Genetic pathway in acquisition and loss of vancomycin resistance in a methicillin resistant Staphylococcus aureus (MRSA) strain of clonal type USA300

PLoS Pathogens

Volumn 8, Issue 2, 2012, Pages

  Gardete, Susana ^a,b   Kim, Choonkeun ^a   Hartmann, Boris M ^c   Mwangi, Michael ^a   Roux, Christelle M ^d   Dunman, Paul M ^d   Chambers, Henry F ^e   Tomasz, Alexander ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VANCOMYCIN; BACTERIAL PROTEIN; VRAS PROTEIN, STAPHYLOCOCCUS AUREUS;

ANTIBIOTIC RESISTANCE; ARTICLE; AUTOLYSIS; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL DIVISION; CELL WALL; CLONE; CONTROLLED STUDY; DISEASE PREDISPOSITION; DOWN REGULATION; FRAMESHIFT MUTATION; GENE EXPRESSION; GENE MUTATION; GENETIC CORRELATION; HOST; IMMUNE SYSTEM; IN VITRO STUDY; IN VIVO STUDY; LSPA GENE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; PHENOTYPE; PLASMID; POINT MUTATION; VRAG GENE; WILD TYPE; YVQF GENE; YYCH GENE; DNA MICROARRAY; DNA SEQUENCE; DRUG EFFECT; GENE EXPRESSION PROFILING; GENETICS; GENOTYPE; HUMAN; MALE; METABOLISM; MICROBIOLOGICAL EXAMINATION; MIDDLE AGED; NUCLEOTIDE SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; STAPHYLOCOCCUS INFECTION;

METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS AUREUS;

BACTERIAL PROTEINS; BASE SEQUENCE; FRAMESHIFT MUTATION; GENE EXPRESSION PROFILING; GENOTYPE; HUMANS; MALE; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ANALYSIS, DNA; STAPHYLOCOCCAL INFECTIONS; VANCOMYCIN; VANCOMYCIN RESISTANCE;

EID: 84860894256     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002505     Document Type: Article

References (70)

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. Pillai SK, Wennersten C, Venkataraman L, Eliopoulos GM, Moellering RC, et al. (2009) Development of reduced vancomycin susceptibility in methicillin-susceptible Staphylococcus aureus. Clin Infect Dis 49: 1169-1174.
3. Hiramatsu K, Aritaka N, Hanaki H, Kawasaki S, Hosoda Y, et al. (1997) Dissemination in Japanese hospitals of strains of Staphylococcus aureus heterogeneously resistant to vancomycin. Lancet 350: 1670-1673.
4. Smith TL, Pearson ML, Wilcox KR, Cruz C, Lancaster MV, et al. (1999) Emergence of vancomycin resistance in Staphylococcus aureus. Glycopeptide-intermediate Staphylococcus aureus Working Group. N Engl J Med 340: 493-501.
5. Sieradzki K, Roberts RB, Haber SW, Tomasz A, (1999) The development of vancomycin resistance in a patient with methicillin-resistant Staphylococcus aureus infection. N Engl J Med 340: 517-523.
6. Sieradzki K, Leski T, Dick J, Borio L, Tomasz A, (2003) Evolution of a vancomycin-intermediate Staphylococcus aureus strain in vivo: Multiple changes in the antibiotic resistance phenotypes of a single lineage of methicillin-resistant S. aureus under the impact of antibiotics administered for chemotherapy. J Clin Microbiol 41: 1687-1693.
7. Mwangi MM, Wu SW, Zhou Y, Sieradzki K, de Lencastre H, et al. (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.
8. Sieradzki K, Tomasz A, (2003) Alterations of cell wall structure and metabolism accompany reduced susceptibility to vancomycin in an isogenic series of clinical isolates of Staphylococcus aureus. J Bacteriol 185: 7103-7110.
9. 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.
10. Gardete S, Aires-De-Sousa M, Faustino A, Ludovice AM, de Lencastre H, (2008) Identification of the first vancomycin intermediate-resistant Staphylococcus aureus (VISA) isolate from a hospital in Portugal. Microb Drug Resist 14: 1-6.
11. Graber CJ, Wong MK, Carleton HA, Perdreau-Remington F, Haller BL, et al. (2007) Intermediate vancomycin susceptibility in a community-associated MRSA clone. Emerg Infect Dis 13: 491-493.
12. Hageman JC, Patel J, Franklin P, Miscavish K, McDougal L, et al. (2008) Occurrence of a USA300 vancomycin-intermediate Staphylococcus aureus. Diagn Microbiol Infect Dis 62: 440-442.
13. De Jonge BL, Chang YS, Gage D, Tomasz A, (1992) Peptidoglycan composition of a highly methicillin-resistant Staphylococcus aureus strain. The role of penicillin binding protein 2A. J Biol Chem 267: 11248-11254.
14. 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.
15. 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.
16. 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.
17. Kato Y, Suzuki T, Ida T, Maebashi K, (2010) Genetic changes associated with glycopeptide resistance in Staphylococcus aureus: predominance of amino acid substitutions in YvqF/VraSR. J Antimicrob Chemother 65: 37-45.
18. Mei JM, Nourbakhsh F, Ford CW, Holden DW, (1997) Identification of Staphylococcus aureus virulence genes in a murine model of bacteraemia using signature-tagged mutagenesis. Mol Microbiol 26: 399-407.
19. Abu-Qatouseh LF, Chinni SV, Seggewiss J, Proctor RA, Brosius J, et al. (2010) Identification of differentially expressed small non-protein-coding RNAs in Staphylococcus aureus displaying both the normal and the small-colony variant phenotype. J Mol Med 88: 565-575.
20. Kuroda M, Kuwahara-Arai K, Hiramatsu K, (2000) Identification of the up- and down-regulated genes in vancomycin-resistant Staphylococcus aureus strains Mu3 and Mu50 by cDNA differential hybridization method. Biochem Biophys Res Commun 269: 485-490.
21. Kuroda M, Kuroda H, Oshima T, Takeuchi F, Mori H, et al. (2003) Two-component system VraSR positively modulates the regulation of cell-wall biosynthesis pathway in Staphylococcus aureus. Mol Microbiol 49: 807-821.
22. Boyle-Vavra S, Yin S, Challapalli M, Daum RS, (2003) Transcriptional induction of the penicillin-binding protein 2 gene in Staphylococcus aureus by cell wall-active antibiotics oxacillin and vancomycin. Antimicrob Agents Chemother 47: 1028-1036.
23. Jordan S, Junker A, Helmann JD, Mascher T, (2006) Regulation of LiaRS-dependent gene expression in Bacillus subtilis: identification of inhibitor proteins, regulator binding sites, and target genes of a conserved cell envelope stress-sensing two-component system. J Bacteriol 188: 5153-5166.
24. Suntharalingam P, Senadheera MD, Mair RW, Levesque CM, Cvitkovitch DG, (2009) The LiaFSR system regulates the cell envelope stress response in Streptococcus mutans. J Bacteriol 191: 2973-2984.
25. Fritsch F, Mauder N, Williams T, Weiser J, Oberle M, et al. (2011) The cell envelope stress response mediated by the LiaFSRLm three-component system of Listeria monocytogenes is controlled via the phosphatase activity of the bifunctional histidine kinase LiaSLm. Microbiology 157: 373-386.
26. McCallum N, Meier PS, Heusser R, Berger-Bachi B, (2011) Mutational analyses of open reading frames within the vraSR operon and their roles in the cell wall stress response of Staphylococcus aureus. Antimicrob Agents Chemother 55: 1391-1402.
27. Szurmant H, Mohan MA, Imus PM, Hoch JA, (2007) YycH and YycI interact to regulate the essential YycFG two-component system in Bacillus subtilis. J Bacteriol 189: 3280-3289.
28. Jansen A, Turck M, Szekat C, Nagel M, Clever I, et al. (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.
29. Reipert A, Ehlert K, Kast T, Bierbaum G, (2003) Morphological and genetic differences in two isogenic Staphylococcus aureus strains with decreased susceptibilities to vancomycin. Antimicrob Agents Chemother 47: 568-576.
30. Cui L, Neoh HM, Shoji M, Hiramatsu K, (2009) Contribution of vraSR and graSR point mutations to vancomycin resistance in vancomycin-intermediate Staphylococcus aureus. Antimicrob Agents Chemother 53: 1231-1234.
31. Howden BP, Stinear TP, Allen DL, Johnson PD, Ward PB, et al. (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.
32. Tjalsma H, Zanen G, Venema G, Bron S, van Dijl JM, (1999) The potential active site of the lipoprotein-specific (type II) signal peptidase of Bacillus subtilis. J Biol Chem 274: 28191-28197.
33. Utaida S, Dunman PM, Macapagal D, Murphy E, Projan SJ, et al. (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.
34. Gardete S, Wu SW, 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.
35. Iandolo JJ, Worrell V, Groicher KH, Qian Y, Tian R, et al. (2002) Comparative analysis of the genomes of the temperate bacteriophages phi 11, phi 12 and phi 13 of Staphylococcus aureus 8325. Gene 289: 109-118.
36. Ohta T, Hirakawa H, Morikawa K, Maruyama A, Inose Y, et al. (2004) Nucleotide substitutions in Staphylococcus aureus strains, Mu50, Mu3, and N315. DNA Res 11: 51-56.
37. 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.
38. Howden BP, Smith DJ, Mansell A, Johnson PD, Ward PB, et al. (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.
39. McAleese F, Wu SW, Sieradzki K, Dunman P, Murphy E, et al. (2006) Overexpression of genes of the cell wall stimulon in clinical isolates of Staphylococcus aureus exhibiting vancomycin-intermediate- S. aureus-type resistance to vancomycin. J Bacteriol 188: 1120-1133.
40. Mongodin E, Finan J, Climo MW, Rosato A, Gill S, et al. (2003) Microarray transcription analysis of clinical Staphylococcus aureus isolates resistant to vancomycin. J Bacteriol 185: 4638-4643.
41. Scherl A, Francois P, Charbonnier Y, Deshusses JM, Koessler T, et al. (2006) Exploring glycopeptide-resistance in Staphylococcus aureus: a combined proteomics and transcriptomics approach for the identification of resistance-related markers. BMC Genomics 7: 296.
42. Li M, Diep BA, Villaruz AE, Braughton KR, Jiang X, et al. (2009) Evolution of virulence in epidemic community-associated methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci U S A 106: 5883-5888.
43. Loffler B, Hussain M, Grundmeier M, Bruck M, Holzinger D, et al. (2010) Staphylococcus aureus panton-valentine leukocidin is a very potent cytotoxic factor for human neutrophils. PLoS Pathog 6: e1000715.
44. Loughman JA, Fritz SA, Storch GA, Hunstad DA, (2009) Virulence gene expression in human community-acquired Staphylococcus aureus infection. J Infect Dis 199: 294-301.
45. Montgomery CP, Boyle-Vavra S, Adem PV, Lee JC, Husain AN, et al. (2008) Comparison of virulence in community-associated methicillin-resistant Staphylococcus aureus pulsotypes USA300 and USA400 in a rat model of pneumonia. J Infect Dis 198: 561-570.
46. Villaruz AE, Bubeck Wardenburg J, Khan BA, Whitney AR, Sturdevant DE, et al. (2009) A point mutation in the agr locus rather than expression of the Panton-Valentine leukocidin caused previously reported phenotypes in Staphylococcus aureus pneumonia and gene regulation. J Infect Dis 200: 724-734.
47. Wang R, Braughton KR, Kretschmer D, Bach TH, Queck SY, et al. (2007) Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat Med 13: 1510-1514.
48. Dunman PM, Murphy E, Haney S, Palacios D, Tucker-Kellogg G, et al. (2001) Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/or sarA loci. J Bacteriol 183: 7341-7353.
49. Said-Salim B, Dunman PM, McAleese FM, Macapagal D, Murphy E, et al. (2003) Global regulation of Staphylococcus aureus genes by Rot. J Bacteriol 185: 610-619.
50. Tegmark K, Karlsson A, Arvidson S, (2000) Identification and characterization of SarH1, a new global regulator of virulence gene expression in Staphylococcus aureus. Mol Microbiol 37: 398-409.
51. Pragman AA, Ji Y, Schlievert PM, (2007) Repression of Staphylococcus aureus SrrAB using inducible antisense srrA alters growth and virulence factor transcript levels. Biochemistry 46: 314-321.
52. Peleg AY, Monga D, Pillai S, Mylonakis E, Moellering RC Jr, et al. (2009) Reduced susceptibility to vancomycin influences pathogenicity in Staphylococcus aureus infection. J Infect Dis 199: 532-536.
53. Lalueza A, Chaves F, San Juan R, Daskalaki M, Otero JR, et al. (2010) Is high vancomycin minimum inhibitory concentration a good marker to predict the outcome of methicillin-resistant Staphylococcus aureus bacteremia? J Infect Dis 201: 311-312 author reply 312-313.
54. Horne KC, Howden BP, Grabsch EA, Graham M, Ward PB, et al. (2009) Prospective comparison of the clinical impacts of heterogeneous vancomycin-intermediate methicillin-resistant Staphylococcus aureus (MRSA) and vancomycin-susceptible MRSA. Antimicrob Agents Chemother 53: 3447-3452.
55. Price J, Atkinson S, Llewelyn M, Paul J, (2009) Paradoxical relationship between the clinical outcome of Staphylococcus aureus bacteremia and the minimum inhibitory concentration of vancomycin. Clin Infect Dis 48: 997-998.
56. Cameron DR, Howden BP, Peleg AY, (2011) The interface between antibiotic resistance and virulence in Staphylococcus aureus and its impact upon clinical outcomes. Clin Infect Dis 53: 576-582.
57. Majcherczyk PA, Barblan JL, Moreillon P, Entenza JM, (2008) Development of glycopeptide-intermediate resistance by Staphylococcus aureus leads to attenuated infectivity in a rat model of endocarditis. Microb Pathog 45: 408-414.
58. Wu S, de Lencastre H, Sali A, Tomasz A, (1996) A phosphoglucomutase-like gene essential for the optimal expression of methicillin resistance in Staphylococcus aureus: molecular cloning and DNA sequencing. Microb Drug Resist 2: 277-286.
59. Maniatis V, Fritsch EF, Sambrook, (1989) Molecular cloning: a laboratory manual Cold Spring Harbor, N.Y. Cold Spring Harbor laboratory press.
60. De Jonge BL, de Lencastre H, Tomasz A, (1991) Suppression of autolysis and cell wall turnover in heterogeneous Tn551 mutants of a methicillin-resistant Staphylococcus aureus strain. J Bacteriol 173: 1105-1110.
61. Lowbury EJ, Babb JR, Brown VL, Collins BJ, (1964) Neomycin-Resistant Staphylococcus aureus In A Burns Unit. J Hyg (Lond) 62: 221-228.
62. Tomasz A, Nachman S, Leaf H, (1991) Stable classes of phenotypic expression in methicillin-resistant clinical isolates of staphylococci. Antimicrob Agents Chemother 35: 124-129.
63. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW, (2010) GenBank. Nucleic Acids Res 38: D46-51.
64. Highlander SK, Hulten KG, Qin X, Jiang H, Yerrapragada S, et al. (2007) Subtle genetic changes enhance virulence of methicillin resistant and sensitive Staphylococcus aureus. BMC Microbiol 7: 99.
65. Beenken KE, Dunman PM, McAleese F, Macapagal D, Murphy E, et al. (2004) Global gene expression in Staphylococcus aureus biofilms. J Bacteriol 186: 4665-4684.
66. Wu ZJ, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F, (2004) A model-based background adjustment for oligonucleotide expression arrays. J Am Stat Assoc 99: 909-917.
67. Kraemer G, Iandolo JJ, (1990) High-frequency transformation of Staphylococcus aureus by electroporation. Curr Microbiol 21: 373-376.
68. Katayama Y, Zhang HZ, Hong D, Chambers HF, (2003) Jumping the barrier to beta-lactam resistance in Staphylococcus aureus. J Bacteriol 185: 5465-5472.
69. Chung M, Antignac A, Kim C, Tomasz A, (2008) Comparative study of the susceptibilities of major epidemic clones of methicillin-resistant Staphylococcus aureus to oxacillin and to the new broad-spectrum cephalosporin ceftobiprole. Antimicrob Agents Chemother 52: 2709-2717.
70. Zhao XJ, Wu HC, (1992) Nucleotide sequence of the Staphylococcus aureus signal peptidase II (lsp) gene. FEBS Lett 299: 80-84.