Role for dnaK locus in tolerance of multiple stresses in Staphylococcus aureus

Microbiology

Volumn 153, Issue 9, 2007, Pages 3162-3173

  Singh, Vineet K ^a   Utaida, Sugunya ^b,c   Jackson, Letitia S ^a   Jayaswal, R K ^b   Wilkinson, Brian J ^b   Chamberlain, Neal R ^a  

^a A T STILL UNIVERSITY   (United States)

^b ILLINOIS STATE UNIVERSITY   (United States)

^c THAMMASAT UNIVERSITY   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOLYSIN; CAROTENOID; KANAMYCIN; METICILLIN; OXACILLIN; PROTEIN DNAK;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC RESISTANCE; ARTICLE; AUTOLYSIS; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CONTROLLED STUDY; FEMALE; GENE CASSETTE; GENE DELETION; GENE INSERTION; GENE LOCUS; HEAT TOLERANCE; HOST RESISTANCE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; WILD TYPE;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BACTERIOLYSIS; FEMALE; HEAT; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; METHICILLIN; METHICILLIN RESISTANCE; MICE; MOLECULAR CHAPERONES; MUTATION; OXACILLIN; OXIDATIVE STRESS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

STAPHYLOCOCCUS AUREUS;

EID: 34948813605     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.2007/009506-0     Document Type: Article

References (72)

1. Abramoff, M. D., Magelhaes, P. J. & Ram, S. J. (2004). Image processing with ImageJ. Biophot Int 11, 36-42.
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 Bacteriol 188, 6739-6756.
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 Biochem 204, 1149-1154.
4. Bal, A. M. & Gould, I. M. (2005). Antibiotic resistance in Staphylococcus aureus and its relevance in therapy. Expert Opin Pharmacother 6, 2257-2269.
5. Berlett, B. S. & Stadtman, E. R. (1997). Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272, 20313-20316.
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 Lett 262, 163-171.
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 19, 4027-4036.
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 Microbiol 47, 1061-1073.
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 Bacteriol 187, 4488-4496.
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 Biochem 248, 848-855.
11. Chopra, I. (2003). Antibiotic resistance in Staphylococcus aureus: concerns, causes and cures. Expert Rev Anti Infect Ther 1, 45-55.
12. Craig, E. A. (1985). The heat shock response. CRC Crit Rev Biochem 18, 239-280.
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 Chemother 50, 428-438.
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 Microbiol 31, 117-131.
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. Biochemistry 37, 9688-9694.
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 A 99, 4626-4631.
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 Microbiol 48, 1565-1578.
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 Microbiol 54, 1445-1462.
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 Chemother 50, 3424-3434.
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 Bacteriol 187, 2426-2438.
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 Tn917: preliminary characterization of mutants displaying acid sensitivity and nutritional requirements. J Bacteriol 178, 4166-4175.
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 Chaperones 4, 118-128.
23. Harrison, C. (2003). GrpE, a nucleotide exchange factor for DnaK. Cell Stress Chaperones 8, 218-224.
24. Harki, F. U. (1996). Molecular chaperones in cellular protein folding. Nature 381, 571-579.
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 Bacteriol 183, 7318-7328.
26. Homuth, G., Masuda, S., Mogk, A., Kobayashi, Y. & Schumann, W. (1997). The dnaK operon of Bacillus subtilis is heptacistronic. J Bacteriol 179, 1153-1164.
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 Bacteriol 184, 5457-5467.
28. Hubbard, T. J. & Sander, C. (1991). The role of heat-shock and chaperone proteins in protein folding: possible molecular mechanisms. Protein Eng 4, 711-717.
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 Immun 70, 1631-1634.
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 Bacteriol 188, 3826-3836.
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. Nature 305, 709-712.
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 Bacteriol 180, 4814-4820.
33. Kuroda, M., Ohta, T., Uchiyama, I., Babe, T., Yuzawa, H., Kobayashi, I., Cui, L., Oguchi, A., Aoki, K. & other authors (2001). Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357, 1225-1240.
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 Microbiol 49, 807-821.
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 A 88, 2874-2878.
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 Med 202, 209-215.
37. Lyczak, J. B., Cannon, C. L. & Pier, G. B. (2002). Lung infections associated with cystic fibrosis. Clin Microbiol Rev 15, 194-222.
38. Maguire, M., Coates, A. R. & Henderson, B. (2002). Chaperonin 60 unfolds its secrets of cellular communication. Cell Stress Chaperones 7, 317-329.
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 Immun 62, 1406-1409.
40. Marshall, J. H. & Wilmoth, G. J. (1981). Pigments of Staphylococcus aureus, a series of triterpenoid carotenoids. J Bacteriol 147, 900-913.
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 Biol 249, 126-137.
42. Mead, D. A., Szczesna-Skorups, E. & Kemper, B. (1986). Single-stranded DNA 'blue' T7 promoter plasmids: a versatile tandem promoter system for cloning and protein engineering. Protein Eng 1, 67-74.
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 Bacteriol 188, 5783-5796.
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 Bacteriol 180, 2895-2900.
45. Mogk, A., Tomoyasu, T., Goloubinoff, P., Rudiger, S., Roder, D., Langan, H. & Bukau, B. (1999). Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB. EMBO J 18, 6934-6949.
46. Novick R. P. (1991). Genetic systems in staphylococci. Methods Enzymol 204, 587-636.
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 Bacteriol 176, 4779-4783.
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 Microbiol 68, 3486-3495.
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 Chemother 44, 294-303.
50. Projan, S. J. & Novick R. P. (1997). The molecular basis of pathogenicity. In The Staphylococci in Human Disease, pp. 55-81. Edited by K. B. Crossley & G. L. Archer. 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 Leeuwenhoek 58, 79-86.
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 Immun 61, 1567-1570.
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 Immun 66, 3024-3027.
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 A 98, 69-74.
55. Schenk S. & Laddaga, R. A. (1992). Improved method for electroporation of Staphylococcus aureus. FEMS Microbiol Lett 73, 133-138.
56. Schito, G. C. (2006). The importance of the development of antibiotic resistance in Staphylococcus aureus. Clin Microbiol Infect 12 (Suppl. 1), 3-8.
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 Bacteriol 178, 1088-1093.
58. Schulz, A., Tzschaschel, B. & Schumann, W. (1995). Isolation and analysis of mutants of the dnaK operon of Bacillus subtilis. Mol Microbiol 15, 421-429.
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 Immun 74, 399-409.
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. Microbiology 149, 2739-2747.
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 Lett 199, 79-84.
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. Microbiology 147, 3037-3045.
63. Stadtman, E. R., Moskovitz, J. & Levine, R. L. (2003). Oxidation of methionine residues of proteins: biological consequences. Antioxid Redox Signal 5, 577-582.
64. Stewart P. S. (2002). Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol 292, 107-113.
65. Sutherland, R. & Rolinson, G. N. (1964). Characteristics of methicillin-resistant staphylococci. J Bacteriol 87, 887-899.
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 Res 30, e104.
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. Microbiology 149, 2719-2732.
68. Walter, S. & Buchner, J. (2002). Molecular chaperones - cellular machines for protein folding. Angew Chem Int Ed Engl 41, 1098-1113.
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 Agents 4, 259-276.
70. Winter, J. & Jakob, U. (2004). Beyond transcription - new mechanisms for the regulation of molecular chaperones. Crit Rev Biochem Mol Biol 39, 297-317.
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. Gene 33, 103-119.
72. Yura, T., Kanemori, M. & Morita, M. T. (2000). The heat shock response: regulation and function. In Bacterial Stress Response, pp. 3-18. Edited by G. Storz & R. Hengge-Aronis. Washington, DC: American Society for Microbiology.