Identification of different clonal complexes and diverse amino acid substitutions in penicillin-binding protein 2 (PBP2) associated with borderline oxacillin resistance in Canadian Staphylococcus aureus isolates

Journal of Medical Microbiology

Volumn 55, Issue 12, 2006, Pages 1675-1683

  Nadarajah, Jeya ^a   Lee, Mark J S ^a   Louie, Lisa ^a   Jacob, Latha ^a   Simor, Andrew E ^a   Louie, Marie ^b   McGavin, Martin J ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAMASE; GAMMA GLUTAMYLTRANSFERASE; GENOMIC DNA; OXACILLIN; PENICILLIN BINDING PROTEIN 2A;

AMINO ACID SUBSTITUTION; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIUM ISOLATE; CANADA; CLONE; GENETIC VARIABILITY; GENOTYPE; MINIMUM INHIBITORY CONCENTRATION; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULSED FIELD GEL ELECTROPHORESIS; SEQUENCE ANALYSIS; SOUTHERN BLOTTING; STAPHYLOCOCCUS AUREUS;

AMINO ACID SUBSTITUTION; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CANADA; DRUG RESISTANCE, BACTERIAL; MOLECULAR SEQUENCE DATA; OXACILLIN; PENICILLIN-BINDING PROTEINS; PEPTIDYL TRANSFERASES; POLYMORPHISM, SINGLE NUCLEOTIDE; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 33845394425     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.46700-0     Document Type: Article

References (59)

1. Archer, G. L. (1998). Staphylococcus aureus: a well-armed pathogen. Clin Infect Dis 26, 1179-1181.
2. Asahi, Y., Takeuchi, Y. & Ubukata, K. (1999). Diversity of substitutions within or adjacent to conserved amino acid motifs of penicillin-binding protein 2X in cephalosporin-resistant Streptococcus pneumoniae isolates. Antimicrob Agents Chemother 43, 1252-1255.
3. Baba, T., Takeuchi, F., Kuroda, M. & 11 other authors (2002). Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359, 1819-1827.
4. Balslev, U., Bremmelgaard, A., Svejgaard, E., Havstreym, J. & Westh, H. (2005). An outbreak of borderline oxacillin-resistant Staphylococcus aureus (BORSA) in a dermatological unit. Microb Drus Resist 11, 78-81.
5. Barg, N., Chambers, H. & Kernodle, D. (1991). Borderline susceptibility to antistaphylococcal penicillins is not conferred exclusively by the hyperproduction of beta-lactamase. Antimicrob Agents Chemother 35, 1975-1979.
6. Boyle-Vavra, S., Yin, S., Challapalli, M. & Daum, R. S. (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.
7. Bradley, A. J. & Green, M. J. (2004). The importance of the nonlactating period in the epidemiology of intramammary infection and strategies for prevention. Vet Clin North Am Food Anim Pract 20, 547-568.
8. Chriel, M. & Dietz, H. H. (2003). Medication of production animals - cure of malfunctioning animals or production systems? Acta Vet Scand 98, 65-70.
9. Dessen, A., Mouz, N., Gordon, E., Hopkins, J. & Dideberg, O. (2001). Crystal structure of PBP2x from a highly penicillin-resistant Streptococcus pneumoniae clinical isolate: a mosaic framework containing 83 mutations. J Biol Chem 276, 45106-45112.
10. Diep, B. A., Gill, S. R., Chang, R. F. & 9 other authors (2006). Complete genome sequence of USA 300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367, 731-739.
11. Enright, M. C., Day, N. P., Davies, C. E., Peacock, S. J. & Spratt, B. G. (2000). Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38, 1008-1015.
12. Enright, M. C., Robinson, D. A., Randle, G., Feil, E. J., Grundmann, H. & Spratt, B. G. (2002). The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci U S A 99, 7687-7692.
13. Feil, E. J. & Enright, M. C. (2004). Analyses of clonality and the evolution of bacterial pathogens. Curr Opin Microbiol 7, 308-313.
14. Feil, E. J., Cooper, J. E., Grundmann, H. & 9 other authors (2003). How clonal is Staphylococcus aureus? J Bacteriol 185, 3307-3316.
15. Feil, E. J., Li, B. C., Aanensen, D. M., Hanage, W. P. & Spratt, B. G. (2004). eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186, 1518-1530.
16. Fitzgerald, J. R., Hartigan, P. J., Meaney, W. J. & Smyth, C. J. (2000). Molecular population and virulence factor analysis of Staphylococcus aureus from bovine intramammary infection. J Appl Microbiol 88, 1028-1037.
17. Frere, J. M. & Joris, B. (1985). Penicillin-sensitive enzymes in peptidoglycan biosynthesis. Crit Rev Microbiol 11, 299-396.
18. Fuller, E., Elmer, C., Mattress, F., Ellis, R., Horne, G., Cook, P. & Fawcett, T. (2005). Beta-lactam resistance in Staphylococcus aureus cells that do not require a cell wall for integrity. Antimicrob Agents Chemother 49, 5075-5080.
19. Ghuysen, J. M. (1991). Serine beta-lactamases and penicillin-binding proteins. Annu Rev Microbiol 45, 37-67.
20. Ghuysen, J. M. (1994). Molecular structures of penicillin-binding proteins and beta-lactamases. Trends Microbiol 2, 372-380.
21. Gillaspy, A. F., Worrell, V., Orvis, J., Roe, B. A., Dyer, D. W. & Iandolo, J. J. (2006). The Staphylococcus aureus NCTC8325 genome. In Gram Positive Pathogens, 2nd edn. Edited by V, Fischetti, R. P. Novick, J. Ferretti, D. Portnoy & J. Rood. Washington, DC: American Society for Microbiology.
22. Grebe, T. & Hakenbeck, R. (1996). Penicillin-binding proteins 2b and 2x of Streptococcus pneumoniae are primary resistance determinants for different classes of beta-lactam antibiotics. Antimicrob Agents Chemother 40, 829-834.
23. Hackbarth, C. J., Kocagoz, T., Kocagoz, S. & Chambers, H. F. (1995). Point mutations in Staphylococcus aureus PBP 2 gene affect penicillin-binding kinetics and are associated with resistance. Antimicrob Agents Chemother 39, 103-106.
24. Hartman, B. J. & Tomasz, A. (1984). Low-affinity penicillin-binding protein associated with beta-lactam resistance in Staphylococcus aureus. J Bacteriol 158, 513-516.
25. Hiramatsu, K., Cui, L., Kuroda, M. & Ito, T. (2001). The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends Microbiol 9, 486-493.
26. Holden, M. T., Feil, E. J., Lindsay, J. A. & 42 other authors (2004). Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci U S A 101, 9786-9791.
27. Ito, T., Katayama, Y., Asada, K., Mori, N., Tsutsumimoto, K., Tiensasitorn, C. & Hiramatsu, K. (2001). Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 45, 1323-1336.
28. Kernodle, D. S., Classen, D. C., Stratton, C. W. & Kaiser, A. B. (1998). Association of borderline oxacillin-susceptible strains of Staphylococcus aureus with surgical wound infections. J Clin Microbiol 36, 219-222.
29. Keseru, J. S., Gal, Z., Barabas, G., Benko, I. & Szabo, I. (2005). Investigation of beta-lactamases in clinical isolates of Staphylococcus aureus for further explanation of borderline methicillin-resistance. Chemotherapy 51, 300-304.
30. Kuroda, M., Ohta, T., Uchiyama, I. & 34 other authors (2001). Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357, 1225-1240.
31. Laible, G., Spratt, B. G. & Hakenbeck, R. (1991). Interspecies recombinational events during the evolution of altered PBP 2x genes in penicillin-resistant clinical isolates of Streptococcus pneumoniae. Mol Microbiol 5, 1993-2002.
32. Leski, T. A. & Tomasz, A. (2005). Role of penicillin-binding protein 2 (PBP2) in the antibiotic susceptibility and cell wall cross-linking of Staphylococcus aureus: evidence for the cooperative functioning of PBP2, PBP4, and PBP2A. J Bacteriol 187, 1815-1824.
33. Lindsay, J. A. & Holden, M. T. (2004). Staphylococcus aureus: superbug, super genome? Trends Microbiol 12, 378-385.
34. Louie, L., Matsumura, S. O., Choi, E., Louie, M. & Simor, A. E. (2000). Evaluation of three rapid methods for detection of methicillin resistance in Staphylococcus aureus. J Clin Microbiol 38, 2170-2173.
35. Louie, L., Goodfellow, J., Mathieu, P., Glatt, A., Louie, M. & Simor, A. E. (2002). Rapid detection of methicillin-resistant staphylococci from blood culture bottles by using a multiplex PCR assay. J Clin Microbiol 40, 2786-2790.
36. Massanari, R. M., Pfaller, M. A., Wakefield, D. S., Hammons, G. T., McNutt, L. A., Woolson, R. F. & Helms, C. M. (1988). Implications of acquired oxacillin resistance in the management and control of Staphylococcus aureus infections. J Infect Dis 158, 702-709.
37. Massidda, O., Montanari, M. P. & Varaldo, P. E. (1992). Evidence for a methicillin-hydrolysing beta-lactamase in Staphylococcus aureus strains with borderline susceptibility to this drug. FEMS Microbiol Lett 71, 223-227.
38. Massidda, O., Montanari, M. P., Mingoia, M. & Varaldo, P. E. (1996). Borderline methicillin-susceptible Staphylococcus aureus strains have more in common than reduced susceptibility to penicillinase-resistant penicillins. Antimicrob Agents Chemother 40, 2769-2774.
39. McDougal, L. K. & Thornsberry, C. (1986). The role of beta-lactamase in staphylococcal resistance to penicillinase-resistant penicillins and cephalosporins. J Clin Microbiol 23, 832-839.
40. McMurray, L. W., Kernodle, D. S. & Barg, N. L. (1990). Characterization of a widespread strain of methicillin-susceptible Staphylococcus aureus associated with nosocomial infections. J Infect Dis 162, 759-762.
41. Mouz, N., Di Guilmi, A. M., Gordon, E., Hakenbeck, R., Dideberg, O. & Vernet, T. (1999). Mutations in the active site of penicillin-binding protein PBP2x from Streptococcus pneumoniae. Role in the specificity for beta-lactam antibiotics. J Biol Chem 274, 19175-19180.
42. Murakami, K., Fujimura, T. & Doi, M. (1994). Nucleotide sequence of the structural gene for the penicillin-binding protein 2 of Staphylococcus aureus and the presence of a homologous gene in other staphylococci. FEMS Microbiol Lett 117, 131-136.
43. National Committee for Clinical Laboratory Standards (2003). Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically: Approved Standard, 6th edn. NCCLS document M7-A6. Wayne PA: National Committee for Clinical Laboratory Standards.
44. Novick, R. P., Ross, H. F., Projan, S. J., Kornblum, J., Kreiswirth, B. & Moghazeh, S. (1993). Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J 12, 3967-3975.
45. Pinho, M. G., de Lencastre, H. & Tomasz, A. (1998). Transcriptional analysis of the Staphylococcus aureus penicillin-binding protein 2 gene. J Bacteriol 180, 6077-6081.
46. Pinho, M. G., de Lencastre, H. & Tomasz, A. (2001a). An acquired and a native penicillin-binding protein cooperate in building the cell wall of drug-resistant staphylococci. Proc Natl Acad Sci U S A 98, 10886-10891.
47. Pinho, M. G., Filipe, S. R., de Lencastre, H. & Tomasz, A. (2001b). Complementation of the essential peptidoglycan transpeptidase function of penicillin-binding protein 2 (PBP2) by the drug resistance protein PBP2A in Staphylococcus aureus. J Bacteriol 183, 6525-6531.
48. Rice, K., Huesca, M., Vaz, D. & McGavin, M. J. (2001). Variance in fibronectin binding and fnb locus polymorphisms in Staphylococcus aureus: identification of antigenic variation in a fibronectin binding protein adhesin of the epidemic CMRSA-1 strain of methicillin-resistant S. aureus. Infect Immun 69, 3791-3799.
49. Robinson, D. A. & Enright, M. C. (2004). Multilocus sequence typing and the evolution of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 10, 92-97.
50. Simor, A. E., Ofner-Agostini, M., Bryce, E., Green, K., McGeer, A., Mulvey, M. & Paton, S. (2001). The evolution of methicillin-resistant Staphylococcus aureus in Canadian hospitals: 5 years of national surveillance. CMAJ 165, 21-26.
51. Simor, A. E., Ofner-Agostini, M., Bryce, E., McGeer, A., Paton, S. & Mulvey, M. R. (2002). Laboratory characterization of methicillin-resistant Staphylococcus aureus in Canadian hospitals: results of 5 years of National Surveillance, 1995-1999. J Infect Dis 186, 652-660.
52. Smith, E. M., Green, L. E., Medley, G. F. & 7 other authors (2005). Multilocus sequence typing of intercontinental bovine Staphylococcus aureus isolates. J Clin Microbiol 43, 4737-4743.
53. Suggs, A. H., Maranan, M. C., Boyle-Vavra, S. & Daum, R. S. (1999). Methicillin-resistant and borderline methicillin-resistant asymptomatic Staphylococcus aureus colonization in children without identifiable risk factors. Pediatr Infect Dis J 18, 410-414.
54. Tortosa, P. & Dubnau, D. (1999). Competence for transformation: a matter of taste. Curr Opin Microbiol 2, 588-592.
55. van Griethuysen, A., Bes, M., Etienne, J., Zbinden, R. & Kluytmans, J. (2001). International multicenter evaluation of latex agglutination tests for identification of Staphylococcus aureus. J Clin Microbiol 39, 86-89.
56. Varaldo, P. E. (1993). The 'borderline methicillin-susceptible' Staphylococcus aureus. J Antimicrob Chemother 31, 1-4.
57. Varaldo, P. E., Montanari, M. P., Biavasco, F., Manso, E., Ripa, S. & Santacroce, F. (1993). Survey of clinical isolates of Staphylococcus aureus for borderline susceptibility to antistaphylococcal penicillins. Eur J Clin Microbiol Infect Dis 12, 677-682.
58. Yamazumi, T., Marshall, S. A., Wilke, W. W., Diekema, D. J., Pfaller, M. A. & Jones, R. N. (2001). Comparison of the Vitek Gram-Positive Susceptibility 106 card and the MRSA-screen latex agglutination test for determining oxacillin resistance in clinical bloodstream isolates of Staphylococcus aureus. J Clin Microbiol 39, 53-56.
59. Yoshida, R., Kuwahara-Arai, K., Baba, T., Cui, L., Richardson, J. F. & Hiramatsu, K. (2003). Physiological and molecular analysis of a mecA-negative Staphylococcus aureus clinical strain that expresses heterogeneous methicillin resistance. J Antimicrob Chemother 51, 247-255.