Coagulase-negative staphylococci as reservoirs of genes facilitating MRSA infection: Staphylococcal commensal species such as Staphylococcus epidermidis are being recognized as important sources of genes promoting MRSA colonization and virulence

BioEssays

Volumn 35, Issue 1, 2013, Pages 4-11

  Otto, Michael ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

CRISPR; Horizontal gene transfer; MRSA; Staphylococcus aureus; Staphylococcus epidermidis

Indexed keywords

MEMBRANE PROTEIN; METICILLIN; PENICILLIN G;

ALLOTYPE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIAL VIRULENCE; COAGULASE NEGATIVE STAPHYLOCOCCUS; DNA SEQUENCE; GENE TRANSFER; IMMUNITY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS INFECTION; MICROBIAL DIVERSITY; MORBIDITY; PATHOGENICITY; PENICILLIN RESISTANCE; PNEUMONIA; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS EPIDERMIDIS; STAPHYLOCOCCUS HAEMOLYTICUS;

ANTI-BACTERIAL AGENTS; COAGULASE; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; HUMANS; INTERSPERSED REPETITIVE SEQUENCES; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS EPIDERMIDIS;

METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS;

EID: 84870990107     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201200112     Document Type: Article

References (68)

1. Lowy FD. 1998. Staphylococcus aureus infections. N Engl J Med 339: 520- 32.
2. Prevost G, Mourey L, Colin DA, Menestrina G. 2001. Staphylococcal pore-forming toxins. Curr Top Microbiol Immunol 257: 53- 83.
3. Wang R, Braughton KR, Kretschmer D, Bach TH, et al. 2007. Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat Med 13: 1510- 4.
4. McCormick JK, Yarwood JM, Schlievert PM. 2001. Toxic shock syndrome and bacterial superantigens: an update. Annu Rev Microbiol 55: 77- 104.
5. Rooijakkers SH, van Kessel KP, van Strijp JA. 2005. Staphylococcal innate immune evasion. Trends Microbiol 13: 596- 601.
6. Schlievert PM. 1993. Role of superantigens in human disease. J Infect Dis 167: 997- 1002.
7. Iwatsuki K, Yamasaki O, Morizane S, Oono T. 2006. Staphylococcal cutaneous infections: invasion, evasion and aggression. J Dermatol Sci 42: 203- 14.
8. Li M, Diep BA, Villaruz AE, Braughton KR, et al. 2009. Evolution of virulence in epidemic community-associated methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci USA 106: 5883- 8.
9. Foster TJ. 2005. Immune evasion by staphylococci. Nat Rev Microbiol 3: 948- 58.
10. von Eiff C, Becker K, Machka K, Stammer H, et al. 2001. Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N Engl J Med 344: 11- 6.
11. Wertheim HF, Melles DC, Vos MC, van Leeuwen W, et al. 2005. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 5: 751- 62.
12. Lowy FD. 2003. Antimicrobial resistance: the example of Staphylococcus aureus. J Clin Invest 111: 1265- 73.
13. Diekema DJ, Pfaller MA, Schmitz FJ, Smayevsky J, et al. 2001. Survey of infections due to Staphylococcus species: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997-1999. Clin Infect Dis 32: S114- 32.
14. Otto M. 2004. Virulence factors of the coagulase-negative staphylococci. Front Biosci 9: 841- 63.
15. Otto M. 2009. Staphylococcus epidermidis - the "accidental" pathogen. Nat Rev Microbiol 7: 555- 67.
16. Naik S, Bouladoux N, Wilhelm C, Molloy MJ, et al. 2012. Compartmentalized control of skin immunity by resident commensals. Science 337: 1115- 9.
17. Otto M. 2008. Staphylococcal biofilms. Curr Top Microbiol Immunol 322: 207- 28.
18. Rautenberg M, Joo HS, Otto M, Peschel A. 2011. Neutrophil responses to staphylococcal pathogens and commensals via the formyl peptide receptor 2 relates to phenol-soluble modulin release and virulence. FASEB J 25: 1254- 63.
19. Cheung GY, Rigby K, Wang R, Queck SY, et al. 2010. Staphylococcus epidermidis strategies to avoid killing by human neutrophils. PLoS Pathog 6: e1001133.
20. Otto M. 2012. Molecular basis of Staphylococcus epidermidis infections. Semin Immunopathol 34: 201- 14.
21. Novick RP, Schlievert P, Ruzin A. 2001. Pathogenicity and resistance islands of staphylococci. Microbes Infect 3: 585- 94.
22. Holden MT, Feil EJ, Lindsay JA, Peacock SJ, et al. 2004. Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci USA 101: 9786- 91.
23. Morikawa K, Inose Y, Okamura H, Maruyama A, et al. 2003. A new staphylococcal sigma factor in the conserved gene cassette: functional significance and implication for the evolutionary processes. Genes Cells 8: 699- 712.
24. Claverys JP, Martin B. 2003. Bacterial "competence" genes: signatures of active transformation, or only remnants? Trends Microbiol 11: 161- 5.
25. Lindsay JA, Holden MT. 2004. Staphylococcus aureus: superbug, super genome? Trends Microbiol 12: 378- 85.
26. Archer GL, Johnston JL. 1983. Self-transmissible plasmids in staphylococci that encode resistance to aminoglycosides. Antimicrob Agents Chemother 24: 70- 7.
27. Katayama Y, Ito T, Hiramatsu K. 2000. A new class of genetic element, staphylococcus cassette chromosome mec, encodes methicillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 44: 1549- 55.
28. Ito T, Katayama Y, Asada K, Mori N, et al. 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- 36.
29. Chambers HF, Hartman BJ, Tomasz A. 1985. Increased amounts of a novel penicillin-binding protein in a strain of methicillin-resistant Staphylococcus aureus exposed to nafcillin. J Clin Invest 76: 325- 31.
30. Couto I, de Lencastre H, Severina E, Kloos W, et al. 1996. Ubiquitous presence of a mecA homologue in natural isolates of Staphylococcus sciuri. Microb Drug Resist 2: 377- 91.
31. Schnellmann C, Gerber V, Rossano A, Jaquier V, et al. 2006. Presence of new mecA and mph(C) variants conferring antibiotic resistance in Staphylococcus spp. isolated from the skin of horses before and after clinic admission. J Clin Microbiol 44: 4444- 54.
32. Ito T, Hiramatsu K, Tomasz A, de Lencastre H, et al. 2012. Guidelines for reporting novel mecA gene homologues. Antimicrob Agents Chemother 56: 4997- 9.
33. Tsubakishita S, Kuwahara-Arai K, Baba T, Hiramatsu K. 2010. Staphylococcal cassette chromosome mec-like element in Macrococcus caseolyticus. Antimicrob Agents Chemother 54: 1469- 75.
34. Garcia-Alvarez L, Holden MT, Lindsay H, Webb CR, et al. 2011. Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect Dis 11: 595- 603.
35. Chatterjee SS, Chen L, Joo HS, Cheung GY, et al. 2011. Distribution and regulation of the mobile genetic element-encoded phenol-soluble modulin PSM-mec in methicillin-resistant Staphylococcus aureus. PLoS ONE 6: e28781.
36. Queck SY, Khan BA, Wang R, Bach TH, et al. 2009. Mobile genetic element-encoded cytolysin connects virulence to methicillin resistance in MRSA. PLoS Pathog 5: e1000533.
37. Wu S, Piscitelli C, de Lencastre H, Tomasz A. 1996. Tracking the evolutionary origin of the methicillin resistance gene: cloning and sequencing of a homologue of mecA from a methicillin susceptible strain of Staphylococcus sciuri. Microb Drug Resist 2: 435- 41.
38. Tsubakishita S, Kuwahara-Arai K, Sasaki T, Hiramatsu K. 2010. Origin and molecular evolution of the determinant of methicillin resistance in staphylococci. Antimicrob Agents Chemother 54: 4352- 9.
39. Barbier F, Ruppe E, Hernandez D, Lebeaux D, et al. 2010. Methicillin-resistant coagulase-negative staphylococci in the community: high homology of SCCmec IVa between Staphylococcus epidermidis and major clones of methicillin-resistant Staphylococcus aureus. J Infect Dis 202: 270- 81.
40. Wisplinghoff H, Rosato AE, Enright MC, Noto M, et al. 2003. Related clones containing SCCmec type IV predominate among clinically significant Staphylococcus epidermidis isolates. Antimicrob Agents Chemother 47: 3574- 9.
41. Archer GL, Thanassi JA, Niemeyer DM, Pucci MJ. 1996. Characterization of IS1272, an insertion sequence-like element from Staphylococcus haemolyticus. Antimicrob Agents Chemother 40: 924- 9.
42. Jones RN, Barry AL, Gardiner RV, Packer RR. 1989. The prevalence of staphylococcal resistance to penicillinase-resistant penicillins. A retrospective and prospective national surveillance trial of isolates from 40 medical centers. Diagn Microbiol Infect Dis 12: 385- 94.
43. Schmitz FJ, Verhoef J, Fluit AC. 1999. Prevalence of resistance to MLS antibiotics in 20 European university hospitals participating in the European SENTRY surveillance programme. Sentry Participants Group. J Antimicrob Chemother 43: 783- 92.
44. Lacey RW. 1972. Transfer of chromosomal genes between staphylococci in mixed cultures. J Gen Microbiol 71: 399- 401.
45. Cohen S, Sweeney HM. 1973. Effect of the prophage and penicillinase plasmid of the recipient strain upon the transduction and the stability of methicillin resistance in Staphylococcus aureus. J Bacteriol 116: 803- 11.
46. Tormo MA, Knecht E, Gotz F, Lasa I, et al. 2005. Bap-dependent biofilm formation by pathogenic species of Staphylococcus: evidence of horizontal gene transfer? Microbiology 151: 2465- 75.
47. Wielders CL, Vriens MR, Brisse S, de Graaf-Miltenburg LA, et al. 2001. In-vivo transfer of mecA DNA to Staphylococcus aureus. Lancet 357: 1674- 5.
48. Diep BA, Gill SR, Chang RF, Phan TH, et al. 2006. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367: 731- 9.
49. Diep BA, Stone GG, Basuino L, Graber CJ, et al. 2008. The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillin-resistant Staphylococcus aureus. J Infect Dis 197: 1523- 30.
50. Montgomery CP, Boyle-Vavra S, Daum RS. 2009. The arginine catabolic mobile element is not associated with enhanced virulence in experimental invasive disease caused by the community-associated methicillin-resistant Staphylococcus aureus USA300 genetic background. Infect Immun 77: 2650- 6.
51. DeLeo FR, Otto M, Kreiswirth BN, Chambers HF. 2010. Community-associated meticillin-resistant Staphylococcus aureus. Lancet 375: 1557- 68.
52. Diep BA, Otto M. 2008. The role of virulence determinants in community-associated MRSA pathogenesis. Trends Microbiol 16: 361- 9.
53. Joshi GS, Spontak JS, Klapper DG, Richardson AR. 2011. Arginine catabolic mobile element encoded speG abrogates the unique hypersensitivity of Staphylococcus aureus to exogenous polyamines. Mol Microbiol 82: 9- 20.
54. Urushibara N, Kawaguchiya M, Kobayashi N. 2012. Two novel arginine catabolic mobile elements and staphylococcal chromosome cassette mec composite islands in community-acquired methicillin-resistant Staphylococcus aureus genotypes ST5-MRSA-V and ST5-MRSA-II. J Antimicrob Chemother 67: 1828- 34.
55. Bartels MD, Hansen LH, Boye K, Sorensen SJ, et al. 2011. An unexpected location of the arginine catabolic mobile element (ACME) in a USA300-related MRSA strain. PLoS ONE 6: e16193.
56. Shore AC, Rossney AS, Brennan OM, Kinnevey PM, et al. 2011. Characterization of a novel arginine catabolic mobile element (ACME) and staphylococcal chromosomal cassette mec composite island with significant homology to Staphylococcus epidermidis ACME type II in methicillin-resistant Staphylococcus aureus genotype ST22-MRSA-IV. Antimicrob Agents Chemother 55: 1896- 905.
57. Barbier F, Lebeaux D, Hernandez D, Delannoy AS, et al. 2011. High prevalence of the arginine catabolic mobile element in carriage isolates of methicillin-resistant Staphylococcus epidermidis. J Antimicrob Chemother 66: 29- 36.
58. Miragaia M, de Lencastre H, Perdreau-Remington F, Chambers HF, et al. 2009. Genetic diversity of arginine catabolic mobile element in Staphylococcus epidermidis. PLoS ONE 4: e7722.
59. Pi B, Yu M, Chen Y, Yu Y, et al. 2009. Distribution of the ACME-arcA gene among meticillin-resistant Staphylococcus haemolyticus and identification of a novel ccr allotype in ACME-arcA-positive isolates. J Med Microbiol 58: 731- 6.
60. Li M, Du X, Villaruz AE, Diep BA, et al. 2012. MRSA epidemic linked to a quickly spreading colonization and virulence determinant. Nat Med 18: 816- 9.
61. Kriegeskorte A, Peters G. 2012. Horizontal gene transfer boosts MRSA spreading. Nat Med 18: 662- 3.
62. Holden MT, Lindsay JA, Corton C, Quail MA, et al. 2010. Genome sequence of a recently emerged, highly transmissible, multi-antibiotic- and antiseptic-resistant variant of methicillin-resistant Staphylococcus aureus, sequence type 239 (TW). J Bacteriol 192: 888- 92.
63. Soderquist B, Andersson M, Nilsson M, Nilsdotter-Augustinsson A, et al. 2009. Staphylococcus epidermidis surface protein I (SesI): a marker of the invasive capacity of S. epidermidis? J Med Microbiol 58: 1395- 7.
64. Massey RC, Horsburgh MJ, Lina G, Hook M, et al. 2006. The evolution and maintenance of virulence in Staphylococcus aureus: a role for host-to-host transmission? Nat Rev Microbiol 4: 953- 8.
65. Jansen R, Embden JD, Gaastra W, Schouls LM. 2002. Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol 43: 1565- 75.
66. Bikard D, Marraffini LA. 2012. Innate and adaptive immunity in bacteria: mechanisms of programmed genetic variation to fight bacteriophages. Curr Opin Immunol 24: 15- 20.
67. Conlan S, Mijares LA, Comp Seq Program N, Becker J, et al. 2012. Staphylococcus epidermidis pan-genome sequence analysis reveals diversity of skin commensal and hospital infection-associated isolates. Genome Biol 13: R64.
68. Marraffini LA, Sontheimer EJ. 2010. Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature 463: 568- 71.