Induction of prophages by fluoroquinolones in Streptococcus pneumoniae: Implications for emergence of resistance in genetically-related clones

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  López, Elena ^a,b   Domenech, Arnau ^b,c   Ferrándiz, María José ^a,b   Frias, Maria João ^d   Ardanuy, Carmen ^b,c   Ramirez, Mario ^d   García, Ernesto ^b,e   Liñares, Josefina ^b,c   De La Campa, Adela G ^a,b,f  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^d INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^e CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^f CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CIPROFLOXACIN; LEVOFLOXACIN; MITOMYCIN; NOVOBIOCIN; QUINOLINE DERIVED ANTIINFECTIVE AGENT; QUINOLONE DERIVATIVE;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIUM ISOLATE; CHRONIC RESPIRATORY TRACT DISEASE; CONTROLLED STUDY; CYTOLYSIS; HUMAN; LYSOGENIZATION; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR CLONING; NONHUMAN; POLYMERASE CHAIN REACTION; PROPHAGE; RETROSPECTIVE STUDY; SOUTHERN BLOTTING; STREPTOCOCCUS PNEUMONIAE; CHRONIC DISEASE; DISEASE COURSE; DRUG EFFECTS; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY; PNEUMOCOCCAL INFECTION; VIROLOGY; VIRUS ACTIVATION;

BLOTTING, SOUTHERN; CHRONIC DISEASE; CIPROFLOXACIN; DISEASE PROGRESSION; DRUG RESISTANCE, BACTERIAL; FLUOROQUINOLONES; HUMANS; LYSOGENY; MITOMYCIN; PNEUMOCOCCAL INFECTIONS; POLYMERASE CHAIN REACTION; PROPHAGES; STREPTOCOCCUS PNEUMONIAE; VIRUS ACTIVATION;

EID: 84899573516     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094358     Document Type: Article

References (32)

1. Austrian R (1981) Some observations on the pneumococcus and on the current status of pneumococcal disease and its prevention. Rev Infect Dis 3 Suppl: S1-17.
2. Jacobs MR, Felmingham D, Appelbaum PC, Grüneberg RN, the Alexander Project Group (2003) The Alexander project 1998-200: susceptibility of pathogens isolated from community-acquired respiratory tract infection to commonly used antimicrobial agents. J Antimicrob Chemother 52: 229-246. (Pubitemid 36986885)
3. McGee L, McDougal L, Zhou J, Spratt BG, Tenover FC, et al. (2001) Nomenclature of major antimicrobial-resistant clones of Streptococcus pneumoniae defined by the pneumococcal molecular epidemiology network. J Clin Microbiol 39: 2565-2571. (Pubitemid 32606233)
4. Mandell LA, Wunderink RG, Anzueto A, Bartlett JG, Campbell GD, et al. (2007) Infectious Diseases Society of America/American Thoracic Society consensus guidelines on the management of community-acquired pneumonia in adults. Clin Infect Dis 44 Suppl 2: S27-72. (Pubitemid 46290553)
5. de la Campa AG, Ardanuy C, Balsalobre L, Pérez-Trallero E, Marimón JM, et al. (2009) Changes in fluoroquinolone-resistant Streptococcus pneumoniae after 7-valent conjugate vaccination, Spain. Emerg Infect Dis 15: 905-911.
6. Domenech A, Ardanuy C, Calatayud L, Santos S, Tubau F, et al. (2011) Serotypes and genotypes of Streptococcus pneumoniae causing pneumonia and acute exacerbations in patients with chronic obstructive pulmonary disease. J Antimicrob Chemother 66: 487-493.
7. de la Campa AG, Balsalobre L, Ardanuy C, Fenoll A, Pérez-Trallero E, et al. (2004) Fluoroquinolone resistance in penicillin-resistant Streptococcus pneumoniae clones, Spain. Emerg Infect Dis 10: 1751-1759. (Pubitemid 39319365)
8. Drlica K, Malik M, Kerns RJ, Zhao X (2008) Quinolone-mediated bacterial death. Antimicrob Agents Chemother 52: 385-392. (Pubitemid 351170804)
9. Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130: 797-810. (Pubitemid 47332566)
10. Balsalobre L, Ortega M, de la Campa AG (2013) Characterization of recombinant fluoroquinolone-resistant pneumococcus-like isolates. Antimicrob Agents Chemother 57:254-260.
11. Balsalobre L, Ferrándiz MJ, Liñares J, Tubau F, de la Campa AG (2003) Viridans group streptococci are donors in horizontal transfer of topoisomerase IV genes to Streptococcus pneumoniae. Antimicrob Agents Chemother 47: 2072-2081. (Pubitemid 36753553)
12. Stanhope MJ, Walsh SL, Becker JA, Italia MJ, Ingraham KA, et al. (2005) Molecular evolution perspectives on intraspecific lateral DNA transfer of topoisomerase and gyrase loci in Streptococcus pneumoniae, with implications for fluoroquinolone resistance development and spread. Antimicrob Agents Chemother 49: 4315-4326. (Pubitemid 41400979)
13. Chen DK, McGeer A, de Azavedo JC, Low DE (1999) Decreased susceptibility of Streptococcus pneumoniae to fluoroquinolones in Canada. N Engl J Med 341: 233-239.
14. Balsalobre L, de la Campa AG (2008) Fitness of Streptococcus pneumoniae fluoroquinolone-resistant strains with topoisomerase IV recombinant genes. Antimicrob Agents Chemother 52: 822-830. (Pubitemid 351358358)
15. Rozen DE, McGee L, Levin BR, Klugman KP (2007) Fitness costs of fluoroquinolone resistance in Streptococcus pneumoniae. Antimicrob Agents Chemother 51: 412-416. (Pubitemid 46185254)
16. Balsalobre L, Ferrandiz MJ, de Alba G, de la Campa AG (2011) Nonoptimal DNA topoisomerases allow maintenance of supercoiling levels and improve fitness of Streptococcus pneumoniae. Antimicrob Agents Chemother 55: 1097-1105.
17. Ingrey KT RJ, Prescott JF (2003) A fluoroquinolone induces a novel mitogen-encoding bacteriophage in Streptococcus canis. Infect Immun 71: 3028-3033.
18. Cirz RT JM, Gingles NA, Minogue TD, Jarrahi B, Peterson SN, Romesberg FE (2007) Complete and SOS-mediated response of Staphylococcus aureus to the antibiotic ciprofloxacin. J Bacteriol 189: 531-539. (Pubitemid 46106385)
19. Selva L, Viana D, Regev-Yochay G, Trzcinski K, Corpa JM, et al. (2009) Killing niche competitors by remote-control bacteriophage induction. Proc Natl Acad Sci USA 106: 1234-1238.
20. Yasmin AKJ, Shankar J, Darby AC, Hall N, Edwards C, et al. (2010) Comparative genomics and transduction potential of Enterococcus faecalis temperate bacteriophages. J Bacteriol 192: 1122-1130.
21. Meessen-Pinard M, Sekulovic O, Fortier LC (2012) Evidence of in vivo prophage induction during Clostridium difficile infection. Appl Environ Microbiol 78: 7662-7670.
22. Bernheimer HP (1979) Lysogenic pneumococci and their bacteriophages. J Bacteriol 138: 618-624.
23. Ramirez M, Severina E, Tomasz A (1999) A high incidence of prophage carriage among natural isolates of Streptococcus pneumoniae. J Bacteriol 181: 3618-3625. (Pubitemid 29283786)
24. Romero P, García E, Mitchell TJ (2009) Development of a prophage typing system and analysis of prophage carriage in Streptococcus pneumoniae. Appl Environ Microbiol 75: 1642-1649.
25. Croucher NJ, Harris SR, Fraser C, Quail MA, Burton J, et al. (2011) Rapid pneumococcal evolution in response to clinical interventions. Science 331: 430-434.
26. Domenech A, Ardanuy C, Balsalobre L, Martí S, Calatayud L, et al. (2012) Pneumococci can persistently colonize adult patients with chronic respiratory disease. J Clin Microbiol 50: 4047-4053.
27. Frias MJ, Melo-Cristino J, Ramirez M (2009) The autolysin LytA contributes to efficient bacteriophage progeny release in Streptococcus pneumoniae. J Bacteriol 191: 5428-5440.
28. Ferrándiz MJ, de la Campa AG (2014) The fluoroquinolone levofloxacin triggers the transcriptional activation of iron transport genes that contribute to cell death in Streptococcus pneumoniae. Antimicrob Agents Chemother 58: 247-257.
29. Martin B, García P, Castanié MP, Claverys JP (1995) The recA gene of Streptococcus pneumoniae is part of a competence-induced operon and controls lysogenic induction. Mol Microbiol 15: 367-379.
30. Prudhomme M, Attaiech L, Sanchez G, Martin B, Claverys JP (2006) Antibiotic stress induces genetic transformability in the human pathogen Streptococcus pneumoniae. Science 313: 89-92. (Pubitemid 44051259)
31. Rodríguez-Valera F, Martín-Cuadrado AB, Rodríguez-Brito B, Pasic L, Thingstad TF, et al. (2009) Explaining microbial population genomics through phage predation. Nat Rev Microbiol 7: 828-836.
32. Wang X, Kim Y, Ma Q, Hong SH, Pokusaeva K, et al. (2010) Cryptic prophages help bacteria cope with adverse environments. Nat Commun 1: 147.