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The Biological Role of the Universally Conserved E. coli Heat Shock Proteins

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Heat Shock

Abstract

The heat shock or stress response has been universally conserved among organisms (reviewed in Morimoto et al., 1990; Georgopoulos et al., 1990; Gross et al., 1990). When the gram-negative bacterium, E. coli is treated with a heat shock, the cell responds by transiently accelerating the rate of transcription of heat shock genes. This increased transcription is promoted by the Eσ32 RNA polymerase holoenzyme. The genes of approximately half of the 20 or so observed heat shock proteins in E. coli have been cloned and their corresponding proteins purified and characterized. Surprisingly, five of the major heat shock genes, namely dnaK, dnaJ, grpE, groES, and groEL, were previously identified because certain mutations in them block bacteriophage λ growth (reviewed in Friedman et al., 1984; Georgopoulos et al., 1990). The dnaK, dnaJ, and grpE gene products are required for bacteriophage λ growth specifically at the level of DNA replication, whereas the groES and groEL gene products are required specifically at the level of prohead assembly. In this paper, we summarize our previous and current studies on these five genes and suggest models for the mechanism of action of their gene products.

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References

  • Alfano, C and McMacken, R, (1989) Heat shock protein-mediated disassembly of nucleoprotein structures is required for the initiation of bacteriophage lambda DNA replication. J. Biol. Chem., 264: 10709–10718.

    PubMed  CAS  Google Scholar 

  • Bardwell, JCA and Craig, EA, (1984) Major heat shock gene of Drosophila and the Escherichia coliheat-inducible dnaK gene are homologous. Proc. Natl. Acad. Sci. USA, 81: 848–852.

    Article  CAS  Google Scholar 

  • Chandrasekhar, GN, Tilly, K, Woolford, C, Hendrix, R and Georgopoulos, C, (1986) Purification and properties of the GroES morphogenetic protein of E. coli. J. Biol. Chem., 261: 12414–12419.

    PubMed  CAS  Google Scholar 

  • Dodson, M, McMacken, R and Echols, H, (1989) Specialized nucleoprotein structures at the origin of replication of bacteriophage lambda. Protein association and disassociation reactions responsible for localized initiation of replication. J. Biol. Chem., 264: 10719–10725.

    PubMed  CAS  Google Scholar 

  • Fayet, O, Louarn, J-M and Georgopoulos, C, (1986) Suppression of the E. coli dnaA46 mutation by amplification of the groES and groEL genes. Mol. Gen. Genet., 202: 435–445.

    Article  PubMed  CAS  Google Scholar 

  • Fayet, O, Ziegelhoffer, T and Georgopoulos, C, (1989) The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. J. Bacteriol., 171: 1379–1385.

    PubMed  CAS  Google Scholar 

  • Flynn, GC, Chappell, TG, Rothman, JE, (1989) Peptide binding and release by proteins implicated as catalysts of protein assembly. Science, 245: 385–390.

    Article  PubMed  CAS  Google Scholar 

  • Friedman, DE, Olson, ER, Georgopoulos, C, Tilly, K, Herskowitz, I and Banuett, F, (1984) Interactions of bacteriophage and host macromolecules in the growth of bacteriophage lambda. Microbiol. Rev., 48: 299–325.

    PubMed  CAS  Google Scholar 

  • Georgopoulos, CP and Eisen, H, (1974) J. Supramol. Struct., 2: 349–359.

    Article  PubMed  CAS  Google Scholar 

  • Georgopoulos, C, Ang, D, Liberek, K and Zylicz, M, (1990) In Morimoto, R, Tissieres, A and Georgopoulos, C, eds, Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y., pp. 191–221.

    Google Scholar 

  • Goloubinoff, P, Christeller, JT, Gatenby, AA and Lorimer, GH, (1989) Reconstitution of active dimeric ribulose bisphosphate carboxylase froman unfolded state depends on two chaperonin proteins and Mg-ATP. Nature, 342: 884–889.

    Article  PubMed  CAS  Google Scholar 

  • Gross, CA, Straus, DB, Erickson, JW and Yura, T, (1990) In Morimoto, R, Tissieres, A and Georgopoulos, C, eds, Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y., pp. 167–189.

    Google Scholar 

  • Hemmingsen, SM, Woolford, C, van der Vies, SM, Tilly, K, Dennis, DT, Georgopoulos, CP, Hendrix, RW and Ellis, RJ, (1988) Homologous plant and bacterial proteins chaperon oligomeric protein asembly. Nature, 333: 330–334.

    Article  PubMed  CAS  Google Scholar 

  • Jenkins, AJ, Marsh, JB, Oliver, IR and Master, M, (1986) A DNA fragment containing the groE genes can suppress mutations in the E. coli dnaA gene. Mol. Gen. Genet., 202: 446–454.

    Article  PubMed  CAS  Google Scholar 

  • Kusukawa, N, Yura, T, Ueguchi, C, Akiyama, Y and Ito, K, (1989) Effects of mutations in heat-shock genes groES and groEL on protein export in Escherichia coli. EMBO J., 8: 3517–3521.

    PubMed  CAS  Google Scholar 

  • Laminet, A, Ziegelhoffer, T, Georgopoulos, C and Plüekthun, A, (1990) The Escherichia coli heat shock proteins GroEL and GroES modulate the folding of the beta-lactamase precursor. EMBO J., 9: 2315–2319

    PubMed  CAS  Google Scholar 

  • Lecker, S, Lill, R, Ziegelhoffer, T, Georgopoulos, C, Bassford, PJ Jr., Kumamoto, CA and Wickner, W, (1989) Three pure chaperon proteins of Ecoli — SecB, trigger factor, and Gro EL — form soluble complexes with precursor proteins in vitro. EMBO J., 8: 2703–2709.

    PubMed  CAS  Google Scholar 

  • Liberek, K, Marszalek, J, Ang, D, Georgopoulos, C and Zylicz, V, submitted.

    Google Scholar 

  • Lubben, TH, Gatenby, AA, Donaldson, GK, Lorimer, GH and Viitanen, PV, (1990) Identification of a groES-like chaperonin in mitochondria that facilitates protein folding. Proc. Natl. Acad. Sci. USA, 87: 7683–7687.

    Article  CAS  Google Scholar 

  • Martel, R, Clones, LP, Pelcher, LE and Hemmingsen, SM, Gene, in press.

    Google Scholar 

  • Mensa-Wilmot, K, Seaby, R, Alfano, C, Wold, MS, Gomes, B and McMacken, R, (1989) Reconstitution of a nine-protein system that initiates bacteriophage lambda DNA replication. J. Biol. Chem., 264: 2853–2861.

    PubMed  CAS  Google Scholar 

  • Morimoto, R, Tissieres, A and Georgopoulos, C, eds, (1990) “Stress proteins in biology and medicine.” ColaSpring Harbor Laboratoiy, Cold Spring Harbor, N.Y.

    Google Scholar 

  • Phillips, GJ and Silhavy, TJ, (1990) Heat-shock proteins DnaK and GroEL facilitate export of LacZ hybrid proteins in E. coli Nature, 344: 882–884.

    Article  PubMed  CAS  Google Scholar 

  • Reading, DS, Hallberg, RLand Myers, AM, (1989) Characterization of the yeast HSP60 gene coding for a mitochondrial assembly factor. Nature, 337: 655–659.

    Article  PubMed  CAS  Google Scholar 

  • Rothman, JE, (1989) Polypeptide chain binding proteins: catalysts of protein folding and related processes in cells. Cell, 59: 591–601.

    Article  PubMed  CAS  Google Scholar 

  • Sadler, I, Chiang, A, Kurihara, T, Rothblatt, J, Way, J and Silver, P, (1989) A yeast gene important for protein assembly into the endoplasmic reticulum and the nucleus has homology to DnaJ, an Escherichia coli heat shock protein. J. Cell Biol., 109: 2665–2675.

    Article  PubMed  CAS  Google Scholar 

  • Skowyra, D, Georgopoulos, C and Zylicz, M, (1990) The E. coli dnaK gene product, the hsp70 homolog, can reactivate heat-inactivated RNA polymerase in an ATP hydrolysis-dependent manner. Cell, 62: 939–944.

    Article  PubMed  CAS  Google Scholar 

  • Tilly, K and Georgopoulos, C, (1982) Evidence that the two E. coli groE morphogenetie gene products interact in vivo. J. Bacteriol., 149: 1082–1088.

    PubMed  CAS  Google Scholar 

  • van Dyk, TK, Gatenby, AA and LaRossa, RA, (1989) Demonstration by genetic suppression of interaction of GroE products with many proteins. Nature, 342: 451–453.

    Article  PubMed  Google Scholar 

  • Viitanen, PV, Lubben, TH, Reed, J, Goloubinoff, P, O’Keefe, DP and Lorimer, GH, (1990) Chaperonin-facilitated refolding of ribulosebisphosphate carboxylase and ATP hydrolisis by chaperonin 60 (groEL) are K+dependent. Bioehemistiy, 29: 5665–5671.

    Article  CAS  Google Scholar 

  • Waters, MG, Chirico, WJ, Henriquez, R and Blobel, G, (1989) Purification of yeast stress proteins based on their ability to facilitate secretory protein translocation. UCLA Symposia on Molecular and Cellular Biology. Pardue, ML, Feramisco, J and Lindquist, S, eds., Alan R. Liss Inc., N.Y., vol. 96, pp 163–174.

    Google Scholar 

  • Zylicz, M, LeBowitz, J, McMacken, R and Georgopoulos, C, (1983) The dnaK protein of E. coli possesses an ATPase and autophosphoiylating activity and is essential in an in vitro DNA replication system. Proc. Natl. Acaa. Sci. USA, 80: 6431–6435.

    Google Scholar 

  • Zylicz, M, An£, D, Liberek, Kand Georgopoulos, C, (1989) Initiation of lambda DNA replication with purified host- and bacteriophage-encoded proteins: the role of the dnaK, dnaJ and grpE heat shock proteins. EMBO J., 8: 1601 - 1608.

    PubMed  CAS  Google Scholar 

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© 1991 Springer-Verlag Berlin Heidelberg

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Ang, D. et al. (1991). The Biological Role of the Universally Conserved E. coli Heat Shock Proteins. In: Maresca, B., Lindquist, S. (eds) Heat Shock. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-76679-4_5

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  • DOI: https://doi.org/10.1007/978-3-642-76679-4_5

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-76681-7

  • Online ISBN: 978-3-642-76679-4

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