Methicillin-resistant staphylococcus aureus antibiotic resistance and virulence

BioScience Trends

Volumn 7, Issue 3, 2013, Pages 113-121

  Xia, Jufeng ^a   Gao, Jianjun ^a   Kokudo, Norihiro ^a   Hasegawa, Kiyoshi ^a   Tang, Wei ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Antibiotic resistance; Biofilm; Mutation; Staphylococcus aureus; Virulence

Indexed keywords

ANTIINFECTIVE AGENT;

BIOFILM; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MUTATION; PATHOGENICITY; PHYSIOLOGY; REVIEW; VIRULENCE;

ANTI-BACTERIAL AGENTS; BIOFILMS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MUTATION; VIRULENCE;

EID: 84880594272     PISSN: 18817815     EISSN: 18817823     Source Type: Journal    
DOI: 10.5582/bst.2013.v7.3.113     Document Type: Review

References (84)

1. Jevons MP, Rolinson GN, Knox R. Celbenin-Resistant Staphylococci. BMJ. 1961; 1:b124-b125.
2. Lowy FD. Medical progress-Staphylococcus aureus infections. N Engl J Med. 1998;339:520-532.
3. Grundmann H, Aanensen DM, van den Wijngaard CC, Spratt BG, Harmsen D, Friedrich AW, Reference ES. Geographic Distribution of Staphylococcus aureus Causing Invasive Infections in Europe: A Molecular-Epidemiological Analysis. PLoS Med. 2010;7:e1000215.
4. Song JH, Hsueh PR, Chung DR, et al. Spread of methicillin-resistant Staphylococcus aureus between the community and the hospitals in Asian countries: an ANSORP study. J Antimicrob Chemother. 2011;66:1061-1069.
5. Mejia C, Zurita J, Guzman-Blanco M, Gram LAWG. Epidemiology and surveillance of methicillin-resistant Staphylococcus aureus in Latin America. Braz J Infect Dis. 2010; 14:S79-S86.
6. Diekema DJ, Pfaller MA, Schmitz FJ, Smayevsky J, Bell J, Jones RN, Beach M, Grp SP. 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. 2001;32:S114-S132.
7. Nakamura A, Miyake K, Misawa S, Kuno Y, Horii T, Hori S, Kondo S, Tabe Y, Ohsaka A. Association between antimicrobial consumption and clinical isolates of methicillin-resistant Staphylococcus aureus: a 14-year study. J Infect Chemother. 2012; 18:90-95.
8. Monecke S, Coombs G, Shore AC, et al. A Field Guide to Pandemic, Epidemic and Sporadic Clones of Methicillin-Resistant Staphylococcus aureus. PLoS One. 2011; 6:e17936.
9. Sanchini A, Campanile F, Monaco M, Cafiso V, Rasigade JP, Laurent F, Etienne J, Stefani S, Pantosti A. DNA microarray-based characterisation of Panton-Valentine leukocidin-positive community-acquired methicillin-resistant Staphylococcus aureus from Italy. Eur J Clin Microbiol Infect Dis. 2011; 30:1399-1408.
10. Pinho MG, de Lencastre H, Tomasz A. 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. 2001; 98:10886-10891.
11. García-Álvarez L, Holden MT, Lindsay H, et al. 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. 2011; 11:595-603.
12. Harris SR, Cartwright EJP, Torok ME, Holden MTG, Brown NM, Ogilvy-Stuart AL, Ellington MJ, Quail MA, Bentley SD, Parkhill J, Peacock SJ. Whole-genome sequencing for analysis of an outbreak of meticillin-resistant Staphylococcus aureus: a descriptive study. Lancet Infect Dis. 2013; 13:130-136.
13. Firth N SR. Gram-positive pathogens. ASM Press, Washington, DC, USA, 2006.
14. Lindsay JA, Moore CE, Day NP, Peacock SJ, Witney AA, Stabler RA, Husain SE, Butcher PD, Hinds J. Microarrays reveal that each of the ten dominant lineages of Staphylococcus aureus has a unique combination of surface-associated and regulatory genes. J Bacteriol. 2006; 188:669-676.
15. Lindsay JA. Genomic variation and evolution of Staphylococcus aureus. Int J Med Microbiol. 2010; 300:98-103.
16. Malachowa N, DeLeo FR. Mobile genetic elements of Staphylococcus aureus. Cell Mol Life Sci. 2010; 67:3057-3071.
17. Enright MC, Day NPJ, Davies CE, Peacock SJ, Spratt BG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol. 2000; 38:1008-1015.
18. Stefani S, Goglio A. Methicillin-resistant Staphylococcus aureus: related infections and antibiotic resistance. Int J Infect Dis. 2010; 14:S19-S22.
19. Novick RP. Staphylococcal Plasmids and Their Replication. Annu Rev Microbiol. 1989; 43:537-565.
20. Campanile F BD, Borbone S, Stefani S. Methicillin-resistant Staphylococcus aureus evolution: the multiple facets of an old pathogen. Eur Infect Dis. 2010; 4:70-76.
21. Waldron DE, Lindsay JA. Sau1: a novel line age-specific type I restriction-modification system that blocks horizontal gene transfer into Staphylococcus aureus and between S-aureus isolates of different lineages. J Bacteriol. 2006; 188:5578-5585.
22. Cockfield JD, Pathak S, Edgeworth JD, Lindsay JA. Rapid determination of hospital-acquired meticillin-resistant Staphylococcus aureus lineages. J Med Microbiol. 2007; 56:614-619.
23. Barber M, Rozwadowskadowzenko M. Infection by Penicillin-Resistant Staphylococci. Lancet. 1948; 255:641-644.
24. Rammelkamp CH, Maxon T. Resistance of Staphylococcus aureus to the action of penicillin. Proc Soc Exp Biol Med. 1942; 51: 386-389.
25. Abraham EP, Chain E. An Enzyme from Bacteria Able to Destroy Penicillin. 1940. (Reprinted from Nature, Vol 146, Pg 837, 1940). Rev Infect Dis. 1988; 10: 677-678.
26. Jevons MP, Coe AW, Parker MT. Methicillin Resistance in Staphylococci. Lancet. 1963; 1:904-907.
27. Shorr AF. Epidemiology of staphylococcal resistance. Clin Infect Dis. 2007; 45: S171-S176.
28. McDougal LK, Fosheim GE, Nicholson A, Bulens SN, Limbago BM, Shearer JES, Summers AO, Patel JB. Emergence of Resistance among USA300 Methicillin-Resistant Staphylococcus aureus Isolates Causing Invasive Disease in the United States. Antimicrob Agents Chemother. 2010; 54:3804-3811.
29. Moellering RC, Jr., Linden PK. The specter of glycopeptide resistance: current trends and future considerations. Introduction. Am J Med. 1998; 104:1S-2S.
30. Sakoulas G MRJ. Increasing antibiotic resistance among methicillin-resistant Staphylococcus aureus strains. Clin Infect Dis. 2008; Suppl 5: S360-S367.
31. Howden BP, Ward PB, Charles PGP, et al. Treatment outcomes for serious infections caused by methicillin-resistant Staphylococcus aureus with reduced vancomycin susceptibility. Clin Infect Dis. 2004; 38:521-528.
32. Tenover FC, Moellering RC. The rationale for revising the Clinical and Laboratory Standards Institute vancomycin minimal inhibitory concentration interpretive criteria for Staphylococcus aureus. Clin Infect Dis. 2007; 44:1208-1215.
33. van Hal SJ, Paterson DL. Systematic Review and Meta-Analysis of the Significance of Heterogeneous Vancomycin-Intermediate Staphylococcus aureus Isolates. Antimicrob Agents Chemother. 2011; 55:405-410.\
34. Peleg AY, Monga D, Pillai S, Mylonakis E, Moellering RC, Eliopoulos GM. Reduced Susceptibility to Vancomycin Influences Pathogenicity in Staphylococcus aureus Infection. J Infect Dis. 2009; 199:532-536.
35. Kennedy AD, Otto M, Braughton KR, Whitney AR, Chen L, Mathema B, Mediavilla JR, Byrne KA, Parkins LD, Tenover FC, Kreiswirth BN, Musser JM, DeLeo FR. Epidemic community-associated methicillin-resistant Staphylococcus aureus: Recent clonal expansion and diversification. Proc Natl Acad Sci U S A. 2008; 105:1327-1332.
36. Peleg AY CD, Ward D. A novel mechanism of reduced susceptibility to vancomycin in Staphylococcus aureus. The Twenty-first European Congress of Clinical Microbiology and Infectious Diseases/Twenty-seventh International Congress of Chemotherapy. Milan, Italy, 2011.
37. Schweizer ML, Furuno JP, Sakoulas G, Johnson JK, Harris AD, Shardell MD, McGregor JC, Thom KA, Perencevich EN. Increased Mortality with Accessory Gene Regulator (agr) Dysfunction in Staphylococcus aureus among Bacteremic Patients. Antimicrob Agents Chemother. 2011; 55:1082-1087.
38. Neoh HM, Cui L, Yuzawa H, Takeuchi F, Matsuo M, Hiramatsu K. Mutated response regulator graR is responsible for phenotypic conversion of Staphylococcus aureus from heterogeneous vancomycin-intermediate resistance to vancomycin-intermediate resistance. Antimicrob Agents Chemother. 2008; 52:45-53.
39. Cui LZ, Isii T, Fukuda M, Ochiai T, Neoh HM, Camargo ILBD, Watanabe Y, Shoji M, Hishinuma T, Hiramatsu K. An RpoB Mutation Confers Dual Heteroresistance to Daptomycin and Vancomycin in Staphylococcus aureus. Antimicrob Agents Chemother. 2010; 54:5222-5233.
40. Watanabe Y, Cui LZ, Katayama Y, Kozue K, Hiramatsu K. Impact of rpoB Mutations on Reduced Vancomycin Susceptibility in Staphylococcus aureus. J Clin Microbiol. 2011; 49:2680-2684.
41. Levine DP, Fromm BS, Reddy BR. Slow Response to Vancomycin or Vancomycin Plus Rifampin in Methicillin-Resistant Staphylococcus aureus Endocarditis. Ann Intern Med. 1991; 115:674-680.
42. Riedel DJ, Weekes E, Forrest GN. Addition of rifampin to standard therapy for treatment of native valve infective endocarditis caused by Staphylococcus aureus. Antimicrob Agents Chemother. 2008; 52:2463-2467.
43. Jang HC, Kim SH, Kim KH, Kim CJ, Lee S, Song KH, Jeon JH, Park WB, Bin Kim H, Park SW, Kim NJ, Kim EC, Oh M, Choe KW. Salvage Treatment for Persistent Methicillin-Resistant Staphylococcus aureus Bacteremia: Efficacy of Linezolid With or Without Carbapenem. Clin Infect Dis. 2009; 49:395-401.
44. Garrigos C, Murillo O, Euba G, Verdaguer R, Tubau F, Cabellos C, Cabo J, Ariza J. Efficacy of Usual and High Doses of Daptomycin in Combination with Rifampin versus Alternative Therapies in Experimental Foreign-Body Infection by Methicillin-Resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2010; 54:5251-5256.
45. Vergidis P, Rouse MS, Euba G, Karau MJ, Schmidt SM, Mandrekar JN, Steckelberg JM, Patel R. Treatment with Linezolid or Vancomycin in Combination with Rifampin Is Effective in an Animal Model of Methicillin-Resistant Staphylococcus aureus Foreign Body Osteomyelitis. Antimicrob Agents Chemother. 2011; 55:1182-1186.
46. Friedman L, Alder JD, Silverman JA. Genetic changes that correlate with reduced susceptibility to daptomycin in Staphylococcus aureus. Antimicrob Agents Chemother. 2006; 50:2137-2145.
47. Peleg AY MA, Miyakis S. Genetic evolution of resistance to daptomycin in Staphylococcus aureus. The Fiftieth Interscience Conference on Antimicrobial Agents and Chemotherapy. American Society for Microbiology. Washington, DC, USA, 2010.
48. Yang SJ, Kreiswirth BN, Sakoulas G, Yeaman MR, Xiong YQ, Sawa A, Bayer AS. Enhanced Expression of dltABCD Is Associated with the Development of Daptomycin Nonsusceptibility in a Clinical Endocarditis Isolate of Staphylococcus aureus. J Infect Dis. 2009;200:1916-1920.
49. Prystowsky J, Siddiqui F, Chosay J, Shinabarger DL, Millichap J, Peterson LR, Noskin GA. Resistance to linezolid: Characterization of mutations in rRNA and comparison of their occurrences in vancomycin-resistant enterococci. Antimicrob Agents Chemother. 2001; 45:2154-2156.
50. Marshall SH, Donskey CJ, Hutton-Thomas R, Salata RA, Rice LB. Gene dosage and linezolid resistance in Enterococcus faecium and Enterococcus faecalis. Antimicrob Agents Chemother. 2002; 46:3334-3336.
51. Besier S, Ludwig A, Zander J, Brade V, Wichelhaus TA. Linezolid resistance in Staphylococcus aureus: Gene dosage effect, stability, fitness costs, and cross-resistances. Antimicrob Agents Chemother. 2008; 52:1570-1572.
52. Meka VG, Pillai SK, Sakoulas G, Wennersten C, Venkataraman L, DeGirolami PC, Eliopoulos GM, Moellering RC, Gold HS. Linezolid resistance in sequential Staphylococcus aureus isolates associated with a T2500A mutation in the 23S rRNA gene and loss of a single copy of rRNA. J Infect Dis. 2004; 190:311-317.
53. Meka VG, Gold HS, Cooke A, Venkataraman L, Eliopoulos GM, Moellering RC, Jenkins SG. Reversion to susceptibility in a linezolid-resistant clinical isolate of Staphylococcus aureus. J Antimicrob Chemother. 2004; 54:818-820.
54. Wertheim HFL, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. 2005; 5:751-762.
55. Mathema B, Holzman RS, Knipe TA, Becker K, von Eiff C, Peters G, Chen L, Kreiswirth BN, Novick RP, Shopsin B. Nasal Carriage as a Source of agr-Defective Staphylococcus aureus Bacteremia. J Infect Dis. 2012; 206:1168-1177.
56. Wertheim HFL, Vos MC, Ott A, van Belkum A, Voss A, Kluytmans JAJW, van Keulen PHJ, Vandenbroucke-Grauls CMJE, Meester MHM, Verbrugh HA. Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet. 2004; 364:703-705.
57. Ammerlaan HSM, Kluytmans JAJW, Berkhout H, et al. Eradication of carriage with methicillin-resistant Staphylococcus aureus: effectiveness of a national guideline. J Antimicrob Chemother. 2011; 66:2409-2417.
58. Mulcahy ME, Geoghegan JA, Monk IR, O'Keeffe KM, Walsh EJ, Foster TJ, McLoughlin RM. Nasal Colonisation by Staphylococcus aureus Depends upon Clumping Factor B Binding to the Squamous Epithelial Cell Envelope Protein Loricrin. PLoS Pathog. 2012; 8:e1003092:
59. Roche FM, Meehan M, Foster TJ. The Staphylococcus aureus surface protein SasG and its homologues promote bacterial adherence to human desquamated nasal epithelial cells. Microbiology. 2003; 149:2759-2767.
60. Li M, Du X, Villaruz AE, Diep BA, Wang DC, Song Y, Tian YR, Hu JH, Yu FY, Lu Y, Otto M. MRSA epidemic linked to a quickly spreading colonization and virulence determinant. Nat Med. 2012; 18:816-217.
61. Andra J, Goldmann T, Ernst CM, Peschel A, Gutsmann T. Multiple Peptide Resistance Factor (MprF)-mediated Resistance of Staphylococcus aureus against Antimicrobial Peptides Coincides with a Modulated Peptide Interaction with Artificial Membranes Comprising Lysyl-Phosphatidylglycerol. J Biol Chem. 2011; 286:18692-18700.
62. Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: From the natural environment to infectious diseases. Nat Rev Microbiol. 2004; 2:95-108.
63. Lear G. Microbial Biofilms: Current Research and Applications. Caister Academic Press, Norwich, UK, 2012.
64. Shopsin B, Drlica-Wagner A, Mathema B, Adhikari RP, Kreiswirth BN, Novick RP. Prevalence of agr dysfunction among colonizing Staphylococcus aureus strains. J Infect Dis. 2008; 198:1171-1174.
65. Amaral MM, Coelho LR, Flores RP, Souza RR, Silva-Carvalho MC, Teixeira LA, Ferrerira-Carvalho BT, Figueiredo AMS. The predominant variant of the Brazilian epidemic clonal complex of methicillin-resistant Staphylococcus aureus has an enhanced ability to produce biofilm and to adhere to and invade airway epithelial cells. J Infect Dis. 2005; 192:801-810.
66. Novick RP, Ross HF, Projan SJ, Kornblum J, Kreiswirth B, Moghazeh S. Synthesis of Staphylococcal Virulence Factors Is Controlled by a Regulatory Rna Molecule. Embo Journal. 1993; 12:3967-3975.
67. Conrady DG, Wilson JJ, Herr AB. Structural basis for Zn2+-dependent intercellular adhesion in staphylococcal biofilms. Proc Natl Acad Sci U S A. 2013; 110:E202-E211.
68. Otto M. Mobile genetic element-encoded cytolysin connects virulence to methicillin resistance in MRSA. Virulence. 2010; 1:49-51.
69. Cheung GYC, Wang R, Khan BA, Sturdevant DE, Otto M. Role of the Accessory Gene Regulator agr in Community-Associated Methicillin-Resistant Staphylococcus aureus Pathogenesis. Infect Immun. 2011; 79:1927-1935.
70. Rudkin JK, Edwards AM, Bowden MG, Brown EL, Pozzi C, Waters EM, Chan WC, Williams P, O'Gara JP, Massey RC. Methicillin Resistance Reduces the Virulence of Healthcare-Associated Methicillin-Resistant Staphylococcus aureus by Interfering With the agr Quorum Sensing System. J Infect Dis. 2012; 205:798-806.
71. Deleo FR, Chambers HF. Reemergence of antibiotic-resistant Staphylococcus aureus in the genomics era. Journal of Clinical Investigation. 2009; 119: 2464-2474.
72. Otto M. Basis of Virulence in Community-Associated Methicillin-Resistant Staphylococcus aureus. Annu Rev Microbiol. 2010; 64:143-162.
73. Thurlow LR, Joshi GS, Clark JR, Spontak JS, Neely CJ, Maile R, Richardson AR. Functional Modularity of the Arginine Catabolic Mobile Element Contributes to the Success of USA300 Methicillin-Resistant Staphylococcus aureus. Cell Host Microbe. 2013; 13:100-107.
74. Vandenesch F, Naimi T, Enright MC, Lina G, Nimmo GR, Heffernan H, Liassine N, Bes M, Greenland T, Reverdy ME, Etienne J. Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: Worldwide emergence. Emerg Infect Dis. 2003; 9:978-984.
75. Li M, Diep BA, Villaruz AE, Braughton KR, Jiang XF, Deleo FR, Chambers HF, Lu Y, Otto M. Evolution of virulence in epidemic community-associated methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci U S A. 2009; 106:5883-5888.
76. Kobayashi SD, Malachowa N, Whitney AR, Braughton KR, Gardner DJ, Long D, BubeckWardenburg J, Schneewind O, Otto M, DeLeo FR. Comparative Analysis of USA300 Virulence Determinants in a Rabbit Model of Skin and Soft Tissue Infection. J Infect Dis. 2011; 204:937-941.
77. Watkins RR, David MZ, Salata RA. Current concepts on the virulence mechanisms of meticillin-resistant Staphylococcus aureus. J Med Microbiol. 2012; 61:1179-1193.
78. Lipinska U, Hermans K, Meulemans L, Dumitrescu O, Badiou C, Duchateau L, Haesebrouck F, Etienne J, Lina G. Panton-Valentine Leukocidin Does Play a Role in the Early Stage of Staphylococcus aureus Skin Infections: A Rabbit Model. PLoS One. 2011; 6:e22864.
79. Periasamy SCS, Cheung GY, Otto M. Phenol-soluble modulins in staphylococci: What are they originally for? Commun Integr Biol. 2012; 5:275-277.
80. Bubeck Wardenburg J, Bae T, Otto M, Deleo FR, Schneewind O. Poring over pores: alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat Med. 2007; 13:1405-1406.
81. Hanberger H, Walther S, Leone M, Barie PS, Rello J, Lipman J, Marshall JC, Anzueto A, Sakr Y, Pickkers P, Felleiter P, Engoren M, Vincent JL, Investigators EIG. Increased mortality associated with meticillin-resistant Staphylococcus aureus (MRSA) infection in the Intensive Care Unit: results from the EPIC II study. Int J Antimicrob Agents. 2011; 38:331-335.
82. Wilson GJ, Seo KS, Cartwright RA, Connelley T, Chuang-Smith ON, Merriman JA, Guinane CM, Park JY, Bohach GA, Schlievert PM, Morrison WI, Fitzgerald JR. A Novel Core Genome-Encoded Superantigen Contributes to Lethality of Community-Associated MRSA Necrotizing Pneumonia. PLoS Pathog. 2011; 7:e1002271.
83. Shinefield H, Black S, Fattom A, Horwith G, Rasgon S, Ordonez J, Yeoh H, Law D, Robbins JB, Schneerson R, Muenz L, Naso R. Use of a Staphylococcus aureus conjugate vaccine in patients receiving hemodialysis. N Engl J Med. 2002; 346:491-496.
84. Anderson AS, Miller AA, Donald RGK, Scully IL, Nanra JS, Cooper D, Jansen KU. Development of a multicomponent Staphylococcus aureus vaccine designed to counter multiple bacterial virulence factors. Hum Vaccin Immunother. 2012; 8:1585-1594.