Evidence for induction of integron-based antibiotic resistance by the SOS response in a clinical setting

PLoS Pathogens

Volumn 8, Issue 6, 2012, Pages

  Hocquet, Didier ^a,b   Llanes, Catherine ^b   Thouverez, Michelle ^c,d   Kulasekara, Hemantha D ^a   Bertrand, Xavier ^c,d   Plésiat, Patrick ^b   Mazel, Didier ^e   Miller, Samuel I ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITÉ DE FRANCHE COMTÉ   (France)

^c UNIVERSITY HOSPITAL OF BESANÇON   (France)

^d université Bourgogne Franche Comté   (France)

^e INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMOXICILLIN PLUS CLAVULANIC ACID; BETA LACTAM ANTIBIOTIC; BETA LACTAMASE; CEFEPIME; CEFTAZIDIME; CEPHALOSPORIN DERIVATIVE; EXTENDED SPECTRUM BETA LACTAMASE; GCUF1 OXA 28 FUSION PROTEIN; HYBRID PROTEIN; IMIPENEM; INTEGRASE; METRONIDAZOLE; MITOMYCIN C; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT;

ADAPTATION; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIUM ISOLATE; BLA OXA 28 GENE; DNA REPAIR; ENZYME RELEASE; GCUF1 GENE; GENE CASSETTE; GENE INDUCTION; GENE INSERTION; GENE REARRANGEMENT; HOST; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INTEGRON; NONHUMAN; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; ADULT; BACTERIAL GENE; DRUG EFFECT; GENETICS; METABOLISM; MICROBIOLOGICAL EXAMINATION; PSEUDOMONAS INFECTION; PULSED FIELD GEL ELECTROPHORESIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

ADAPTATION, PHYSIOLOGICAL; ADULT; ANTI-BACTERIAL AGENTS; BETA-LACTAMASES; CEFTAZIDIME; DRUG RESISTANCE, MICROBIAL; ELECTROPHORESIS, GEL, PULSED-FIELD; GENES, BACTERIAL; HUMANS; INTEGRONS; METRONIDAZOLE; MICROBIAL SENSITIVITY TESTS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SOS RESPONSE (GENETICS);

EID: 84864075483     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002778     Document Type: Article

References (49)

1. Partridge SR, Tsafnat G, Coiera E, Iredell JR, (2009) Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev 33: 757-784.
2. Collis CM, Hall RM, (1992) Gene cassettes from the insert region of integrons are excised as covalently closed circles. Mol Microbiol 6: 2875-2885.
3. Cambray G, Guerout AM, Mazel D, (2010) Integrons. Annu Rev Genet 44: 141-166.
4. Jové T, Da Ré S, Denis F, Mazel D, Ploy MC, (2010) Inverse correlation between promoter strength and excision activity in class 1 integrons. PLoS Genet 6: e1000793.
5. Coyne S, Guigon G, Courvalin P, Périchon B, (2010) Screening and quantification of the expression of antibiotic resistance genes in Acinetobacter baumannii with a microarray. Antimicrob Agents Chemother 54: 333-340.
6. Jacquier H, Zaoui C, Sanson-le Pors M-J, Mazel D, Berçot B, (2009) Translation regulation of integrons gene cassette expression by the attC sites. Mol Microbiol 72: 1475-1486.
7. Erill I, Campoy S, Barbe J, (2007) Aeons of distress: an evolutionary perspective on the bacterial SOS response. FEMS Microbiol Rev 31: 637-656.
8. Guerin E, Cambray G, Sanchez-Alberola N, Campoy S, Erill I, et al. (2009) The SOS response controls integron recombination. Science 324: 1034.
9. Cambray G, Sanchez-Alberola N, Campoy S, Guerin E, Da Re S, et al. (2011) Prevalence of SOS-mediated control of integron integrase expression as an adaptive trait of chromosomal and mobile integrons. Mobile DNA 2: 6.
10. Baharoglu Z, Bikard D, Mazel D, (2010) Conjugative DNA transfer induces the bacterial SOS response and promotes antibiotic resistance development through integron activation. PLoS Genet 6: e1001165.
11. Baharoglu Z, Mazel D, (2011) Vibrio cholerae triggers SOS and mutagenesis in response to a wide range of antibiotics: a route towards multiresistance. Antimicrob Agents Chemother 55: 2438-2441.
12. Blazquez J, Gomez-Gomez JM, Oliver A, Juan C, Kapur V, et al. (2006) PBP3 inhibition elicits adaptive responses in Pseudomonas aeruginosa. Mol Microbiol 62: 84-99.
13. Miller C, Thomsen LE, Gaggero C, Mosseri R, Ingmer H, et al. (2004) SOS response induction by β-lactams and bacterial defense against antibiotic lethality. Science 305: 1629-1631.
14. Hocquet D, Dehecq B, Bertrand X, Plésiat P, (2011) A strain-tailored double-disc synergy test detects extended-spectrum oxacillinases in Pseudomonas aeruginosa. J Clin Microbiol 49: 2262-2265.
15. Hocquet D, Plésiat P, Dehecq B, Mariotte P, Talon D, et al. (2010) Nationwide investigation of extended-spectrum β-lactamases, metallo-β-lactamases, and extended-spectrum oxacillinases produced by ceftazidime-resistant Pseudomonas aeruginosa strains in France. Antimicrob Agents Chemother 54: 3512-3515.
16. Bert F, Branger C, Lambert-Zechovsky N, (2002) Identification of PSE and OXA β-lactamase genes in Pseudomonas aeruginosa using PCR-restriction fragment length polymorphism. J Antimicrob Chemother 50: 11-18.
17. Fluit AC, Schmitz FJ, (2004) Resistance integrons and super-integrons. Clin Microbiol Infect 10: 272-288.
18. Galimand M, Lambert T, Gerbaud G, Courvalin P, (1993) Characterization of the aac(6′)-Ib gene encoding an aminoglycoside 6′-N-acetyltransferase in Pseudomonas aeruginosa BM2656. Antimicrob Agents Chemother 37: 1456-1462.
19. Poirel L, Girlich D, Naas T, Nordmann P, (2001) OXA-28, an extended-spectrum variant of OXA-10 β-lactamase from Pseudomonas aeruginosa and its plasmid- and integron-located gene. Antimicrob Agents Chemother 45: 447-453.
20. Koshland D, Botstein D, (1980) Secretion of β-lactamase requires the carboxy end of the protein. Cell 20: 749-760.
21. O'Donnell SM, Janssen GR, (2001) The initiation codon affects ribosome binding and translational efficiency in Escherichia coli of cI mRNA with or without the 5′ untranslated leader. J Bacteriol 183: 1277-1283.
22. Shine J, Dalgarno L, (1974) The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci U S A 71: 1342-1346.
23. Salis HM, Mirsky EA, Voigt CA, (2009) Automated design of synthetic ribosome binding sites to control protein expression. Nat Biotechnol 27: 946-950.
24. Quillardet P, Hofnung M, (1993) The SOS chromotest: a review. Mutat Res 297: 235-279.
25. Guérin E, Jové T, Tabesse A, Mazel D, Ploy M-C, (2011) High-level Gene cassette transcription prevents integrase expression in class 1 integrons. J Bacteriol 193: 5675-5682.
26. Deana A, Belasco JG, (2005) Lost in translation: the influence of ribosomes on bacterial mRNA decay. Gene Dev 19: 2526-2533.
27. Kuhn A, (1987) Bacteriophage M13 procoat protein inserts into the plasma membrane as a loop structure. Science 238: 1413-1415.
28. Bouvier M, Ducos-Galand M, Loot C, Bikard D, Mazel D, (2009) Structural features of single-stranded integron cassette attC sites and their role in strand selection. PLoS Genet 5: e1000632.
29. Frumerie C, Ducos-Galand M, Gopaul DN, Mazel D, (2010) The relaxed requirements of the integron cleavage site allow predictable changes in integron target specificity. Nucleic Acids Res 38: 559-569.
30. Cipriano Souza R, Vicente AC, Vieira VV, Marques SG, Soares MdGA, et al. (2008) Clindamycin and metronidazole as independent risk factors for nosocomial acquisition of multidrug-resistant Pseudomonas aeruginosa. J Hosp Infect 69: 402-403.
31. Löfmark S, Edlund C, Nord CE, (2010) Metronidazole is still the drug of choice for treatment of anaerobic infections. Clin Infect Dis 50: S16-S23.
32. Sisson G, Jeong J-Y, Goodwin A, Bryden L, Rossler N, et al. (2000) Metronidazole activation is mutagenic and causes DNA fragmentation in Helicobacter pylori and in Escherichia coli containing a cloned H. pylori rdxA+ (nitroreductase) gene. J Bacteriol 182: 5091-5096.
33. Tocher JH, Edwards DI, (1994) Evidence for the direct interaction of reduced metronidazole derivatives with DNA bases. Biochem Pharmacol 48: 1089-1094.
34. Menéndez D, Rojas E, Herrera LA, López MC, Sordo M, et al. (2001) DNA breakage due to metronidazole treatment. Mutat Res 478: 153-158.
35. Livermore DM, (2002) Multiple mechanisms of antimicrobial resistance in Pseudomonas aeruginosa: our worst nightmare? Clin Infect Dis 34: 634-640.
36. Depardieu F, Podglajen I, Leclercq R, Collatz E, Courvalin P, (2007) Modes and modulations of antibiotic resistance gene expression. Clin Microbiol Rev 20: 79-114.
37. Foucault ML, Depardieu F, Courvalin P, Grillot-Courvalin C, (2010) Inducible expression eliminates the fitness cost of vancomycin resistance in enterococci. Proc Natl Acad Sci U S A 107: 16964-16969.
38. Andersson DI, Hughes D, (2010) Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Microbiol 8: 260-271.
39. Lu TK, Collins JJ, (2009) Engineered bacteriophage targeting gene networks as adjuvants for antibiotic therapy. Proc Natl Acad Sci U S A 106: 4629-4634.
40. Cirz RT, Chin JK, Andes DR, de Crécy-Lagard V, Craig WA, et al. (2005) Inhibition of mutation and combating the evolution of antibiotic resistance. PLoS Biol 3: e176.
41. Cline DJ, Holt SL, Singleton SF, (2007) Inhibition of Escherichia coli RecA by rationally redesigned N-terminal helix. Org Biomolec Chem 5: 1525-1528.
42. Sexton JZ, Wigle TJ, He Q, Hughes MA, Smith GR, et al. (2010) Novel inhibitors of Escherichia coli RecA ATPase activity. Curr Chem Genomics 4: 34-42.
43. Wigle TJ, Sexton JZ, Gromova AV, Hadimani MB, Hughes MA, et al. (2009) Inhibitors of RecA activity discovered by high-throughput screening: cell-permeable small molecules attenuate the SOS response in Escherichia coli. J Biomol Screen 14: 1092-1101.
44. Talon D, Cailleaux V, Thouverez M, Michel-Briand Y, (1996) Discriminatory power and usefulness of pulsed-field gel electrophoresis in epidemiological studies of Pseudomonas aeruginosa. J Hosp Infect 32: 135-145.
45. CLSI (2009) Method for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standard - eighth edition, CLSI document M7-A7.
46. Dumas J-L, van Delden C, Perron K, Köhler T, (2006) Analysis of antibiotic resistance gene expression in Pseudomonas aeruginosa by quantitative real-time-PCR. FEMS Microbiol Lett 254: 217-225.
47. Choi KH, Schweizer HP, (2005) An improved method for rapid generation of unmarked Pseudomonas aeruginosa deletion mutants. BMC Microbiol 5: 30.
48. Schweizer HP, (1992) Allelic exchange in Pseudomonas aeruginosa using novel ColE1-type vectors and a family of cassettes containing a portable oriT and the counter-selectable Bacillus subtilis sacB marker. Mol Microbiol 6: 1195-1204.
49. Dilger K, Fux R, Röck D, Mörike K, Gleiter CH, (2007) Effect of high-dose metronidazole on pharmacokinetics of oral budesonide and vice versa: a double drug interaction study. J Clin Pharmacol 47: 1532-1539.