Involvement of the putative ATP-dependent efflux proteins PatA and PatB in fluoroquinolone resistance of a multidrug-resistant mutant of Streptococcus pneumoniae

Antimicrobial Agents and Chemotherapy

Volumn 50, Issue 2, 2006, Pages 685-693

  Marrer, Estelle ^a,b,d   Schad, Karen ^a,b   Satoh, Andreas T ^a   Page, Malcolm G P ^a   Johnson, Maggie M ^c   Piddock, Laura J V ^c  

^a BASILEA PHARMACEUTICA INTERNATIONAL LTD   (Switzerland)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBENZOIC ACID; ABC TRANSPORTER; ACTINONIN; ADENOSINE TRIPHOSPHATE; AZITHROMYCIN; BACITRACIN; BLASTICIDIN S; CERULENIN; CHLORAMPHENICOL; CHOLINE; CLARITHROMYCIN; CLINDAMYCIN; DACTINOMYCIN; DAUNORUBICIN; DISTAMYCIN A; DOXORUBICIN; ERYTHROMYCIN; FOSFOMYCIN; FUSIDIC ACID; GRAMICIDIN; LINCOMYCIN; MITOMYCIN C; MONENSIN; NALIDIXIC ACID; NIGERICIN; PSEUDOMONIC ACID; QUINOLINE DERIVED ANTIINFECTIVE AGENT; UNINDEXED DRUG; XANTHINE;

AMINO ACID SYNTHESIS; ARTICLE; BACTERIUM MUTANT; GENE DISRUPTION; GENE MUTATION; GENE OVEREXPRESSION; METABOLIC ACTIVATION; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FAMILY; STRAIN DIFFERENCE; STREPTOCOCCUS INFECTION; STREPTOCOCCUS PNEUMONIAE;

ANTI-INFECTIVE AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; CIPROFLOXACIN; DRUG RESISTANCE, MULTIPLE, BACTERIAL; FLUOROQUINOLONES; MICROBIAL SENSITIVITY TESTS; MUTATION; NORFLOXACIN; PHENOTYPE; RESERPINE; RNA, MESSENGER; STREPTOCOCCUS PNEUMONIAE;

EID: 31944438999     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.50.2.685-693.2006     Document Type: Article

References (53)

1. Ahmed, M., C. M. Borsch, A. A. Neyfakh, and S. Schuldiner. 1993. Mutants of the Bacillus subtilis multidrug transporter Bmr with altered sensitivity to the antihypertensive alkaloid reserpine. J. Biol. Chem. 268:11086-11089.
2. Ahmed, M., L. Lyass, P. N. Markham, S. S. Taylor, N. Vazquez-Laslop, and A. A. Neyfakh. 1995. Two highly similar multidrug transporters of Bacillus subtilis whose expression is differentially regulated. J. Bacteriol. 177:3904-3910.
3. Andrews, J. M. 2001. Determination of minimum inhibitory concentrations. J. Antimicrob. Chemother. 48(Suppl. 1):5-16.
4. Aparicio, J. F., R. Fouces, M. V. Mendes, N. Olivera, and J. F. Martin. 2000. A complex multienzyme system encoded by five polyketide synthase genes is involved in the biosynthesis of the 26-membered polyene macrolide pimaricin in Streptomyces natalensis. Chem. Biol. 7:895-905.
5. Baranova, N. N., and A. A. Neyfakh. 1997. Apparent involvement of a multidrug transporter in the fltuoroquinolone resistance of Streptococcus pneumoniae. Antimicrob. Chemother. 41:1396-1398.
6. Beyer, R., E. Pestova, J. J. Millichap, V. Stosor, G. A. Noskin, and L. R. Peterson. 2000. A convenient assay for estimating the possible involvement of efflux of fluoroquinolones by Streptococcus pneumoniae and Staphylococcus aureus: evidence for diminished moxifloxacin, sparfloxacin, and trovafloxacin efflux. Antimicrob. Agents Chemother. 44:798-801.
7. Bolhuis, H., H. W. Van Veen, B. Poolman, A. J. M. Driessen, and W. N. Konings. 1997. Mechanisms of multidrug transporters. FEMS Microbiol. Rev. 21:55-84.
8. Brautaset, T., O. N. Sekurova, H. Sletta, T. E. Ellingsen, A. R. Strom, S. Valla, and S. B. Zotchev. 2000. Biosynthesis of the polyene antifungal antibiotic nystatin in Streptomyces noursei ATCC 1145: analysis of the gene cluster and deduction of the biosynthetic pathway. Chem. Biol. 7:395-403.
9. Brenwald, N. P., M. J. Gill, and R. Wise. 1997. The effect of reserpine, an inhibitor of multi-drug efflux pumps, on the in vitro susceptibilities of fluoroquinolone-resistant strains of Streptococcus pneumoniae to norfloxacin. J. Antimicrob. Chemother. 40:458-460.
10. Brenwald, N. P., M. J. Gill, and R. Wise. 1998. Prevalence of a putative efflux mechanism among fluoroquinolone-resistant clinical isolates of Streptococcus pneumoniae. Antimicrob. Agents Chemother. 42:2032-2035.
11. Brenwald, N. P., P. Appelbaum, T. Davies, and M. J. Gill. 2003. Evidence for efflux pumps other than PmrA associated with fluoroquinolone resistance in Streptococcus pneumoniae. Clin. Microbiol. Infect. 9:140-143.
12. Caffrey, P., S. Lynch, E. Flood, S. Finnan, and M. Oliynyk. 2001. Amphotericin biosynthesis in Streptomyces nodosus: deductions from analysis of polyketide synthase and late genes. Chem. Biol. 8:713-723.
13. Canton, R., M. Morosini, M. C. Enright, and I. Morrissey. 2003. Worldwide incidence, molecular epidemiology and mutations implicated in fluoroquinolone-resistant Streptococcus pneumoniae: data from the PROTEKT surveillance programme. J. Antimicrob. Chemother. 52:944-952.
14. Carlo, D. J., J. Y. Zeltner, T. H. Stoudt, K. H. Nollstadt, and R. B. Walton. 1980. South African patent SFXXABZA 7806664 1980730.
15. Chen, J. D., and D. A. Morrison. 1988. Construction and properties of a new insertion vector, pJDC9, that is protected by transcriptional terminators and useful for cloning of DNA from Streptococcus pneumoniae. Gene 64:155-164.
16. Daly, M. M., S. Doktor, R. Flamm, and D. Shortridge. 2004. Characterization and prevalence of MefA, MefE, and the associated msr(D) gene in Streptococcus pneumoniae clinical isolates. J. Clin. Microbiol. 42:3570-3574.
17. Daporta, M. T., J. L. Munoz Bellido, G. Y. Guirao, M. S. Hernandez, and J. A. Garcia-Rodriguez. 2004. In vitro activity of older and newer fluoroquinolones against efflux-mediated high-level ciprofloxacin-resistant Streptococcus pneumoniae. Int. J. Antimicrob. Agents 24:185-187.
18. Davies, T. A., G. A. Pankuch, B. E. Dewasses, M. R Jacobs, and P. C. Appelbaum. 1999. In vitro development of resistance to five quinolones and amoxicillin-clavulanate in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 43:1177-1182.
19. de Saizieu, A., U. Certa, J. Warrington, C. Gray, W. Keck, and J. Mous. 1998. Bacterial transcript imaging by hybridization of total RNA to oligonucleotide arrays. Nat. Biotechnol. 16:45-48.
20. de Saizieu, A., C. Gardès, N. Flint, C. Wagner, M. Kamber, T. J. Mitchell, W. Keck, K. E. Amrein, and R. Lange. 2000. Microarray-based identification of a novel Streptococcus pneumoniae regulon controlled by an autoinduced peptide. J. Bacteriol. 182:4696-4703.
21. Gibbons, S., and E. E. Udo. 2000. The effect of reserpine, a modulator of multidrug efflux pumps, on the in vitro activity of tetracycline against clinical isolates of methicillin resistant Staphylococcus aureus (MRSA) possessing the tet(K) determinant. Phytother. Res. 14:139-140.
22. Gill, M. J., N. P. Brenwald, and R. Wise. 1999. Identification of an efflux pump gene, pmrA, associated with fluoroquinolone resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 43:187-189.
23. Godreuil, S., M. Galimand, G. Gerbaud, C. Jacquet, and P. Courvalin. 2003. Efflux pump Lde is associated with fluoroquinolone resistance in Listeria monocytogenes. Antimicrob. Agents Chemother. 47:704-708.
24. Grkovic, S., M. H. Brown, and R. A. Skurray. 2001. Transcriptional regulation of multidrug efflux pumps in bacteria. Semin. Cell Dev. Biol. 12:225-237.
25. Hakenbeck, R., N. Balmelle, B. Weber, C. Gardès, W. Keck, and A. de Saizieu. 2001. Mosaic genes and mosaic chromosomes: intra- and interspecies genomic variation of Streptococcus pneumoniae. Infect. Immun. 69:2477-2486.
26. Havarstein, L. S., G. Coomaraswamy, and D. A. Morrison. 1995. An unmodified heptadecapeptide pheromone induces competence for genetic transformation in Streptococcus pneumoniae. Proc. Natl. Acad. Sci. USA 92:11140-11144.
27. Hoskins, J., W. E. Alborn, Jr., J. Arnold, L. C. Blaszczak, S. Burgett, B. S. De Hoff, S. T. Estrem, L. Fritz, D. J. Fu, W. Fuller, C. Geringer, R. Gilmour, J. S. Glass, H. Khoja, A. R. Kraft, R. E. Lagace, D. J. Le Blanc, L. N. Lee, E. J. Lefkowitz, J. Lu, P. Matsushima, S. M. McAhren, M. McHenney, K. McLeaster, C. W. Mundy, T. I. Nicas, F. H. Norris, M. O'Gara, R. B. Peery, G. T. Robertson, P. Rockey, P. M. Sun, M. E. Winkler, Y. Yang, M. Young-Bellido, G. Zhao, C. A. Zook, R. H. Baltz, S. R. Jaskunas, P. R. Rosteck, Jr., P. L. Skatrud, and J. I. Glass. 2001. Genome of the bacterium Streptococcus pneumoniae strain R6. J. Bacteriol. 183:5709-5717.
28. Huang, J., P. W. O'Toole, W. Shen, H. Amrine-Madsen, X. Jiang, N. Lobo, L. M. Palmer, L. Voelker, F. Fan, M. N. Gwynn, and D. McDevitt. 2004. Novel chromosomally encoded multidrug efflux transporter MdeA in Staphylococcus aureus. Antimicrob. Agents Chemother. 48:909-917.
29. Kaatz, G. W., and S. M. Seo. 1995. Inducible NorA-mediated multidrug resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 39:2650-2655.
30. Lacks, S., and R. D. Hotchkiss. 1960. A study of the genetic material determining an enzyme activity in pneumococcus. Biochim. Biophys. Acta 39:508-517.
31. Lee, E.-W., M. N. Huda, T. Kuroda, T. Mizushima, and T. Tsuchiya. 2003. EfrAB, an ABC multidrug efflux pump in Enterococcus faecalis. Antimcrob. Agents Chemother. 47:3733-3738.
32. Lockhart, D. J., H. Dong, M. C. Byrne, M. T. Follettie, M. V. Gallo, M. S. Chee, M. Mittmann, C. Wang, M. Kobayashi, H. Horton, and E. L. Brown. 1996. Expression monitoring by hybridization to high-density oligonucleotide arrays. Nat. Biotechnol. 14:1675-1680.
33. Lubelski, J., R. Van Merkerk, W. N. Konings, and A. J. M. Driessen. 2004. ydaG and ydbA of Lactococcus lactis encode a heterodimeric ABC-type multidrug transporter, abstr. C1-1190, p. 79. In Abstracts 44th Interscience Conference on Antimicrobial Agents and Chemotherapy. American Society for Microbiology, Washington, D.C.
34. Madaras-Kelly, K. J., C. Daniels, M. Hegbloom, and M. Thompson. 2002. Pharmacodynamic characterization of efflux and topoisomerase IV-mediated fluoroquinolone resistance in Streptococcus pneumoniae. J. Antimicrob. Chemother. 50:211-218.
35. Markham, P. N. 1999. Inhibition of the emergence of ciprofloxacin resistance in Streptococcus pneumoniae by the multidrug efflux inhibitor reserpine. Antimicrob. Agents Chemother. 43:988-989.
36. Marrer, E., A. T. Satoh, M. M. Johnson, L. J. V. Piddock, and M. G. P. Page. 2005. Global transcriptome analysis of the responses of a fluoroquinolone-resistant Streptococcus pneumoniae mutant and its parent to ciprofloxacin. Antimicrob. Agents Chemother. 50:269-278.
37. Masaoka, Y., Y. Ueno, Y. Morita, T. Kuroda, T. Mizushima, and T. Tsuchiya. 2000. A two-component multidrug efflux pump, EbrAB, in Bacillus subtilis. J. Bacteriol. 182:2307-2310.
38. Messing, J., C. Yanisch-Perron, and J. Vieira. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.
39. Montanari, M. P., E. Tili, I. Cochetti, M. Mingoia, A. Manzin, and P. E. Varaldo. 2004. Molecular characterization of clinical Streptococcus pneumoniae isolates with reduced susceptibility to fluoroquinolones emerging in Italy. Microb. Drug Resist. 10:209-217.
40. Morita, Y., T. Murata, T. Mima, S. Shiota, T. Kuroda, T. Mizushima, N. Gotoh, T. Nishino, and T. Tsuchiya. 2003. Induction of mexCD-oprJ operon for a multidrug efflux pump by disinfectants in wild-type Pseudomonas aeruginosa PAO1. J. Antimicrob. Chemother. 51:991-994.
41. Mortimer, P. G. S., and L. J. V. Piddock. 1991. Comparison for the methods used for measuring the accumulation of quinolones into Enterobacteriaceae, Pseudomonas aeruginosa and Staphylococcus aureus. J. Antimicrob. Chemother. 28:639-653.
42. Nair, B. M., K.-J. Cheung, Jr., A. Griffith, and J. L. Burns. 2004. Salicylate induces an antibiotic efflux pump in Burkholderia cepacia complex genomovar III (B. cenocepacia). J. Clin. Investig. 113:464-473.
43. Pestova, E., J. J. Millichap, F. Siddiqui, G. A. Noskin, and L. R. Peterson. 2002. Non-PmrA-mediated multidrug resistance in Streptococcus pneumoniae. J. Antimicrob. Chemother. 49:553-556.
44. Piddock, L. J. V., M. Johnson, V. Ricci, and S. L. Hill. 1998. Activities of new fluoroquinolones against fluoroquinolone-resistant pathogens of the lower respiratory tract. Antimicrob. Agents Chemother. 42:2956-2960.
45. Piddock, L. J. V., M. M. Johnson, S. Simjee, and L. Pumbwe. 2002. Expression of the efflux pump gene pmrA in fluoroquinolone-resistant and -susceptible clinical isolates of Streptococcus pneumoniae. Antimicrob. Agents Chemother. 46:808-812.
46. Piddock, L. J. V., and M. M. Johnson. 2002. Accumulation of 10 fluoroquinolones by wild-type or efflux mutant Streptococcus pneumoniae. Antimicrob. Agents Chemother. 46:813-820.
47. Rouquette-Loughlin, C., I. Stojiljkovic, T. Hrobowski, J. T. Balthazar, and W. M. Shafer. 2002. Inducible, but not constitutive, resistance of gonococci to hydrophobic agents due to the MtrC-MtrD-MtrE efflux pump requires TonB-ExbB-ExbD proteins. Antimicrob. Agents Chemother. 46:561-565.
48. Schmitz, F.-J., A. C. Fluit, M. Luckefahr, B. Engler, B. Hofmann, J. Vernoef, H.-P. Heinz, U. Hadding, and M. E. Jones. 1998. The effect of reserpine, an inhibitor of multidrug efflux pumps, on the in-vitro activities of ciprofloxacin, sparfloxacin and moxifloxacin against clinical isolates of Staphylococcus aureus. J. Antimicrob. Chemother. 42:807-810.
49. Stieger, M., B. Wohlgensinger, M. Kamber, R. Lutz, and W. Keck. 1999. Integrational plasmids for the tetracycline-regulated expression of genes in Streptococcus pneumoniae. Gene 226:243-251.
50. Tanabe, H., K. Yamasaki, M. Furue, K. Yamamoto, A. Katoh, M. Yamamoto, S. Yoshioka, H. Tagami, H. Aiba, and R. Utsumi. 1997. Growth phase-dependent transcription of emrKY, a homolog of multidrug efflux emrAB genes of Escherichia coli, is induced by tetracycline. J. Gen. Appl. Microbiol. 43:257-263.
51. Teran, W., A. Felipe, A. Segura, A. Rojas, J.-L. Ramos, and M.-T. Gallegos. 2003. Antibiotic-dependent induction of Pseudomonas putida DOT-TIE TtgABC efflux pump is mediated by the drug binding represser TtgR. Antimicrob. Agents Chemother. 47:3067-3072.
52. Tettelin, H., K. E. Nelson, I. T. Paulsen, J. A. Eisen, T. D. Read, S. Peterson, J. Heidelberg, R. T. DeBoy, D. H. Haft, R. J. Dodson, A. S. Durkin, M. Gwinn, J. F. Kolonay, W. C. Nelson, J. D. Peterson, L. A. Umayam, O. White, S. L. Salzberg, M. R. Lewis, D. Radune, E. Holtzapple, H. Khouri, A. M. Wolf, T. R. Utterback, C. L. Hansen, L. A. McDonald, T. V. Feldblyum, S. Angiuoli, T. Dickinson, E. K. Hickey, I. E. Holt, B. J. Loftus, F. Yang, H. O. Smith, J. C. Venter, B. A. Dougherty, D. A. Morrison, S. K. Hollingshead, and C. M. Fraser. 2001. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293:498-506.
53. Zeller, V., C. Janoir, M.-D. Kitzis, L. Gutmann, and N. J. Moreau. 1997. Active efflux as a mechanism of resistance to ciprofloxacin in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 41:1973-1978.