1887

Abstract

The mechanisms responsible for the increase in ceftazidime MIC in two selected mutants, Caz/20-1 and Caz/20-2, were studied. OmpF loss and overexpression of , and that were associated with and mutations and overexpression, together with mutations A233T and I332V in FtSI (PBP3) resulted in ceftazidime resistance in Caz/20-2, multiplying by 128-fold the ceftazidime MIC in the parental clinical isolate PS/20. Absence of detectable β-lactamase hydrolytic activity in the crude extract of Caz/20-2 was observed, and coincided with Q191K and P209S mutations in AmpC and a nucleotide substitution at −28 in the promoter, whereas β-lactamase hydrolytic activity in crude extracts of PS/20 and Caz/20-1 strains was detected. Nevertheless, a fourfold increase in ceftazidime MIC in Caz/20-1 compared with that in PS/20 was due to the increased transcript level of derived from mutation. The two Caz mutants and PS/20 showed the same mutations in AmpG and ParE.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.063727-0
2014-01-01
2020-01-24
Loading full text...

Full text loading...

/deliver/fulltext/jmm/63/1/56.html?itemId=/content/journal/jmm/10.1099/jmm.0.063727-0&mimeType=html&fmt=ahah

References

  1. Ahmed A. M., Shimamoto T.. ( 2008;). Emergence of a cefepime- and cefpirome-resistant Citrobacter freundii clinical isolate harbouring a novel chromosomally encoded AmpC beta-lactamase, CMY-37. . Int J Antimicrob Agents 32:, 256–261. [CrossRef][PubMed]
    [Google Scholar]
  2. Alekshun M. N., Levy S. B.. ( 1999;). Characterization of MarR superrepressor mutants. . J Bacteriol 181:, 3303–3306.[PubMed]
    [Google Scholar]
  3. Alekshun M. N., Levy S. B., Mealy T. R., Seaton B. A., Head J. F.. ( 2001;). The crystal structure of MarR, a regulator of multiple antibiotic resistance, at 2.3 A resolution. . Nat Struct Biol 8:, 710–714. [CrossRef][PubMed]
    [Google Scholar]
  4. Aono R., Tsukagoshi N., Yamamoto M.. ( 1998;). Involvement of outer membrane protein TolC, a possible member of the mar-sox regulon, in maintenance and improvement of organic solvent tolerance of Escherichia coli K-12. . J Bacteriol 180:, 938–944.[PubMed]
    [Google Scholar]
  5. Asako H., Nakajima H., Kobayashi K., Kobayashi M., Aono R.. ( 1997;). Organic solvent tolerance and antibiotic resistance increased by overexpression of marA in Escherichia coli.. Appl Environ Microbiol 63:, 1428–1433.[PubMed]
    [Google Scholar]
  6. Barbosa A. R., Giufrè M., Cerquetti M., Bajanca-Lavado M. P.. ( 2011;). Polymorphism in ftsI gene and β-lactam susceptibility in Portuguese Haemophilus influenzae strains: clonal dissemination of β-lactamase-positive isolates with decreased susceptibility to amoxicillin/clavulanic acid. . J Antimicrob Chemother 66:, 788–796. [CrossRef][PubMed]
    [Google Scholar]
  7. Beadle B. M., Shoichet B. K.. ( 2002;). Structural bases of stability-function tradeoffs in enzymes. . J Mol Biol 321:, 285–296. [CrossRef][PubMed]
    [Google Scholar]
  8. Betts M. J., Russell R.. ( 2003;). Amino acid properties and consequences of substitutions. . In Bioinformatics for Geneticists, pp. 289–316. Edited by Barnes M. R., Gray I. C... Chichester:: John Wiley & Sons, Ltd;. [CrossRef]
    [Google Scholar]
  9. Blázquez J., Gómez-Gómez J. M., Oliver A., Juan C., Kapur V., Martín S.. ( 2006;). PBP3 inhibition elicits adaptive responses in Pseudomonas aeruginosa.. Mol Microbiol 62:, 84–99. [CrossRef][PubMed]
    [Google Scholar]
  10. Caroff N., Espaze E., Gautreau D., Richet H., Reynaud A.. ( 2000;). Analysis of the effects of -42 and -32 ampC promoter mutations in clinical isolates of Escherichia coli hyperproducing ampC. . J Antimicrob Chemother 45:, 783–788. [CrossRef][PubMed]
    [Google Scholar]
  11. Cayô R., Rodríguez M. C., Espinal P., Fernández-Cuenca F., Ocampo-Sosa A. A., Pascual A., Ayala J. A., Vila J., Martínez-Martínez L.. ( 2011;). Analysis of genes encoding penicillin-binding proteins in clinical isolates of Acinetobacter baumannii.. Antimicrob Agents Chemother 55:, 5907–5913. [CrossRef][PubMed]
    [Google Scholar]
  12. Cheng Q., Park J. T.. ( 2002;). Substrate specificity of the AmpG permease required for recycling of cell wall anhydro-muropeptides. . J Bacteriol 184:, 6434–6436. [CrossRef][PubMed]
    [Google Scholar]
  13. CLSI ( 2006;). Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically; Approved Standard M7–A7, 7th edn. Wayne, PA:: Clinical and Laboratory Standards Institute;.
    [Google Scholar]
  14. Corvec S., Caroff N., Espaze E., Marraillac J., Drugeon H., Reynaud A.. ( 2003;). Comparison of two RT-PCR methods for quantifying ampC specific transcripts in Escherichia coli strains. . FEMS Microbiol Lett 228:, 187–191. [CrossRef][PubMed]
    [Google Scholar]
  15. Corvec S., Prodhomme A., Giraudeau C., Dauvergne S., Reynaud A., Caroff N.. ( 2007;). Most Escherichia coli strains overproducing chromosomal AmpC β-lactamase belong to phylogenetic group A. . J Antimicrob Chemother 60:, 872–876. [CrossRef][PubMed]
    [Google Scholar]
  16. Curtis N. A. C., Orr D., Ross G. W., Boulton M. G.. ( 1979;). Competition of β-lactam antibiotics for the penicillin-binding proteins of Pseudomonas aeruginosa, Enterobacter cloacae, Klebsiella aerogenes, Proteus rettgeri, and Escherichia coli: comparison with antibacterial activity and effects upon bacterial morphology. . Antimicrob Agents Chemother 16:, 325–328. [CrossRef][PubMed]
    [Google Scholar]
  17. Doi Y., Wachino J., Ishiguro M., Kurokawa H., Yamane K., Shibata N., Shibayama K., Yokoyama K., Kato H.. & other authors ( 2004;). Inhibitor-sensitive AmpC β-lactamase variant produced by an Escherichia coli clinical isolate resistant to oxyiminocephalosporins and cephamycins. . Antimicrob Agents Chemother 48:, 2652–2658. [CrossRef][PubMed]
    [Google Scholar]
  18. Domka J., Lee J., Wood T. K.. ( 2006;). YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signaling. . Appl Environ Microbiol 72:, 2449–2459. [CrossRef][PubMed]
    [Google Scholar]
  19. Dubus A., Ledent P., Lamotte-Brasseur J., Frère J. M.. ( 1996;). The roles of residues Tyr150, Glu272, and His314 in class C β-lactamases. . Proteins 25:, 473–485.[PubMed]
    [Google Scholar]
  20. Eberhardt C., Kuerschner L., Weiss D. S.. ( 2003;). Probing the catalytic activity of a cell division-specific transpeptidase in vivo with β-lactams. . J Bacteriol 185:, 3726–3734. [CrossRef][PubMed]
    [Google Scholar]
  21. Fernández-Cuenca F., Pascual A., Martínez-Martínez L.. ( 2005;). Hyperproduction of AmpC β-lactamase in a clinical isolate of Escherichia coli associated with a 30 bp deletion in the attenuator region of ampC.. J Antimicrob Chemother 56:, 251–252. [CrossRef][PubMed]
    [Google Scholar]
  22. Georgopapadakou N. H.. ( 1993;). Penicillin-binding proteins and bacterial resistance to β-lactams. . Antimicrob Agents Chemother 37:, 2045–2053. [CrossRef][PubMed]
    [Google Scholar]
  23. Griffith K. L., Shah I. M., Wolf R. E. Jr. ( 2004;). Proteolytic degradation of Escherichia coli transcription activators SoxS and MarA as the mechanism for reversing the induction of the superoxide (SoxRS) and multiple antibiotic resistance (Mar) regulons. . Mol Microbiol 51:, 1801–1816. [CrossRef][PubMed]
    [Google Scholar]
  24. Jacoby G. A.. ( 2009;). AmpC β-lactamases. . Clin Microbiol Rev 22:, 161–182. [CrossRef][PubMed]
    [Google Scholar]
  25. Jaurin B., Grundström T., Normark S.. ( 1982;). Sequence elements determining ampC promoter strength in E. coli.. EMBO J 1:, 875–881.[PubMed]
    [Google Scholar]
  26. Keck W., Glauner B., Schwarz U., Broome-Smith J. K., Spratt B. G.. ( 1985;). Sequences of the active-site peptides of three of the high-Mr penicillin-binding proteins of Escherichia coli K-12. . Proc Natl Acad Sci U S A 82:, 1999–2003. [CrossRef][PubMed]
    [Google Scholar]
  27. Keeney D., Ruzin A., McAleese F., Murphy E., Bradford P. A.. ( 2008;). MarA-mediated overexpression of the AcrAB efflux pump results in decreased susceptibility to tigecycline in Escherichia coli.. J Antimicrob Chemother 61:, 46–53. [CrossRef][PubMed]
    [Google Scholar]
  28. Kern W. V., Oethinger M., Jellen-Ritter A. S., Levy S. B.. ( 2000;). Non-target gene mutations in the development of fluoroquinolone resistance in Escherichia coli.. Antimicrob Agents Chemother 44:, 814–820. [CrossRef][PubMed]
    [Google Scholar]
  29. Kobayashi K., Tsukagoshi N., Aono R.. ( 2001;). Suppression of hypersensitivity of Escherichia coli acrB mutant to organic solvents by integrational activation of the acrEF operon with the IS1 or IS2 element. . J Bacteriol 183:, 2646–2653. [CrossRef][PubMed]
    [Google Scholar]
  30. Komp Lindgren P., Marcusson L. L., Sandvang D., Frimodt-Møller N., Hughes D.. ( 2005;). Biological cost of single and multiple norfloxacin resistance mutations in Escherichia coli implicated in urinary tract infections. . Antimicrob Agents Chemother 49:, 2343–2351. [CrossRef][PubMed]
    [Google Scholar]
  31. Lee A., Mao W., Warren M. S., Mistry A., Hoshino K., Okumura R., Ishida H., Lomovskaya O.. ( 2000;). Interplay between efflux pumps may provide either additive or multiplicative effects on drug resistance. . J Bacteriol 182:, 3142–3150. [CrossRef][PubMed]
    [Google Scholar]
  32. Lee J., Jayaraman A., Wood T. K.. ( 2007;). Indole is an inter-species biofilm signal mediated by SdiA. . BMC Microbiol 7:, 42. [CrossRef][PubMed]
    [Google Scholar]
  33. Linde H. J., Notka F., Metz M., Kochanowski B., Heisig P., Lehn N.. ( 2000;). In vivo increase in resistance to ciprofloxacin in Escherichia coli associated with deletion of the C-terminal part of MarR. . Antimicrob Agents Chemother 44:, 1865–1868. [CrossRef][PubMed]
    [Google Scholar]
  34. Maejima T., Inoue M., Mitsuhashi S.. ( 1991;). In vitro antibacterial activity of KP-736, a new cephem antibiotic. . Antimicrob Agents Chemother 35:, 104–110. [CrossRef][PubMed]
    [Google Scholar]
  35. Maqbool A., Levdikov V. M., Blagova E. V., Hervé M., Horler R. S. P., Wilkinson A. J., Thomas G. H.. ( 2011;). Compensating stereochemical changes allow murein tripeptide to be accommodated in a conventional peptide-binding protein. . J Biol Chem 286:, 31512–31521. [CrossRef][PubMed]
    [Google Scholar]
  36. Martínez-Martínez L., Conejo M. C., Pascual A., Hernández-Allés S., Ramírez de Arellano-Ramos E., Benedí J., Perea J.. ( 2000;). Activities of imipenem and cephalosporins against clonally related strains of Escherichia coli hyperproducing chromosomal β-lactamase and showing altered porin profiles. . Antimicrob Agents Chemother 44:, 2534–2536. [CrossRef][PubMed]
    [Google Scholar]
  37. Morgan-Linnell S. K., Becnel Boyd L., Steffen D., Zechiedrich L.. ( 2009;). Mechanisms accounting for fluoroquinolone resistance in Escherichia coli clinical isolates. . Antimicrob Agents Chemother 53:, 235–241. [CrossRef][PubMed]
    [Google Scholar]
  38. Moyá B., Beceiro A., Cabot G., Juan C., Zamorano L., Alberti S., Oliver A.. ( 2012;). Pan-β-lactam resistance development in Pseudomonas aeruginosa clinical strains: molecular mechanisms, penicillin-binding protein profiles, and binding affinities. . Antimicrob Agents Chemother 56:, 4771–4778. [CrossRef][PubMed]
    [Google Scholar]
  39. Nguyen-Distèche M., Fraipont C., Buddelmeijer N., Nanninga N.. ( 1998;). The structure and function of Escherichia coli penicillin-binding protein 3. . Cell Mol Life Sci 54:, 309–316. [CrossRef][PubMed]
    [Google Scholar]
  40. Nicoloff H., Perreten V., McMurry L. M., Levy S. B.. ( 2006;). Role for tandem duplication and lon protease in AcrAB-TolC- dependent multiple antibiotic resistance (Mar) in an Escherichia coli mutant without mutations in marRAB or acrRAB.. J Bacteriol 188:, 4413–4423. [CrossRef][PubMed]
    [Google Scholar]
  41. Nishino K., Yamada J., Hirakawa H., Hirata T., Yamaguchi A.. ( 2003;). Roles of TolC-dependent multidrug transporters of Escherichia coli in resistance to beta-lactams. . Antimicrob Agents Chemother 47:, 3030–3033. [CrossRef][PubMed]
    [Google Scholar]
  42. Nordmann P., Mammeri H.. ( 2007;). Extended-spectrum cephalosporinases: structure, detection and epidemiology. . Future Microbiol 2:, 297–307. [CrossRef][PubMed]
    [Google Scholar]
  43. Oteo J., Navarro C., Cercenado E., Delgado-Iribarren A., Wilhelmi I., Orden B., García C., Miguelañez S., Pérez-Vázquez M.. & other authors ( 2006;). Spread of Escherichia coli strains with high-level cefotaxime and ceftazidime resistance between the community, long-term care facilities, and hospital institutions. . J Clin Microbiol 44:, 2359–2366. [CrossRef][PubMed]
    [Google Scholar]
  44. Oteo J., Cercenado E., Cuevas O., Bautista V., Delgado-Iribarren A., Orden B., Pérez-Vázquez M., García-Cobos S., Campos J.. ( 2010;). AmpC beta-lactamases in Escherichia coli: emergence of CMY-2-producing virulent phylogroup D isolates belonging mainly to STs 57, 115, 354, 393, and 420, and phylogroup B2 isolates belonging to the international clone O25b-ST131. . Diagn Microbiol Infect Dis 67:, 270–276. [CrossRef][PubMed]
    [Google Scholar]
  45. Park J. T., Raychaudhuri D., Li H., Normark S., Mengin-Lecreulx D.. ( 1998;). MppA, a periplasmic binding protein essential for import of the bacterial cell wall peptide L-alanyl-γ-D-glutamyl-meso-diaminopimelate. . J Bacteriol 180:, 1215–1223.[PubMed]
    [Google Scholar]
  46. Pérez-Capilla T., Baquero M. R., Gómez-Gómez J. M., Ionel A., Martín S., Blázquez J.. ( 2005;). SOS-independent induction of dinB transcription by beta-lactam-mediated inhibition of cell wall synthesis in Escherichia coli. . J Bacteriol 187:, 1515–1518. [CrossRef][PubMed]
    [Google Scholar]
  47. Peter-Getzlaff S., Polsfuss S., Poledica M., Hombach M., Giger J., Böttger E. C., Zbinden R., Bloemberg G. V.. ( 2011;). Detection of AmpC beta-lactamase in Escherichia coli: comparison of three phenotypic confirmation assays and genetic analysis. . J Clin Microbiol 49:, 2924–2932. [CrossRef][PubMed]
    [Google Scholar]
  48. Piette A., Fraipont C., Den Blaauwen T., Aarsman M. E. G., Pastoret S., Nguyen-Distèche M.. ( 2004;). Structural determinants required to target penicillin-binding protein 3 to the septum of Escherichia coli.. J Bacteriol 186:, 6110–6117. [CrossRef][PubMed]
    [Google Scholar]
  49. Pomposiello P. J., Bennik M. H. J., Demple B.. ( 2001;). Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate. . J Bacteriol 183:, 3890–3902. [CrossRef][PubMed]
    [Google Scholar]
  50. Queenan A. M., Shang W., Kania M., Page M. G. P., Bush K.. ( 2007;). Interactions of ceftobiprole with β-lactamases from molecular classes A to D. . Antimicrob Agents Chemother 51:, 3089–3095. [CrossRef][PubMed]
    [Google Scholar]
  51. Ruiz J., Casellas S., Jiménez de Anta M. T., Vila J.. ( 1997;). The region of the parE gene, homologous to the quinolone-resistant determining region of the gyrB gene, is not linked with the acquisition of quinolone resistance in Escherichia coli clinical isolates. . J Antimicrob Chemother 39:, 839–840. [CrossRef][PubMed]
    [Google Scholar]
  52. Sánchez-Céspedes J., Vila J.. ( 2007;). Partial characterisation of the acrAB locus in two Citrobacter freundii clinical isolates. . Int J Antimicrob Agents 30:, 259–263. [CrossRef][PubMed]
    [Google Scholar]
  53. Song W., Bae I. K., Lee Y.-N., Lee C. H., Lee S. H., Jeong S. H.. ( 2007;). Detection of extended-spectrum beta-lactamases by using boronic acid as an AmpC beta-lactamase inhibitor in clinical isolates of Klebsiella spp. and Escherichia coli. . J Clin Microbiol 45:, 1180–1184. [CrossRef][PubMed]
    [Google Scholar]
  54. Tavío M. M., Aquili V. D., Poveda J. B., Antunes N. T., Sánchez-Céspedes J., Vila J.. ( 2010;). Quorum-sensing regulator sdiA and marA overexpression is involved in in vitro-selected multidrug resistance of Escherichia coli.. J Antimicrob Chemother 65:, 1178–1186. [CrossRef][PubMed]
    [Google Scholar]
  55. Tracz D. M., Boyd D. A., Bryden L., Hizon R., Giercke S., Van Caeseele P., Mulvey M. R.. ( 2005;). Increase in ampC promoter strength due to mutations and deletion of the attenuator in a clinical isolate of cefoxitin-resistant Escherichia coli as determined by RT-PCR. . J Antimicrob Chemother 55:, 768–772. [CrossRef][PubMed]
    [Google Scholar]
  56. Tracz D. M., Boyd D. A., Hizon R., Bryce E., McGeer A., Ofner-Agostini M., Simor A. E., Paton S., Mulvey M. R..Canadian Nosocomial Infection Surveillance Program ( 2007;). ampC gene expression in promoter mutants of cefoxitin-resistant Escherichia coli clinical isolates. . FEMS Microbiol Lett 270:, 265–271. [CrossRef][PubMed]
    [Google Scholar]
  57. Trépanier S., Knox J. R., Clairoux N., Sanschagrin F., Levesque R. C., Huletsky A.. ( 1999;). Structure-function studies of Ser-289 in the class C β-lactamase from Enterobacter cloacae P99. . Antimicrob Agents Chemother 43:, 543–548.[PubMed]
    [Google Scholar]
  58. Uchida Y., Mochimaru T., Morokuma Y., Kiyosuke M., Fujise M., Eto F., Harada Y., Kadowaki M., Shimono N., Kang D.. ( 2010;). Geographic distribution of fluoroquinolone-resistant Escherichia coli strains in Asia. . Int J Antimicrob Agents 35:, 387–391. [CrossRef][PubMed]
    [Google Scholar]
  59. Wang H., Dzink-Fox J. L., Chen M., Levy S. B.. ( 2001;). Genetic characterization of highly fluoroquinolone-resistant clinical Escherichia coli strains from China: role of acrR mutations. . Antimicrob Agents Chemother 45:, 1515–1521. [CrossRef][PubMed]
    [Google Scholar]
  60. Watanabe R., Doukyu N.. ( 2012;). Contributions of mutations in acrR and marR genes to organic solvent tolerance in Escherichia coli.. AMB Express 2:, 58. [CrossRef][PubMed]
    [Google Scholar]
  61. Webber M. A., Piddock L. J. V.. ( 2001;). Absence of mutations in marRAB or soxRS in acrB-overexpressing fluoroquinolone-resistant clinical and veterinary isolates of Escherichia coli.. Antimicrob Agents Chemother 45:, 1550–1552. [CrossRef][PubMed]
    [Google Scholar]
  62. Wei Y., Lee J. M., Smulski D. R., LaRossa R. A.. ( 2001a;). Global impact of sdiA amplification revealed by comprehensive gene expression profiling of Escherichia coli.. J Bacteriol 183:, 2265–2272. [CrossRef][PubMed]
    [Google Scholar]
  63. Wei Y., Vollmer A. C., LaRossa R. A.. ( 2001b;). In vivo titration of mitomycin C action by four Escherichia coli genomic regions on multicopy plasmids. . J Bacteriol 183:, 2259–2264. [CrossRef][PubMed]
    [Google Scholar]
  64. White D. G., Goldman J. D., Demple B., Levy S. B.. ( 1997;). Role of the acrAB locus in organic solvent tolerance mediated by expression of marA, soxS, or robA in Escherichia coli.. J Bacteriol 179:, 6122–6126.[PubMed]
    [Google Scholar]
  65. Wissel M. C., Weiss D. S.. ( 2004;). Genetic analysis of the cell division protein FtsI (PBP3): amino acid substitutions that impair septal localization of FtsI and recruitment of FtsN. . J Bacteriol 186:, 490–502. [CrossRef][PubMed]
    [Google Scholar]
  66. Yang S., Clayton S. R., Zechiedrich E. L.. ( 2003;). Relative contributions of the AcrAB, MdfA and NorE efflux pumps to quinolone resistance in Escherichia coli.. J Antimicrob Chemother 51:, 545–556. [CrossRef][PubMed]
    [Google Scholar]
  67. Yu W., Bing L., Zhenhua L.. ( 2009;). AmpC promoter and attenuator mutations affect function of three Escherichia coli strains. . Curr Microbiol 59:, 244–247. [CrossRef][PubMed]
    [Google Scholar]
  68. Zheng J., Cui S., Meng J.. ( 2008;). Effect of transcriptional activators RamA and SoxS on expression of multidrug efflux pumps AcrAB and AcrEF in fluoroquinolone-resistant Salmonella Typhimurium. . J Antimicrob Chemother 63:, 95–102. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.063727-0
Loading
/content/journal/jmm/10.1099/jmm.0.063727-0
Loading

Data & Media loading...

Supplements

Supplementary material 

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error