMC Genomics 12:81

    PubMed Central  PubMed  Google Scholar 

  • Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, Li H, Kenyon C (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424(6946):277–283

    CAS  PubMed  Google Scholar 

  • Nakagawa M, Tsujimoto N, Nakagawa H, Iwaki T, Fukumaki Y, Iwaki A (2001) Association of HSPB2, a member of the small heat shock protein family, with mitochondria. Exp Cell Res 271(1):161–168

    CAS  PubMed  Google Scholar 

  • Neal SJ, Karunanithi S, Best A, So AK, Tanguay RM, Atwood HL, Westwood JT (2006) Thermoprotection of synaptic transmission in a Drosophila heat shock factor mutant is accompanied by increased expression of Hsp83 and DnaJ-1. Physiol Genomics 25(3):493–501

    CAS  PubMed  Google Scholar 

  • Pal S, St Leger RJ, Wu LP (2007) Fungal peptide Destruxin A plays a specific role in suppressing the innate immune response in Drosophila melanogaster. J Biol Chem 282(12):8969–8977

    CAS  PubMed  Google Scholar 

  • Parcellier A, Schmitt E, Gurbuxani S, Seigneurin-Berny D, Pance A, Chantome A, Plenchette S, Khochbin S, Solary E, Garrido C (2003) HSP27 is a ubiquitin-binding protein involved in I-kappaBalpha proteasomal degradation. Mol Cell Biol 23(16):5790–5802

    CAS  PubMed Central  PubMed  Google Scholar 

  • Qin W, Neal SJ, Robertson RM, Westwood JT, Walker VK (2005) Cold hardening and transcriptional change in Drosophila melanogaster. Insect Mol Biol 14(6):607–613

    CAS  PubMed  Google Scholar 

  • Ren J, Jegga AG, Zhang M, Deng J, Liu J, Gordon CB, Aronow BJ, Lu LJ, Zhang B, Ma J (2011) A Drosophila model of the neurodegenerative disease SCA17 reveals a role of RBP-J/Su(H) in modulating the pathological outcome. Hum Mol Genet 20(17):3424–3436

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rosenbaum EE, Brehm KS, Vasiljevic E, Liu CH, Hardie RC, Colley NJ (2011) XPORT-dependent transport of TRP and rhodopsin. Neuron 72(4):602–615

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396(6709):336–342

    CAS  PubMed  Google Scholar 

  • Schoenherr JA, Drennan JM, Martinez JS, Chikka MR, Hall MC, Chang HC, Clemens JC (2012) Drosophila activated Cdc42 kinase has an anti-apoptotic function. PLoS Genet 8(5):e1002725

    CAS  PubMed Central  PubMed  Google Scholar 

  • Seit-Nebi AS, Datskevich P, Gusev NB (2013) Commentary on paper: small heat shock proteins and the cytoskeleton: an essential interplay for cell integrity? (Wettstein et al.). Int J Biochem Cell Biol 45(2):344–346

    CAS  PubMed  Google Scholar 

  • Senthilan PR, Piepenbrock D, Ovezmyradov G, Nadrowski B, Bechstedt S, Pauls S, Winkler M, Mobius W, Howard J, Gopfert MC (2012) Drosophila auditory organ genes and genetic hearing defects. Cell 150(5):1042–1054

    CAS  PubMed  Google Scholar 

  • Sharma A, Mishra M, Ram KR, Kumar R, Abdin MZ, Chowdhuri DK (2011) Transcriptome analysis provides insights for understanding the adverse effects of endosulfan in Drosophila melanogaster. Chemosphere 82(3):370–376

    CAS  PubMed  Google Scholar 

  • Sharma A, Mishra M, Shukla AK, Kumar R, Abdin MZ, Chowdhuri DK (2012) Organochlorine pesticide, endosulfan induced cellular and organismal response in Drosophila melanogaster. J Hazard Mater 221–222:275–287

    PubMed  Google Scholar 

  • Shen J, Tower J (2010) Drosophila foxo acts in males to cause sexual-dimorphism in tissue-specific p53 life span effects. Exp Gerontol 45(2):97–105

    PubMed Central  PubMed  Google Scholar 

  • Shen J, Tower J (2013) Aging, MnSOD, and hormesis mechanisms converge on liver mUPR. Cell Cycle 12(20):3237–3238

    CAS  PubMed Central  PubMed  Google Scholar 

  • Singh MP, Reddy MM, Mathur N, Saxena DK, Chowdhuri DK (2009) Induction of hsp70, hsp60, hsp83 and hsp26 and oxidative stress markers in benzene, toluene and xylene exposed Drosophila melanogaster: role of ROS generation. Toxicol Appl Pharmacol 235(2):226–243

    CAS  PubMed  Google Scholar 

  • Singh MP, Ram KR, Mishra M, Shrivastava M, Saxena DK, Chowdhuri DK (2010) Effects of co-exposure of benzene, toluene and xylene to Drosophila melanogaster: alteration in hsp70, hsp60, hsp83, hsp26, ROS generation and oxidative stress markers. Chemosphere 79(5):577–587

    CAS  PubMed  Google Scholar 

  • Soh JW, Marowsky N, Nichols TJ, Rahman AM, Miah T, Sarao P, Khasawneh R, Unnikrishnan A, Heydari AR, Silver RB, Arking R (2013) Curcumin is an early-acting stage-specific inducer of extended functional longevity in Drosophila. Exp Gerontol 48(2):229–239

    CAS  PubMed  Google Scholar 

  • Steller H (2008) Regulation of apoptosis in Drosophila. Cell Death Differ 15(7):1132–1138

    CAS  PubMed  Google Scholar 

  • Stuart LM, Boulais J, Charriere GM, Hennessy EJ, Brunet S, Jutras I, Goyette G, Rondeau C, Letarte S, Huang H, Ye P, Morales F, Kocks C, Bader JS, Desjardins M, Ezekowitz RA (2007) A systems biology analysis of the Drosophila phagosome. Nature 445(7123):95–101

    CAS  PubMed  Google Scholar 

  • Sun X, Seeberger J, Alberico T, Wang C, Wheeler CT, Schauss AG, Zou S (2010) Acai palm fruit (Euterpe oleracea Mart.) pulp improves survival of flies on a high fat diet. Exp Gerontol 45(3):243–251

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takahashi KH, Rako L, Takano-Shimizu T, Hoffmann AA, Lee SF (2010) Effects of small Hsp genes on developmental stability and microenvironmental canalization. BMC Evol Biol 10:284

    PubMed Central  PubMed  Google Scholar 

  • Tanguay RM, Morrow G (2008) Neuronal expression of small heat shock proteins influences longevity and resistance to oxidative stress. In: Asea AAA, Brown IR (eds) Heat shock proteins and the brain: implications for neurodegenerative diseases and neuroprotection. Springer, New York, pp 319–336

    Google Scholar 

  • Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, Garofalo RS (2001) A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292(5514):107–110

    CAS  PubMed  Google Scholar 

  • Telonis-Scott M, van Heerwaarden B, Johnson TK, Hoffmann AA, Sgro CM (2013) New levels of transcriptome complexity at upper thermal limits in wild Drosophila revealed by exon expression analysis. Genetics 195(3):809–830

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tomancak P, Berman BP, Beaton A, Weiszmann R, Kwan E, Hartenstein V, Celniker SE, Rubin GM (2007) Global analysis of patterns of gene expression during Drosophila embryogenesis. Genome Biol 8(7):R145

    PubMed Central  PubMed  Google Scholar 

  • Tower J, Landis G, Gao R, Luan A, Lee J, Sun Y (2014) Variegated expression of Hsp22 transgenic reporters indicates cell-specific patterns of aging in Drosophila oenocytes. J Gerontol A Biol Sci Med Sci 69(3):253–259

    CAS  PubMed  Google Scholar 

  • Treusch S, Hamamichi S, Goodman JL, Matlack KE, Chung CY, Baru V, Shulman JM, Parrado A, Bevis BJ, Valastyan JS, Han H, Lindhagen-Persson M, Reiman EM, Evans DA, Bennett DA, Olofsson A, DeJager PL, Tanzi RE, Caldwell KA, Caldwell GA, Lindquist S (2011) Functional links between Abeta toxicity, endocytic trafficking, and Alzheimer’s disease risk factors in yeast. Science 334(6060):1241–1245

    CAS  PubMed Central  PubMed  Google Scholar 

  • van den IJssel P, Wheelock R, Prescott A, Russell P, Quinlan RA (2003) Nuclear speckle localisation of the small heat shock protein alpha B-crystallin and its inhibition by the R120G cardiomyopathy-linked mutation. Exp Cell Res 287(2):249–261

    PubMed  Google Scholar 

  • van der Straten A, Rommel C, Dickson B, Hafen E (1997) The heat shock protein 83 (Hsp83) is required for Raf-mediated signalling in Drosophila. EMBO J 16(8):1961–1969

    PubMed Central  PubMed  Google Scholar 

  • van Montfort RL, Basha E, Friedrich KL, Slingsby C, Vierling E (2001) Crystal structure and assembly of a eukaryotic small heat shock protein. Nat Struct Biol 8(12):1025–1030

    PubMed  Google Scholar 

  • van Noort JM, Bsibsi M, Nacken P, Gerritsen WH, Amor S (2012) The link between small heat shock proteins and the immune system. Int J Biochem Cell Biol 44(10):1670–1679

    PubMed  Google Scholar 

  • Vesala L, Salminen TS, Laiho A, Hoikkala A, Kankare M (2012) Cold tolerance and cold-induced modulation of gene expression in two Drosophila virilis group species with different distributions. Insect Mol Biol 21(1):107–118

    CAS  PubMed  Google Scholar 

  • Vos MJ (2009) Small heat shock proteins; implications for neurodegeneration and longevity. Thesis, University of Groningen, The Netherlands.

    Google Scholar 

  • Wadhwa R, Ryu J, Gao R, Choi IK, Morrow G, Kaur K, Kim I, Kaul SC, Yun CO, Tanguay RM (2010) Proproliferative functions of Drosophila small mitochondrial heat shock protein 22 in human cells. J Biol Chem 285(6):3833–3839

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang MC, Bohmann D, Jasper H (2003) JNK signaling confers tolerance to oxidative stress and extends lifespan in Drosophila. Dev Cell 5(5):811–816

    CAS  PubMed  Google Scholar 

  • Wang HD, Kazemi-Esfarjani P, Benzer S (2004) Multiple-stress analysis for isolation of Drosophila longevity genes. Proc Natl Acad Sci U S A 101(34):12610–12615

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang MC, Bohmann D, Jasper H (2005) JNK extends life span and limits growth by antagonizing cellular and organism-wide responses to insulin signaling. Cell 121(1):115–125

    CAS  PubMed  Google Scholar 

  • Wang L, Colodner KJ, Feany MB (2011) Protein misfolding and oxidative stress promote glial-mediated neurodegeneration in an Alexander disease model. J Neurosci 31(8):2868–2877

    CAS  PubMed Central  PubMed  Google Scholar 

  • Waters ER (2013) The evolution, function, structure, and expression of the plant sHSPs. J Exp Bot 64(2):391–403

    CAS  PubMed  Google Scholar 

  • Wettstein G, Bellaye PS, Micheau O, Bonniaud P (2012) Small heat shock proteins and the cytoskeleton: an essential interplay for cell integrity? Int J Biochem Cell Biol 44(10):1680–1686

    CAS  PubMed  Google Scholar 

  • Xi Z, Gavotte L, Xie Y, Dobson SL (2008) Genome-wide analysis of the interaction between the endosymbiotic bacterium Wolbachia and its Drosophila host. BMC Genomics 9:1

    PubMed Central  PubMed  Google Scholar 

  • Yang J, Tower J (2009) Expression of hsp22 and hsp70 transgenes is partially predictive of drosophila survival under normal and stress conditions. J Gerontol A Biol Sci Med Sci 64(8):828–838

    PubMed  Google Scholar 

  • Yepiskoposyan H, Egli D, Fergestad T, Selvaraj A, Treiber C, Multhaup G, Georgiev O, Schaffner W (2006) Transcriptome response to heavy metal stress in Drosophila reveals a new zinc transporter that confers resistance to zinc. Nucleic Acids Res 34(17):4866–4877

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localization. Proteins 64(3):643–651

    CAS  PubMed  Google Scholar 

  • Zamparini AL, Davis MY, Malone CD, Vieira E, Zavadil J, Sachidanandam R, Hannon GJ, Lehmann R (2011) Vreteno, a gonad-specific protein, is essential for germline development and primary piRNA biogenesis in Drosophila. Development 138(18):4039–4050

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhai B, Villen J, Beausoleil SA, Mintseris J, Gygi SP (2008) Phosphoproteome analysis of Drosophila melanogaster embryos. J Proteome Res 7(4):1675–1682

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang D, Ke L, Mackovicova K, Van Der Want JJ, Sibon OC, Tanguay RM, Morrow G, Henning RH, Kampinga HH, Brundel BJ (2011a) Effects of different small HSPB members on contractile dysfunction and structural changes in a Drosophila melanogaster model for Atrial Fibrillation. J Mol Cell Cardiol 51(3):381–389

    CAS  PubMed  Google Scholar 

  • Zhang J, Marshall KE, Westwood JT, Clark MS, Sinclair BJ (2011b) Divergent transcriptomic responses to repeated and single cold exposures in Drosophila melanogaster. J Exp Biol 214(Pt 23):4021–4029

    PubMed  Google Scholar 

  • Zhao Y, Sun H, Lu J, Li X, Chen X, Tao D, Huang W, Huang B (2005) Lifespan extension and elevated hsp gene expression in Drosophila caused by histone deacetylase inhibitors. J Exp Biol 208(Pt 4):697–705

    CAS  PubMed  Google Scholar 

  • Zimmermann G, Furlong EE, Suyama K, Scott MP (2006) Mes2, a MADF-containing transcription factor essential for Drosophila development. Dev Dyn 235(12):3387–3395

    CAS  PubMed  Google Scholar 

  • Zou S, Meadows S, Sharp L, Jan LY, Jan YN (2000) Genome-wide study of aging and oxidative stress response in Drosophila melanogaster. Proc Natl Acad Sci U S A 97(25):13726–13731

    CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Dr. Halim Maaroufi for his advice regarding the sHsp sequence analysis. This work was supported by grants from the Canadian Institutes of Health Research and the National Sciences Engineering Research Council to RMT.

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  1. Department of Molecular Biology, Medical Biochemistry & Pathology Medical School Lab Cell & Developmental Genetics IBIS, Pavillon C.E. Marchand 1030 Ave de la médecine Université Laval, Québec, QC, Canada, G1V 0A6

    Geneviève Morrow & Robert M. Tanguay

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Correspondence to Robert M. Tanguay .

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  1. Department of Molecular Biology, Medical Biochemistry & Pathology Medical School Lab Cell & Developmental Genetics IBIS, Université Laval, Quebec, Québec, Canada

    Robert M. Tanguay

  2. Department of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut, USA

    Lawrence E. Hightower

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Morrow, G., Tanguay, R.M. (2015). Drosophila Small Heat Shock Proteins: An Update on Their Features and Functions. In: Tanguay, R., Hightower, L. (eds) The Big Book on Small Heat Shock Proteins. Heat Shock Proteins, vol 8. Springer, Cham. https://doi.org/10.1007/978-3-319-16077-1_25

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