Skip to main content
Log in

Tissue-specific targeting of Hsp26 has no effect on heat resistance of neural function in larval Drosophila

  • Original Paper
  • Published:
Cell Stress and Chaperones Aims and scope

Abstract

Hsp26 belongs to the small heat-shock protein family and is normally expressed in all cells during heat stress. We aimed to determine if overexpression of this protein protects behavior and neural function in Drosophila melanogaster during heat stress, as has previously been shown for Hsp70. We used the UAS-GAL4 expression system to drive expression of Hsp26 in the whole animal (ubiquitously), in the motoneurons, and in the muscles of wandering third-instar larvae. There were slight increases in time to crawling failure and normalized excitatory junction potential (EJP) area for some of the transgenic lines, but these were not consistent. In addition, Hsp26 had no effect on the temperature at failure of EJPs, normalized EJP peak amplitude, and normalized EJP half-width. Overexpression larvae had a similar number of motoneuronal boutons and length of nerve terminals as controls, indicating that the occasional protective effects on locomotion were not due to changes at the synapse. We conclude that overexpression had a small thermoprotective effect on locomotion and no effect on neural function. As it has been shown that Hsp26 requires action of other Hsps to reactivate the denatured proteins to which it binds, we propose that at least in larvae, the function of Hsp26 was masked in the relative absence of other Hsps.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aberle H, Haghighi AP, Fetter RD, McCabe BD, Magalhaes TR, Goodman CS (2002) Wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 33:545–558

    Article  PubMed  CAS  Google Scholar 

  • Barclay JW, Atwood HL, Robertson RM (2002) Impairment of central pattern generation in Drosophila cysteine string protein mutants. J Comp Physiol A 188:71–78

    Article  Google Scholar 

  • Batulan Z, Taylor DM, Aarons RJ, Minotti S, Doroudchi MM, Nalbantoglu J, Durham HD (2006) Induction of multiple heat shock proteins and neuroprotection in a primary culture model of familial amyotrophic lateral sclerosis. Neurobiol Dis 24:213–225

    Article  PubMed  CAS  Google Scholar 

  • Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 11:401–415

    Google Scholar 

  • Cashikar AG, Duennwald M, Lindquist SM (2005) A chaperone pathway in protein disaggregation: Hsp26 alters the nature of protein aggregates to facilitate reactivation by Hsp104. J Biol Chem 280:23869–23875

    Article  PubMed  CAS  Google Scholar 

  • Curci A, Bevilacqua A, Magia F (1987) Lack of heat shock response in preovulatory mouse oocytes. Developmental Biology 123:154–160

    Article  PubMed  CAS  Google Scholar 

  • Cullheim S, Kellerth JO (1978) A morphological study of the axons and recurrent axon collaterals of cat a-motoneurones supplying different hind limb muscles. J. Physiol. 281:285–299

    PubMed  CAS  Google Scholar 

  • DiAntonio A, Petersen SA, Heckmann M, Goodman CS (1999) Glutamate receptor expression regulates quantal size and quantal content at the Drosophila neuromuscular junction. The Journal of Neuroscience 19:3023–3032

    PubMed  CAS  Google Scholar 

  • Dunn TW, Mercier AJ (2003) Synaptic modulation by a neuropeptide depends on temperature and extracellular calcium. J Physiol 89:1807–1814

    CAS  Google Scholar 

  • Feder ME, Cartano NV, Milos L, Krebs RA, Lindquist S (1996) Effect of engineering Hsp70 copy number on Hsp70 expression and tolerance of ecologically relevant heat shock in larvae and pupae of Drosophila melanogaster. J Exp Biol 199:1837–1844

    PubMed  CAS  Google Scholar 

  • Garlick KM, Robertson RM (2007) Cytoskeletal stability and heat shock-mediated thermoprotection of central pattern generation in Locusta migratoria. Comp Biochem Physiol A 147:344–348

    Article  Google Scholar 

  • Glaser RL, Wolfner MF, Lis JT (1986) Spatial and temporal pattern of hsp26 expression during normal development. EMBO J 5:747–754

    PubMed  CAS  Google Scholar 

  • Gorczyca MG, Budnik V, White K, Wu CF (1991) Dual muscarinic and nicotinic action on a motor program in Drosophila. J Neurobiol 22:391–404

    Article  PubMed  CAS  Google Scholar 

  • Haslbeck M (2002) sHsps and their role in the chaperone network. Cell Mol Life Sci 59:1649–1657

    Article  PubMed  CAS  Google Scholar 

  • Haslbeck M, Walke S, Stromer T, Ehrnsperger M, White HE, Chen S, Saibil HR, Buchner J (1999) Hsp26: a temperature-regulated chaperone. EMBO J 18:6744–6761

    Article  PubMed  CAS  Google Scholar 

  • Johnston RM, Levine RB (1996) Crawling motor patterns induced by pilocarpine in isolated larval nerve cords of Manduca sexta. J Neurophysiol 76:3178–3195

    PubMed  CAS  Google Scholar 

  • Karunanithi S, Barclay JW, Robertson RM, Brown IR, Atwood HL (1999) Neuroprotection at Drosophila synapses conferred by prior heat shock. J Neurosci 19:4360–4369

    PubMed  CAS  Google Scholar 

  • Karunanithi S, Barclay JW, Brown IR, Robertson RM, Atwood HL (2002) Enhancement of presynaptic performance in transgenic Drosophila overexpressing heat shock protein HSP70. Synapse 44:8–14

    Article  PubMed  CAS  Google Scholar 

  • Kelty JD, Noseworthy PA, Feder ME, Robertson RM, Ramirez JM (2002) Thermal preconditioning and heat-shock protein 72 preserve synaptic transmission during thermal stress. J Neurosci 22:RC193

    PubMed  Google Scholar 

  • Klose MK, Armstrong G, Robertson RM (2004) A role for the cytoskeleton in heat shock-mediated thermoprotection of locust neuromuscular junctions. J Neurobiol 60:453–462

    Article  PubMed  CAS  Google Scholar 

  • Klose MK, Chu D, Xiao C, Seroude L, Robertson RM (2005) Heat shock-mediated thermoprotection of larval locomotion compromised by ubiquitous expression of Hsp70 in Drosophila melanogaster. J Neurophysiol 94:3563–3572

    Article  PubMed  CAS  Google Scholar 

  • Kramer JM, Staveley BE (2003) GAL4 causes developmental defects and apoptosis when expressed in the developing eye of Drosophila melanogaster. Genet Mol Res 2:43–47

    PubMed  CAS  Google Scholar 

  • Kurdyak P, Atwood HL, Stewart BA, Wu CF (1994) Differential morphology and physiology of motor axons to ventral longitudinal muscles in larval Drosophila. J Comp Neurol 350:463–472

    Article  PubMed  CAS  Google Scholar 

  • Lee GJ, Vierling E (2000) A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Fiziol Rast 122:189–197

    CAS  Google Scholar 

  • Leicht BG, Biessman H, Balter KB, Bonner JJ (1986) Small heat shock proteins of Drosophila associate with the cytoskeleton. Proc Natl Acad Sci 83:90–94

    Article  PubMed  CAS  Google Scholar 

  • Li H, Peng X, Cooper RL (2002) Development of Drosophila larval neuromuscular junctions: maintaining synaptic strength. Neuroscience 115:505–513

    Article  PubMed  CAS  Google Scholar 

  • Lnenicka GA, Mellon D (1983) Changes in electrical properties and quantal current during growth of identified muscle fibers in the crayfish. J Physiol 345:261–284

    PubMed  CAS  Google Scholar 

  • Macleod GT, Hegstrom-Wojtowicz M, Charlton MP, Atwood HL (2002) Fast calcium signals in Drosophila motor neuron terminals. J Neurosci 88:2659–2663

    CAS  Google Scholar 

  • Morrow G, Tanguay RM (2003) Heat shock proteins and ageing in Drosophila melanogaster. Semin Cell Dev Biol 14:291–299

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  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 11:51–60

    Article  PubMed  CAS  Google Scholar 

  • Mounier N, Arrigo AP (2002) Actin cytoskeleton and small heat shock proteins: how do they interact. Cell Stress Chaperones 7:167–176

    Article  PubMed  CAS  Google Scholar 

  • Newman AEM, Xiao C, Robertson RM (2005) Synaptic thermoprotection is a desert-dwelling Drosophila species. J Neurobiol 64:170–180

    Article  PubMed  CAS  Google Scholar 

  • Parkes TL, Elia AJ, Dickinson D, Hilliker AJ, Phillips JP, Boulianne GL (1998) Extension of Drosophila lifespan by overexpression of human SOD1 in motoneurons. Nat Genet 19:171–174

    Article  PubMed  CAS  Google Scholar 

  • Patel YJK, Smith MDP, de Belleroche J, Latchman DS (2005) Hsp27 and Hsp70 administered in combination have a potent protective effect against FALS-associated SOD1-mutant-induced cell death in mammalian neuronal cells. Mol Brain Res 134:256–274

    Article  PubMed  CAS  Google Scholar 

  • Petko L, Lindquist S (1986) Hsp26 is not required for growth at high temperatures, nor for thermotolerance, spore development, or germination. Cell 45:885–894

    Article  PubMed  CAS  Google Scholar 

  • Robertson RM (1993) Effects of temperature on synaptic potentials in the locust flight system. J Neurophysiol 70:2197–2204

    PubMed  CAS  Google Scholar 

  • Robertson RM (2004) Thermal stress and neural function: adaptive mechanisms in insect model systems. J Therm Biol 29:351–358

    Article  CAS  Google Scholar 

  • Rohrbough J, O’Dowd DK, Baines RA, Broadie K (2003) Cellular bases of behavioral plasticity: establishing and modifying synaptic circuits in the Drosophila genetic system. J Neurobiol 54:254–271

    Article  PubMed  CAS  Google Scholar 

  • Ryckebusch S, Laurent G (1993) Rhythmic patterns evoked in locust leg motor neurons by the muscarinic agonist pilocarpine. J Neurophysiol 69(5):1583–1595

    PubMed  CAS  Google Scholar 

  • Sirotkin K, Davidson N (1981) Developmentally regulated transcription from Drosophila melanogaster chromosomal site 67B. Dev Biol 89:196–210

    Article  Google Scholar 

  • Stewart BA, Atwood HL, Renger JJ, Wang J, Wu CF (1994) Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J Comp Physiol A 175:179–191

    Article  PubMed  CAS  Google Scholar 

  • Stewart BA, Schuster CM, Goodman CS, Atwood HL (1996) Homeostasis of synaptic transmission in Drosophila with genetically altered nerve terminal morphology. J Neurosci 16:3877–3886

    PubMed  CAS  Google Scholar 

  • Stromer T, Ehrnsperger M, Gaestel M, Buchner J (2003) Analysis of the interaction of small heat shock proteins with unfolding proteins. J Biol Chem 278:18015–18021

    Article  PubMed  CAS  Google Scholar 

  • Wan HI, DiAntonio A, Fetter RD, Bergstrom K, Strauss R, Goodman C (2000) Highwire regulates synaptic growth in Drosophila. Neuron 26:313–329

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Xiao C, Mileva-Seitz V, Seroude L, Robertson RM (2007) Targeting HSP70 to motoneurons protects locomotor activity from hyperthermia in Drosophila. Dev Neurobiol 67:438–455

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank CIHR for supporting this work. In addition, we thank Seymour Benzer and his lab for providing us flies with the UAS insertion points. Thanks also to Dr. Robert Tanguay for providing us with Hsp26 antibody.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. Meldrum Robertson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mileva-Seitz, V., Xiao, C., Seroude, L. et al. Tissue-specific targeting of Hsp26 has no effect on heat resistance of neural function in larval Drosophila . Cell Stress and Chaperones 13, 85–95 (2008). https://doi.org/10.1007/s12192-008-0016-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12192-008-0016-6

Keywords

Navigation