Impact of quinolone-resistance acquisition on biofilm production and fitness in Salmonella enterica

Journal of Antimicrobial Chemotherapy

Volumn 69, Issue 7, 2014, Pages 1815-1824

  Fàbrega, Anna ^a   Soto, Sara M ^a   Ballesté Delpierre, Clara ^a   Fernández Orth, Dietmar ^a   Jiménez de Anta, M Teresa ^a   Vila, Jordi ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

CsgB; Efflux; RamA; Rdar morphotype; Salmonella Typhimurium

Indexed keywords

CIPROFLOXACIN; ENVELOPE PROTEIN; NALIDIXIC ACID; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; QUINOLONE DERIVATIVE;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATION; BIOFILM; GENE MUTATION; IN VITRO STUDY; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; REGULATOR GENE; SALMONELLA TYPHIMURIUM; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETIC SELECTION; GROWTH, DEVELOPMENT AND AGING; HUMAN; ISOLATION AND PURIFICATION; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MUTATION; PHYSIOLOGY; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLOSIS; VIRUS CULTURE;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BIOFILMS; CIPROFLOXACIN; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION PROFILING; HUMANS; MICROBIAL SENSITIVITY TESTS; MUTATION; NALIDIXIC ACID; QUINOLONES; REAL-TIME POLYMERASE CHAIN REACTION; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SELECTION, GENETIC; SERIAL PASSAGE;

EID: 84902440133     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dku078     Document Type: Article

References (62)

1. Coburn B, Grassl GA, Finlay BB. Salmonella, the host and disease: a brief review. Immunol Cell Biol 2007; 85: 112-8.
2. Fabrega A, Vila J. Salmonella enterica serovar Typhimurium skills to succeed in the host: virulence and regulation. Clin Microbiol Rev 2013; 26: 308-41.
3. Hohmann EL. Nontyphoidal salmonellosis. Clin Infect Dis 2001; 32: 263-9.
4. Whichard JM, Gay K, Stevenson JE et al. Human Salmonella and concurrent decreased susceptibility to quinolones and extendedspectrum cephalosporins. Emerg Infect Dis 2007; 13: 1681-8.
5. BiedenbachDJ, TolemanM,Walsh TR et al. Analysis of Salmonella spp. with resistance to extended-spectrum cephalosporins and fluoroquinolones isolated in North America and Latin America: report from the SENTRY Antimicrobial Surveillance Program (1997-2004). Diagn Microbiol Infect Dis 2006; 54: 13-21.
6. Threlfall EJ, Fisher IS, Berghold C et al. Antimicrobial drug resistance in isolates of Salmonella enterica from cases of salmonellosis in humans in Europe in 2000: results of international multi-centre surveillance. Euro Surveill 2003; 8: 41-5.
7. Meakins S, Fisher IS, Berghold C et al. Antimicrobial drug resistance in human nontyphoidal Salmonella isolates in Europe 2000-2004: a report from the Enter-net International Surveillance Network. Microb Drug Resist 2008; 14: 31-5.
8. Cozzarelli NR. DNA gyrase and the supercoiling of DNA. Science 1980; 207: 953-60.
9. Kato J, Nishimura Y, Imamura R et al. New topoisomerase essential for chromosome segregation in E. coli. Cell 1990; 63: 393-404.
10. Fabrega A, Madurga S, Giralt E et al. Mechanism of action of and resistance to quinolones. Microb Biotechnol 2009; 2: 40-61.
11. Ruiz J, Pons MJ, Gomes C. Transferable mechanisms of quinolone resistance. Int J Antimicrob Agents 2012; 40: 196-203.
12. Baucheron S, Imberechts H, Chaslus-Dancla E et al. The AcrB multidrug transporter plays a major role in high-level fluoroquinolone resistance in Salmonella enterica serovar typhimurium phage type DT204. Microb Drug Resist 2002; 8: 281-9.
13. Chen S, Cui S, McDermott PF et al. Contribution of target gene mutations and efflux to decreased susceptibility of Salmonella enterica serovar Typhimurium to fluoroquinolones and other antimicrobials. Antimicrob Agents Chemother 2007; 51: 535-42.
14. Fabrega A, du Merle L, Le Bouguenec C et al. Repression of invasion genes and decreased invasion in a high-level fluoroquinolone-resistant Salmonella Typhimurium mutant. PLoS One 2009; 4: e8029.
15. Parry CM, Threlfall EJ. Antimicrobial resistance in typhoidal and nontyphoidal salmonellae. Curr Opin Infect Dis 2008; 21: 531-8.
16. Olliver A, Valle M, Chaslus-Dancla E et al. Role of an acrR mutation in multidrug resistance of in vitro-selected fluoroquinolone-resistant mutants of Salmonella enterica serovar Typhimurium. FEMS Microbiol Lett 2004; 238: 267-72.
17. Sulavik MC, Dazer M, Miller PF. The Salmonella typhimurium mar locus: molecular and genetic analyses and assessment of its role in virulence. J Bacteriol 1997; 179: 1857-66.
18. Pomposiello PJ, Demple B. Identification of SoxS-regulated genes in Salmonella enterica serovar Typhimurium. J Bacteriol 2000; 182: 23-9.
19. van der Straaten T, Janssen R, Mevius DJ et al. Salmonella gene rma (ramA) and multiple-drug-resistant Salmonella enterica serovar typhimurium. Antimicrob Agents Chemother 2004; 48: 2292-4.
20. Abouzeed YM, Baucheron S, Cloeckaert A. ramR mutations involved in efflux-mediated multidrug resistance in Salmonella enterica serovar Typhimurium. Antimicrob Agents Chemother 2008; 52: 2428-34.
21. Caldwell DE, Costerton JW. Are bacterial biofilms constrained to Darwin's concept of evolution through natural selection? Microbiologia 1996; 12: 347-58.
22. Majtan J, Majtanova L, Xu M et al. In vitro effect of subinhibitory concentrations of antibiotics on biofilm formation by clinical strains of Salmonella enterica serovar Typhimurium isolated in Slovakia. J Appl Microbiol 2008; 104: 1294-301.
23. Zogaj X, Nimtz M, Rohde M et al. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 2001; 39: 1452-63.
24. O'Toole G, Kaplan HB, Kolter R. Biofilm formation as microbial development. Annu Rev Microbiol 2000; 54: 49-79.
25. Austin JW, Sanders G, Kay WW et al. Thin aggregative fimbriae enhance Salmonella enteritidis biofilm formation. FEMS Microbiol Lett 1998; 162: 295-301.
26. Solano C, Garcia B, Valle J et al. Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol Microbiol 2002; 43: 793-808.
27. Romling U, Bian Z, Hammar M et al. Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 1998; 180: 722-31.
28. Wang YP, Li L, Shen JZ et al. Quinolone-resistance in Salmonella is associated with decreased mRNA expression of virulence genes invA and avrA, growth and intracellular invasion and survival. Vet Microbiol 2009; 133: 328-34.
29. O'Regan E, Quinn T, Frye JG et al. Fitness costs and stability of a high-level ciprofloxacin resistance phenotype in Salmonella enterica serotype Enteritidis: reduced infectivity associated with decreased expression of Salmonella pathogenicity island 1 genes. Antimicrob Agents Chemother 2010; 54: 367-74.
30. Soto SM, Smithson A, Martinez JA et al. Biofilm formation in uropathogenic Escherichia coli strains: relationship with prostatitis, urovirulence factors and antimicrobial resistance.J Urol 2007; 177: 365-8.
31. Rodriguez-Bano J, Marti S, Soto S et al. Biofilm formation in Acinetobacter baumannii: associated features and clinical implications. Clin Microbiol Infect 2008; 14: 276-8.
32. Baugh S, Ekanayaka AS, Piddock LJV et al. Loss of or inhibition of all multidrug resistance efflux pumps of Salmonella enterica serovar Typhimurium results in impaired ability to form a biofilm. J Antimicrob Chemother 2012; 67: 2409-17.
33. Da Re S, Ghigo JM. A CsgD-independent pathway for cellulose production and biofilm formation in Escherichia coli. J Bacteriol 2006; 188: 3073-87.
34. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing: Twenty-third Informational Supplement M100-S23. CLSI, Wayne, PA, USA, 2013.
35. Balleste-Delpierre C, Sole M, Domenech O et al. Molecular study of quinolone resistance mechanisms and clonal relationship of Salmonella enterica clinical isolates. Int J Antimicrob Agents 2013; 43: 121-5.
36. Mortimer PG, Piddock LJV. A comparison of methods used for measuring the accumulation of quinolones by Enterobacteriaceae, Pseudomonas aeruginosa and Staphylococcus aureus. J Antimicrob Chemother 1991; 28: 639-53.
37. Giraud E, Cloeckaert A, Kerboeuf D et al. Evidence for active efflux as the primary mechanism of resistance to ciprofloxacin in Salmonella enterica serovar Typhimurium. Antimicrob Agents Chemother 2000; 44: 1223-8.
38. Piddock LJV, White DG, Gensberg K et al. Evidence for an efflux pump mediating multiple antibiotic resistance in Salmonella enterica serovar Typhimurium. Antimicrob Agents Chemother 2000; 44: 3118-21.
39. Koutsolioutsou A, Martins EA, White DG et al. A soxRS-constitutive mutation contributing to antibiotic resistance in a clinical isolate of Salmonella enterica (serovar Typhimurium). Antimicrob Agents Chemother 2001; 45: 38-43.
40. Ariza RR, Cohen SP, Bachhawat N et al. Repressor mutations in the marRAB operon that activate oxidative stress genes and multiple antibiotic resistance in Escherichia coli. J Bacteriol 1994; 176: 143-8.
41. Zheng J, Cui S, Meng J. Effect of transcriptional activators RamA and SoxS on expression of multidrug efflux pumps AcrAB and AcrEF in fluoroquinolone-resistant Salmonella Typhimurium. J Antimicrob Chemother 2009; 63: 95-102.
42. Jellen-Ritter AS, Kern WV. Enhanced expression of the multidrug efflux pumps AcrAB and AcrEF associated with insertion element transposition in Escherichia coli mutants selected with a fluoroquinolone. Antimicrob Agents Chemother 2001; 45: 1467-72.
43. Kobayashi K, Tsukagoshi N, Aono R. Suppression of hypersensitivity of Escherichia coli acrB mutant to organic solvents by integrational activation of the acrEF operon with the IS1 or IS2 element. J Bacteriol 2001; 183: 2646-53.
44. Olliver A, Valle M, Chaslus-Dancla E et al. Overexpression of the multidrug efflux operon acrEF by insertional activation with IS1 or IS10 elements in Salmonella enterica serovar Typhimurium DT204 acrB mutants selected with fluoroquinolones. Antimicrob Agents Chemother 2005; 49: 289-301.
45. Latasa C, Roux A, Toledo-Arana A et al. BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol Microbiol 2005; 58: 1322-39.
46. Romling U, Rohde M, Olsen A et al. AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol 2000; 36: 10-23.
47. Giraud E, Brisabois A, Martel JL et al. Comparative studies of mutations in animal isolates and experimental in vitro-and in vivo-selected mutants of Salmonella spp. suggest a counterselection of highly fluoroquinoloneresistant strains in the field. Antimicrob Agents Chemother 1999; 43: 2131-7.
48. Hirose K, Hashimoto A, Tamura K et al. DNA sequence analysis of DNA gyrase and DNA topoisomerase IV quinolone resistance-determining regions of Salmonella enterica serovar Typhi and serovar Paratyphi A. Antimicrob Agents Chemother 2002; 46: 3249-52.
49. Hakanen A, Kotilainen P, Jalava J et al. Detection of decreased fluoroquinolone susceptibility in salmonellas and validation of nalidixic acid screening test. J Clin Microbiol 1999; 37: 3572-7.
50. Eaves DJ, Randall L, Gray DT et al. Prevalence of mutations within the quinolone resistance-determining region of gyrA, gyrB, parC, and parE and association with antibiotic resistance in quinolone-resistant Salmonella enterica. Antimicrob Agents Chemother 2004; 48: 4012-5.
51. Baucheron S, Chaslus-Dancla E, Cloeckaert A et al. High-level resistance to fluoroquinolones linked to mutations in gyrA, parC, and parE in Salmonella enterica serovar Schwarzengrund isolates from humans in Taiwan. Antimicrob Agents Chemother 2005; 49: 862-3.
52. Baucheron S, Tyler S, Boyd D et al. AcrAB-TolC directs efflux-mediated multidrug resistance in Salmonella enterica serovar typhimurium DT104. Antimicrob Agents Chemother 2004; 48: 3729-35.
53. Yang S, Clayton SR, Zechiedrich EL. Relative contributions of the AcrAB, MdfA and NorE efflux pumps to quinolone resistance in Escherichia coli. J Antimicrob Chemother 2003; 51: 545-56.
54. Ricci V, Tzakas P, Buckley A et al. Ciprofloxacin-resistant Salmonella enterica serovar Typhimurium strains are difficult to select in the absence of AcrB and TolC. Antimicrob Agents Chemother 2006; 50: 38-42.
55. Giraud E, Cloeckaert A, Baucheron S et al. Fitness cost of fluoroquinolone resistance in Salmonella enterica serovar Typhimurium. J Med Microbiol 2003; 52: 697-703.
56. Marcusson LL, Frimodt-Moller N, Hughes D. Interplay in the selection of fluoroquinolone resistance and bacterial fitness. PLoS Pathog 2009; 5: e1000541.
57. Soto SM, Jimenez de Anta MT, Vila J. Quinolones induce partial or total loss of pathogenicity islands in uropathogenic Escherichia coli by SOS-dependent or-independent pathways, respectively. Antimicrob Agents Chemother 2006; 50: 649-53.
58. Buckley AM,Webber MA, Cooles S et al. The AcrAB-TolC efflux system of Salmonella enterica serovar Typhimuriumplays a role in pathogenesis. Cell Microbiol 2006; 8: 847-56.
59. Virlogeux-Payant I, Baucheron S, Pelet J et al. TolC, but not AcrB, is involved in the invasiveness of multidrug-resistant Salmonella enterica serovar Typhimurium by increasing type III secretion system-1 expression. Int J Med Microbiol 2008; 298: 561-9.
60. Baucheron S, Mouline C, Praud K et al. TolC but not AcrB is essential for multidrug-resistant Salmonella enterica serotype Typhimurium colonization of chicks. J Antimicrob Chemother 2005; 55: 707-12.
61. Bailey AM, Ivens A, Kingsley R et al. RamA, a member of the AraC/XylS family, influences both virulence and efflux in Salmonella enterica serovar Typhimurium. J Bacteriol 2010; 192: 1607-16.
62. Spengler G, Rodrigues L, Martins A et al. Genetic response of Salmonella enterica serotype Enteritidis to thioridazine rendering the organism resistant to the agent. Int J Antimicrob Agents 2012; 39: 16-21.