Decreased vancomycin susceptibility in Staphylococcus aureus caused by IS256 tempering of walKR expression

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 7, 2013, Pages 3240-3249

  McEvoy, Christopher R E ^a   Tsuji, Brian ^b   Gao, Wei ^a,c,d   Seemann, Torsten ^c   Porter, Jessica L ^a   Doig, Kenneth ^a   Ngo, Dung ^b   Howden, Benjamin P ^a,c,d   Stinear, Timothy P ^a,d  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY AT BUFFALO   (United States)

^c MONASH UNIVERSITY   (Australia)

^d AUSTIN HEALTH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOLYSIN; BACTERIAL PROTEIN; DAPTOMYCIN; GREEN FLUORESCENT PROTEIN; PROTEIN WALKR; UNCLASSIFIED DRUG; VANCOMYCIN;

5' UNTRANSLATED REGION; ANTIBIOTIC SENSITIVITY; AREA UNDER THE CURVE; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; DNA SEQUENCE; DRUG BLOOD LEVEL; DRUG EXPOSURE; GENE EXPRESSION; GENE FUNCTION; GENE INSERTION; GENE LOCUS; GENE MUTATION; GENE SEQUENCE; HOLLOW FIBER; INFECTION; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; SITE DIRECTED MUTAGENESIS; UPREGULATION; VANCOMYCIN INTERMEDIATE STAPHYLOCOCCUS AUREUS;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BASE SEQUENCE; DAPTOMYCIN; DNA TRANSPOSABLE ELEMENTS; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; MUTAGENESIS, SITE-DIRECTED; PEPTIDOGLYCAN GLYCOSYLTRANSFERASE; PROMOTER REGIONS, GENETIC; PROTEIN KINASES; SEQUENCE ANALYSIS, DNA; VANCOMYCIN; VANCOMYCIN RESISTANCE;

EID: 84879015137     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00279-13     Document Type: Article

References (46)

1. Howden BP, Davies JK, Johnson PD, Stinear TP, Grayson ML. 2010. Reduced vancomycin susceptibility in Staphylococcus aureus, including vancomycin-intermediate and heterogeneous vancomycin-intermediate strains: resistance mechanisms, laboratory detection, and clinical implications. Clin. Microbiol. Rev. 23:99-139.
2. Hiramatsu K, Aritaka N, Hanaki H, Kawasaki S, Hosoda Y, Hori S, Fukuchi Y, Kobayashi I. 1997. Dissemination in Japanese hospitals of strains of Staphylococcus aureus heterogeneously resistant to vancomycin. Lancet 350:1670-1673. (Pubitemid 28036828)
3. Hiramatsu K. 1998. Vancomycin resistance in staphylococci. Drug Resist. Updat. 1:135-150.
4. Weigel LM, Clewell DB, Gill SR, Clark NC, McDougal LK, Flannagan SE, Kolonay JF, Shetty J, Killgore GE, Tenover FC. 2003. Genetic analysis of a high-level vancomycin-resistant isolate of Staphylococcus aureus. Science 302:1569-1571. (Pubitemid 37475701)
5. Howden BP, Ward PB, Charles PG, Korman TM, Fuller A, du Cros P, Grabsch EA, Roberts SA, Robson J, Read K, Bak N, Hurley J, Johnson PD, Morris AJ, Mayall BC, Grayson ML. 2004. Treatment outcomes for serious infections caused by methicillin-resistant Staphylococcus aureus with reduced vancomycin susceptibility. Clin. Infect. Dis. 38:521-528. (Pubitemid 38250962)
6. Lin SH, Liao WH, Lai CC, Liao CH, Tan CK, Wang CY, Huang YT, Hsueh PR. 2010. Risk factors for mortality in patients with persistent methicillin-resistant Staphylococcus aureus bacteraemia in a tertiary care hospital in Taiwan. J. Antimicrob. Chemother. 65:1792-1798.
7. van Hal SJ, Lodise TP, Paterson DL. 2012. The clinical significance of vancomycin minimum inhibitory concentration in Staphylococcus aureus infections: a systematic review and meta-analysis. Clin. Infect. Dis. 54: 755-771.
8. Wi YM, Kim JM, Joo EJ, Ha YE, Kang CI, Ko KS, Chung DR, Song JH, Peck KR. 2012. High vancomycin minimum inhibitory concentration is a predictor of mortality in meticillin-resistant Staphylococcus aureus bacteraemia. Int. J. Antimicrob. Agents 40:108-113.
9. Howden BP, McEvoy CR, Allen DL, Chua K, Gao W, Harrison PF, Bell J, Coombs G, Bennett-Wood V, Porter JL, Robins-Browne R, Davies JK, Seemann T, Stinear TP. 2011. Evolution of multidrug resistance during Staphylococcus aureus infection involves mutation of the essential two component regulator WalKR. PLoS Pathog. 7:e1002359. doi:10.1371/journal.ppat.1002359.
10. Howden BP, Smith DJ, Mansell A, Johnson PD, Ward PB, Stinear TP, Davies JK. 2008. Different bacterial gene expression patterns and attenuated host immune responses are associated with the evolution of low-level vancomycin resistance during persistent methicillin-resistant Staphylococcus aureus bacteraemia. BMC Microbiol. 8:39.
11. Mwangi MM, Wu SW, Zhou Y, Sieradzki K, de Lencastre H, Richardson P, Bruce D, Rubin E, Myers E, Siggia ED, Tomasz A. 2007. Tracking the in vivo evolution of multidrug resistance in Staphylococcus aureus by whole-genome sequencing. Proc. Natl. Acad. Sci. U. S. A. 104:9451-9456. (Pubitemid 47185800)
12. Neoh HM, Cui L, Yuzawa H, Takeuchi F, Matsuo M, Hiramatsu K. 2008. Mutated response regulator graR is responsible for phenotypic conversion of Staphylococcus aureus from heterogeneous vancomycinintermediate resistance to vancomycin-intermediate resistance. Antimicrob. Agents Chemother. 52:45-53.
13. Shoji M, Cui L, Iizuka R, Komoto A, Neoh HM, Watanabe Y, Hishinuma T, Hiramatsu K. 2011. walK and clpP mutations confer reduced vancomycin susceptibility in Staphylococcus aureus. Antimicrob. Agents Chemother. 55:3870-3881.
14. Cameron DR, Ward DV, Kostoulias X, Howden BP, Moellering RC, Jr, Eliopoulos GM, Peleg AY. 2012. Serine/threonine phosphatase Stp1 contributes to reduced susceptibility to vancomycin and virulence in Staphylococcus aureus. J. Infect. Dis. 205:1677-1687.
15. Cui L, Neoh HM, Shoji M, Hiramatsu K. 2009. Contribution of vraSR and graSR point mutations to vancomycin resistance in vancomycinintermediate Staphylococcus aureus. Antimicrob. Agents Chemother. 53: 1231-1234.
16. Doddangoudar VC, O'Donoghue MM, Chong EY, Tsang DN, Boost MV. 2012. Role of stop codons in development and loss of vancomycin non-susceptibility in methicillin-resistant Staphylococcus aureus. J. Antimicrob. Chemother. 67:2101-2106.
17. Gardete S, Kim C, Hartmann BM, Mwangi M, Roux CM, Dunman PM, Chambers HF, Tomasz A. 2012. Genetic pathway in acquisition and loss of vancomycin resistance in a methicillin resistant Staphylococcus aureus (MRSA) strain of clonal type USA300. PLoS Pathog. 8:e1002505. doi:10.1371/journal.ppat.1002505.
18. Howden BP, Stinear TP, Allen DL, Johnson PD, Ward PB, Davies JK. 2008. Genomic analysis reveals a point mutation in the two-component sensor gene graS that leads to intermediate vancomycin resistance in clinical Staphylococcus aureus. Antimicrob. Agents Chemother. 52:3755-3762.
19. Ohta T, Hirakawa H, Morikawa K, Maruyama A, Inose Y, Yamashita A, Oshima K, Kuroda M, Hattori M, Hiramatsu K, Kuhara S, Hayashi H. 2004. Nucleotide substitutions in Staphylococcus aureus strains, Mu50, Mu3, and N315. DNA Res. 11:51-56. (Pubitemid 40036634)
20. Hafer C, Lin Y, Kornblum J, Lowy FD, Uhlemann AC. 2012. Contribution of selected gene mutations to resistance in clinical isolates of vancomycin-intermediate Staphylococcus aureus. Antimicrob. Agents Chemother. 56:5845-5851.
21. Delaune A, Poupel O, Mallet A, Coic YM, Msadek T, Dubrac S. 2011. Peptidoglycan crosslinking relaxation plays an important role in Staphylococcus aureus WalKR-dependent cell viability. PLoS One 6:e17054. doi: 10.1371/journal.pone.0017054.
22. Dubrac S, Bisicchia P, Devine KM, 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.
23. Dubrac S, Boneca IG, Poupel O, 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. (Pubitemid 350178938)
24. Jansen A, Turck M, Szekat C, Nagel M, Clever I, Bierbaum G. 2007. Role of insertion elements and yycFG in the development of decreased susceptibility to vancomycin in Staphylococcus aureus. Int. J. Med. Microbiol. 297:205-215. (Pubitemid 46830043)
25. Howden BP, Johnson PD, Ward PB, Stinear TP, Davies JK. 2006. Isolates with low-level vancomycin resistance associated with persistent methicillin-resistant Staphylococcus aureus bacteremia. Antimicrob. Agents Chemother. 50:3039-3047. (Pubitemid 44396410)
26. Tsuji BT, Brown T, Parasrampuria R, Brazeau DA, Forrest A, Kelchlin PA, Holden PN, Peloquin CA, Hanna D, Bulitta JB. 2012. Front-loaded linezolid regimens result in increased killing and suppression of the accessory gene regulator system of Staphylococcus aureus. Antimicrob. Agents Chemother. 56:3712-3719.
27. Gao W, Chua K, Davies JK, Newton HJ, Seemann T, Harrison PF, Holmes NE, Rhee HW, Hong JI, Hartland EL, Stinear TP, Howden BP. 2010. Two novel point mutations in clinical Staphylococcus aureus reduce linezolid susceptibility and switch on the stringent response to promote persistent infection. PLoS Pathog. 6:e1000944. doi:10.1371/journal.ppat.1000944.
28. Burian M, Rautenberg M, Kohler T, Fritz M, Krismer B, Unger C, Hoffmann WH, Peschel A, Wolz C, Goerke C. 2010. Temporal expression of adhesion factors and activity of global regulators during establishment of Staphylococcus aureus nasal colonization. J. Infect. Dis. 201:1414-1421.
29. Lloyd AL, Marshall BJ, Mee BJ. 2005. Identifying cloned Helicobacter pylori promoters by primer extension using a FAM-labelled primer and Gene Scan analysis. J. Microbiol. Methods 60:291-298. (Pubitemid 40093056)
30. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. Web Logo: a sequence logo generator. Genome Res. 14:1188-1190.
31. Bateman BT, Donegan NP, Jarry TM, Palma M, Cheung AL. 2001. Evaluation of a tetracycline-inducible promoter in Staphylococcus aureus in vitro and in vivo and its application in demonstrating the role of sigB in microcolony formation. Infect. Immun. 69:7851-7857. (Pubitemid 33086616)
32. 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)
33. Tsien RY. 1998. The green fluorescent protein. Annu. Rev. Biochem. 67:509-544. (Pubitemid 28411137)
34. Howden BP, Seemann T, Harrison PF, McEvoy CR, Stanton JA, Rand CJ, Mason CW, Jensen SO, Firth N, Davies JK, Johnson PD, Stinear TP. 2010. Complete genome sequence of Staphylococcus aureus strain JKD6008, an ST239 clone of methicillin-resistant Staphylococcus aureus with intermediate-level vancomycin resistance. J. Bacteriol. 192:5848-5849.
35. Sng LH, Koh TH, Wang GC, Hsu LY, Kapi M, Hiramatsu K. 2005. Heterogeneous vancomycin-resistant Staphylococcus aureus (hetero-VISA) in Singapore. Int. J. Antimicrob. Agents 25:177-179. (Pubitemid 40138957)
36. Dubrac S, Msadek T. 2004. Identification of genes controlled by the essential YycG/YycF two-component system of Staphylococcus aureus. J. Bacteriol. 186:1175-1181. (Pubitemid 38209478)
37. Blake KL, O'Neill AJ. 2013. Transposon library screening for identification of genetic loci participating in intrinsic susceptibility and acquired resistance to antistaphylococcal agents. J. Antimicrob. Chemother. 68:12-16.
38. Delaune A, Dubrac S, Blanchet C, Poupel O, Mader U, Hiron A, Leduc A, Fitting C, Nicolas P, Cavaillon JM, Adib-Conquy M, Msadek T. 2012. The WalKR system controls major staphylococcal virulence genes and is involved in triggering the host inflammatory response. Infect. Immun. 80:3438-3453.
39. Martin PK, Li T, Sun D, Biek DP, Schmid MB. 1999. Role in cell permeability of an essential two-component system in Staphylococcus aureus. J. Bacteriol. 181:3666-3673. (Pubitemid 29283792)
40. Stapleton MR, Horsburgh MJ, Hayhurst EJ, Wright L, Jonsson IM, Tarkowski A, Kokai-Kun JF, Mond JJ, Foster SJ. 2007. Characterization of IsaA and SceD, two putative lytic transglycosylases of Staphylococcus aureus. J. Bacteriol. 189:7316-7325. (Pubitemid 47557346)
41. Cafiso V, Bertuccio T, Spina D, Purrello S, Campanile F, Di Pietro C, Purrello M, Stefani S. 2012. Modulating activity of vancomycin and daptomycin on the expression of autolysis cell-wall turnover and membrane charge genes in hVISA and VISA strains. PLoS One 7:e29573. doi: 10.1371/journal.pone.0029573.
42. Pieper R, Gatlin-Bunai CL, Mongodin EF, Parmar PP, Huang ST, Clark DJ, Fleischmann RD, Gill SR, Peterson SN. 2006. Comparative proteomic analysis of Staphylococcus aureus strains with differences in resistance to the cell wall-targeting antibiotic vancomycin. Proteomics 6:4246-4258. (Pubitemid 44277028)
43. Drummelsmith J, Winstall E, Bergeron MG, Poirier GG, Ouellette M. 2007. Comparative proteomics analyses reveal a potential biomarker for the detection of vancomycin-intermediate Staphylococcus aureus strains. J. Proteome Res. 6:4690-4702.
44. Park C, Shin NY, Byun JH, Shin HH, Kwon EY, Choi SM, Kim SH, Kwon JC, Park SH, Choi JH, Yoo JH, Yoo JI, Chung GT, Lee DG. 2012. Downregulation of RNAIII in vancomycin-intermediate Staphylococcus aureus strains regardless of the presence of agr mutation. J. Med. Microbiol. 61:345-352.
45. Peleg AY, Monga D, Pillai S, Mylonakis E, Moellering RC, Jr, Eliopoulos GM. 2009. Reduced susceptibility to vancomycin influences pathogenicity in Staphylococcus aureus infection. J. Infect. Dis. 199:532-536.
46. Kreiswirth BN, Lofdahl S, Betley MJ, O'Reilly M, Schlievert PM, Bergdoll MS, Novick RP. 1983. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709-712. (Pubitemid 13021519)