1887

Abstract

Heat-shock proteins are essential for stress tolerance and allowing organisms to survive conditions that cause protein unfolding. The role of the DnaK system in tolerance of various stresses was studied by disruption of by partial deletion and insertion of a kanamycin gene cassette. Deletion of in strain COL resulted in poor growth at temperatures of 37 °C and above, and reduced carotenoid production. The mutant strain also exhibited increased susceptibility to oxidative and cell-wall-active antibiotic stress conditions. In addition, the mutant strain had slower rates of autolysis, suggesting a correlation between DnaK and functional expression of staphylococcal autolysins. Deletion of also resulted in a decrease in the ability of the organism to survive in a mouse host during a systemic infection. In summary, the DnaK system in plays a significant role in the survival of under various stress conditions.

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2007-09-01
2020-08-06
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References

  1. Abramoff M. D., Magelhaes P. J., Ram S. J.. 2004; Image processing with ImageJ. Biophot Int11:36–42
    [Google Scholar]
  2. Anderson K. L., Roberts C., Disz T., Vonstein V., Hwang K., Overbeek R., Olson P. D., Projan S. J., Dunman P. M.. 2006; Characterization of the Staphylococcus aureus heat shock, cold shock, stringent, and SOS responses and their effects on log-phase mRNA turnover. J Bacteriol188:6739–6756
    [Google Scholar]
  3. Augustin J., Rosenstein R., Wieland B., Schneider U., Schnell N., Engelke G., Entian K. D., Gotz F.. 1992; Genetic analysis of epidermin biosynthetic genes and epidermin-negative mutants of Staphylococcus epidermidis. Eur J Biochem204:1149–1154
    [Google Scholar]
  4. Bal A. M., Gould I. M.. 2005; Antibiotic resistance in Staphylococcus aureus and its relevance in therapy. Expert Opin Pharmacother6:2257–2269
    [Google Scholar]
  5. Berlett B. S., Stadtman E. R.. 1997; Protein oxidation in aging, disease, and oxidative stress. J Biol Chem272:20313–20316
    [Google Scholar]
  6. Boyle-Vavra S., Yin S., Daum R. S.. 2006; The VraS/VraR two-component regulatory system required for oxacillin resistance in community-acquired methicillin-resistant Staphylococcus aureus. FEMS Microbiol Lett262:163–171
    [Google Scholar]
  7. Bukau B., Walker G. C.. 1990; Mutations altering heat shock specific subunit of RNA polymerase suppress major cellular defects of E. coli mutants lacking the DnaK chaperone. EMBO J9:4027–4036
    [Google Scholar]
  8. Chastanet A., Fert J., Msadek T.. 2003; Comparative genomics reveal novel heat shock regulatory mechanisms in Staphylococcus aureus and other Gram-positive bacteria. Mol Microbiol47:1061–1073
    [Google Scholar]
  9. Chatterjee I., Becker P., Grundmeier M., Bischoff M., Somerville G. A., Peters G., Sinha B., Harraghy N., Proctor R. A., Herrmann M.. 2005; Staphylococcus aureus ClpC is required for stress resistance, aconitase activity, growth recovery, and death. J Bacteriol187:4488–4496
    [Google Scholar]
  10. Checa S. K., Viale A. M.. 1997; The 70-kDa heat-shock protein/DnaK chaperone system is required for the productive folding of ribulose-biphosphate carboxylase subunits in Escherichia coli. Eur J Biochem248:848–855
    [Google Scholar]
  11. Chopra I.. 2003; Antibiotic resistance in Staphylococcus aureus: concerns, causes and cures. Expert Rev Anti Infect Ther1:45–55
    [Google Scholar]
  12. Craig E. A.. 1985; The heat shock response. CRC Crit Rev Biochem18:239–280
    [Google Scholar]
  13. Cui L., Iwamoto A., Lian J. Q., Neoh H. M., Maruyama T., Horikawa Y., Hiramatsu K.. 2006; Novel mechanism of antibiotic resistance originating in vancomycin-intermediate Staphylococcus aureus. Antimicrob Agents Chemother50:428–438
    [Google Scholar]
  14. Derre I., Rapoport G., Msadek T.. 1999; CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in Gram-positive bacteria. Mol Microbiol31:117–131
    [Google Scholar]
  15. Diamant S., Goloubinoff P.. 1998; Temperature-controlled activity of DnaK-DnaJ-GrpE chaperones: protein-folding arrest and recovery during and after heat shock depends on the substrate protein and the GrpE concentration. Biochemistry37:9688–9694
    [Google Scholar]
  16. Echave P., Esparza-Ceron M. A., Cabiscol E., Tamarit J., Ros J., Membrillo-Hernandez J., Lin E. 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]
  17. Frees D., Qazi S. N., Hill P. J., Ingmer H.. 2003; Alternative roles of ClpX and ClpP in Staphylococcus aureus stress tolerance and virulence. Mol Microbiol48:1565–1578
    [Google Scholar]
  18. Frees D., Chastanet A., Qazi S., Sorensen K., Hill P., Msadek T., Ingmer H.. 2004; Clp ATPases are required for stress tolerance, intracellular replication and biofilm formation in Staphylococcus aureus. Mol Microbiol54:1445–1462
    [Google Scholar]
  19. Gardete S., Wu S. W., Gill S., Tomasz A.. 2006; Role of VraSR in antibiotic resistance and antibiotic-induced stress response in Staphylococcus aureus. Antimicrob Agents Chemother50:3424–3434
    [Google Scholar]
  20. Gill S. R., Fouts D. E., Archer G. L., Mongodin E. F., Deboy R. T., Ravel J., Paulsen I. T., Kolonay J. F., Brinkac L.. other authors 2005; Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol187:2426–2438
    [Google Scholar]
  21. Gutierrez J. A., Crowley P. J., Brown D. P., Hillman J. D., Youngman P., Bleiweis A. S.. 1996; Insertional mutagenesis and recovery of interrupted genes of Streptococcus mutans by using transposon Tn 917: preliminary characterization of mutants displaying acid sensitivity and nutritional requirements. J Bacteriol178:4166–4175
    [Google Scholar]
  22. Hanawa T., Fukuda M., Kawakami H., Hirano H., Kamiya S., Yamamoto T.. 1999; The Listeria monocytogenes DnaK chaperone is required for stress tolerance and efficient phagocytosis with macrophages. Cell Stress Chaperones4:118–128
    [Google Scholar]
  23. Harrison C.. 2003; GrpE, a nucleotide exchange factor for DnaK. Cell Stress Chaperones8:218–224
    [Google Scholar]
  24. Hartl F. U.. 1996; Molecular chaperones in cellular protein folding. Nature381:571–579
    [Google Scholar]
  25. Helmann J. D., Wu M. F., Kobel P. A., Gamo F. J., Wilson M., Morshedi M. M., Navre M., Paddon C.. 2001; Global transcriptional response of Bacillus subtilis to heat shock. J Bacteriol183:7318–7328
    [Google Scholar]
  26. Homuth G., Masuda S., Mogk A., Kobayashi Y., Schumann W.. 1997; The dnaK operon of Bacillus subtilis is heptacistronic. J Bacteriol179:1153–1164
    [Google Scholar]
  27. Horsburgh M. J., Aish J. L., White I. J., Shaw L., Lithgow J. K., Foster S. J.. 2002; SigmaB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325–4. J Bacteriol184:5457–5467
    [Google Scholar]
  28. Hubbard T. J., Sander C.. 1991; The role of heat-shock and chaperone proteins in protein folding: possible molecular mechanisms. Protein Eng4:711–717
    [Google Scholar]
  29. Kohler S., Ekaza E., Paquet J. Y., Walravens K., Teyssier J., Godfroid J., Liautard J. P.. 2002; Induction of dnaK through its native heat shock promoter is necessary for intramacrophagic replication of Brucella suis. Infect Immun70:1631–1634
    [Google Scholar]
  30. Korch S. B., Hill T. M.. 2006; Ectopic overexpression of wild-type and mutant hipA genes in Escherichia coli: effects on macromolecular synthesis and persister formation. J Bacteriol188:3826–3836
    [Google Scholar]
  31. Kreiswirth B. N., Lofdahl S., Betley M. J., O'Reilly M., Schlievert P. M., Bergdoll M. S., Novick R. P.. 1983; The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature305:709–712
    [Google Scholar]
  32. Kullik I., Giachino P., Fuchs T.. 1998; Deletion of the alternative sigma factor sigmaB in Staphylococcus aureus reveals its function as a global regulator of virulence genes. J Bacteriol180:4814–4820
    [Google Scholar]
  33. Kuroda M., Ohta T., Uchiyama I., Baba T., Yuzawa H., Kobayashi I., Cui L., Oguchi A., Aoki K.. other authors 2001; Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet357:1225–1240
    [Google Scholar]
  34. Kuroda M., Kuroda H., Oshima T., Takeuchi F., Mori H., Hiramatsu K.. 2003; Two-component system VraSR positively modulates the regulation of cell-wall biosynthesis pathway in Staphylococcus aureus. Mol Microbiol49:807–821
    [Google Scholar]
  35. Liberek K., Marszalek J., Ang D., Georgopoulos C., Zylicz M.. 1991; Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc Natl Acad Sci U S A88:2874–2878
    [Google Scholar]
  36. Liu G. Y., Essex A., Buchanan J. T., Datta V., Hoffman H. M., Bastian J. F., Fierer J., Nizet V.. 2005; Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity. J Exp Med202:209–215
    [Google Scholar]
  37. Lyczak J. B., Cannon C. L., Pier G. B.. 2002; Lung infections associated with cystic fibrosis. Clin Microbiol Rev15:194–222
    [Google Scholar]
  38. Maguire M., Coates A. R., Henderson B.. 2002; Chaperonin 60 unfolds its secrets of cellular communication. Cell Stress Chaperones7:317–329
    [Google Scholar]
  39. Mani N., Baddour L. M., Offutt D. Q., Vijaranakul U., Nadakavukaren M. J., Jayaswal R. K.. 1994; Autolysis-defective mutant of Staphylococcus aureus: pathological considerations, genetic mapping, and electron microscopic studies. Infect Immun62:1406–1409
    [Google Scholar]
  40. Marshall J. H., Wilmoth G. J.. 1981; Pigments of Staphylococcus aureus, a series of triterpenoid carotenoids. J Bacteriol147:900–913
    [Google Scholar]
  41. McCarty J. S., Buchberger A., Reinstein J., Bukau B.. 1995; The role of ATP in the functional cycle of the DnaK chaperone system. J Mol Biol249:126–137
    [Google Scholar]
  42. Mead D. A., Szczesna-Skorupa E., Kemper B.. 1986; Single-stranded DNA ‘blue’ T7 promoter plasmids: a versatile tandem promoter system for cloning and protein engineering. Protein Eng1:67–74
    [Google Scholar]
  43. Michel A., Agerer F., Hauck C. R., Herrmann M., Ullrich J., Hacker J., Ohlsen K.. 2006; Global regulatory impact of ClpP protease of Staphylococcus aureus on regulons involved in virulence, oxidative stress response, autolysis, and DNA repair. J Bacteriol188:5783–5796
    [Google Scholar]
  44. Mogk A., Völker A., Engelmann S., Hecker M., Schumann W., Völker U.. 1998; Nonnative proteins induce expression of the Bacillus subtilis CIRCE regulon. J Bacteriol180:2895–2900
    [Google Scholar]
  45. Mogk A., Tomoyasu T., Goloubinoff P., Rudiger S., Roder 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]
  46. Novick R. P.. 1991; Genetic systems in staphylococci. Methods Enzymol204:587–636
    [Google Scholar]
  47. Ohta T., Saito K., Kuroda M., Honda K., Hirata H., Hayashi H.. 1994; Molecular cloning of two new heat shock genes related to the hsp70 genes in Staphylococcus aureus. J Bacteriol176:4779–4783
    [Google Scholar]
  48. Periago P. M., van Schaik W., Abee T., Wouters J. A.. 2002; Identification of proteins involved in the heat stress response of Bacillus cereus ATCC 14579. Appl Environ Microbiol68:3486–3495
    [Google Scholar]
  49. Pfeltz R. F., Singh V. K., Schmidt J. L., Batten M. A., Baranyk C. S., Nadakavukaren M. J., Jayaswal R. K., Wilkinson B. J.. 2000; Characterization of passage-selected vancomycin-resistant Staphylococcus aureus strains of diverse parental backgrounds. Antimicrob Agents Chemother44:294–303
    [Google Scholar]
  50. Projan S. J., Novick R. P.. 1997; The molecular basis of pathogenicity. In The Staphylococci in Human Disease pp55–81 Edited by Crossley K. B., Archer G. L.. New York: Churchill Livingstone;
  51. Qoronfleh M. W., Streips U. N., Wilkinson B. J.. 1990; Basic features of the staphylococcal heat shock response. Antonie Van Leeuwenhoek58:79–86
    [Google Scholar]
  52. Qoronfleh M. W., Weraarchakul W., Wilkinson B. J.. 1993; Antibodies to a range of Staphylococcus aureus and Escherichia coli heat shock proteins in sera from patients with S. aureus endocarditis. Infect Immun61:1567–1570
    [Google Scholar]
  53. Qoronfleh M. W., Bortner C. A., Schwartzberg P., Wilkinson B. J.. 1998; Enhanced levels of Staphylococcus aureus stress protein GroEL and DnaK homologs early in infection of human epithelial cells. Infect Immun66:3024–3027
    [Google Scholar]
  54. Requena J. R., Chao C. C., Levine R. L., Stadtman E. R.. 2001; Glutamic and aminoadipic semialdehydes are the main carbonyl products of metal-catalyzed oxidation of proteins. Proc Natl Acad Sci U S A98:69–74
    [Google Scholar]
  55. Schenk S., Laddaga R. A.. 1992; Improved method for electroporation of Staphylococcus aureus. FEMS Microbiol Lett73:133–138
    [Google Scholar]
  56. Schito G. C.. 2006; The importance of the development of antibiotic resistance in Staphylococcus aureus. Clin Microbiol Infect12:Suppl. 13–8
    [Google Scholar]
  57. Schulz A., Schumann W.. 1996; hrcA, the first gene of the Bacillus subtilis dnaK operon encodes a negative regulator of class I heat shock genes. J Bacteriol178:1088–1093
    [Google Scholar]
  58. Schulz A., Tzschaschel B., Schumann W.. 1995; Isolation and analysis of mutants of the dnaK operon of Bacillus subtilis. Mol Microbiol15:421–429
    [Google Scholar]
  59. Schwan W. R., Lehmann L., McCormick J.. 2006; Transcriptional activation of the Staphylococcus aureus putP gene by low-proline–high-osmotic conditions and during infection of murine and human tissues. Infect Immun74:399–409
    [Google Scholar]
  60. Singh V. K., Moskovitz J.. 2003; Multiple methionine sulfoxide reductase genes in Staphylococcus aureus: expression of activity and roles in tolerance of oxidative stress. Microbiology149:2739–2747
    [Google Scholar]
  61. Singh V. K., Jayaswal R. K., Wilkinson B. J.. 2001a; Cell wall-active antibiotic induced proteins of Staphylococcus aureus identified using a proteomic approach. FEMS Microbiol Lett199:79–84
    [Google Scholar]
  62. Singh V. K., Moskovitz J., Wilkinson B. J., Jayaswal R. K.. 2001b; Molecular characterization of a chromosomal locus in Staphylococcus aureus that contributes to oxidative defence and is highly induced by the cell-wall-active antibiotic oxacillin. Microbiology147:3037–3045
    [Google Scholar]
  63. Stadtman E. R., Moskovitz J., Levine R. L.. 2003; Oxidation of methionine residues of proteins: biological consequences. Antioxid Redox Signal5:577–582
    [Google Scholar]
  64. Stewart P. S.. 2002; Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol292:107–113
    [Google Scholar]
  65. Sutherland R., Rolinson G. N.. 1964; Characteristics of methicillin-resistant staphylococci. J Bacteriol87:887–899
    [Google Scholar]
  66. Talaat A. M., Howard S. T., Hale W. T., Lyons R., Garner H., Johnston S. A.. 2002; Genomic DNA standards for gene expression profiling in Mycobacterium tuberculosis. Nucleic Acids Res30:e104
    [Google Scholar]
  67. Utaida S., Dunman P. M., Macapagal D., Murphy E., Projan S. J., Singh V. K., Jayaswal R. K., Wilkinson B. J.. 2003; Genome-wide transcriptional profiling of the response of Staphylococcus aureus to cell-wall-active antibiotics reveals a cell-wall-stress stimulon. Microbiology149:2719–2732
    [Google Scholar]
  68. Walter S., Buchner J.. 2002; Molecular chaperones – cellular machines for protein folding. Angew Chem Int Ed Engl41:1098–1113
    [Google Scholar]
  69. Wilkinson B. J., Muthaiyan A., Jayaswal R. K.. 2005; The cell wall stress stimulon of Staphylococcus aureus and other Gram-positive bacteria. Curr Med Chem Anti-Infect Agents4:259–276
    [Google Scholar]
  70. Winter J., Jakob U.. 2004; Beyond transcription – new mechanisms for the regulation of molecular chaperones. Crit Rev Biochem Mol Biol39:297–317
    [Google Scholar]
  71. Yanisch-Perron C., Vieira J., Messing J.. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene33:103–119
    [Google Scholar]
  72. Yura T., Kanemori M., Morita M. T.. 2000; The heat shock response: regulation and function. In Bacterial Stress Response pp3–18 Edited by Storz R., Hengge-Aronis G.. Washington, DC: American Society for Microbiology;
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