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Expression of Heat Shock Genes (hsp70) in the Mammalian Nervous System

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Heat Shock and Development

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 17))

Abstract

Studies on heat shock proteins have dealt with a wide range of organisms including E. coli, Saccharomyces, Drosophila and vertebrate cells grown in culture (Schlesinger et al. 1982; Pardue et al. 1989), however, comparatively little work has been carried out on intact thermoregulating animals. Obviously, it is of interest to ascertain whether the heat shock response is physiologically relevant. For example, are heat shock genes turned on in the mammalian nervous system following feverlike temperatures, ischemia, or tissue wounding and if so, which cell types show induction? As will be shown in this article, initial experiments in this area demonstrated the prominent induction of a 70-kD heat shock protein (Hsp70) when labeled brain proteins isolated from hyperthermic animals were analyzed. Recently, in situ hybridization and immunocytochemistry have been utilized to map out the pattern of expression of both constitutively expressed and stress-inducible members of the hsp70 multigene family. Different types of neural trauma have been found to induce characteristic cellular responses in the mammalian brain with regard to the type of brain cell that responds by inducing Hsp70 and the timing of the induction response. The pattern of induction of Hsp70 has been found to be a useful early marker of cellular injury in the nervous system and may identify previously unrecognized areas of vulnerability.

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References

  • Barbe MF, Tytell M, Gower DJ, Welch WJ (1988) Hyperthermia protects against light damage in the rat retina. Science 241: 1817–1820

    Article  CAS  PubMed  Google Scholar 

  • Blake MJ, Nowak TS, Holbrook NJ (1990) In vivo hyperthermia induces expression of HSP70 mRNA in brain regions controlling the neuroendocrine response to stress. Mol Brain Res 8: 89–92

    Article  CAS  PubMed  Google Scholar 

  • Brown IR (1983) Hyperthermia induces the synthesis of a heat shock protein by polysomes isolated from the fetal and neonatal mammalian brain. J Neurochem 40: 1490–1493

    Article  CAS  PubMed  Google Scholar 

  • Brown IR (1985a) Effect of hyperthermia and LSD on gene expression in the mammalian brain and other organs. In: Atkinson BG, Walden CB (eds) Changes in eukaryotic gene expression in response to environment stress. Academic Press, Orlando, pp 211–225

    Chapter  Google Scholar 

  • Brown IR (1985b) Modification of gene expression in the mammalian brain after hyperthermia. In: Zomzely-Neurath C, Walker WA (eds) Gene expression in brain. John Wiley, New York, pp 157–171

    Google Scholar 

  • Brown IR, Rush SJ (1990) Expression of heat shock genes (hsp70) in the mammalian brain: distinguishing constitutively expressed and hyperthermia-inducible species. J Neurosci Res 25: 14–19

    Article  CAS  PubMed  Google Scholar 

  • Brown IR, Heikkila JJ, Cosgrove JW (1982) Analysis of protein synthesis in the mammalian brain using LSD and hyperthermia as experimental probes. In: Brown IR (ed) Molecular approaches to neurobiology. Academic Press, New York, pp 221–253

    Google Scholar 

  • Brown IR, Lowe DG, Moran LA (1985) Expression of a heat shock gene in fetal and maternal rabbit brain. Neurochem Res 10: 1277–1284

    Article  CAS  PubMed  Google Scholar 

  • Brown IR, Rush SJ, Ivy GO (1989) Induction of a heat shock gene at the site of tissue injury in the rat brain. Neuron 2: 1559–1564

    Article  CAS  PubMed  Google Scholar 

  • Clark BD, Brown IR (1982) Protein synthesis in the mammalian retina following the intravenous administration of LSD. Brain Res 247: 97–104

    Article  CAS  PubMed  Google Scholar 

  • Clark BD, Brown IR (1985) Axonal transport of a heat shock protein in the rabbit visual system. Proc Natl Acad Sci USA 82: 1281–1285

    Article  CAS  PubMed  Google Scholar 

  • Clark BD, Brown IR (1986a) Induction of a heat shock protein in the isolated mammalian retina. Neurochem Res 11: 269–279

    Article  CAS  PubMed  Google Scholar 

  • Clark BD, Brown IR (1986b) A retinal heat shock protein is associated with elements of the cytoskeleton and binds to calmodulin. Biochem Biophys Res Commun 139: 974–981

    Article  CAS  PubMed  Google Scholar 

  • Clark BD, Brown IR (1987) Altered expression of a heat shock protein in the mammalian nervous system in the presence of agents which effect microtubule stability. Neurochem Res 12: 819–823

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove JW, Brown IR (1983) Heat shock protein in the mammalian brain and other organs following a physiologically relevant increase in body temperature induced by LSD. Proc Natl Acad Sci USA 80: 569–573

    Article  CAS  PubMed  Google Scholar 

  • Craig EA (1985) The heat shock response. CRC Crit Rev Biochem 18: 239–280

    Article  CAS  PubMed  Google Scholar 

  • Currie RW, White FP (1981) Trauma-induced protein in rat tissues: a physiological role for a “heat shock” protein? Science 214: 72–73

    Article  CAS  PubMed  Google Scholar 

  • de Waegh S, Brady ST (1989) Axonal transport of a clathrin uncoating ATPase (HSC70): a role for HSC70 in the modulation of coated vesicle assembly in vivo. J Neurosci Res 23: 433–440

    Article  PubMed  Google Scholar 

  • Dienel GA, Kiessling M, Jacewicz M, Pulsinelli WA (1986) Synthesis of heat shock proteins in rat brain cortex after transient ischemia. J Cereb Blood Flow Metab 6: 505–510

    Article  CAS  PubMed  Google Scholar 

  • Dwyer BE, Nishimura RN, Brown IR (1989) Synthesis of the major inducible heat shock protein in rat hippocampus after neonatal hypoxia-ischemia. Exp Neurol 104: 28–31

    Article  CAS  PubMed  Google Scholar 

  • Ferriero DM, Soberano HQ, Simon RP, Sharp FR (1990) Hypoxia-ischemia induces heat shock protein-like (HSP72) immunoreactivity in neonatal rat brain. Dev Brain Res 53: 145–150

    Article  CAS  Google Scholar 

  • Freedman MS, Clark BD, Cruz TF, Gurd JW, Brown IR (1981) Selective effects of LSD and hyperthermia on the synthesis of synaptic proteins and glycoproteins. Brain Res 207: 129–145

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez MF, Shiraishi K, Hisanaga K, Sagar SM, Mandabach M, Sharp FR (1989) Heat shock proteins as markers of neural injury. Mol Brain Res 6: 93–100

    Article  CAS  PubMed  Google Scholar 

  • Gower DJ, Holtman C, Lee KS, Tytell MT (1989) Spinal cord injury and the stress protein response. J Neurosurg 70: 605–611

    Article  CAS  PubMed  Google Scholar 

  • Greenberg SC, Lasek RJ (1985) Comparison of labelled heat shock proteins in neuronal and non-neuronal cells of Aplysia californica. Neuroscience 5: 1239–1245

    CAS  PubMed  Google Scholar 

  • Hightower LE, Guidon PT (1989) Selective release from cultured mammalian cells of heat-shock (stress) proteins that resemble glia-axon transfer proteins. J Cell Physiol 138: 257–266

    Article  CAS  PubMed  Google Scholar 

  • Jacewicz MJ, Kiessling M, Pulsinelli WA (1986) Selective gene expression in focal cerebral ischemia. J Cereb Blood Flow Metab 6: 263–272

    Article  CAS  PubMed  Google Scholar 

  • Johnston RN, Kucey BL (1988) Competitive inhibition of hsp70 gene expression causes thermosensitivity. Science 242: 1551–1554

    Article  CAS  PubMed  Google Scholar 

  • Kiessling M, Dienel GA, Jacewicz M, Pulsinelli WA (1986) Protein synthesis in postischemic rat brain: a two dimensional electrophoretic analysis. J Cereb Blood Flow Metab 6: 642–649

    Article  CAS  PubMed  Google Scholar 

  • Lim L, Hall C, Leung T, Whatley S (1984) The relationship of the rat brain 68kDa microtubuleassociated protein with synaptosomal plasma membranes and with the Drosophila 70kDa heat-shock protein. Biochem J 224: 677–680

    CAS  PubMed  Google Scholar 

  • Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55: 1151–1191

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lowenstein D, Gonzalez M, Simon R, Sharp F (1989) The pattern of 72kd heat shock protein-like immunoreactivity in the rat brain following generalized status epilepticus. Soc Neurosci Abstr 15: 1030

    Google Scholar 

  • Manrezza P, Brown IR (1990) Time course of induction of a heat shock gene (hsp70) in the rabbit cerebellum after LSD in vivo: involvement of drug-induced hyperthermia. Neurochem Res 15: 53–59

    Article  Google Scholar 

  • Marini AM, Kozuka M, Lipsky RH, Nowak TS (1990) 70-kilodalton heat shock protein induction in cerebellar astrocytes and cerebellar granule cells in vitro: comparison with immunocytochemical localization after hyperthermia in vivo. J Neurochem 54: 1509–1516

    Google Scholar 

  • Masing TE, Brown IR (1989) Cellular localization of heat shock gene expression in rabbit cerebellum by in situ hybridization with plastic-embedded tissue. Neurochem Res 14: 725–731

    Article  CAS  PubMed  Google Scholar 

  • Miller EK, Raese JD, Morrison-Bogorad MR (1989) The family of heat shock protein 70 mRNAs are differentially induced in rat cerebellum, cortex, and non-neuronal tissues. Soc Neurosci Abstr 15: 1127

    Google Scholar 

  • Moran LA, Chauvin M, Kennedy MD, Korri M, Lowe DG, Nicholson RC, Perry MD (1983) The major heat-shock protein (hsp70) gene family: related sequences in mouse, Drosophila and yeast. Can J Biochem Cell Biol 61: 488–499

    Article  CAS  PubMed  Google Scholar 

  • Morrison-Bogorad MR, Groshan K, Miller EK, Raese JD (1989) In situ quantitation of heat shock 70 mRNAs in rat cerebellum after amphetamine-induced hyperthermia. Soc Neurosci Abstr 15: 11–27

    Google Scholar 

  • New GA, Hendrickson BR, Jones KJ (1989) Induction of heat shock protein 70 mRNA in adult hamster facial nuclear groups following axotomy of the facial nerve. Metab Brain Dis 4: 273–279

    Article  CAS  PubMed  Google Scholar 

  • Nishimura RN, Dwyer BE, Welch W, Cole R, de Vellis J, Liotta K (1988) The induction of the major heat-stress protein in purified rat glial cells. J Neurosci Res 20: 12–18

    Article  CAS  PubMed  Google Scholar 

  • Nishimura RN, Dwyer BE, Clegg K, Cole R, de Vellis J (1991) Comparison of the heat shock response in cultured cortical neurons and astrocytes. Mol Brain Res 9: 39–45

    Article  CAS  PubMed  Google Scholar 

  • Nowak TS (1985) Synthesis of a stress protein following transient ischemia in the gerbil. J Neurochem 45: 1635–1641

    Article  CAS  PubMed  Google Scholar 

  • Nowak TS (1988) Effects of amphetamine on protein synthesis and energy metabolism in mouse brain: role of drug-induced hyperthermia. J Neurochem 50: 285–294

    Article  CAS  PubMed  Google Scholar 

  • Nowak TS (1989) Heat shock response in gerbil brain after ischemia-in situ hybridization analysis. Soc Neurosci Abstr 15: 11–28

    Google Scholar 

  • Nowak TS, Bond U, Schlesinger MJ (1990) Heat shock RNA levels in brain and other tissues after hyperthermia and transient ischemia. J Neurochem 54: 451–458

    Article  CAS  PubMed  Google Scholar 

  • Pardue ML, Feramisco JR, Lindquist S (1989) Stress-induced proteins. UCLA Symp Mol Cell Biol New Series v 96, Alan R Liss, New York

    Google Scholar 

  • Pelham HRB (1989) Heat shock and the sorting of luminal proteins. EMBO J 8: 3171–3176

    CAS  PubMed  Google Scholar 

  • Riabowol KT, Mizzen LA, Welch WJ (1988) Heat shock is lethal to fibroblasts microinjected with antibodies against hsp70. Science 242: 433–436

    Article  CAS  PubMed  Google Scholar 

  • Schlesinger MJ (1986) Heat shock proteins: the search for functions. J Cell Biol 103: 321–325

    Article  CAS  PubMed  Google Scholar 

  • Schlesinger MJ, Ashburner M, Tissieres A (eds) (1982) Heat shock: from bacteria to man. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sprang GK, Brown IR (1987) Selective induction of a heat shock gene in fibre tracts and cerebellar neurons of the rabbit brain detected by in situ hybridization. Mol Brain Res 3: 89–93

    Article  Google Scholar 

  • Stevenson MA, Calderwood SK (1990) Members of the 70-kilodalton heat shock protein family contain a highly conserved calmodulin-binding domain. Mol Cell Biol 10: 1234–1238

    CAS  PubMed  Google Scholar 

  • Subjeck JR, Shyy TT (1986) Stress protein systems of mammalian cells. Am J Physiol 250 (Cell Physiol 19): C1 - C17

    CAS  PubMed  Google Scholar 

  • Tytell M, Barbe MF (1987) Synthesis and axonal transport of heat shock proteins. In: Smith RS, Bisby MA (eds) Axonal transport. Neurology and neurobiology, Vol 25. Alan R Liss, New York, pp 473–492

    Google Scholar 

  • Tytell M, Greenberg SG, Lasek RJ (1986) Heat shock-like protein is transferred from glial to axon. Brain Res 363: 161–164

    Article  CAS  PubMed  Google Scholar 

  • Tytell M, Barbe MF, Gower DJ, Brown IR (1989a) Localization of retinal heat shock (stress) protein and mRNA induced by hyperthemia. Soc Neurosci Abstr 15: 116

    Google Scholar 

  • Tytell M, Barbe MF, Gower DJ (1989b) Photoreceptor protection from light damage by hyperthermia. In: LaVail ML (ed) Inherited and environmentally induced retinal degenerations. Alan R Liss, New York, pp 523–538

    Google Scholar 

  • Uhl GR (1986) In situ hybridization in brain. Plenum, New York

    Google Scholar 

  • Uney JB, Leigh PN, Marsden CD, Lees A, Anderton BH (1988) Stereotaxic injection of kainic acid into the striatum of rats induces synthesis of mRNA for heat shock protein 70. FEBS Lett 235: 215–218

    Article  CAS  PubMed  Google Scholar 

  • Vass K, Welch WJ, Nowak TS (1988) Localization of 70 kDa stress protein induction in gerbil brain after ischemia. Acta Neuropathol (Berl) 77: 128–135

    CAS  Google Scholar 

  • Vass K, Berger ML, Nowak TS, Welch WJ, Lassmann H (1989) Induction of stress protein hsp70 in nerve cells after status epilepticus in the rat. Neurosci Lett 100: 254–259

    Article  Google Scholar 

  • Walsh DA, Klein NW, Hightower LE, Edwards MJ (1987) Heat shock and thermotolerance during early rat embryo development. Teratology 36: 181–191

    Article  CAS  PubMed  Google Scholar 

  • Walsh DA, Li K, Speirs J, Crowther CE, Edwards MJ (1989) Regulation of the inducible heat-shock 71 genes in early neural development of cultured rat embryos. Teratology 40: 321–334

    Article  CAS  PubMed  Google Scholar 

  • Watowich SS, Morimoto R (1988) Complex regulation of heat shock-and glucose-responsive genes in human cells. Mol Cell Biol 8: 393–405

    CAS  PubMed  Google Scholar 

  • Welch WJ (1990) The mammalian stress response: cell physiology and biochemistry of stress proteins. In: Morimoto R, Georgopoulos C, Tissieres, A. (eds) Role of the heat shock or stress protein response in human disease and medicine. Cold Spring Harbor Laboratory Press, New York, pp 223–278

    Google Scholar 

  • Welch WJ, Feramisco JR (1982) Purification of the major mammalian heat shock proteins. J Biol Chem 257: 14949–14959

    CAS  PubMed  Google Scholar 

  • Welch WJ, Mizzen LA, Arrigo AP (1989) Structure and function of mammalian stress proteins. In: Pardue ML, Feramisco JR, Lindquist S (eds) Stress-induced proteins. UCLA Symp Molec Cell Biol New Series v 96. Alan R Liss, New York, pp 187–202

    Google Scholar 

  • Whatley SA, Leung T, Hall C, Lim L (1986) The brain 68-kilodalton microtubule-associated protein is a cognate form of the 70-kilodalton mammalian heat-shock protein and is present as a specific isoform in synaptosomal membranes. J Neurochem 47: 1576–1583

    Article  CAS  PubMed  Google Scholar 

  • Wu B, Hunt C, Morimoto R (1985) Structure and expression of the human gene encoding major heat shock protein HSP70. Mol Cell Biol 5: 330–341

    CAS  PubMed  Google Scholar 

  • Yost HJ, Lindquist S (1986) RNA splicing is interrupted by heat shock and is rescued by heat shock protein synthesis. Cell 45: 185–193

    Article  CAS  PubMed  Google Scholar 

  • Yost HJ, Lindquist S (1988) Translation of unspliced transcripts after heat shock. Science 242: 1544–1548

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Zoology, University of Toronto, Scarborough Campus, West Hill, Ontario, Canada, M1C 1A4

    Ian R. Brown

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  1. Ian R. Brown
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Editors and Affiliations

  1. Department of Molecular and Cell Biology, The University of Connecticut, 75 North Eagleville Road, 06269-3044, Storrs, CT, USA

    Lawrence Hightower

  2. Institut für Biochemie der Pflanzen, Weinberg 3, D-4050, Halle (O), Federal Republic of Germany

    Lutz Nover

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© 1991 Springer-Verlag Berlin Heidelberg

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Brown, I.R. (1991). Expression of Heat Shock Genes (hsp70) in the Mammalian Nervous System. In: Hightower, L., Nover, L. (eds) Heat Shock and Development. Results and Problems in Cell Differentiation, vol 17. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-46712-0_15

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  • DOI: https://doi.org/10.1007/978-3-540-46712-0_15

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-662-21993-5

  • Online ISBN: 978-3-540-46712-0

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