GraXSR proteins interact with the VraFG ABC transporter to form a five-component system required for cationic antimicrobial peptide sensing and resistance in Staphylococcus aureus

Antimicrobial Agents and Chemotherapy

Volumn 56, Issue 2, 2012, Pages 1047-1058

  Falord, Mélanie ^a,b,c   Karimova, Gouzel ^a,b   Hiron, Aurélia ^a,b   Msadeka, Tarek ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; PHOSPHATIDYLGLYCEROL; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN GRAXSR; PROTEIN VRAFG; TEICHOIC ACID; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; CELL MEMBRANE; CELL SURFACE; DNA FLANKING REGION; DRUG RESISTANCE; ENZYME SYNTHESIS; GENETIC TRANSCRIPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; STRUCTURE ANALYSIS; TWO HYBRID SYSTEM;

ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MEMBRANE TRANSPORT PROTEINS; MICROBIAL SENSITIVITY TESTS; MUTAGENESIS, SITE-DIRECTED; PLASMIDS; PROTEIN KINASES; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS;

EID: 84856069886     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.05054-11     Document Type: Article

References (49)

1. Alexeyev MF, Winkler HH. 1999. Membrane topology of the Rickettsia prowazekii ATP/ADP translocase revealed by novel dual pho-lac reporters. J. Mol. Biol. 285:1503-1513. (Pubitemid 29060451)
2. Archambaud C, Gouin E, Pizarro-Cerda J, Cossart P, 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. (Pubitemid 40516779)
3. Arnaud M, Chastanet A, Debarbouille M. 2004. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, Gram-positive bacteria. Appl. Environ. Microbiol. 70:6887-6891. (Pubitemid 39518603)
4. Bernard R, Guiseppi A, Chippaux M, Foglino M, 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. (Pubitemid 350210033)
5. 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.
6. Buelow DR, Raivio TL. 2010. Three (and more) component regulatory systems - auxiliary regulators of bacterial histidine kinases. Mol. Microbiol. 75:547-566.
7. Claros MG, von Heijne G. 1994. TopPred II: an improved software for membrane protein structure predictions. Comput. Appl. Biosci. 10:685-686.
8. Coumes-Florens S, Brochier-Armanet C, Guiseppi A, Denizot F, 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.
9. Cui L, Lian JQ, Neoh HM, Reyes E, Hiramatsu K. 2005. DNA microarray-based identification of genes associated with glycopeptide resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 49:3404-3413. (Pubitemid 41060589)
10. Dautin N, Karimova G, Ullmann A, Ladant D. 2000. Sensitive genetic screen for protease activity based on a cyclic AMP signaling cascade in Escherichia coli. J. Bacteriol. 182:7060-7066. (Pubitemid 32259611)
11. Dintner S, et al. 2011. Coevolution of ABC transporters and two-component regulatory systems as resistance modules against antimicrobial peptides in Firmicutes bacteria. J. Bacteriol. 193:3851-3862.
12. Engelman DM, Steitz TA, Goldman A. 1986. Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu. Rev. Biophys. Biophys. Chem. 15:321-353.
13. Falord M, Mader U, Hiron A, Debarbouille M, Msadek T. 2011. Investigation of the Staphylococcus aureus GraSR regulon reveals novel links to virulence, stress response and cell wall signal transduction pathways. PLoS One 6:e21323.
14. Hale JD, Hancock RE. 2007. Alternative mechanisms of action of cationic antimicrobial peptides on bacteria. Expert Rev. Anti Infect. Ther. 5:951-959. (Pubitemid 350303026)
15. Hancock RE, Sahl HG. 2006. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 24:1551-1557. (Pubitemid 44967479)
16. Herbert S, et al. 2007. Molecular basis of resistance to muramidase and cationic antimicrobial peptide activity of lysozyme in staphylococci. PLoS Pathog. 3:e102.
17. Herbert S, et al. 2010. Repair of global regulators in Staphylococcus aureus 8325 and comparative analysis with other clinical isolates. Infect. Immun. 78:2877-2889.
18. Higgins CF. 2001. ABC transporters: physiology, structure and mechanism - an overview. Res. Microbiol. 152:205-210. (Pubitemid 32436480)
19. Hiron A, Falord M, Valle J, Debarbouille M, Msadek T. 2011. 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. Mol. Microbiol. 81:602-622.
20. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59. (Pubitemid 19125653)
21. Hoch JA, Silhavy TJ (ed). 1995. Two-component signal transduction. ASM Press, Washington, DC.
22. Jenssen H, Hamill P, Hancock RE. 2006. Peptide antimicrobial agents. Clin. Microbiol. Rev. 19:491-511. (Pubitemid 44137212)
23. Jordan S, Hutchings MI, Mascher T. 2008. Cell envelope stress response in Gram-positive bacteria. FEMS Microbiol. Rev. 32:107-146. (Pubitemid 350293914)
24. Joseph P, Fichant G, Quentin Y, Denizot F. 2002. Regulatory relationship of two-component and ABC transport systems and clustering of their genes in the Bacillus/Clostridium group, suggest a functional link between them. J. Mol. Microbiol. Biotechnol. 4:503-513. (Pubitemid 35291219)
25. Karimova G, Dautin N, Ladant D. 2005. Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J. Bacteriol. 187:2233-2243. (Pubitemid 40389120)
26. Karimova G, Pidoux J, Ullmann A, Ladant D. 1998. A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc. Natl. Acad. Sci. U. S. A. 95:5752-5756. (Pubitemid 28224168)
27. Karimova G, Robichon C, Ladant D. 2009. Characterization of YmgF, a 72-residue inner membrane protein that associates with the Escherichia coli cell division machinery. J. Bacteriol. 191:333-346.
28. Karimova G, Ullmann A, Ladant D. 2000. A bacterial two-hybrid system that exploits a cAMP signaling cascade in Escherichia coli. Methods Enzymol. 328:59-73.
29. Karimova G, Ullmann A, Ladant D. 2001. Protein-protein interaction between Bacillus stearothermophilus tyrosyl-tRNA synthetase subdomains revealed by a bacterial two-hybrid system. J. Mol. Microbiol. Biotechnol. 3:73-82. (Pubitemid 32094171)
30. Kobayashi K, et al. 2001. Comprehensive DNA microarray analysis of Bacillus subtilis two-component regulatory systems. J. Bacteriol. 183:7365-7370. (Pubitemid 33121870)
31. Kreiswirth BN, et al. 1983. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709-712. (Pubitemid 13021519)
32. Kuroda M, et al. 2001. Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357:1225-1240. (Pubitemid 32539050)
33. Li M, et al. 2007. The antimicrobial peptide-sensing system aps of Staphylococcus aureus. Mol. Microbiol. 66:1136-1147. (Pubitemid 350115022)
34. Li M, et al. 2007. Gram-positive three-component antimicrobial peptide-sensing system. Proc. Natl. Acad. Sci. U. S. A. 104:9469-9474. (Pubitemid 47185803)
35. Lowy FD. 2003. Antimicrobial resistance: the example of Staphylococcus aureus. J. Clin. Invest. 111:1265-1273. (Pubitemid 36554694)
36. Lowy FD. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339:520-532.
37. Mascher T. 2006. Intramembrane-sensing histidine kinases: a new family of cell envelope stress sensors in Firmicutes bacteria. FEMS Microbiol. Lett. 264:133-144. (Pubitemid 44630119)
38. Mascher T, Helmann JD, Unden G. 2006. Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol. Mol. Biol. Rev. 70:910-938. (Pubitemid 44958261)
39. Meehl M, Herbert S, Gotz F, 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. (Pubitemid 47206200)
40. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
41. Nizet V. 2006. Antimicrobial peptide resistance mechanisms of human bacterial pathogens. Curr. Issues Mol. Biol. 8:11-26. (Pubitemid 43141388)
42. Pietiäinen M, et al. 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.
43. Rietkötter E, Hoyer D, Mascher T. 2008. Bacitracin sensing in Bacillus subtilis. Mol. Microbiol. 68:768-785. (Pubitemid 351490195)
44. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
45. Sass P, et al. 2008. The lantibiotic mersacidin is a strong inducer of the cell wall stress response of Staphylococcus aureus. BMC Microbiol. 8:186.
46. Stock JB, Ninfa AJ, Stock AM. 1989. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol. Rev. 53:450-490. (Pubitemid 20006368)
47. Tetsch L, Jung K. 2009. The regulatory interplay between membrane-integrated sensors and transport proteins in bacteria. Mol. Microbiol. 73:982-991.
48. Volz K. 1995. Structural and functional conservation in response regulators, p 53-64. In Hoch JA and Silhavy TJ (ed), Two-component signal transduction. ASM Press, Washington, DC.
49. Yang SJ, et al. 2012. The Staphylococcus aureus two-component regulatory system, GraRS, senses and confers resistance to selected cationic antimicrobial peptides. Infect. Immun. 80:74-81.