Fitness of Streptococcus pneumoniae fluoroquinolone-resistant strains with topoisomerase IV recombinant genes

Antimicrobial Agents and Chemotherapy

Volumn 52, Issue 3, 2008, Pages 822-830

  Balsalobre, Luz ^a   De La Campa, Adela G ^a  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING) A; DNA TOPOISOMERASE IV; LEVOFLOXACIN; PROTEIN PARC; PROTEIN PARE; QUINOLONE DERIVATIVE; SPARFLOXACIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATE; BACTERIUM TRANSFORMATION; FITNESS; GENETIC TRANSCRIPTION; MUTANT; NONHUMAN; POINT MUTATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STREPTOCOCCUS MITIS; STREPTOCOCCUS PNEUMONIAE;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BASE SEQUENCE; CIPROFLOXACIN; DNA TOPOISOMERASE IV; DRUG RESISTANCE, BACTERIAL; FLUOROQUINOLONES; HUMANS; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; MUTATION; RECOMBINATION, GENETIC; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTION, GENETIC;

EID: 40549112302     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.00731-07     Document Type: Article

References (46)

1. Andersson, D. I., and B. R. Levin. 1999. The biological cost of antibiotic resistance. Curr. Opin. Microbiol. 2:489-493.
2. Balas, D., E. Fernández-Moreira, and A. G. de la Campa. 1998. Molecular characterization of the gene encoding the DNA gyrase A subunit of Streptococcus pneumoniae. J. Bacteriol. 180:2854-2861.
3. Balsalobre, L., M. J. Ferrándiz, J. Liñares, F. Tubau, and A. G. de la Campa. 2003. Viridans group streptococci are donors in horizontal transfer of topoisomerase IV genes to Streptococcus pneumoniae. Antimicrob. Agents Chemother. 47:2072-2081.
4. Barnard, F. M., and A. Maxwell. 2001. Interaction between DNA gyrase and quinolones: effects of alanine mutations at GyrA subunit residues Ser83 and Asp87. Antimicrob. Agents Chemother. 45:1994-2000.
5. Bast, D. J., J. C. de Azevedo, T. Y. Tam, L. Kilburn, C. Duncan, L. A. Mandell, R. J. Davidson, and D. E. Low. 2001. Interspecies recombination contributes minimally to fluoroquinolone resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 45:2631-2634.
6. Bjorkholm, B., A. Lundin, A. Sillen, K. Guillemin, N. Salama, C. Rubio, J. I. Gordon, P. Falk, and L. Engstrand. 2001. Comparison of genetic divergence and fitness between two subclones of Helicobacter pylori. Infect. Immun. 69:7832-7838.
7. Bjorkman, J., D. Hughes, and D. I. Andersson. 1998. Virulence of antibiotic-resistant Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 95:3949-3953.
8. Chen, D. K., A. McGeer, J. C. de Azavedo, and D. E. Low. 1999. Decreased susceptibility of Streptococcus pneumoniae to fluoroquinolones in Canada. N. Engl. J. Med. 341:233-239.
9. Davidson, R., R. Cavalcanti, J. L. Brunton, D. J. Bast, J. C. de Azevedo, P. Kibsey, C. Fleming, and D. E. Low. 2002. Resistance to levofloxacin and failure of treatment of pneumococcal pneumonia. N. Engl. J. Med. 346:747-750.
10. de Azevedo, J. C., L. Trpeski, S. Pong-Porter, S. Matsumura, and D. E. Low. 1999. In vitro activity of fluoroquinolones against antibiotic-resistant blood culture isolates of viridans group streptococci across Canada. Antimicrob. Agents Chemother. 43:2299-2301.
11. de la Campa, A. G., L. Balsalobre, C. Ardanuy, A. Fenoll, E. Pérez-Trallero, and J. Liñares. 2004. Fluoroquinolone resistance in penicillin-resistant Streptococcus pneumoniae clones, Spain. Emerg. Infect. Dis. 10:1751-1759.
12. de la Campa, A. G., M. J. Ferrándiz, F. Tubau, R. Pallarés, F. Manresa, and J. Liñares. 2003. Genetic characterization of fluoroquinolone-resistant Streptococcus pneumoniae strains isolated during ciprofloxacin therapy from a patient with bronchiectasis. Antimicrob. Agents Chemother. 47:1419-1422.
13. Doern, G. V., K. P. Heilmann, H. K. Huynh, P. R. Rhomberg, S. L. Coffman, and A. B. Brueggemann. 2001. Antimicrobial resistance among clinical isolates of Streptococcus pneumoniae in the United States during 1999-2000, including a comparison of resistance rates since 1994-1995. Antimicrob. Agents Chemother. 45:1721-1729.
14. Ender, M., N. McCallum, R. Adhikari, and B. Berger-Bachi. 2004. Fitness cost of SCCmec and methicillin resistance levels in Staphylococcus aureus. Antimicrob. Agents Chemother. 48:2295-2297.
15. Fernández-Moreira, E., D. Balas, I. González, and A. G. de la Campa. 2000. Fluoroquinolones inhibit preferentially Streptococcus pneumoniae DNA topoisomerase IV than DNA gyrase native proteins. Microb. Drug Resist. 6:259-267.
16. Ferrándiz, M. J., A. Fenoll, J. Linares, and A. G. de la Campa. 2000. Horizontal transfer of parC and gyrA in fluoroquinolone-resistant clinical isolates of Streptococcus pneumoniae. Antimicrob. Agents Chemother. 44:840-847.
17. Gagneux, S., C. D. Long, P. M. Small, T. Van, G. K. Schoolnik, and B. J. Bohannan. 2006. The competitive cost of antibiotic resistance in Mycobacterium tuberculosis. Science 312:1944-1946.
18. Gillespie, S. H., L. L. Voelker, J. E. Ambler, C. Traini, and A. Dickens. 2003. Fluoroquinolone resistance in Streptococcus pneumoniae: evidence that gyrA mutations arise at a lower rate and that mutation in gyrA or parC predisposes to further mutation. Microb. Drug Resist. 9:17-24.
19. González, I., M. Georgiou, F. Alcaide, D. Balas, J. Liñares, and A. G. de la Campa. 1998. Fluoroquinolone resistance mutations in the parC, parE, and gyrA genes of clinical isolates of viridans group streptococci. Antimicrob. Agents Chemother. 42:2792-2798.
20. Houssaye, S., L. Gutmann, and E. Varon. 2002. Topoisomerase mutations associated with in vitro selection of resistance to moxifloxacin in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 46:2712-2715.
21. Jacobs, M. R., D. Felmingham, P. C. Appelbaum, R. N. Grüneberg, and the Alexander Project Group. 2003. The Alexander project 1998-2000: susceptibility of pathogens isolated from community-acquired respiratory tract infection to commonly used antimicrobial agents. J. Antimicrob. Chemother. 52:229-246.
22. Janoir, C., I. Podglajen, M. D. Kitzis, C. Poyart, and L. Gutmann. 1999. In vitro exchange of fluoroquinolone resistance determinants between Streptococcus pneumoniae and viridans streptococci and genomic organization of the parE-parC region in S. mitis. J. Infect. Dis. 180:555-558.
23. Janoir, C., V. Zeller, M.-D. Kitzis, N. J. Moreau, and L. Gutmann. 1996. High-level fluoroquinolone resistance in Streptococcus pneumoniae requires mutations in parC and gyrA. Antimicrob. Agents Chemother. 40:2760-2764.
24. Johnson, C. N., D. E. Briles, W. H. Benjamin, Jr., S. K. Hollingshead, and K. B. Waites. 2005. Relative fitness of fluoroquinolone-resistant Streptococcus pneumoniae. Emerg. Infect. Dis. 11:814-820.
25. Kusuma, C., A. Jadanova, T. Chanturiya, and J. F. Kokai-Kun. 2007. Lysostaphin-resistant variants of Staphylococcus aureus demonstrate reduced fitness in vitro and in vivo. Antimicrob. Agents Chemother. 51:475-482.
26. Lacks, S. A. 1966. Integration efficiency and genetic recombination in pneumococcal transformation. Genetics 53:207-235.
27. Liñares, J., A. G. de la Campa, and R. Pallarés. 1999. Fluoroquinolone resistance in Streptococcus pneumoniae. N. Engl. J. Med. 341:1546-1547.
28. Luo, N., S. Pereira, O. Sahin, J. Lin, S. Huang, L. Michel, and Q. Zhang. 2005. Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacter jejuni in the absence of antibiotic selection pressure. Proc. Natl. Acad. Sci. USA 102:541-546.
29. Maisnier-Patin, S., and D. I. Andersson. 2004. Adaptation to the deleterious effects of antimicrobial drug resistance mutations by compensatory evolution. Res. Microbiol. 155:360-369.
30. Mandell, L. A., R. G. Wunderink, A. Anzueto, J. G. Bartlett, G. D. Campbell, N. C. Dean, S. F. Dowell, T. M. File, Jr., D. M. Musher, M. S. Niederman, A. Torres, and C. G. Whitney. 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-S72.
31. Martín-Galiano, A. J., and A. G. de la Campa. 2003. High-efficiency generation of antibiotic-resistant strains of Streptococcus pneumoniae by PCR and transformation. Antimicrob. Agents Chemother. 47:1257-1261.
32. Morais Cabral, J. H., A. P. Jackson, C. V. Smith, N. Shikotra, A. Maxwell, and R. C. Liddington. 1997. Crystal structure of the breakage-reunion domain of DNA gyrase. Nature 388:903-906.
33. Muñoz, R., and A. G. de la Campa. 1996. ParC subunit of DNA topoisomerase IV of Streptococcus pneumoniae is a primary target of fluoroquinolones and cooperates with DNA gyrase A subunit in forming resistance phenotype. Antimicrob. Agents Chemother. 40:2252-2257.
34. Nollmann, M., M. D. Stone, Z. Bryant, J. Gore, N. J. Crisona, S. C. Hong, S. Mitelheiser, A. Maxwell, C. Bustamante, and N. R. Cozzarelli. 2007. Multiple modes of Escherichia coli DNA gyrase activity revealed by force and torque. Nat. Struct. Mol. Biol. 14:264-271.
35. Pan, X.-S., J. Ambler, S. Mehtar, and L. M. Fisher. 1996. Involvement of topoisomerase IV and DNA gyrase as ciprofloxacin targets in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 40:2321-2326.
36. Pan, X.-S., and L. M. Fisher. 1996. Cloning and characterization of the parC and parE genes of Streptococcus pneumoniae encoding DNA topoisomerase IV: role in fluoroquinolone resistance. J. Bacteriol. 178:4060-4069.
37. Pérez-Trallero, E., J. M. García-Arenzana, J. A. Jímenez, and A. Peris. 1990. Therapeutic failure and selection of resistance to quinolones in a case of pneumococcal pneumonia treated with ciprofloxacin. Eur. J. Clin. Microbiol. Infect. Dis. 9:905-906.
38. Pérez-Trallero, E., J. M. Marimón, L. Iglesias, and J. Larruskain. 2003. Fluoroquinolone and macrolide treatment failure in pneumococcal pneumonia and selection of multidrug-resistant isolates. Emerg. Infect. Dis. 9:1159-1162.
39. Rozen, D. E., L. McGee, B. R. Levin, and K. P. Klugman. 2007. Fitness costs of fluoroquinolone resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 51:412-416.
40. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Schmitz, F. J., A. Fisher, M. Boos, S. Mayer, D. Milatovic, and A. C. Fluit. 2001. Quinolone-resistance mechanisms and in vitro susceptibility patterns among European isolates of Streptococcus mitis, Streptococcus sanguis, and Streptococcus pneumoniae. Eur. J. Clin. Microbiol. Infect. Dis. 20:219-222.
42. Stanhope, M. J., S. L. Walsh, J. A. Becker, M. J. Italia, K. A. Ingraham, M. N. Gwynn, T. Mathie, J. A. Poupard, L. A. Miller, J. R. Brown, and H. Amrine-Madsen. 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.
43. Tankovic, J., B. Perichon, J. Duval, and P. Courvalin. 1996. Contribution of mutations in gyrA and parC genes to fluoroquinolone resistance of mutants of Streptococcus pneumoniae obtained in vivo and in vitro. Antimicrob. Agents Chemother. 40:2505-2510.
44. Urban, C., N. Rahman, X. Zhao, N. Mariano, S. A. Segal-maurer, K. Drlica, and J. J. Rahal. 2001. Fluoroquinolone-resistant Streptococcus pneumoniae associated with levofloxacin therapy. J. Infect. Dis. 184:794-798.
45. Varon, E., C. Janoir, M.-D. Kitzis, and L. Gutmann. 1999. ParC and GyrA may be interchangeable initial targets of some fluoroquinolones in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 43:302-306.
46. Yokota, S., K. Sato, O. Kuwahara, S. Habadera, N. Tsukamoto, H. Ohuchi, H. Akizawa, T. Himi, and N. Fujii. 2002. Fluoroquinolone-resistant Streptococcus pneumoniae occurs frequently in elderly patients in Japan. Antimicrob. Agents Chemother. 46:3311-3315.