Bacitracin and nisin resistance in Staphylococcus aureus: A novel pathway involving the BraS/BraR two-component system (SA2417/SA2418) and both the BraD/BraE and VraD/VraE ABC transporters

Molecular Microbiology

Volumn 81, Issue 3, 2011, Pages 602-622

  Hiron, Aurélia ^a,b   Falord, Mélanie ^a,b   Valle, Jaione ^c   Débarbouillé, Michel ^a,b   Msadek, Tarek ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c PUBLIC UNIVERSITY OF NAVARRE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; BACITRACIN; NISIN; PROTEIN BRAD; PROTEIN BRAE; PROTEIN BRAR; PROTEIN BRAS; PROTEIN VRAD; PROTEIN VRAE; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BRADE GENE; BRARS GENE; CONTROLLED STUDY; DETOXIFICATION; ENZYME ACTIVATION; ESCHERICHIA COLI; GENE EXPRESSION; GENE STRUCTURE; GENETIC TRANSCRIPTION; NONHUMAN; OPERON; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; VRADE GENE;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SEQUENCE; ANTIMICROBIAL CATIONIC PEPTIDES; ATP-BINDING CASSETTE TRANSPORTERS; BACITRACIN; BASE SEQUENCE; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MICROBIAL SENSITIVITY TESTS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; NISIN; OPERON; PROMOTER REGIONS, GENETIC; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS;

STAPHYLOCOCCUS AUREUS;

EID: 79960701758     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07735.x     Document Type: Article

References (68)

1. Archambaud, C., Gouin, E., Pizarro-Cerda, J., Cossart, P., and Dussurget, O. (2005) Translation elongation factor EF-Tu is a target for Stp, a serine-threonine phosphatase involved in virulence of Listeria monocytogenes. Mol Microbiol 56: 383-396.
2. Arnaud, M., Chastanet, A., and Debarbouille, M. (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70: 6887-6891.
3. Azevedo, E.C., Rios, E.M., Fukushima, K., and Campos-Takaki, G.M. (1993) Bacitracin production by a new strain of Bacillus subtilis. Extraction, purification, and characterization. Appl Biochem Biotechnol 42: 1-7.
4. Belcheva, A., and Golemi-Kotra, D. (2008) A close-up view of the VraSR two-component system. A mediator of Staphylococcus aureus response to cell wall damage. J Biol Chem 283: 12354-12364.
5. Bernard, R., El Ghachi, M., Mengin-Lecreulx, D., Chippaux, M., and Denizot, F. (2005) BcrC from Bacillus subtilis acts as an undecaprenyl pyrophosphate phosphatase in bacitracin resistance. J Biol Chem 280: 28852-28857.
6. Bernard, R., Guiseppi, A., Chippaux, M., Foglino, M., and Denizot, F. (2007) Resistance to bacitracin in Bacillus subtilis: unexpected requirement of the BceAB ABC transporter in the control of expression of its own structural genes. J Bacteriol 189: 8636-8642.
7. Blake, K.L., Randall, C.P., and O'Neill, A.J. (2011) In vitro studies indicate a high resistance potential for the lantibiotic nisin in Staphylococcus aureus and define a genetic basis for nisin resistance. Antimicrob Agents Chemother 55: 2362-2368.
8. Blanco, A.G., Sola, M., Gomis-Ruth, F.X., and Coll, M. (2002) Tandem DNA recognition by PhoB, a two-component signal transduction transcriptional activator. Structure 10: 701-713.
9. Bradford, 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.
10. Breukink, E., and de Kruijff, B. (2006) Lipid II as a target for antibiotics. Nat Rev Drug Discov 5: 321-332.
11. Cain, B.D., Norton, P.J., Eubanks, W., Nick, H.S., and Allen, C.M. (1993) Amplification of the bacA gene confers bacitracin resistance to Escherichia coli. J Bacteriol 175: 3784-3789.
12. Chalker, A.F., Ingraham, K.A., Lunsford, R.D., Bryant, A.P., Bryant, J., Wallis, N.G., etal. (2000) The bacA gene, which determines bacitracin susceptibility in Streptococcus pneumoniae and Staphylococcus aureus, is also required for virulence. Microbiology 146: 1547-1553.
13. Chastanet, A., Prudhomme, M., Claverys, J.P., and Msadek, T. (2001) Regulation of Streptococcus pneumoniae clp genes and their role in competence development and stress survival. J Bacteriol 183: 7295-7307.
14. Claros, M.G., and von Heijne, G. (1994) TopPred II: an improved software for membrane protein structure predictions. Comput Appl Biosci 10: 685-686.
15. Coumes-Florens, S., Brochier-Armanet, C., Guiseppi, A., Denizot, F., and Foglino, M. (2011) A new highly conserved antibiotic sensing/resistance pathway in firmicutes involves an ABC transporter interplaying with a signal transduction system. PLoS ONE 6: e15951.
16. Dubrac, S., and Msadek, T. (2004) Identification of genes controlled by the essential YycG/YycF two-component system of Staphylococcus aureus. J Bacteriol 186: 1175-1181.
17. Dubrac, S., and Msadek, T. (2008) Tearing down the wall: peptidoglycan metabolism and the WalK/WalR (YycG/YycF) essential two-component system. Adv Exp Med Biol 631: 214-228.
18. Dubrac, S., Boneca, I.G., Poupel, O., and Msadek, T. (2007) New insights into the WalK/WalR (YycG/YycF) essential signal transduction pathway reveal a major role in controlling cell wall metabolism and biofilm formation in Staphylococcus aureus. J Bacteriol 189: 8257-8269.
19. Dubrac, S., Bisicchia, P., Devine, K.M., and Msadek, T. (2008) A matter of life and death: cell wall homeostasis and the WalKR (YycGF) essential signal transduction pathway. Mol Microbiol 70: 1307-1322.
20. Even, S., Burguiere, P., Auger, S., Soutourina, O., Danchin, A., and Martin-Verstraete, I. (2006) Global control of cysteine metabolism by CymR in Bacillus subtilis. J Bacteriol 188: 2184-2197.
21. Gardete, S., Wu, S.W., Gill, S., and Tomasz, A. (2006) Role of VraSR in antibiotic resistance and antibiotic-induced stress response in Staphylococcus aureus. Antimicrob Agents Chemother 50: 3424-3434.
22. Giraudo, A.T., Calzolari, A., Cataldi, A.A., Bogni, C., and Nagel, R. (1999) The sae locus of Staphylococcus aureus encodes a two-component regulatory system. FEMS Microbiol Lett 177: 15-22.
23. Herbert, S., Bera, A., Nerz, C., Kraus, D., Peschel, A., Goerke, C., etal. (2007) Molecular basis of resistance to muramidase and cationic antimicrobial peptide activity of lysozyme in staphylococci. PLoS Pathog 3: e102.
24. Herbert, S., Ziebandt, A.K., Ohlsen, K., Schafer, T., Hecker, M., Albrecht, D., etal. (2010) Repair of global regulators in Staphylococcus aureus 8325 and comparative analysis with other clinical isolates. Infect Immun 78: 2877-2889.
25. Higgins, D.G., Bleasby, A.J., and Fuchs, R. (1992) clustal v- improved software for multiple sequence alignment. Comput Appl Biosci 8: 189-191.
26. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., and Pease, L.R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51-59.
27. Hoch, J.A., and Silhavy, T.J. (1995) Two-Component Signal Transduction. Washington, DC: ASM Press.
28. Horton, R.M., Hunt, H.D., Ho, S.N., Pullen, J.K., and Pease, L.R. (1989) Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77: 61-68.
29. Ishihama, A. (1993) Protein-protein communication within the transcription apparatus. J Bacteriol 175: 2483-2489.
30. Ishihara, H., Takoh, M., Nishibayashi, R., and Sato, A. (2002) Distribution and variation of bacitracin synthetase gene sequences in laboratory stock strains of Bacillus licheniformis. Curr Microbiol 45: 18-23.
31. Joanne, P., Falord, M., Chesneau, O., Lacombe, C., Castano, S., Desbat, B., etal. (2009) Comparative study of two plasticins: specificity, interfacial behavior, and bactericidal activity. Biochemistry 48: 9372-9383.
32. Johnson, B.A., Anker, H., and Meleney, F.L. (1945) Bacitracin: a new antibiotic produced by a member of the B. subtilis group. Science 102: 376-377.
33. Jordan, S., Hutchings, M.I., and Mascher, T. (2008) Cell envelope stress response in Gram-positive bacteria. FEMS Microbiol Rev 32: 107-146.
34. Kobayashi, K., Ogura, M., Yamaguchi, H., Yoshida, K., Ogasawara, N., Tanaka, T., and Fujita, Y. (2001) Comprehensive DNA microarray analysis of Bacillus subtilis two-component regulatory systems. J Bacteriol 183: 7365-7370.
35. Kolar, S.L., Nagarajan, V., Oszmiana, A., Rivera, F.E., Miller, H.K., Davenport, J.E., etal. (2011) NsaRS is a cell-envelope-stress sensing two-component system of Staphylococcus aureus. Microbiology (in press).
36. Kreiswirth, B.N., Lofdahl, S., Betley, M.J., O'Reilly, M., Schlievert, P.M., Bergdoll, M.S., and Novick, R.P. (1983) The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305: 709-712.
37. Kuroda, M., Ohta, T., Uchiyama, I., Baba, T., Yuzawa, H., Kobayashi, I., etal. (2001) Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357: 1225-1240.
38. Kuroda, M., Kuroda, H., Oshima, T., Takeuchi, F., Mori, H., and Hiramatsu, K. (2003) Two-component system VraSR positively modulates the regulation of cell-wall biosynthesis pathway in Staphylococcus aureus. Mol Microbiol 49: 807-821.
39. Li, M., Cha, D.J., Lai, Y., Villaruz, A.E., Sturdevant, D.E., and Otto, M. (2007) The antimicrobial peptide-sensing system aps of Staphylococcus aureus. Mol Microbiol 66: 1136-1147.
40. Lowy, F.D. (1998) Staphylococcus aureus infections. N Engl J Med 339: 520-532.
41. Lowy, F.D. (2003) Antimicrobial resistance: the example of Staphylococcus aureus. J Clin Invest 111: 1265-1273.
42. Martin, P.K., Li, T., Sun, D., Biek, D.P., and Schmid, M.B. (1999) Role in cell permeability of an essential two-component system in Staphylococcus aureus. J Bacteriol 181: 3666-3673.
43. Martinez-Hackert, E., and Stock, A.M. (1997) Structural relationships in the OmpR family of winged-helix transcription factors. J Mol Biol 269: 301-312.
44. Mascher, T. (2006) Intramembrane-sensing histidine kinases: a new family of cell envelope stress sensors in Firmicutes bacteria. FEMS Microbiol Lett 264: 133-144.
45. Mascher, T., Margulis, N.G., Wang, T., Ye, R.W., and Helmann, J.D. (2003) Cell wall stress responses in Bacillus subtilis: the regulatory network of the bacitracin stimulon. Mol Microbiol 50: 1591-1604.
46. Mascher, T., Zimmer, S.L., Smith, T.A., and Helmann, J.D. (2004) Antibiotic-inducible promoter regulated by the cell envelope stress-sensing two-component system LiaRS of Bacillus subtilis. Antimicrob Agents Chemother 48: 2888-2896.
47. Mascher, T., Helmann, J.D., and Unden, G. (2006) Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 70: 910-938.
48. Matsuo, M., Kato, F., Oogai, Y., Kawai, T., Sugai, M., and Komatsuzawa, H. (2010) Distinct two-component systems in methicillin-resistant Staphylococcus aureus can change the susceptibility to antimicrobial agents. J Antimicrob Chemother 65: 1536-1537.
49. Meehl, M., Herbert, S., Gotz, F., and Cheung, A. (2007) Interaction of the GraRS two-component system with the VraFG ABC transporter to support vancomycin-intermediate resistance in Staphylococcus aureus. Antimicrob Agents Chemother 51: 2679-2689.
50. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
51. Mizuno, T., and Tanaka, I. (1997) Structure of the DNA-binding domain of the OmpR family of response regulators. Mol Microbiol 24: 665-667.
52. Moody, J.E., Millen, L., Binns, D., Hunt, J.F., and Thomas, P.J. (2002) Cooperative, ATP-dependent association of the nucleotide binding cassettes during the catalytic cycle of ATP-binding cassette transporters. J Biol Chem 277: 21111-21114.
53. Murphy, E. (1985) Nucleotide sequence of a spectinomycin adenyltransferase AAD(9) determinant from Staphylococcus aureus and its relationship to AAD(3″) (9). Mol Gen Genet 200: 33-39.
54. Novick, R.P. (2003) Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 48: 1429-1449.
55. Ohki, R., Giyanto, Tateno, K., Masuyama, W., Moriya, S., Kobayashi, K., and Ogasawara, N. (2003) The BceRS two-component regulatory system induces expression of the bacitracin transporter, BceAB, in Bacillus subtilis. Mol Microbiol 49: 1135-1144.
56. O'Neill, A.J. (2010) Staphylococcus aureus SH1000 and 8325-4: comparative genome sequences of key laboratory strains in staphylococcal research. Lett Appl Microbiol 51: 358-361.
57. Ouyang, J., Tian, X.L., Versey, J., Wishart, A., and Li, Y.H. (2010) The BceABRS four-component system regulates the bacitracin-induced cell envelope stress response in Streptococcus mutans. Antimicrob Agents Chemother 54: 3895-3906.
58. Pietiäinen, M., Francois, P., Hyyrylainen, H.L., Tangomo, M., Sass, V., Sahl, H.G., etal. (2009) Transcriptome analysis of the responses of Staphylococcus aureus to antimicrobial peptides and characterization of the roles of vraDE and vraSR in antimicrobial resistance. BMC Genomics 10: 429.
59. Rietkötter, E., Hoyer, D., and Mascher, T. (2008) Bacitracin sensing in Bacillus subtilis. Mol Microbiol 68: 768-785.
60. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
61. Sass, P., Jansen, A., Szekat, C., Sass, V., Sahl, H.G., and Bierbaum, G. (2008) The lantibiotic mersacidin is a strong inducer of the cell wall stress response of Staphylococcus aureus. BMC Microbiol 8: 186.
62. Siewert, G., and Strominger, J.L. (1967) Bacitracin: an inhibitor of the dephosphorylation of lipid pyrophosphate, an intermediate in the biosynthesis of the peptidoglycan of bacterial cell walls. Proc Natl Acad Sci USA 57: 767-773.
63. Staron, A., Finkeisen, D.E., and Mascher, T. (2011) Peptide antibiotic sensing and detoxification modules of Bacillus subtilis. Antimicrob Agents Chemother 55: 515-525.
64. Stone, J.L. (1949) Induced resistance to bacitracin in cultures of Staphylococcus aureus. J Infect Dis 85: 91-96.
65. Stone, K.J., and Strominger, J.L. (1971) Mechanism of action of bacitracin: complexation with metal ion and C 55-isoprenyl pyrophosphate. Proc Natl Acad Sci USA 68: 3223-3227.
66. Sullivan, M.A., Yasbin, R.E., and Young, F.E. (1984) New shuttle vectors for Bacillus subtilis and Escherichia coli which allow rapid detection of inserted fragments. Gene 29: 21-26.
67. Toledo-Arana, A., Merino, N., Vergara-Irigaray, M., Debarbouille, M., Penades, J.R., and Lasa, I. (2005) Staphylococcus aureus develops an alternative, ica-independent biofilm in the absence of the arlRS two-component system. J Bacteriol 187: 5318-5329.
68. Yoshida, Y., Matsuo, M., Oogai, Y., Kato, F., Nakamura, N., Sugai, M., and Komatsuzawa, H. (2011) Bacitracin sensing and resistance in Staphylococcus aureus. FEMS Microbiol Lett 320: 33-39.