Genetic determinants involved in the susceptibility of Pseudomonas aeruginosa to β-lactam antibiotics

Antimicrobial Agents and Chemotherapy

Volumn 54, Issue 10, 2010, Pages 4159-4167

  Alvarez Ortega, Carolina ^a,b   Wiegand, Irith ^c,d   Olivares, Jorge ^a,b   Hancock, Robert E W ^c   Martínez, José Luis ^a,b  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b CIBER EPIDEMIOLOGÍA Y SALUD PÚBLICA CIBERESP   (Spain)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d AiCuris GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINIC ACID; BETA LACTAMASE; CEFTAZIDIME; IMIPENEM; MEROPENEM;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIUM MUTANT; BIOSYNTHESIS; DRUG STRUCTURE; ENZYME SYNTHESIS; EPSILOMETER TEST; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SCREENING;

BACTERIAL PROTEINS; BETA-LACTAMASES; BETA-LACTAMS; GENETIC COMPLEMENTATION TEST; MICROBIAL SENSITIVITY TESTS; MUTATION; PHENOTYPE; PSEUDOMONAS AERUGINOSA; SERINE ENDOPEPTIDASES; SIGMA FACTOR;

EID: 77957362579     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00257-10     Document Type: Article

References (65)

1. Bagge, N., M. Schuster, M. Hentzer, O. Ciofu, M. Givskov, E. P. Greenberg, and N. Hoiby. 2004. Pseudomonas aeruginosa biofilms exposed to imipenem exhibit changes in global gene expression and beta-lactamase and alginate production. Antimicrob. Agents Chemother. 48:1175-1187.
2. Balcewich, M. D., T. M. Reeve, E. A. Orlikow, L. J. Donald, D. J. Vocadlo, and B. L. Mark. 2010. Crystal structure of the AmpR effector binding domain provides insight into the molecular regulation of inducible AmpC beta-lactamase. J. Mol. Biol. 400:998-1010.
3. Balke, B., L. Hoy, H. Weissbrodt, and S. Haussler. 2004. Comparison of the Micronaut Merlin automated broth microtiter system with the standard agar dilution method for antimicrobial susceptibility testing of mucoid and non-mucoid Pseudomonas aeruginosa isolates from cystic fibrosis patients. Eur. J. Clin. Microbiol. Infect. Dis. 23:765-771.
4. Baquero, F. 2001. Low-level antibacterial resistance: a gateway to clinical resistance. Drug Resist. Updat. 4:93-105.
5. Baquero, F., M. C. Negri, M. I. Morosini, and J. Blazquez. 1998. Selection of very small differences in bacterial evolution. Int. Microbiol. 1:295-300.
6. Blázquez, J., J. M. Gomez-Gomez, A. Oliver, C. Juan, V. Kapur, and S. Martin. 2006. PBP3 inhibition elicits adaptive responses in Pseudomonas aeruginosa. Mol. Microbiol. 62:84-99.
7. Boucher, J. C., J. Martinez-Salazar, M. J. Schurr, M. H. Mudd, H. Yu, and V. Deretic. 1996. Two distinct loci affecting conversion to mucoidy in Pseudomonas aeruginosa in cystic fibrosis encode homologs of the serine protease HtrA. J. Bacteriol. 178:511-523.
8. Breidenstein, E. B., B. K. Khaira, I. Wiegand, J. Overhage, and R. E. Hancock. 2008. Complex ciprofloxacin resistome revealed by screening a Pseudomonas aeruginosa mutant library for altered susceptibility. Antimicrob. Agents Chemother. 52:4486-4491.
9. Cao, L., R. Srikumar, and K. Poole. 2004. MexAB-OprM hyperexpression in NalC-type multidrug-resistant Pseudomonas aeruginosa: identification and characterization of the nalC gene encoding a repressor of PA3720-PA3719. Mol. Microbiol. 53:1423-1436.
10. Craig, W. A. 1997. The pharmacology of meropenem, a new carbapenem antibiotic. Clin. Infect. Dis. 24(Suppl. 2):S266-S275.
11. De Groote, V. N., N. Verstraeten, M. Fauvart, C. I. Kint, A. M. Verbeeck, S. Beullens, P. Cornelis, and J. Michiels. 2009. Novel persistence genes in Pseudomonas aeruginosa identified by high-throughput screening. FEMS Microbiol. Lett. 297:73-79.
12. DeVries, C. A., and D. E. Ohman. 1994. Mucoid-to-nonmucoid conversion in alginate-producing Pseudomonas aeruginosa often results from spontaneous mutations in algT, encoding a putative alternate sigma factor, and shows evidence for autoregulation. J. Bacteriol. 176:6677-6687.
13. Dötsch, A., T. Becker, C. Pommerenke, Z. Magnowska, L. Jansch, and S. Haussler. 2009. Genomewide identification of genetic determinants of antimicrobial drug resistance in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 53:2522-2531.
14. Eisen, M. B., P. T. Spellman, P. O. Brown, and D. Botstein. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 95:14863-14868.
15. El'Garch, F., K. Jeannot, D. Hocquet, C. Llanes-Barakat, and P. Plesiat. 2007. Cumulative effects of several nonenzymatic mechanisms on the resistance of Pseudomonas aeruginosa to aminoglycosides. Antimicrob. Agents Chemother. 51:1016-1021.
16. Fajardo, A., N. Martinez-Martin, M. Mercadillo, J. C. Galan, B. Ghysels, S. Matthijs, P. Cornelis, L. Wiehlmann, B. Tummler, F. Baquero, and J. L. Martinez. 2008. The neglected intrinsic resistome of bacterial pathogens. PLoS One 3:e1619.
17. Ghosh, A. S., A. K. Kar, and M. Kundu. 1999. Impaired imipenem uptake associated with alterations in outer membrane proteins and lipopolysaccharides in imipenem-resistant Shigella dysenteriae. J. Antimicrob. Chemother. 43:195-201.
18. Giamarellou, H., and K. Kanellakopoulou. 2008. Current therapies for Pseudomonas aeruginosa. Crit. Care Clin. 24:261-278.
19. Girgis, H. S., A. K. Hottes, and S. Tavazoie. 2009. Genetic architecture of intrinsic antibiotic susceptibility. PLoS One 4:e5629.
20. Girlich, D., T. Naas, and P. Nordmann. 2004. Biochemical characterization of the naturally occurring oxacillinase OXA-50 of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 48:2043-2048.
21. Godfrey, A. J., L. Hatlelid, and L. E. Bryan. 1984. Correlation between lipopolysaccharide structure and permeability resistance in beta-lactam- resistant Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 26:181-186.
22. He, J., R. L. Baldini, E. Deziel, M. Saucier, Q. Zhang, N. T. Liberati, D. Lee, J. Urbach, H. M. Goodman, and L. G. Rahme. 2004. The broad host range pathogen Pseudomonas aeruginosa strain PA14 carries two pathogenicity islands harboring plant and animal virulence genes. Proc. Natl. Acad. Sci. U. S. A. 101:2530-2535.
23. Hervé, M., A. Boniface, S. Gobec, D. Blanot, and D. Mengin-Lecreulx. 2007. Biochemical characterization and physiological properties of Escherichia coli UDP-N-acetylmuramate:L-alanyl-gamma-D-glutamyl- mesodiaminopimelate ligase. J. Bacteriol. 189:3987-3995.
24. Juan, C., B. Moya, J. L. Perez, and A. Oliver. 2006. Stepwise upregulation of the Pseudomonas aeruginosa chromosomal cephalosporinase conferring high-level beta-lactam resistance involves three AmpD homologues. Antimicrob. Agents Chemother. 50:1780-1787.
25. King, J. D., D. Kocincova, E. L. Westman, and J. S. Lam. 2009. Review: Lipopolysaccharide biosynthesis in Pseudomonas aeruginosa. Innate Immun. 15:261-312.
26. Kong, K. F., S. R. Jayawardena, S. D. Indulkar, A. Del Puerto, C. L. Koh, N. Hoiby, and K. Mathee. 2005. Pseudomonas aeruginosa AmpR is a global transcriptional factor that regulates expression of AmpC and PoxB beta-lactamases, proteases, quorum sensing, and other virulence factors. Antimicrob. Agents Chemother. 49:4567-4575.
27. Kovach, M. E., P. H. Elzer, D. S. Hill, G. T. Robertson, M. A. Farris, R. M. Roop II, and K. M. Peterson. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
28. Laubacher, M. E., and S. E. Ades. 2008. The Rcs phosphorelay is a cell envelope stress response activated by peptidoglycan stress and contributes to intrinsic antibiotic resistance. J. Bacteriol. 190:2065-2074.
29. Lee, S. W., E. J. Foley, and J. A. Epstein. 1944. Mode of action of penicillin: I. Bacterial growth and penicillin activity-Staphylococcus aureus FDA. J. Bacteriol. 48:393-399.
30. Lewenza, S., R. K. Falsafi, G. Winsor, W. J. Gooderham, J. B. McPhee, F. S. Brinkman, and R. E. Hancock. 2005. Construction of a mini-Tn5-luxCDABE mutant library in Pseudomonas aeruginosa PAO1: a tool for identifying differentially regulated genes. Genome Res. 15:583-589.
31. Liberati, N. T., J. M. Urbach, S. Miyata, D. G. Lee, E. Drenkard, G. Wu, J. Villanueva, T. Wei, and F. M. Ausubel. 2006. An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc. Natl. Acad. Sci. U. S. A. 103:2833-2838.
32. Lister, P. D., D. J. Wolter, and N. D. Hanson. 2009. Antibacterial- resistant Pseudomonas aeruginosa: clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clin. Microbiol. Rev. 22:582-610.
33. Lyczak, J. B., C. L. Cannon, and G. B. Pier. 2002. Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15:194-222.
34. Martinez, J. L., and F. Baquero. 2000. Mutation frequencies and antibiotic resistance. Antimicrob. Agents Chemother. 44:1771-1777.
35. Martínez, J. L., F. Baquero, and D. I. Andersson. 2007. Predicting antibiotic resistance. Nat. Rev. Microbiol. 5:958-965.
36. Martinez, J. L., A. Fajardo, L. Garmendia, A. Hernandez, J. F. Linares, L. Martinez-Solano, and M. B. Sanchez. 2009. A global view of antibiotic resistance. FEMS Microbiol. Rev. 33:44-65.
37. Martínez-Solano, L., M. D. Macia, A. Fajardo, A. Oliver, and J. L. Martinez. 2008. Chronic Pseudomonas aeruginosa infection in chronic obstructive pulmonary disease. Clin. Infect. Dis. 47:1526-1533.
38. Masuda, N., E. Sakagawa, S. Ohya, N. Gotoh, and T. Nishino. 2001. Hypersusceptibility of the Pseudomonas aeruginosa nfxB mutant to beta-lactams due to reduced expression of the ampC beta-lactamase. Antimicrob. Agents Chemother. 45:1284-1286.
39. Masuda, N., E. Sakagawa, S. Ohya, N. Gotoh, H. Tsujimoto, and T. Nishino. 2000. Substrate specificities of MexAB-OprM, MexCD-OprJ, and MexXY-oprM efflux pumps in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 44:3322-3327.
40. Moya, B., A. Dotsch, C. Juan, J. Blazquez, L. Zamorano, S. Haussler, and A. Oliver. 2009. Beta-lactam resistance response triggered by inactivation of a nonessential penicillin-binding protein. PLoS Pathog. 5:e1000353.
41. Navon-Venezia, S., R. Ben-Ami, and Y. Carmeli. 2005. Update on Pseudomonas aeruginosa and Acinetobacter baumannii infections in the healthcare setting. Curr. Opin. Infect. Dis. 18:306-313.
42. Negri, M. C., M. Lipsitch, J. Blazquez, B. R. Levin, and F. Baquero. 2000. Concentration-dependent selection of small phenotypic differences in TEM beta-lactamase-mediated antibiotic resistance. Antimicrob. Agents Chemother. 44:2485-2491.
43. Okamoto, K., N. Gotoh, and T. Nishino. 2001. Pseudomonas aeruginosa reveals high intrinsic resistance to penem antibiotics: penem resistance mechanisms and their interplay. Antimicrob. Agents Chemother. 45:1964-1971.
44. Oliveros, J. C. 2007 posting date. VENNY. An interactive tool for comparing lists with Venn Diagrams. http://bioinfogp.cnb.csic.es/tools/venny/ index.html.
45. Pai, H., J. Kim, J. Kim, J. H. Lee, K. W. Choe, and N. Gotoh. 2001. Carbapenem resistance mechanisms in Pseudomonas aeruginosa clinical isolates. Antimicrob. Agents Chemother. 45:480-484.
46. Poole, K. 2004. Resistance to beta-lactam antibiotics. Cell Mol. Life Sci. 61:2200-2223.
47. Poon, K. K., E. L. Westman, E. Vinogradov, S. Jin, and J. S. Lam. 2008. Functional characterization of MigA and WapR: putative rhamnosyltransferases involved in outer core oligosaccharide biosynthesis of Pseudomonas aeruginosa. J. Bacteriol. 190:1857-1865.
48. Queenan, A. M., W. Shang, R. Flamm, and K. Bush. 2010. Hydrolysis and inhibition profiles of beta-lactamases from molecular classes A to D with doripenem, imipenem, and meropenem. Antimicrob. Agents Chemother. 54:565-569.
49. Ramsey, D. M., and D. J. Wozniak. 2005. Understanding the control of Pseudomonas aeruginosa alginate synthesis and the prospects for management of chronic infections in cystic fibrosis. Mol. Microbiol. 56:309-322.
50. Reguera, J. A., F. Baquero, J. C. Perez-Diaz, and J. L. Martinez. 1991. Factors determining resistance to beta-lactam combined with beta-lactamase inhibitors in Escherichia coli. J. Antimicrob. Chemother. 27:569-575.
51. Reguera, J. A., F. Baquero, J. C. Perez-Diaz, and J. L. Martinez. 1988. Synergistic effect of dosage and bacterial inoculum in TEM-1 mediated antibiotic resistance. Eur. J. Clin. Microbiol. Infect. Dis. 7:778-779.
52. Schurek, K. N., A. K. Marr, P. K. Taylor, I. Wiegand, L. Semenec, B. K. Khaira, and R. E. Hancock. 2008. Novel genetic determinants of low-level aminoglycoside resistance in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 52:4213-4219.
53. Schweizer, H. P. 1994. A method for construction of bacterial hosts for lac-based cloning and expression vectors: alpha-complementation and regulated expression. Biotechniques 17:452-454, 456.
54. Smith, E. E., D. G. Buckley, Z. Wu, C. Saenphimmachak, L. R. Hoffman, D. A. D'Argenio, S. I. Miller, B. W. Ramsey, D. P. Speert, S. M. Moskowitz, J. L. Burns, R. Kaul, and M. V. Olson. 2006. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc. Natl. Acad. Sci. U. S. A. 103:8487-8492.
55. Steinkraus, G., R. White, and L. Friedrich. 2007. Vancomycin MIC creep in non-vancomycin-intermediate Staphylococcus aureus (VISA), vancomycin- susceptible clinical methicillin-resistant S. aureus (MRSA) blood isolates from 2001-05. J. Antimicrob. Chemother. 60:788-794.
56. Taccetti, G., S. Campana, A. S. Neri, V. Boni, and F. Festini. 2008. Antibiotic therapy against Pseudomonas aeruginosa in cystic fibrosis. J. Chemother. 20:166-169.
57. Uehara, T., and J. T. Park. 2002. Role of the murein precursor UDP-N-acetyl- muramyl-L-Ala-gamma-D-Glu-meso-diaminopimelicacid-D-Ala-D-Ala in repression of beta-lactamase induction in cell division mutants. J. Bacteriol. 184:4233-4239.
58. Vorachek-Warren, M. K., S. Ramirez, R. J. Cotter, and C. R. Raetz. 2002. A triple mutant of Escherichia coli lacking secondary acyl chains on lipid A. J. Biol. Chem. 277:14194-14205.
59. Walsh, C. 2003. Antibiotics that act on cell wall biosynthesis, p. 23-49. In C. Walsh (ed.), Antibiotics: actions, origins, resistance. ASM Press, Washington, DC.
60. Weiss, D. S. 2004. Bacterial cell division and the septal ring. Mol. Microbiol. 54:588-597.
61. Wiedemann, B., D. Pfeifle, I. Wiegand, and E. Janas. 1998. Beta-lactamase induction and cell wall recycling in gram-negative bacteria. Drug Resist. Updat. 1:223-226.
62. Wiegand, I., K. Hilpert, and R. E. Hancock. 2008. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc. 3:163-175.
63. Wiegand, I., A. K. Marr, E. B. Breidenstein, K. N. Schurek, P. Taylor, and R. E. Hancock. 2008. Mutator genes giving rise to decreased antibiotic susceptibility in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 52:3810-3813.
64. Wolter, D. J., N. D. Hanson, and P. D. Lister. 2005. AmpC and OprD are not involved in the mechanism of imipenem hypersusceptibility among Pseudomonas aeruginosa isolates overexpressing the mexCD-oprJ efflux pump. Antimicrob. Agents Chemother. 49:4763-4766.
65. Wood, L. F., A. J. Leech, and D. E. Ohman. 2006. Cell wall-inhibitory antibiotics activate the alginate biosynthesis operon in Pseudomonas aeruginosa: Roles of sigma (AlgT) and the AlgW and Prc proteases. Mol. Microbiol. 62:412-426.