PBP3 inhibition elicits adaptive responses in Pseudomonas aeruginosa

Molecular Microbiology

Volumn 62, Issue 1, 2006, Pages 84-99

  Blázquez, Jesús ^a   Gómez Gómez, José María ^a   Oliver, Antonio ^b   Juan, Carlos ^b   Kapur, Vivek ^c   Martín, Soledad ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b HOSPITAL UNIVERSITARIO SON ESPASES   (Spain)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBAPENEM; CEFTAZIDIME; CIPROFLOXACIN; CYCLOSERINE; DNA POLYMERASE; DNA TOPOISOMERASE (ATP HYDROLYSING); FOSFOMYCIN; IMIPENEM; MITOMYCIN C; PENICILLIN BINDING PROTEIN; PENICILLIN BINDING PROTEIN 3; QUINOLINE DERIVED ANTIINFECTIVE AGENT; SOS PROTEIN; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA MODIFICATION; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; ENZYME INHIBITION; GENE EXPRESSION; GENETIC TRANSCRIPTION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; OPPORTUNISTIC INFECTION; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA;

PSEUDOMONAS AERUGINOSA;

EID: 33748675915     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05366.x     Document Type: Article

References (55)

1. Aertsen, A., and Michiels, C.W. (2005) Diversify or die: generation of diversity in response to stress. Crit Rev Microbiol 31: 69-78.
2. Arends, S.J., and Weiss, D.S. (2004) Inhibiting cell division in Escherichia coli has little if any effect on gene expression. J. Bacteriol 186: 880-884.
3. Bagge, N., Schuster, M., Hentzer, M., Ciofu, O., Givskov, M., Greenberg, P., and Høiby, N. (2004) Pseudomonas aeruginosa biofilms exposed to imipenem exhibit changes in global gene expression and β-lactamase and alginate production. Antimicrob Agents Chemother 48: 1175-1187.
4. Baldi, P., and Long, A.D. (2001) A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17: 509-519.
5. Blázquez, J. (2003) Hypermutation as a factor contributing to the acquisition of antimicrobial resistance. Clin Infect Dis 37: 1201-1209.
6. Boles, B.R., Thoendel, M., and Singh, P.K. (2004) Self-generated diversity produces 'insurance effects' in biofilm communities. Proc Natl Acad Sci USA 101: 16630-16635.
7. Brazas, M.D., and Hancock, R.E. (2005a) Ciprofloxacin induction of a susceptibility determinant in Pseudomonas aeruginosa. Antimicrob Agents Chemother 49: 3222-3227.
8. Brazas, M.D., and Hancock, R.E. (2005b) Using microarray gene signatures to elucidate mechanisms of antibiotic action and resistance. Drug Discov Today 10: 1245-1252.
9. Chang, W., Small, D.A., Toghrol, F., and Bentley, W.E. (2005) Microarray analysis of Pseudomonas aeruginosa reveals induction of pyocin genes in response to hydrogen peroxide. BMC Genomics 6: 115.
10. Ciofu, O., Giwercman, B., Pedersen, S.S., and Hoiby, N. (1994) Development of antibiotic resistance in Pseudomonas aeruginosa during two decades of antipseudomonal treatment at the Danish CF center. APMIS 102: 674-680.
11. Ciofu, O., Riis, B., Pressler, T., Poulsen, E.E., and Hoiby, N. (2005) Occurrence of hypermutable Pseudomonas aeruginosa in cystic fibrosis patients is associated with the oxidative stress caused by chronic lung inflammation. Antimicrob Agents Chemother 49: 2276-2282.
12. Cirz, R.T., and Romesberg, F.E. (2006) Induction and inhibition of ciprofloxacin resistance-conferring mutations in hypermutator bacteria. Antimicrob Agents Chemother 50:220-225.
13. Cirz, R.T., Chin, J.K., Andes, D.R., de Crécy-Lagard, V., Craig, W.A., and Romesberg, F.E. (2005) Inhibition of mutation and combating the evolution of antibiotic resistance. PLoS Biol 3: e176.
14. Conway, T., and Schoolnik, G.K. (2003) Microarray expression profiling: capturing a genome-wide portrait of the transcriptome. Mol Microbiol 47: 879-889.
15. Courcelle, J., Khodursky, A., Peter, B., Brown, P.O., and Hanawalt, P.C. (2001) Comparative gene expression rofiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158: 41-64.
16. Debouck, C., and Goodfellow, P.N. (1999) DNA microarrays in drug discovery and development. Nat Genet 21: 48-50.
17. Goh, E-B., Yim, G., Tsui, W., McClure, J., Surette, M.G., and Davies, J. (2002) Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. Proc Natl Acad Sci USA 99: 17025-17030.
18. Goodman, A.L., and Lory, S. (2004) Analysis of regulatory networks in Pseudomonas aeruginosa by genomewide transcriptional profiling. Curr Opin Microbiol 7: 39-44.
19. Grkovic, S., Brown, M.H., and Skurray, R.A. (2002) Regulation of bacterial drug export systems. Microbiol Mol Biol Rev 66: 671-701.
20. Hatfield, G.W., Hung, S.P., and Baldi, P. (2003) Differential analysis of DNA microarray gene expression data. Mol Microbiol 47: 871-877.
21. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U., and Speed, T.P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
22. Juan, C., Maciá, M.D., Gutiérrez, O., Vidal, C., Pérez, J.L., and Oliver, A. (2005) Molecular mechanisms of β-lactam resistance mediated by AmpC hyperproduction in Pseudomonas aeruginosa clinical strains. Antimicrob Agents Chemother 49: 4733-4738.
23. Juan, C., Moya, B., Perez, J.L., and Oliver, A. (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.
24. Kaldalu, N., Mei, R., and Lewis, K. (2004) Killing by ampicillin and ofloxacin induces overlapping changes in Escherichia coli transcription profile. Antimicrob Agents Chemother 48:890-896.
25. Khil, P.P., and Camerini-Otero, D. (2002) Over 1000 genes are involved in the DNA damage response of Escherichia coli. Mol Microbiol 44: 89-105.
26. Kim, S. R., Maenhaut, M.G., Yamada, M., Yamamoto, Y., Matsui, K., Sofuni, T., et al. (1997) Multiple pathways for SOS-induced mutagenesis in Escherichia coli: an over-expression of dinB/dinP results in strongly enhancing mutagenesis in the absence of any exogenous treatment to damage DNA. Proc Natl Acad Sci USA 94: 13792-13797.
27. Kohler, T., Michea-Hamzehpour, M., Epp, S.F., and Pechere, J.C. (1999) Carbapenem activities against Pseudomonas aeruginosa: respective contributions of OprD and efflux systems. Antimicrob Agents Chemother 43: 424-427.
28. Lewenza, S., Falsafi, R.K., Winsor, G., Gooderham, W.J., MacPhee, J.B., Brinkman, F.S., and Hancock, R.E. (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.
29. Lyczak, J.B., Cannon, C.L., and Pier, G.B. (2002) Lung infections associated with cystic fibrosis. Clin Microbiol Rev 15:194-222.
30. Macia, M.D., Blanquer, D., Togores, B., Sauleda, J., Pérez, J.L., and Oliver, A. (2005) Hypermutation is a key factor in development of multiple-antimicrobial resistance in Pseudomonas aeruginosa strains causing chronic lung infections. Antimicrob Agents Chemother 49: 3382-3386.
31. Masuda, N., Sakagawa, E., Ohya, S., Gotoh, N., Tsujimoto, H., and Nishino, T. (2000) Substrate specificities of MexAB-OprM, MexCD-OprJ, and MexXY-OprM efflux pumps in Pseudomonas aeruginosa. Antimicrob Agents Chemother 44: 3322-3327.
32. Matsui, H., Sano, Y., Ishihara, H., and Shinomiya, T. (1993) Regulation of pyocin genes in Pseudomonas aeruginosa by postive (prtN) and negative (prtR) regulatory genes. J Bacteriol 175: 1257-1263.
33. Michel-Briand, Y., and Baysse, C. (2002) The pyocins of Pseudomonas aeruginosa. Biochimie 84: 499-510.
34. Miller, C., Thomsen, L.E., Gaggero, C., Mosseri, R., Ingmer, H., and Cohen, S.N. (2004) SOS response induction by beta-lactams and bacterial defense against antibiotic lethality. Science 305: 1629-1631.
35. Nakayama, K., Takashima, K., Ishihara, H., Shinomiya, T., Kageyama, M., Knaya, S., et al. (2000) The R-type pyocin of Pseudomonas aeruginosa is related to P2 phage, and the F-type is related to lambda phage. Mol Microbiol 38:213-231.
36. National Committee for Clinical Laboratory Standards (NCCLS) (1999) Methods for determining bactericidal activity of antimicrobial agents. Approved Standard M21-A. Wayne, PA: NCCLS.
37. Nees, M., and Woodworth, C.D. (2001) Microarrays. spotlight on gene function and pharmacogenomics. Curr Cancer Drug Targets 2: 155-175.
38. Ochsner, U.A., Wilderman, P.J., Vasil, A.I., and Vasil, M.L. (2002) GeneChip expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol Microbiol 45:1277-1287.
39. Oliver, A., Cantón, R., Campo, P., Baquero, F., and Blázquez, J. (2000) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288: 1251-1253.
40. Oliver, A., Levin, B.R., Juan, C., Baquero, F., and Blázquez, J. (2004) Hypermutation and the pre-existence of antibiotic resistance Pseudomonas aeruginosa mutants: implications for susceptibility testing and treatment of chronic infections. Antimicrob Agents Chemother 48: 4226-4233.
41. Patten, C.L., Kirchhof, M.G., Schertzberg, M.R., Morton, R.A., and Schellhorn, H.E. (2004) Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol Genet Genomics 272: 580-591.
42. Pérez-Capilla, T., Baquero, M.R., Gómez-Gómez, J.M., Ionel, A., Martín, S., and Blázquez, J. (2005) SOS-independent induction of dinB transcription by beta-lactammediated inhibition of cell wall synthesis in Escherichia coli. J Bacteriol 187: 1515-1518.
43. Radman, M., Taddei, F., and Matic, I. (2000) Evolution-driving genes. Res Microbiol 151: 91-95.
44. Rosenberg, S.M. (2001) Evolving responsively: adaptive mutation. Nat Rev Genet 2: 504-515.
45. Saint-Ruf, C., Taddei, F., and Matic, I. (2004) Stress and survival of aging Escherichia coli rpoS colonies. Genetics 168: 541-546.
46. Schoolnik, G.K. (2002) Microarray analysis of bacterial pathogenicity. Adv Microb Physiol 46: 1-45.
47. Shaw, K.J., Miller, N., Liu, X., Lerner, D., Wan, J., Bittner, A., and Morrow, B.J. (2003) Comparison of the changes in global gene expression of Escherichia coli induced by four bactericidal agents. J Mol Microbiol Biotechnol 5:105-122.
48. Storz, G., and Hengge-Aronis, R. (2000) Bacterial Stress Responses. Washington, DC: American Society for Microbiology.
49. Stover, C.K., Pham, X.Q., Erwin, A.L., Mizoguchi, S.D., Warrener, P., Hickey, M.J., et al. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959-964.
50. Tegova, R., Tover, A., Tarassova, K., Tark, M., and Kivisaar, M. (2004) Involvement of error-prone DNA polymerase IV in stationary-phase mutagenesis in Pseudomonas putida. J Bacteriol 186: 2735-2744.
51. Utaida, S., Dunman, P.M., Macapagal, D., Murphy, E., Projan, S.J., Singh, V.K., et al. (2003) Genome-wide transcriptional profiling of the response of Staphylococcus aureus to cell-wall-active antibiotics reveals a cell-wall-stress stimulon. Microbiology 149: 2719-2732.
52. Villarino, A., Bouvet, O.M.M., Regnault, B., Martin-Delautre, S., and Grimont, P.A.D. (2000) Exploring the frontier between life and death in Escherichia coli: evaluation of different viability markers in live and heat- or UV-killed cells. Res Microbiol 155: 755-768.
53. Vincent, J.L. (2003) Nosocomial infections in adult intensive-care units. Lancet 361: 2068-2077.
54. Webb, J.S., Lau, M., and Kjelleberg, S. (2004) Bacteriophage and phenotypic variation in Pseudomonas aeruginosa biofilm development. J Bacteriol 186: 8066-8073.
55. Ysern, P., Clerch, B., Castaño, M., Gilbert, I., Barbé, J., and Llagostera, M. (1990) Induction of SOS genes in Escherichia coli and mutagenesis in Salmonella typhimurium by fluoroquinolones. Mutagenesis 5: 63-66.