Activity of ceftazidime/avibactam against isogenic strains of Escherichia coli containing KPC and SHV β-lactamases with single amino acid substitutions in the Ω-loop

Journal of Antimicrobial Chemotherapy

Volumn 70, Issue 8, 2015, Pages 2279-2286

  Winkler, Marisa L ^a,b   Papp Wallace, Krisztina M ^b,c   Bonomo, Robert A ^a,b,c  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antibiotic resistance; ESBLs; Extended spectrum lactamases; lactamase inhibitors

Indexed keywords

AVIBACTAM PLUS CEFTAZIDIME; BETA LACTAMASE; BETA LACTAMASE KPC; BETA LACTAMASE SHV; CEFTAZIDIME; NITROCEFIN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; AVIBACTAM, CEFTAZIDIME DRUG COMBINATION; AZABICYCLO DERIVATIVE; MUTANT PROTEIN;

AGAR DILUTION; AMINO ACID SUBSTITUTION; ANTIBACTERIAL ACTIVITY; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL STRAIN; BIOCHEMICAL ANALYSIS; ENZYME KINETICS; ESCHERICHIA COLI; HYDROLYSIS; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PURIFICATION; ANTIBIOTIC RESISTANCE; DRUG EFFECTS; ENZYMOLOGY; GENETICS; METABOLISM; MICROBIAL SENSITIVITY TEST;

AMINO ACID SUBSTITUTION; ANTI-BACTERIAL AGENTS; AZABICYCLO COMPOUNDS; BETA-LACTAMASES; CEFTAZIDIME; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; MICROBIAL SENSITIVITY TESTS; MUTANT PROTEINS;

EID: 84939545950     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkv094     Document Type: Article

References (48)

1. Ambler RP, Coulson AF, Frere JM et al. A standard numbering scheme for the class A βlactamases. Biochem J 1991; 276: 269-70.
2. Bush K, Jacoby GA, Medeiros AA. A functional classification scheme for βlactamases and its correlation with molecular structure. Antimicrob Agents Chemother 1995; 39: 1211-33.
3. Bush K, Jacoby GA. Updated functional classification of βlactamases. Antimicrob Agents Chemother 2010; 54: 969-76.
4. Vakulenko SB, Toth M, Taibi P et al. Effects of Asp-179 mutations in TEMpUC19 βlactamase on susceptibility to βlactams. Antimicrob Agents Chemother 1995; 39: 1878-80.
5. Palzkill T, Le QQ, Venkatachalam KV et al. Evolution of antibiotic resistance: several different amino acid substitutions in an active site loop alter the substrate profile of βlactamase. Mol Microbiol 1994; 12: 217-29.
6. Petrosino JF, Palzkill T. Systematic mutagenesis of the active site omega loop of TEM-1 βlactamase. J Bacteriol 1996; 178: 1821-8.
7. Vakulenko SB, Taibi-Tronche P, TothMet al. Effects on substrate profile by mutational substitutions at positions 164 and 179 of the class A TEMpUC19 βlactamase from Escherichia coli. J Biol Chem 1999; 274: 23052-60.
8. Arpin C, Labia R, Andre C et al. SHV-16, a βlactamase with a pentapeptide duplication in the omega loop. Antimicrob Agents Chemother 2001; 45: 2480-5.
9. Yi H, Cho KH, Cho YS et al. Twelve positions in a βlactamase that can expand its substrate spectrum with a single amino acid substitution. PLoS One 2012; 7: e37585.
10. Banerjee S, Pieper U, Kapadia G et al. Role of the ω-loop in the activity, substrate specificity, and structure of class A βlactamase. Biochemistry 1998; 37: 3286-96.
11. Guillaume G, Vanhove M, Lamotte-Brasseur J et al. Site-directed mutagenesis of glutamate 166 in two βlactamases. Kinetic and molecular modeling studies. J Biol Chem 1997; 272: 5438-44.
12. Delmas J, Robin F, Bittar F et al. Unexpected enzyme TEM-126: role of mutation Asp179Glu. Antimicrob Agents Chemother 2005; 49: 4280-7.
13. Poirel L, Naas T, Le Thomas I et al. CTX-M-type extended-spectrum βlactamase that hydrolyzes ceftazidime through a single amino acid substitution in the omega loop. Antimicrob Agents Chemother 2001; 45: 3355-61.
14. Kurokawa H, Yagi T, Shibata N et al. A new SHV-derived extendedspectrum βlactamase (SHV-24) that hydrolyzes ceftazidime through a single-amino-acid substitution (D179G) in the ω-loop. Antimicrob Agents Chemother 2000; 44: 1725-7.
15. Levitt PS, Papp-Wallace KM, Taracila MA et al. Exploring the role of a conserved class A residue in the ω-loop of KPC-2 βlactamase: a mechanism for ceftazidime hydrolysis. J Biol Chem 2012; 287: 31783-93.
16. Sampson JM, Ke W, Bethel CR et al. Ligand-dependent disorder of the ω loop observed in extended-spectrum SHV-type βlactamase. Antimicrob Agents Chemother 2011; 55: 2303-9.
17. Bae IK, Lee BH, Hwang HY et al. A novel ceftazidime-hydrolysing extended-spectrum βlactamase, CTX-M-54, with a single amino acid substitution at position 167 in the omega loop. J Antimicrob Chemother 2006; 58: 315-9.
18. Ma L, Alba J, Chang FY et al. Novel SHV-derived extended-spectrum βlactamase, SHV-57, that confers resistance to ceftazidime but not cefazolin. Antimicrob Agents Chemother 2005; 49: 600-5.
19. Sturenburg E, Kuhn A, Mack D et al. A novel extended-spectrum βlactamase CTX-M-23 with a P167 T substitution in the active-site omega loop associated with ceftazidime resistance. J Antimicrob Chemother 2004; 54: 406-9.
20. Chanal C, Poupart MC, Sirot D et al. Nucleotide sequences of CAZ-2, CAZ-6, and CAZ-7 βlactamase genes. Antimicrob Agents Chemother 1992; 36: 1817-20.
21. Gutmann L, Kitzis MD, Billot-Klein D et al. Plasmid-mediated βlactamase (TEM-7) involved in resistance to ceftazidime and aztreonam. Rev Infect Dis 1988; 10: 860-6.
22. Kurokawa H, Shibata N, Doi Y et al. A new TEM-derived extendedspectrum βlactamase (TEM-91) with an R164C substitution at the ω-loop confers ceftazidime resistance. Antimicrob Agents Chemother 2003; 47: 2981-3.
23. Paul GC, Gerbaud G, Bure A et al. TEM-4, a new plasmid-mediated βlactamase that hydrolyzes broad-spectrum cephalosporins in a clinical isolate of Escherichia coli. Antimicrob Agents Chemother 1989; 33: 1958-63.
24. Petit A, Sirot DL, Chanal CM et al. Novel plasmid-mediated βlactamase in clinical isolates of Klebsiella pneumoniae more resistant to ceftazidime than to other broad-spectrum cephalosporins. Antimicrob Agents Chemother 1988; 32: 626-30.
25. Quinn JP, Miyashiro D, Sahm D et al. Novel plasmid-mediated βlactamase (TEM-10) conferring selective resistance to ceftazidime and aztreonam in clinical isolates of Klebsiella pneumoniae. Antimicrob Agents Chemother 1989; 33: 1451-6.
26. SougakoffW, Petit A, Goussard S et al. Characterization of the plasmid genes blaT-4 and blaT-5 which encode the broad-spectrum βlactamases TEM-4 and TEM-5 in Enterobacteriaceae. Gene 1989; 78: 339-48.
27. Rasheed JK, Jay C, Metchock B et al. Evolution of extended-spectrum βlactam resistance (SHV-8) in a strain of Escherichia coli during multiple episodes of bacteremia. Antimicrob Agents Chemother 1997; 41: 647-53.
28. Arlet G, Rouveau M, Philippon A. Substitution of alanine for aspartate at position 179 in the SHV-6 extended-spectrum βlactamase. FEMS Microbiol Lett 1997; 152: 163-7.
29. Lahiri SD, Johnstone MR, Ross PL et al. Avibactam and class C βlactamases: mechanism of inhibition, conservation of the binding pocket, and implications for resistance. Antimicrob Agents Chemother 2014; 58: 5704-13.
30. Keepers TR, Gomez M, Celeri C et al. Bactericidal activity, absence of serum effect, and time-kill kinetics of ceftazidime-avibactam against βlactamase-producing Enterobacteriaceae and Pseudomonas aeruginosa. Antimicrob Agents Chemother 2014; 58: 5297-305.
31. Sader HS, Castanheira M, Flamm RK et al. Antimicrobial activity of ceftazidime-avibactam against Gram-negative organisms collected from U.S. medical centers in 2012. Antimicrob Agents Chemother 2014; 58: 1684-92.
32. Wang X, Zhang F, Zhao C et al. In vitro activities of ceftazidimeavibactam and aztreonam-avibactam against 372 Gram-negative bacilli collected in 2011 and 2012 from 11 teaching hospitals in China. Antimicrob Agents Chemother 2014; 58: 1774-8.
33. Porres-Osante N, Dupont H, Torres C et al. Avibactam activity against extended-spectrum AmpC βlactamases. J Antimicrob Chemother 2014; 69: 1715-6.
34. Falagas ME, Karageorgopoulos DE. Extended-spectrum βlactamaseproducing organisms. J Hosp Infect 2009; 73: 345-54.
35. Afridi FI, Farooqi BJ. Activity of βlactam βlactamase inhibitor combinations against extended spectrum βlactamase producing Enterobacteriaceae in urinary isolates. J Coll Physicians Surg Pak 2012; 22: 358-62.
36. Papp-Wallace KM, Taracila M, Hornick JM et al. Substrate selectivity and a novel role in inhibitor discrimination by residue 237 in the KPC-2 βlactamase. Antimicrob Agents Chemother 2010; 54: 2867-77.
37. Kuzin AP, Nukaga M, Nukaga Y et al. Structure of the SHV-1 βlactamase. Biochemistry 1999; 38: 5720-7.
38. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing: Twenty-fourth Informational Supplement M100-S24. CLSI, Wayne, PA, USA, 2014.
39. Papp-Wallace KM, Bethel CR, Distler AM et al. Inhibitor resistance in the KPC-2 βlactamase, a preeminent property of this class A βlactamase. Antimicrob Agents Chemother 2010; 54: 890-7.
40. Padayatti PS, Sheri A, Totir MA et al. Rational design of a βlactamase inhibitor achieved via stabilization of the trans-enamine intermediate: 1.28Åcrystal structure of wt SHV-1 complex with a penam sulfone. J Am Chem Soc 2006; 128: 13235-42.
41. Papp-Wallace KM, Winkler ML, Gatta JA et al. Reclaiming the efficacy of βlactam-βlactamase inhibitor combinations: avibactam restores the susceptibility of CMY-2-producing Escherichia coli to ceftazidime. Antimicrob Agents Chemother 2014; 58: 4290-7.
42. Ehmann DE, Jahic H, Ross PL et al. Kinetics of avibactam inhibition against class A, C, and D βlactamases. J Biol Chem 2013; 288: 27960-71.
43. Bethel CR, Hujer AM, Hujer KM et al. Role of Asp104 in the SHV βlactamase. Antimicrob Agents Chemother 2006; 50: 4124-31.
44. HuangW, Palzkill T. A natural polymorphism in βlactamase is a global suppressor. Proc Natl Acad Sci USA 1997; 94: 8801-6.
45. Marciano DC, Pennington JM, Wang X et al. Genetic and structural characterization of an L201P global suppressor substitution in TEM-1 βlactamase. J Mol Biol 2008; 384: 151-64.
46. Sun T, Bethel CR, Bonomo RA et al. Inhibitor-resistant class A βlactamases: consequences of the Ser130-to-Gly mutation seen in Apo and tazobactam structures of the SHV-1 variant. Biochemistry 2004; 43: 14111-7.
47. Winkler ML, Rodkey EA, Taracila MA et al. Design and exploration of novel boronic acid inhibitors reveals important interactions with a clavulanic acid-resistant sulfhydryl-variable (SHV) βlactamase. J Med Chem 2013; 56: 1084-97.
48. Helfand MS, Hujer AM, Sonnichsen FD et al. Unexpected advanced generation cephalosporinase activity of the M69F variant of SHV βlactamase. J Biol Chem 2002; 277: 47719-23.