1887

Abstract

The small heat-shock proteins IbpA/B are molecular chaperones that bind denatured proteins and facilitate their subsequent refolding by the ATP-dependent chaperones DnaK, DnaJ, GrpE and ClpB. In this report, we demonstrate that IbpA/B participate in the defence against copper-induced stress under aerobic conditions. In the presence of oxygen, Δ cells exhibit increased sensitivity to copper ions and accumulate elevated amounts of oxidized proteins, while under oxygen depletion, the Δ mutation has no effect on copper tolerance. This indicates that IbpA/B protect cells from oxidative damage caused by copper. We show that AdhE, one of the proteins exposed to oxidation, is protected by IbpA/B against copper-mediated inactivation both and .

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2008-06-01
2024-10-05
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References

  1. Allen S. P., Polazzi J. O., Gierse J. K., Easton A. M. 1992; Two novel heat shock genes encoding proteins produced in response to heterologous protein experession in Escherichia coli . J Bacteriol 174:6938–6947
    [Google Scholar]
  2. Avery S. V., Howlett N. G., Radice S. 1996; Copper toxicity towards Saccharomyces cerevisiae : dependence on plasma membrane fatty acid composition. Appl Environ Microbiol 62:3960–3966
    [Google Scholar]
  3. Bradford M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254
    [Google Scholar]
  4. Cecarini V., Gee J., Fioretii E., Amici M., Angeletti M., Eleuteri A. M., Keller J. N. 2007; Protein oxidation and cellular homeostasis: emphasis on metabolism. Biochim Biophys Acta 177393–104
    [Google Scholar]
  5. DiGiuseppe P. A., Silhavy T. J. 2003; Signal detection and target gene induction by the CpxRA two-component system. J Bacteriol 185:2432–2440
    [Google Scholar]
  6. Dukan S., Nyström T. 1998; Bacterial senescence: stasis results in increased and differential oxidation of cytoplasmic proteins leading to developmental induction of the heat shock regulon. Genes Dev 12:3431–3441
    [Google Scholar]
  7. Echave P., Esparca-Ceron M. A., Cabiscol E., Tamarit J., Ros J., Membrillo-Hernández J., Lin E. C. C. 2002; DnaK dependence of mutant ethanol oxidoreductases evolved for aerobic function and protective role of the chaperone against protein oxidative damage in Escherichia coli . Proc Natl Acad Sci U S A 99:4626–4631
    [Google Scholar]
  8. Egler M., Grosse C., Grass G., Nies D. H. 2005; Role of extracytoplasmic function protein family sigma factor RpoE in metal resistance of Escherichia coli . J Bacteriol 187:2297–2307
    [Google Scholar]
  9. Fredriksson A., Ballesteros M., Dukan S., Nyström T. 2005; Defence against protein carbonylation by DnaK/DnaJ and proteases of the heat shock regulon. J Bacteriol 187:4207–4213
    [Google Scholar]
  10. Ganadu M. L., Aru M., Mura G. M., Coi A., Mlynarz P., Kozlowski H. 2004; Effects of divalent metal ions on the alphaB-crystallin chaperone-like activity: spectroscopic evidence for a complex between copper(II) and protein. J Inorg Biochem 98:1103–1109
    [Google Scholar]
  11. Geuskens V., Mhammedi-Alaoui A., Desmet L., Toussaint A. 1992; Virulence in bacteriophage Mu: a case of transdominant proteolysis by the Escherichia coli Clp serine protease. EMBO J 11:5121–5127
    [Google Scholar]
  12. Grass G., Rensing C. 2001; Genes involved in copper homeostasis in Escherichia coli . J Bacteriol 183:2145–2147
    [Google Scholar]
  13. Haslbeck M., Franzmann T., Weinfurtner D., Buchner J. 2005; Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12:842–846
    [Google Scholar]
  14. Hiniker A., Collet J. F., Bardwell J. C. 2005; Copper stress causes an in vivo requirement for the Escherichia coli disulfide isomerase DsbC. J Biol Chem 280:33785–33791
    [Google Scholar]
  15. Jiao W., Li P., Zhang J., Zhang H., Chang Z. 2005; Small heat-shock proteins function in the insoluble protein complex. Biochem Biophys Res Commun 335:227–231
    [Google Scholar]
  16. Kershaw C. J., Brown N. L., Constantinidou C., Patel M. D., Hobman J. L. 2005; The expression profile of Escherichia coli K-12 in response to minimal, optimal and excess copper concentrations. Microbiology 151:1187–1198
    [Google Scholar]
  17. Kessler D., Herth W., Knappe J. 1992; Ultrastructure and pyruvate formate-lyase radical quenching property of the multienzymic AdhE protein of Escherichia coli . J Biol Chem 267:18073–18079
    [Google Scholar]
  18. Kitagawa M., Miyakawa M., Matsumura Y., Tsuchido T. 2000; Small heat shock proteins, IbpA and IbpB, are involved in resistances to heat and superoxide stress in Escherichia coli . FEMS Microbiol Lett 184:165–171
    [Google Scholar]
  19. Kitagawa M., Miyakawa M., Matsumura Y., Tsuchido T. 2002; Escherichia coli small heat shock proteins, IbpA and IbpB, protect enzymes from inactivation by heat and oxidants. Eur J Biochem 269:2907–2917
    [Google Scholar]
  20. Kucharczyk K., Laskowska E., Taylor A. 1991; Response of Escherichia coli cell membranes to induction of lambda cl857 prophage by heat shock. Mol Microbiol 5:2935–2945
    [Google Scholar]
  21. Kuczyńska-Wiśnik D., Kędzierska S., Matuszewska E., Lund P., Taylor A., Lipińska B., Laskowska E. 2002; The Escherichia coli small heat-shock proteins IbpA and IbpB prevent the aggregation of endogenous proteins denatured in vivo during extreme heat shock. Microbiology 148:1757–1765
    [Google Scholar]
  22. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
    [Google Scholar]
  23. Laskowska E., Wawrzynów A., Taylor A. 1996; IbpA and IbpB, the new heat shock proteins, bind to endogenous Escherichia coli proteins aggregated intracellularly by heat shock. Biochimie 78:117–122
    [Google Scholar]
  24. Laskowska E., Kuczyńska-Wiśnik D., Bąk M., Lipińska B. 2003; Trimethoprim induces heat shock proteins and protein aggregation in E. coli cells. Curr Microbiol 47:286–289
    [Google Scholar]
  25. Macomber L., Rensing C., Imlay J. A. 2007; Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli . J Bacteriol 189:1616–1626
    [Google Scholar]
  26. Matayoshi S., Oda H., Sarwar G. 1989; Relationship between the production of spirosomes and anaerobic glycolysis activity in Escherichia coli B. J Gen Microbiol 135:525–529
    [Google Scholar]
  27. Matuszewska M., Kuczyńska-Wiśnik D., Laskowska E., Liberek K. 2005; The small heat shock protein IbpA from Escherichia coli cooperates with IbpB in stabilization of thermally aggregated proteins in a disaggregation competent state. J Biol Chem 280:12292–12298
    [Google Scholar]
  28. Membrillo-Hernández J., Echave P., Cabiscol E., Tamarit J., Ros J., Lin E. C. C. 2000; Evolution of the adhE gene product of Escherichia coli from a functional reductase to a dehydrogenase. Genetic and biochemical studies of the mutant proteins. J Biol Chem 275:33869–33875
    [Google Scholar]
  29. Mogk A., Tomoyasu T., Goloubinoff P., Rüdiger S., Röder D., Langen H., Bukau B. 1999; Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB. EMBO J 18:6934–6949
    [Google Scholar]
  30. Mogk A., Deuerling E., Vorderwülbecke S., Vierling E., Bukau B. 2003a; Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol Microbiol 50:585–595
    [Google Scholar]
  31. Mogk A., Schlieker C., Friedrich K. L., Schönfeld H. J., Vierling E., Bukau B. 2003b; Refolding of substrates bound to small Hsps relies on a disaggregation reaction mediated most efficiently by ClpB/DnaK. J Biol Chem 278:31033–31042
    [Google Scholar]
  32. Moschini R., Marini I., Malerba M., Cappiello M., Del Corso A., Mura U. 2006; Chaperone-like activity of α -crystallin toward aldose reductase oxidatively stressed by copper ion. Arch Biochem Biophys 453:13–17
    [Google Scholar]
  33. Nakamoto H., Vigh L. 2007; The small heat shock proteins and their clients. Cell Mol Life Sci 64:294–306
    [Google Scholar]
  34. Narberhaus F. 2002; α -Crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol Mol Biol Rev 66:64–93
    [Google Scholar]
  35. Nnyepi M. R., Peng Y., Broderick J. B. 2007; Inactivation of E. coli pyruvate formate-lyase: role of AdhE and small molecules. Arch Biochem Biophys 459:1–9
    [Google Scholar]
  36. Nyström T. 2005; Role of oxidative carbonylation in protein quality control and senescence. EMBO J 24:1311–1317
    [Google Scholar]
  37. Outten F. W., Huffman D. L., Hale J. A., O'Halloran T. V. 2001; The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli . J Biol Chem 276:30670–30677
    [Google Scholar]
  38. Pérez J. M., Calderón I. L., Arenas F. A., Fuentes D. E., Pradenas G. A., Fuentes E. L., Sandoval J. M., Castro M. E., Elías A. O., Vásquez C. C. 2007; Bacterial toxicity of potassium tellurite: unveiling an ancient enigma. PLoS ONE 2:e211
    [Google Scholar]
  39. Silver S., Phung L. T. 2005; A bacterial view of the periodic table: genes and proteins for toxic inorganic ions. J Ind Microbiol Biotechnol 32:587–605
    [Google Scholar]
  40. Stadtman E. R. 1991; Ascorbic acid and oxidative inactivation of proteins. Am J Clin Nutr 54:1125S–1128S
    [Google Scholar]
  41. Storz G., Imlay J. A. 1999; Oxidative stress. Curr Opin Microbiol 2:188–194
    [Google Scholar]
  42. Suwalsky M., Ungerer B., Quevedo L., Aguilar F., Sotomayor C. P. 1998; Cu2+ ions interact with cell membranes. J Inorg Biochem 70:233–238
    [Google Scholar]
  43. Tamarit J., Cabiscol E., Ros J. 1998; Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress. J Biol Chem 273:3027–3032
    [Google Scholar]
  44. Tree J. J., Kidd S. P., Jennings M. P., McEwan A. G. 2005; Copper sensitivity of cueO mutants of Escherichia coli K-12 and the biochemical suppression of this phenotype. Biochem Biophys Res Commun 328:1205–1210
    [Google Scholar]
  45. Veinger L., Diamant S., Buchner J., Goloubinoff P. 1998; The small heat-shock protein IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network. J Biol Chem 273:11032–11037
    [Google Scholar]
  46. Winter J., Linke K., Jatzek A., Jakob U. 2005; Severe oxidative stress causes inactivation of DnaK and activation of the redox-regulated chaperone Hsp33. Mol Cell 17:381–392
    [Google Scholar]
  47. Yamamoto K., Ishihama A. 2005; Transcriptional response of Escherichia coli to external copper. Mol Microbiol 56:215–227
    [Google Scholar]
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