Skip to main content
SpringerLink
Log in

Ecological and evolutionary physiology of heat shock proteins and the stress response in Drosophila: Complementary insights from genetic engineering and natural variation

  • Chapter
Environmental Stress, Adaptation and Evolution

Part of the book series: Experientia Supplementum ((EXS,volume 83))

Summary

Classical adaptational and genetic engineering approaches offer complementary insights to understanding biological variation: the former elucidates the origins, magnitude and ecological context of natural variation, while the latter establishes which genes can underlie natural variation. Studies of the stress or heat shock response in Drosophila illustrate this point. At the cellular level, heat shock proteins (Hsps) function as molecular chaperones, minimizing aggregation of peptides in non-native conformations. To understand the adaptive significance of Hsps, we have characterized thermal stress that Drosophila experience in nature, which can be substantial. We used these findings to design ecologically relevant experiments with engineered Drosophila strains generated by unequal site-specific homologous recombination; these strains differ in hsp70 copy number but share sites of transgene integration. hsp70 copy number markedly affects Hsp70 levels in intact Drosophila and strains with extra hsp70 copies exhibit corresponding differences in inducible thermotolerance and reactivation of a key enzyme after thermal stress. Elevated Hsp70 levels, however, are not without penalty; these levels retard growth and increase mortality. Transgenic variation in hsp70 copy number has counterparts in nature: isofemale lines from nature vary significantly in Hsp70 expression, and this variation is also correlated with both inducible thermotolerance and mortality in the absence of stress.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Ashburner, M. (1989) Drosophila: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

    Google Scholar 

  • Chambers, G.K. (1988) The Drosophila alcohol dehydrogenase gene-enzyme system. Adv. Genet. 25:39–108.

    Article  CAS  Google Scholar 

  • Coleman, J.S., Heckathorn, S.A. and Hallberg, R.L. (1995) Heat-shock proteins and thermotolerance: Linking ecological and molecular perspectives. Trend Ecol. Evolut. 10:305–306.

    Article  CAS  Google Scholar 

  • Cossins, A.R. and Bowler, K. (1987) Temperature Biology of Animals. Chapman and Hall, London.

    Book  Google Scholar 

  • David, J.R., Allemand, R., Van Herrewege, J. and Cohet, Y. (1983) Ecophysiology: Abiotic factors. In: M. Ashburner, H.L. Carson and J.N. Thompson (eds): The Genetics and Biology of Drosophila, third Edition. Academic Press, London, pp. 105–170.

    Google Scholar 

  • diIorio, P.J., Holsinger, K., Schultz, R.J. and Hightower, L.E. (1996) Quantitative evidence that both Hsc70 and Hsp70 contribute to thermal adaptation in hybrids of the livebearing fishes Poeciliopsis. Cell Stress & Chaperones 1: 139–147.

    Article  CAS  Google Scholar 

  • Dorner, A.J., Krane, M.G. and Kaufman, R.J. (1988) Reduction of endogenous GRP78 levels improves secretion of a heterologous protein in CHO cells. Mol. Cell. Biol. 8:4063–4070.

    PubMed  CAS  Google Scholar 

  • Dorner, A.J., Wasley, L.C. and Kaufman, R.J. (1992) Overexpression of GRP78 mitigates stress induction of glucose regulated proteins and blocks secretion of selective proteins in Chinese hamster ovary cells. EMBOJ. 11:1563–1571.

    CAS  Google Scholar 

  • Edgecomb, R.S., Harth, C.E. and Schneiderman, A.M. (1994) Regulation of feeding behaviour in adult Drosophila melanogaster varies with feeding regime and nutritional state. J. Exp. Biol. 197:215–236.

    PubMed  CAS  Google Scholar 

  • Feder, J.H., Rossi, J.M., Solomon, J., Solomon, N. and Lindquist, S. (1992) The consequences of expressing hsp70 in Drosophila cells at normal temperatures. Genes & Develop. 6: 1402–1413.

    Article  CAS  Google Scholar 

  • Feder, M.E. (1996) Ecological and evolutionary physiology of stress proteins and the stress response: The Drosophila melanogaster model. In:I.A. Johnston and A.F. Bennett (eds): Animals and Temperature: Phenotypic and Evolutionary Adaptation. Cambridge University Press, Cambridge, pp. 79–102.

    Chapter  Google Scholar 

  • Feder, M.E. and Block, B.A. (1991) On the future of physiological ecology. Funct. Ecol. 5:136–144.

    Article  Google Scholar 

  • Feder, M.E. and Watt, W.B. (1993). Functional biology of adaptation. In: R.J. Berry, T.J. Crawford and G.M. Hewitt (eds): Genes in Ecology. Blackwell Scientific Publications, Oxford, pp. 365–391.

    Google Scholar 

  • Feder, M.E., Parsell, D.A. and Lindquist, S.L. (1995). The stress response and stress proteins. In: J.J. Lemasters and C. Oliver (eds): Cell Biology of Trauma. CRC Press, Boca Raton, FL, pp. 177–191.

    Google Scholar 

  • Feder, M.E., Cartaño, N.V., Milos, L., Krebs, R.A. and Lindquist, S.L. (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 

  • Feder, M.E., Blair, N. and Figueras, H. (1997a) Natural thermal stress and heat-shock protein expression in Drosophila larvae and pupae. Funct. Ecol. 11:90–100.

    Article  Google Scholar 

  • Feder, M.E., Blair, N. and Figueras, H. (1997b) Oviposition site selection and temperature: Unresponsiveness of ovipositing Drosophila to cues of potential thermal stress on offspring. Anim. Behay. 53:585–588.

    Article  Google Scholar 

  • Fogleman, J. (1979) Oviposition site preference for temperature in D. melanogaster. Behay. Genet. 9:407–412.

    CAS  Google Scholar 

  • Golic, K.G. and Lindquist, S. (1989) The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59:499–509.

    Article  PubMed  CAS  Google Scholar 

  • Hartl, F.U. (1996) Molecular chaperones in cellular protein folding. Nature 381:571–580.

    Article  PubMed  CAS  Google Scholar 

  • Heads, R.J., Latchman, D.S. and Yellon, D.M. (1994) Stable high level expression of a trans-fected human HSP70 gene protects a heart-derived muscle cell line against thermal stress. J. Mol. Cell. Cardiol. 26:695–699.

    Article  PubMed  CAS  Google Scholar 

  • Huey, R.B., Crill, W.D., Kingsolver, J.G. and Weber, K.E. (1992) A method for rapid measurement of heat or cold resistance of small insects. Funct. Ecol. 6:489–494.

    Article  Google Scholar 

  • Ish-Horowicz, D., Pinchin, S.M., Schedl, P., Artavanis, T.S. and Mirault, M.E. (1979) Genetic and molecular analysis of the 87A7 and 87C1 heat-inducible loci of D. melanogaster. Cell 18:1351–1358.

    Article  PubMed  CAS  Google Scholar 

  • Koehn, R.K. (1987) The importance of genetics to physiological ecology. In: M.E. Feder, A.F. Bennett, W.W. Burggren and R.B. Huey (eds): New Directions in Ecological Physiology. Cambridge University Press, Cambridge, pp. 170–185.

    Google Scholar 

  • Krebs, R.A. and Bean, K.L. (1991) The mating behavior of Drosophila mojavensis on organ pipe and agria cactus. Psyche 98:101–109.

    Article  Google Scholar 

  • Krebs, R.A. and Feder, M.E. (1997a) Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress & Chaperones 2:60–71.

    Article  CAS  Google Scholar 

  • Krebs, R.A. and Feder, M.E. (1997b) Natural variation in the expression of the heat-shock protein Hsp70 in a population of Drosophila melanogaster and its correlation with tolerance of ecologically relevant thermal stress. Evolution 51:173–179.

    Article  Google Scholar 

  • Krebs, R.A. and Loeschcke, V. (1994a) Costs and benefits of activation of the heat-shock response in Drosophila melanogaster. Funct. Ecol. 8:730–737.

    Article  Google Scholar 

  • Krebs, R.A. and Loeschcke, V. (1994b) Response to environmental change: Genetic variation and fitness in Drosophila buzzatii following temperature stress. In: V. Loeschcke, J. Tomiuk and S.K. Jain (eds): Conservation Genetics. Birkhäuser, Basel, pp. 309–321.

    Chapter  Google Scholar 

  • Lee, Y.J., Kim, D., Hou, Z.Z., Curetty, L., Borrelli, M.J. and Corry, P.M. (1993) Alteration of heat sensitivity by introduction of hsp70 or anti-hsp70 in CHO cells. J. Therm. Biol. 18:229–236.

    Article  CAS  Google Scholar 

  • Lewontin, R.C. (1978) Adaptation. Sci. Amer. 239:156–169.

    Article  Google Scholar 

  • Li, G.C., Li, L.G., Liu, Y.K., Mak, J.Y., Chen, L.L. and Lee, W.M. (1991) Thermal response of rat fibroblasts stably transfected with the human 70-kDa heat shock protein-encoding gene. Proc. Natl. Acad. Sci. USA 88:1681–1685.

    Article  PubMed  CAS  Google Scholar 

  • Li, L., Shen, G. and Li, G.C. (1995) Effects of expressing human Hsp70 and its deletion derivatives on heat killing and on RNA and protein synthesis. Exp. Cell Res. 217:460468.

    Google Scholar 

  • Lindquist, S. (1980) Translational efficiency of heat-induced messages in Drosophila melanogaster cells. J. Mol. Biol. 137:151–158.

    Article  PubMed  CAS  Google Scholar 

  • Lindquist, S. (1993) Autoregulation of the heat-shock response. In: J. Ilan (ed.) Translational Regulation of Gene Expression 2. Plenum Press, New York, pp. 279–320.

    Chapter  Google Scholar 

  • Lindquist, S. and Craig, E.A. (1988) The heat-shock proteins. Annu. Rev. Genet. 22:631–677.

    Article  PubMed  CAS  Google Scholar 

  • Lis, J., Neckameyer, W, Mirault, M.E., Artavanis, T.S., Lall, P, Martin, G. and Schedl, P. (1981a) DNA sequences flanking the starts of the hsp70 and alpha beta heat shock genes are homologous. Dev. Biol. 83:291–300.

    Article  PubMed  CAS  Google Scholar 

  • Lis, J.T., Ish, H.D. and Pinchin, S.M. (1981b) Genomic organization and transcription of the alpha beta heat shock DNA in Drosophila melanogaster. Nucleic Acids Res. 9:5297–5310.

    Article  PubMed  CAS  Google Scholar 

  • Lis, J.T., Neckameyer, W, Dubensky, R. and Costlow, N. (1981c) Cloning and characterization of nine heat-shock-induced mRNAs of Drosophila melanogaster. Gene 15: 67–80.

    Article  PubMed  CAS  Google Scholar 

  • Liu, R.Y., Li, X., Li, L. and Li, G.C. (1992) Expression of human hsp70 in rat fibroblasts enhances cell survival and facilitates recovery from translational and transcriptional inhibition following heat shock. Cancer Res. 52:3667–3673.

    PubMed  CAS  Google Scholar 

  • Mailhos, C., Howard, M.K. and Latchman, D.S. (1994) Heat shock proteins hsp90 and hsp70 protect neuronal cells from thermal stress but not from programmed cell death. J. Neurochem. 63: 1787–1795.

    Article  PubMed  CAS  Google Scholar 

  • Marber, M.S., Mestril, R., Chi, S.H., Sayen, M.R., Yellon, D.M. and Dillmann, W.H. (1995) Overexpression of the rat inducible 70-kD heat stress protein in a transgenic mouse increases the resistance of the heart to ischemic injury. J. Clin. Invest. 95:1446–1456.

    Article  PubMed  CAS  Google Scholar 

  • McColl, G., Hoffmann, A.A. and McKechnie, S.W. (1996) Response of two heat shock genes to selection for knockdown heat resistance in Drosophila melanogaster. Genetics 143:1615–1627.

    PubMed  CAS  Google Scholar 

  • McKechnie, S.W. and Geer, B.W. (1984) Regulation of alcohol dehydrogenase in Drosophila melanogaster by dietary alcohol and carbohydrate. Insect Biochem. 14, 231–242.

    Article  CAS  Google Scholar 

  • Mirault, M.E., Goldschmidt, C.M., Artavanis, T.S. and Schedl, P. (1979) Organization of the multiple genes for the 70,000-dalton heat-shock protein in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 76:5254–5258.

    Article  PubMed  CAS  Google Scholar 

  • Moreau, N., Laine, M.C., Billoud, B. and Angelier, N. (1994) Transcription of amphibian lamp-brush chromosomes is disturbed by microinjection of HSP70 monoclonal antibodies. Exp. Cell Res. 211:108–114.

    Article  PubMed  CAS  Google Scholar 

  • Morimoto, R.I., Tissieres, A. and Georgopoulos, C. (eds) (1994) The Biology of Heat Shock Proteins and Molecular Chaperones. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

    Google Scholar 

  • Nakata, N., Kato, H. and Kogure, K. (1993) Inhibition of ischaemic tolerance in the gerbil hippocampus by quercetin and anti-heat shock protein-70 antibody. Neuroreport 4: 695–698.

    Article  PubMed  CAS  Google Scholar 

  • Palter, K.B., Watanabe, M., Stinson, L., Mahowald, A.P. and Craig, E.A. (1986) Expression and localization of Drosophila melanogaster hsp70 cognate proteins. Mol. Cell. Biol. 6:1187–1203.

    PubMed  CAS  Google Scholar 

  • Parsell, D.A. and Lindqust, S. (1993) The function of heat-shock proteins in stress tolerance: Degradation and reactivation of damaged proteins. Annu. Rev. Genet. 27: 437–496.

    Article  PubMed  CAS  Google Scholar 

  • Parsell, D.A., Kowal, A.S., Singer, M.A. and Lindquist, S. (1994) Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372: 475–478.

    Article  PubMed  CAS  Google Scholar 

  • Parsons, P. (1978) Boundary conditions for Drosophila resource utilization in temperate regions, especially at low temperatures. Am. Nat. 112, 1063–1074.

    Article  Google Scholar 

  • Partridge, L. (1994) Genetic and nongenetic approaches to questions about sexual selection. In: C.R.B. Boake (ed): Quantitative Genetic Studies of Behavioral Evolution. University of Chicago Press, Chicago, pp. 126–141.

    Google Scholar 

  • Plumier, J.C., Ross, B.M., Currie, R.W., Angelidis, C.E., Kazlaris, H., Kollias, G. and Pagoulatos, G.N. (1995) Transgenic mice expressing the human heat shock protein 70 have improved post-ischemic myocardial recovery. J. Clin. Invest. 95:1854–1860.

    Article  PubMed  CAS  Google Scholar 

  • Powers, D.A., Smith, M., Gonzalez-Villasenor, I., DiMichele, L., Crawford, D.L., Bernardi, G. and Lauerman, T. (1993) A multidisciplinary approach to the selectionist/neutralist controversy using the model teleost Fundulus heteroclitus. In: D. Futuyma and J. Antonovics (eds): Oxford Surveys in Evolutionary Biology 9, pp. 43–107.

    Google Scholar 

  • Precht, H., Christophersen, J., Hensel, H. and Larcher, W. (eds) (1973) Temperature and Life. Springer-Verlag, Berlin.

    Google Scholar 

  • Riabowol, K.T., Mizzen, L.A. and Welch, W.J. (1988) Heat shock is lethal to fibroblasts micro-injected with antibodies against hsp70. Science 242:433–436.

    Article  PubMed  CAS  Google Scholar 

  • Sampsell, B.M. and Barnette, V.C. (1985) Effects of environment temperatures on alcohol dehydrogenase activity levels in Drosophila melanogaster. Biochem. Genet. 23:53–59.

    Article  PubMed  CAS  Google Scholar 

  • Sampsell, B.M. and Sims, S. (1982) Effect of Adh genotype and heat stress on alcohol tolerance in Drosophila melanogaster. Nature 296:853–855.

    Article  PubMed  CAS  Google Scholar 

  • Schnebel, E.M. and Grossfield, J. (1986) Oviposition temperature range in four Drosophila species triads from different ecological backgrounds. Am. Midi. Nat. 116:25–35.

    Article  Google Scholar 

  • Simon, M.M., Reikerstorfer, A., Schwarz, A., Krone, C., Luger, T.A., Jaattela, M. and Schwarz, T. (1995) Heat shock protein 70 overexpression affects the response to ultraviolet light in murine fibroblasts: Evidence for increased cell viability and suppression of cytokine release. J. Clin. Invest. 95:926–933.

    Article  PubMed  CAS  Google Scholar 

  • Sinervo, B. and Basolo, A. (1996). Testing adaptation using phenotypic manipulations. In: M.R. Rose and G.V. Lauder (eds): Adaptation. Academic Press, New York, pp. 149–185.

    Google Scholar 

  • Solomon, J.M., Rossi, J.M., Golic, K., McGarry, T. and Lindquist, S. (1991) Changes in csp70 alter thermotolerance and heat-shock regulation in Drosophila. The New Biologist 3:1106–1120.

    PubMed  CAS  Google Scholar 

  • Stearns, S.C. and Kaiser, M. (1996) Effects on fitness components of P-element inserts in Drosophila melanogaster: Analysis of tradeoffs. Evolution 50: 795–806.

    Article  Google Scholar 

  • Velazquez, J.M., DiDomenico, B.J. and Lindquist, S. (1980) Intracellular localization of heat shock proteins in Drosophila. Cell 20:679–689.

    Article  PubMed  CAS  Google Scholar 

  • Velazquez, J.M. and Lindquist, S. (1984) Hsp70: Nuclear concentration during environmental stress and cytoplasmic storage during recovery. Cell 36:655–662.

    Article  PubMed  CAS  Google Scholar 

  • Velazquez, J.M., Sonoda, S., Bugaisky, G. and Lindquist, S. (1983) Is the major Drosophila heat shock protein present in cells that have not been heat shocked? J. Cell. Biol. 96:286–290.

    Article  PubMed  CAS  Google Scholar 

  • Weite, M.A., Tetrault, J.M., Dellavalle, R.P. and Lindquist, S.L. (1993) A new method for manipulating transgenes: Engineering heat tolerance in a complex, multicellular organism. Curr. Biol. 3:842–853.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Organismal Biology and Anatomy, The University of Chicago, 1027 East 57th Street, Chicago, IL, 60637, USA

    Martin E. Feder & Robert A. Krebs

  2. The Committee on Evolutionary Biology, and The College, The University of Chicago, 1027 East 57th Street, Chicago, IL, 60637, USA

    Martin E. Feder

Authors
  1. Martin E. Feder
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert A. Krebs
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Genetics, University of Groningen, Kerklaan 30, NL-9751 NN, Haren, The Netherlands

    R. Bijlsma

  2. Department of Ecology and Genetics, University of Aarhus, Ny Munkegade, Building 540, DK-8000, Aarhus, Denmark

    V. Loeschcke

Rights and permissions

Reprints and permissions

Copyright information

© 1997 Springer Basel AG

About this chapter

Cite this chapter

Feder, M.E., Krebs, R.A. (1997). Ecological and evolutionary physiology of heat shock proteins and the stress response in Drosophila: Complementary insights from genetic engineering and natural variation. In: Bijlsma, R., Loeschcke, V. (eds) Environmental Stress, Adaptation and Evolution. Experientia Supplementum, vol 83. Birkhäuser, Basel. https://doi.org/10.1007/978-3-0348-8882-0_9

Download citation

  • DOI: https://doi.org/10.1007/978-3-0348-8882-0_9

  • Publisher Name: Birkhäuser, Basel

  • Print ISBN: 978-3-0348-9813-3

  • Online ISBN: 978-3-0348-8882-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation