Simulated antibiotic exposures in an in vitro hollow-fiber infection model influence toxin gene expression and production in community-associated methicillin-resistant Staphylococcus aureus strain MW2

Antimicrobial Agents and Chemotherapy

Volumn 56, Issue 1, 2012, Pages 140-147

  Pichereau, Solen ^a,b   Pantrangi, Madhulatha ^c   Couet, William ^b   Badiou, Cedric ^d   Lina, Gerard ^d   Shukla, Sanjay K ^c   Rosea, Warren E ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITÉ DE POITIERS   (France)

^c MARSHFIELD CLINIC   (United States)

^d HOSPICES CIVILS DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CLINDAMYCIN; COTRIMOXAZOLE; ENTEROTOXIN; LINEZOLID; MINOCYCLINE; PANTON VALENTINE LEUKOCIDIN; PROTEIN SEC4; PROTEIN SEK; PROTEIN SEL2; PROTEIN SEQ; UNCLASSIFIED DRUG; VANCOMYCIN;

ANTIBIOTIC SENSITIVITY; ARTICLE; COMMUNITY ASSOCIATED METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; CYTOTOXICITY; DOWN REGULATION; DRUG HALF LIFE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE CONTROL; GENE EXPRESSION; HOLLOW FIBER; HUMAN; HUMAN CELL; MAXIMUM PLASMA CONCENTRATION; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION;

ACETAMIDES; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CELL CULTURE TECHNIQUES; CLINDAMYCIN; COMMUNITY-ACQUIRED INFECTIONS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXOTOXINS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; LEUKOCIDINS; LEUKOCYTES, MONONUCLEAR; METHICILLIN RESISTANCE; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; MINOCYCLINE; MODELS, BIOLOGICAL; OXAZOLIDINONES; REAL-TIME POLYMERASE CHAIN REACTION; STAPHYLOCOCCAL INFECTIONS; TRIMETHOPRIM-SULFAMETHOXAZOLE COMBINATION; VANCOMYCIN; VIRULENCE FACTORS;

EID: 84455169884     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.05113-11     Document Type: Article

References (57)

1. Azeh I, et al. 2002. Protein synthesis inhibiting clindamycin improves outcome in a mouse model of Staphylococcus aureus sepsis compared with the cell wall active ceftriaxone. Crit. Care Med. 30:1560-1564. (Pubitemid 34756241)
2. Baba T, et al. 2002. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359:1819-1827. (Pubitemid 34607058)
3. Badiou C, et al. 2010. Rapid detection of Staphylococcus aureus Panton- Valentine leukocidin in clinical specimens by enzyme-linked immunosorbent assay and immunochromatographic tests. J. Clin. Microbiol. 48: 1384-1390.
4. Besseyre des Horts T, et al. 2010. A histidine-to-arginine substitution in Panton-Valentine leukocidin from USA300 community-acquired methicillin-resistant Staphylococcus aureus does not impair its leukotoxicity. Infect. Immun. 78:260-264.
5. Bishburg E, Bishburg K. 2009. Minocycline- an old drug for a new century: emphasis on methicillin-resistant Staphylococcus aureus (MRSA) and Acinetobacter baumannii. Int. J. Antimicrob. Agents. 34:395-401.
6. Boakes E, et al. 2011. Distinct bacteriophages encoding Panton-Valentine leukocidin (PVL) among international methicillin-resistant Staphylococcus aureus clones harboring PVL. J. Clin. Microbiol. 49:684-692.
7. Bowker KE, Noel AR, Macgowan AP. 2008. Pharmacodynamics of minocycline against Staphylococcus aureus in an in vitro pharmacokinetic model. Antimicrob. Agents Chemother. 52:4370-4373.
8. Bronner S, Monteil H, Prevost G. 2004. Regulation of virulence determinants in Staphylococcus aureus: complexity and applications. FEMS Microbiol. Rev. 28:183-200. (Pubitemid 38510501)
9. Bubeck Wardenburg J, Bae T, Otto M, Deleo FR, Schneewind O. 2007. Poring over pores: alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat. Med. 13:1405-1406. (Pubitemid 350224232)
10. Bubeck Wardenburg J, Palazzolo-Ballance AM, Otto M, Schneewind O, DeLeo FR. 2008. Panton-Valentine leukocidin is not a virulence determinant in murine models of community-associated methicillin-resistant Staphylococcus aureus disease. J. Infect. Dis. 198:1166-1170.
11. Chambers HF. 2009. Pathogenesis of staphylococcal infection: a manner of expression. J. Infect. Dis. 199:291-293.
12. Clements MO, Foster SJ. 1999. Stress resistance in Staphylococcus aureus. Trends Microbiol. 7:458-462. (Pubitemid 29528234)
13. Clinical Laboratory Standards Institute. 2009. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard, 9th ed. Clinical and Laboratory Standards Institute, Wayne, PA.
14. Cremieux AC, et al. 2009. Panton-valentine leukocidin enhances the severity of community-associated methicillin-resistant Staphylococcus aureus rabbit osteomyelitis. PLoS One 4:e7204.
15. Darley ES, MacGowan AP. 2004. Antibiotic treatment of gram-positive bone and joint infections. J. Antimicrob. Chemother. 53:928-935. (Pubitemid 38811422)
16. Daum RS, et al. 2002. A novel methicillin-resistance cassette in community-acquired methicillin-resistant Staphylococcus aureus isolates of diverse genetic backgrounds. J. Infect. Dis. 186:1344-1347. (Pubitemid 35193015)
17. Dehghanyar P, et al. 2005. Penetration of linezolid into soft tissues of healthy volunteers after single and multiple doses. Antimicrob. Agents Chemother. 49:2367-2371. (Pubitemid 40734468)
18. Dennis PP. 1976. Effects of chloramphenicol on the transcriptional activities of ribosomal RNA and ribosomal protein genes in Escherichia coli. J. Mol. Biol. 108:535-546. (Pubitemid 8008274)
19. Diep BA, et al. 2010. Polymorphonuclear leukocytes mediate Staphylococcus aureus Panton-Valentine leukocidin-induced lung inflammation and injury. Proc. Natl. Acad. Sci. U. S. A. 107:5587-5592.
20. Drusano GL, Liu W, Brown DL, Rice LB, Louie A. 2009. Impact of short-course quinolone therapy on susceptible and resistant populations of Staphylococcus aureus. J. Infect. Dis. 199:219-226.
21. Dumitrescu O, et al. 2007. Effect of antibiotics on Staphylococcus aureus producing Panton-Valentine leukocidin. Antimicrob. Agents Chemother. 51:1515-1519. (Pubitemid 46586841)
22. Erill I, Campoy S, Barbe J. 2007. Aeons of distress: an evolutionary perspective on the bacterial SOS response. FEMS Microbiol. Rev. 31: 637-656. (Pubitemid 47621761)
23. Foster TJ, Hook M. 1998. Surface protein adhesins of Staphylococcus aureus. Trends Microbiol. 6:484-488. (Pubitemid 29002881)
24. Fridkin SK, et al. 2005. Methicillin-resistant Staphylococcus aureus disease in three communities. N. Engl. J. Med. 352:1436-1444.
25. Gillet Y, et al. 2002. Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet 359: 753-759. (Pubitemid 34215075)
26. Goerke C, Koller J, Wolz C. 2006. Ciprofloxacin and trimethoprim cause phage induction and virulence modulation in Staphylococcus aureus. Antimicrob. Agents Chemother. 50:171-177. (Pubitemid 43042918)
27. Gonzalez BE, et al. 2005. Severe staphylococcal sepsis in adolescents in the era of community-acquired methicillin-resistant Staphylococcus aureus. Pediatrics. 115:642-648. (Pubitemid 43378904)
28. Hamilton SM, et al. 2007. In vitro production of Panton-Valentine leukocidin among strains of methicillin-resistant Staphylococcus aureus causing diverse infections. Clin. Infect. Dis. 45:1550-1558. (Pubitemid 351411838)
29. Hirata N, et al. 2001. Pretreatment of mice with clindamycin improves survival of endotoxic shock by modulating the release of inflammatory cytokines. Antimicrob. Agents Chemother. 45:2638-2642. (Pubitemid 32801924)
30. Joo HS, Chan JL, Cheung GY, Otto M. 2010. Subinhibitory concentrations of protein synthesis-inhibiting antibiotics promote increased expression of the agr virulence regulator and production of phenol-soluble modulin cytolysins in community-associated methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 54:4942-4944.
31. Kaplan SL, et al. 2005. Three-year surveillance of community-acquired Staphylococcus aureus infections in children. Clin. Infect. Dis. 40: 1785-1791. (Pubitemid 40799948)
32. Karlstrom A, Boyd KL, English BK, McCullers JA. 2009. Treatment with protein synthesis inhibitors improves outcomes of secondary bacterial pneumonia after influenza. J. Infect. Dis. 199:311-319.
33. Labandeira-Rey M, et al. 2007. Staphylococcus aureus Panton-Valentine leukocidin causes necrotizing pneumonia. Science 315:1130-1133. (Pubitemid 46328024)
34. LaPlante KL, Leonard SN, Andes DR, Craig WA, Rybak MJ. 2008. Activities of clindamycin, daptomycin, doxycycline, linezolid, trimethoprim- sulfamethoxazole, and vancomycin against community-associated methicillin-resistant Staphylococcus aureus with inducible clindamycin resistance in murine thigh infection and in vitro pharmacodynamic models. Antimicrob. Agents Chemother. 52:2156-2162. (Pubitemid 351758553)
35. Lewin CS, Amyes SG. 1991. The role of the SOS response in bacteria exposed to zidovudine or trimethoprim. J. Med. Microbiol. 34:329-332.
36. Li M, et al. 2010. Comparative analysis of virulence and toxin expression of global community-associated methicillin-resistant Staphylococcus aureus strains. J. Infect. Dis. 202:1866-1876.
37. Li M, et al. 2009. Evolution of virulence in epidemic community-associated methicillin-resistant Staphylococcus aureus. Proc. Natl. Acad. Sci. U. S. A. 106:5883-5888.
38. Liu C, et al. 2011. Clinical practice guidelines by the Infectious Diseases Society of America for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children. Clin. Infect. Dis. 52:e18-55.
39. Loffler B, et al. 2010. Staphylococcus aureus Panton-Valentine leukocidin is a very potent cytotoxic factor for human neutrophils. PLoS Pathog. 6:e1000715.
40. 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.
41. Maguire BA. 2009. Inhibition of bacterial ribosome assembly: a suitable drug target? Microbiol. Mol. Biol. Rev. 73:22-35.
42. McCormick JK, Yarwood JM, Schlievert PM. 2001. Toxic shock syndrome and bacterial superantigens: an update. Annu. Rev. Microbiol. 55: 77-104. (Pubitemid 32978101)
43. Miller LG, et al. 2005. Necrotizing fasciitis caused by community-associated methicillin-resistant Staphylococcus aureus in Los Angeles. N. Engl. J. Med. 352:1445-1453. (Pubitemid 40471452)
44. Montgomery CP, Daum RS. 2009. Transcription of inflammatory genes in the lung after infection with community-associated methicillin-resistant Staphylococcus aureus: a role for Panton-Valentine leukocidin? Infect. Immun. 77:2159-2167.
45. Pantrangi M, Singh VK, Wolz C, Shukla SK. 2010. Staphylococcal superantigen-like genes, ssl5 and ssl8, are positively regulated by sae and negatively by agr in the Newman strain. FEMS Microbiol. Lett. 308: 175-184.
46. Perbet S, et al. 2010. Multifocal community-acquired necrotizing fasciitis caused by a Panton-Valentine leukocidin-producing methicillin- sensitive Staphylococcus aureus. Infection 38:223-225.
47. Plaisance KI, Drusano GL, Forrest A, Townsend RJ, Standiford HC. 1989. Pharmacokinetic evaluation of two dosage regimens of clindamycin phosphate. Antimicrob. Agents Chemother. 33:618-620. (Pubitemid 19119999)
48. Rose WE, Knier RM, Hutson PR. 2010. Pharmacodynamic effect of clinical vancomycin exposures on cell wall thickness in heterogeneous vancomycin-intermediate Staphylococcus aureus. J. Antimicrob. Chemother. 65:2149-2154.
49. Rybak M, et al. 2009. Therapeutic monitoring of vancomycin in adult patients: a consensus review of the American Society of Health-System Pharmacists, the Infectious Diseases Society of America, and the Society of Infectious Diseases Pharmacists. Am. J. Health Syst. Pharm. 66:82-98.
50. Sammons LR. 2010. In vitro regulation of the seq and sek staphylococcal enterotoxin genes among four allelic variants. M.S. thesis. University of Wisconsin- La Crosse, La Crosse, WI.
51. Schlievert PM, Case LC. 2007. Molecular analysis of staphylococcal superantigens. Methods Mol. Biol. 391:113-126. (Pubitemid 350190020)
52. Shukla SK, et al. 2010. Virulence genes and genotypic associations in nasal carriage, community-associated methicillin-susceptible and methicillin-resistant USA400 Staphylococcus aureus isolates. J. Clin. Microbiol. 48:3582-3592.
53. Stevens DL, et al. 2007. Impact of antibiotics on expression of virulence-associated exotoxin genes in methicillin-sensitive and methicillin-resistant Staphylococcus aureus. J. Infect. Dis. 195:202-211. (Pubitemid 46080052)
54. Varoquaux O, et al. 1985. Pharmacokinetics of the trimethoprimsulphamethoxazole combination in the elderly. Br. J. Clin. Pharmacol. 20:575-581.
55. Voyich JM, et al. 2006. Is Panton-Valentine leukocidin the major virulence determinant in community-associated methicillin-resistant Staphylococcus aureus disease? J. Infect. Dis. 194:1761-1770. (Pubitemid 44902009)
56. Welling PG, Shaw WR, Uman SJ, Tse FL, Craig WA. 1975. Pharmacokinetics of minocycline in renal failure. Antimicrob. Agents Chemother. 8:532-537.
57. Yanagihara K, et al. 2009. Efficacy of linezolid against Panton-Valentine leukocidin (PVL)-positive methicillin-resistant Staphylococcus aureus (MRSA) in a mouse model of haematogenous pulmonary infection. Int. J. Antimicrob. Agents. 34:477-481.