Antibiotic pressure compensates the biological cost associated with Pseudomonas aeruginosa hypermutable phenotypes in vitro and in a murine model of chronic airways infection

Journal of Antimicrobial Chemotherapy

Volumn 67, Issue 4, 2012, Pages 962-969

  Alcalá Franco, Beatriz ^a   Montanari, Sara ^a   Cigana, Cristina ^a   Bertoni, Giovanni ^b   Oliver, Antonio ^c   Bragonzi, Alessandra ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c HOSPITAL UNIVERSITARIO SON ESPASES   (Spain)

Author keywords

Chronic airway infection; Cystic fibrosis; Hypermutators; Mouse model; P. aeruginosa

Indexed keywords

CIPROFLOXACIN; STREPTOMYCIN;

ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL STRAIN; CYSTIC FIBROSIS; DISEASE COURSE; GENOTYPE; HISTOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PATHOGENICITY; PHENOTYPE; PSEUDOMONAS AERUGINOSA; RESPIRATORY TRACT INFECTION; WILD TYPE;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL LOAD; CHRONIC DISEASE; CYSTIC FIBROSIS; DRUG RESISTANCE, BACTERIAL; HUMANS; LUNG; MALE; MICE; MICE, INBRED C57BL; MUTATION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RESPIRATORY TRACT INFECTIONS; SURVIVAL ANALYSIS;

EID: 84858673034     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkr587     Document Type: Article

References (34)

1. Strausbaugh S, Davis PB. Cystic fibrosis: a review of epidemiology and pathobiology. Clin Chest Med 2007; 28: 279-88.
2. Doring G, Hoiby N. Consensus Study Group. Early intervention and prevention of lung disease in cystic fibrosis: a European consensus. J Cyst Fibros 2004; 3: 67-91.
3. Arnold D, Jackson RW, Waterfield NR et al. Evolution of microbial virulence: the benefits of stress. Trends Genet 2007; 23: 293-300.
4. Bragonzi A, Paroni M, Nonis A et al. Pseudomonas aeruginosa microevolution during cystic fibrosis lung infection establishes clones with adapted virulence. Am J Respir Crit Care Med 2009; 180: 138-45.
5. Martinez J, Baquero F. Mutation frequencies and antibiotic resistance. Antimicrob Agents Chemother 2000; 44: 1771-7.
6. Livermore D. Multiple mechanisms of antimicrobial resistance in Pseudomonas aeruginosa: our worst nightmare? Clin Infect Dis 2002; 34: 634-40.
7. Sundin G, Weigand MR. The microbiology of mutability. FEMS Microbiol Lett 2007; 277: 11-20.
8. Giraud A, Matic I, Radman M et al. Mutator bacteria as a risk factor in treatment of infectious diseases. Antimicrob Agents Chemother 2002; 46: 863-5.
9. Oliver A, Cantón R, Campo P et al. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 2000; 288: 1251-4.
10. Ciofu O, Fussing V, Bagge N et al. Characterization of paired mucoid/non-mucoid Pseudomonas aeruginosa isolates from Danish cystic fibrosis patients: antibiotic resistance, β-lactamase activity and RiboPrinting. J Antimicrob Chemother 2001; 48: 391-6.
11. Maciá M, Blanquer D, Togores B et al. Hypermutation is a key factor in development of multiple-antimicrobial resistance in Pseudomonas aeruginosa strains causing chronic lung infections. Antimicrob Agents Chemother 2005; 49: 3382-6.
12. Mena A, Smith EE, Burns JL et al. Genetic adaptation of Pseudomonas aeruginosa to the airways of cystic fibrosis patients is catalyzed by hypermutation. J Bacteriol 2008; 190: 7910-7.
13. Montanari S, Oliver A, Salerno P et al. Biological cost of hypermutation in Pseudomonas aeruginosa strains from patients with cystic fibrosis. Microbiology 2007; 153: 1445-54.
14. Kenna D, Doherty CJ, Foweraker J et al. Hypermutability in environmental Pseudomonas aeruginosa and in populations causing pulmonary infection in individuals with cystic fibrosis. Microbiology 2007; 153: 1852-9.
15. Waine D, Honeybourne D, Smith EG et al. Association between hypermutator phenotype, clinical variables, mucoid phenotype, and antimicrobial resistance in Pseudomonas aeruginosa. J Clin Microbiol 2008; 46: 3491-3.
16. Ferroni A, Guillemot D, Moumile K et al. Effect of mutator P. aeruginosa on antibiotic resistance acquisition and respiratory function in cystic fibrosis. Pediatr Pulmonol 2009; 44: 820-5.
17. Bragonzi A, Wiehlmann L, Klockgether J et al. Sequence diversity of the mucABD locus in Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Microbiology 2006; 152: 3261-9.
18. Stover CK, Pham XQ, Erwin AL et al. Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 2000; 406: 959-64.
19. Oliver A, Levin BR, Juan C et al. Hypermutation and the preexistence of antibiotic-resistant Pseudomonas aeruginosa mutants: implications for susceptibility testing and treatment of chronic infections. Antimicrob Agents Chemother 2004; 48: 4226-33.
20. Hava D, Camilli A. Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol Microbiol 2002; 45: 1389-406.
21. Cash H, Woods DE, McCullough B et al. A rat model of chronic respiratory infection with Pseudomonas aeruginosa. Am Rev Respir Dis 1979; 119: 453-9.
22. Bragonzi A, Worlitzsch D, Pier GB et al. Nonmucoid Pseudomonas aeruginosa expresses alginate in the lungs of patients with cystic fibrosis and in a mouse model. J Infect Dis 2005; 192: 410-9.
23. Pier G, Meluleni G, Neuger E. A murine model of chronic mucosal colonization by Pseudomonas aeruginosa. Infect Immun1992;60: 4768-76.
24. Maciá M, Borrell N, Segura M et al. Efficacy and potential for resistance selection of antipseudomonal treatments in a mouse model of lung infection by hypermutable Pseudomonas aeruginosa. Antimicrob Agents Chemother 2006; 50: 975-83.
25. Bianconi I, Milani A, Paroni M et al. Positive signature-tagged mutagenesis in Pseudomonas aeruginosa: tracking patho-adaptive mutations promoting long-term airways chronic infection. PLoS Pathogen 2011; 7: e1001270.
26. Maciá M, Borrell N, Pérez JL et al. Detection and susceptibility testing of hypermutable Pseudomonas aeruginosa strains with the Etest and disk diffusion. Antimicrob Agents Chemother 2004; 48: 2665-72.
27. Smith EE, Buckley DG, Wu Z et al. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 2006; 30: 8487-92.
28. Mowat E, Paterson S, Fothergill JL et al. Pseudomonas aeruginosa population diversity and turnover in cystic fibrosis chronic infections. Am J Respir Crit Care Med 2011; 183: 1674-9.
29. Yang L, Jelsbak L, Marvig RL et al. Evolutionary dynamics of bacteria in a human host environment. Proc Natl Acad Sci USA 2011; 108: 7481-6.
30. Cramer N, Klockgether J, Wrasman K et al. Microevolution of the major common Pseudomonas aeruginosa clones C and PA14 in cystic fibrosis lungs. Environ Microbiol 2011; 13: 1690-704.
31. Mena A, Macià MD, Borrell N et al. Inactivation of the mismatch repair system in Pseudomonas aeruginosa attenuates virulence but favours persistence of oropharyngeal colonization in cystic fibrosis mice. J Bacteriol 2007; 189: 3665-8.
32. Plasencia V, Borrell N, Maciá MD et al. Influence of high mutation rates on the mechanisms and dynamics of in vitro and in vivo resistance development to single or combined antipseudomonal agents. Antimicrob Agents Chemother 2007; 51: 2574-81.
33. Wiehlmann L, Wagner G, Cramer N et al. Population structure of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 2007; 104: 8101-6.
34. Pandey R, Khuller GK. Nanoparticle-based oral drug delivery system for an injectable antibiotic-streptomycin. Evaluation in a murine tuberculosis model. Chemotherapy 2007; 53: 437-41.