1887

Microbiology

Volume 154, Issue 6

heat-shock proteins IbpA/B are involved in resistance to oxidative stress induced by copper Free

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 .

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): DNP, 2,4-dinitrophenol , DNPH, 2,4-dinitrophenylhydrazine , Hsp, heat-shock protein , MCO, metal-catalysed oxidation , ROS, reactive oxygen species and sHsp, small heat-shock protein
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/014696-0
2008-06-01
2021-02-27
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/6/1739.html?itemId=/content/journal/micro/10.1099/mic.0.2007/014696-0&mimeType=html&fmt=ahah

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 Bacteriol174:6938–6947
     [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 Microbiol62:3960–3966
     [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 Biochem72:248–254
     [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 1773;93–104
     [Google Scholar]
  5. DiGiuseppe P. A., Silhavy T. J.. 2003; Signal detection and target gene induction by the CpxRA two-component system. J Bacteriol185:2432–2440
     [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 Dev12:3431–3441
     [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 A99:4626–4631
     [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 Bacteriol187:2297–2307
     [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 Bacteriol187:4207–4213
     [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 Biochem98:1103–1109
     [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 J11:5121–5127
     [Google Scholar]
  12. Grass G., Rensing C.. 2001; Genes involved in copper homeostasis in Escherichia coli . J Bacteriol183:2145–2147
     [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 Biol12:842–846
     [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 Chem280:33785–33791
     [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 Commun335:227–231
     [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. Microbiology151:1187–1198
     [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 Chem267:18073–18079
     [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 Lett184:165–171
     [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 Biochem269:2907–2917
     [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 Microbiol5:2935–2945
     [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. Microbiology148:1757–1765
     [Google Scholar]
  22. Laemmli U. K.. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227:680–685
     [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. Biochimie78:117–122
     [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 Microbiol47:286–289
     [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 Bacteriol189:1616–1626
     [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 Microbiol135:525–529
     [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 Chem280:12292–12298
     [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 Chem275:33869–33875
     [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 J18:6934–6949
     [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 Microbiol50:585–595
     [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 Chem278:31033–31042
     [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 Biophys453:13–17
     [Google Scholar]
  33. Nakamoto H., Vigh L.. 2007; The small heat shock proteins and their clients. Cell Mol Life Sci64:294–306
     [Google Scholar]
  34. Narberhaus F.. 2002; α -Crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol Mol Biol Rev66:64–93
     [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 Biophys459:1–9
     [Google Scholar]
  36. Nyström T.. 2005; Role of oxidative carbonylation in protein quality control and senescence. EMBO J24:1311–1317
     [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 Chem276:30670–30677
     [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 ONE2: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 Biotechnol32:587–605
     [Google Scholar]
  40. Stadtman E. R.. 1991; Ascorbic acid and oxidative inactivation of proteins. Am J Clin Nutr54:1125S–1128S
     [Google Scholar]
  41. Storz G., Imlay J. A.. 1999; Oxidative stress. Curr Opin Microbiol2:188–194
     [Google Scholar]
  42. Suwalsky M., Ungerer B., Quevedo L., Aguilar F., Sotomayor C. P.. 1998; Cu2+ ions interact with cell membranes. J Inorg Biochem70:233–238
     [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 Chem273:3027–3032
     [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 Commun328:1205–1210
     [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 Chem273:11032–11037
     [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 Cell17:381–392
     [Google Scholar]
  47. Yamamoto K., Ishihama A.. 2005; Transcriptional response of Escherichia coli to external copper. Mol Microbiol56:215–227
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/014696-0
Loading
Escherichia coli heat-shock proteins IbpA/B are involved in resistance to oxidative stress induced by copper
Microbiology 154, 1739 (2008); https://doi.org/10.1099/mic.0.2007/014696-0
/content/journal/micro/10.1099/mic.0.2007/014696-0
/content/journal/micro/10.1099/mic.0.2007/014696-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error