Structural insight into potent broad-spectrum inhibition with reversible recyclization mechanism: Avibactam in complex with CTX-M-15 and pseudomonas aeruginosa AmpC β-lactamases

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 6, 2013, Pages 2496-2505

  Lahiri, Sushmita D ^a   Mangani, Stefano ^b   Durand Reville, Thomas ^a   Benvenuti, Manuela ^b   De Luca, Filomena ^b   Sanyal, Gautam ^a   Docquier, Jean Denis ^b  

^a ASTRAZENECA   (United Kingdom)

^b UNIVERSITY OF SIENA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AVIBACTAM; BETA LACTAMASE AMPC; CTX M 15; EXTENDED SPECTRUM BETA LACTAMASE; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; ARTICLE; CRYSTALLIZATION; DRUG STRUCTURE; ENZYME BINDING; IN VITRO STUDY; NONHUMAN; PARAMETERS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; PSEUDOMONAS AERUGINOSA;

ACYLATION; ANTI-BACTERIAL AGENTS; AZABICYCLO COMPOUNDS; BACTERIAL PROTEINS; BETA-LACTAMASES; BETA-LACTAMS; BINDING SITES; CRYSTALLIZATION; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PSEUDOMONAS AERUGINOSA; STRUCTURE-ACTIVITY RELATIONSHIP; X-RAY DIFFRACTION;

EID: 84877842576     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02247-12     Document Type: Article

References (46)

1. Nordmann P, Naas T, Poirel L. 2011. Global spread of carbapenemaseproducing Enterobacteriaceae. Emerg. Infect. Dis. 17:1791-1798.
2. Borer A, Saidel-Odes L, Riesenberg K, Eskira S, Peled N, Nativ R, Schlaeffer F, Sherf M. 2009. Attributable mortality rate for carbapenemresistant Klebsiella pneumoniae bacteremia. Infect. Control Hosp. Epidemiol. 30:972-976.
3. Snitkin ES, Zelazny AM, Thomas PJ, Stock F, NISC Comparative Sequencing Program, Henderson DK, Palmore TN, Segre JA. 2012. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci. Transl. Med. 4:148ra116. doi:10.1126/scitranslmed.3004129.
4. Kanoksil M, Jatapai A, Peacock SJ, Limmathurotsakul D. 2013. Epidemiology, microbiology and mortality associated with communityacquired bacteremia in northeast Thailand: A multicenter surveillance study. PLoS One 8:e54714. doi:10.1371/journal.pone.0054714.
5. Patel G, Bonomo RA. 2011. Status report on carbapenemases: Challenges and prospects. Expert Rev. Anti Infect. Ther. 9:555-570.
6. Neuner EA, Yeh JY, Hall GS, Sekeres J, Endimiani A, Bonomo RA, Shrestha NK, Fraser TG, van Duin D. 2011. Treatment and outcomes in carbapenem-resistant Klebsiella pneumoniae bloodstream infections. Diagn. Microbiol. Infect. Dis. 69:357-362.
7. Bush K. 2010. The coming of age of antibiotics: Discovery and therapeutic value. Ann. N. Y. Acad. Sci. 1213:1-4.
8. Bush K, Fisher JF. 2011. Epidemiological expansion, structural studies, and clinical challenges of new beta-lactamases from gram-negative bacteria. Annu. Rev. Microbiol. 65:455-478.
9. Bebrone C, Lassaux P, Vercheval L, Sohier J, Jehaes A, Sauvage E, Galleni M. 2010. Current challenges in antimicrobial chemotherapy: Focus on beta-lactamase inhibition. Drugs 70:651-679.
10. Bush K. 2010. Bench-to-bedside review: The role of beta-lactamases in antibiotic-resistant Gram-negative infections. Crit. Care 14:224.
11. Biondi S, Long S, Panunzio M, Qin WL. 2011. Current trends in betalactam based beta-lactamases inhibitors. Curr. Med. Chem. 18:4223-4236.
12. Totir MA, Cha J, Ishiwata A, Wang B, Sheri A, Anderson VE, Buynak J, Mobashery S, Carey PR. 2008. Why clinically used tazobactam and sulbactam are poor inhibitors of OXA-10 beta-lactamase: Raman crystallographic evidence. Biochemistry 47:4094-4101.
13. Bush K. 2012. Improving known classes of antibiotics: An optimistic approach for the future. Curr. Opin. Pharmacol. 12:527-534.
14. Bush K, Macielag MJ. 2010. New beta-lactam antibiotics and betalactamase inhibitors. Expert Opin. Ther. Pat. 20:1277-1293.
15. Bonnefoy A, Dupuis-Hamelin C, Steier V, Delachaume C, Seys C, Stachyra T, Fairley M, Guitton M, Lampilas M. 2004. In vitro activity of AVE1330A, an innovative broad-spectrum non-beta-lactam betalactamase inhibitor. J. Antimicrob. Chemother. 54:410-417.
16. Stachyra T, Levasseur P, Pechereau MC, Girard AM, Claudon M, Miossec C, Black MT. 2009. In vitro activity of the β-lactamase inhibitor NXL104 against KPC-2 carbapenemase and Enterobacteriaceae expressing KPC carbapenemases. J. Antimicrob. Chemother. 64:326-329.
17. Coleman K. 2011. Diazabicyclooctanes (DBOs): A potent new class of non-beta-lactam beta-lactamase inhibitors. Curr. Opin. Microbiol. 14: 550-555.
18. Aszodi J, Rowlands DA, Mauvais P, Collette P, Bonnefoy A, Lampilas M. 2004. Design and synthesis of bridged gamma-lactams as analogues of beta-lactam antibiotics. Bioorg. Med. Chem. Lett. 14:2489-2492.
19. Wiskirchen DE, Crandon JL, Furtado GH, Williams G, Nicolau DP. 2011. In vivo efficacy of a human-simulated regimen of ceftaroline combined with NXL104 against extended-spectrum-beta-lactamase (ESBL)-producing and non-ESBL-producing Enterobacteriaceae. Antimicrob. Agents Chemother. 55:3220-3225.
20. Cattoir V. 2011. NXL-104, a novel beta-lactamase inhibitor with broadspectrum activity. J. Anti-Infect. 13:20-24.
21. Aktas Z, Kayacan C, Oncul O. 2012. In vitro activity of avibactam (NXL104) in combination with beta-lactams against Gram-negative bacteria, including OXA-48 beta-lactamase-producing Klebsiella pneumoniae. Int. J. Antimicrob. Agents 39:86-89.
22. Endimiani A, Hujer KM, Hujer AM, Pulse ME, Weiss WJ, Bonomo RA. 2011. Evaluation of ceftazidime and NXL104 in two murine models of infection due to KPC-producing Klebsiella pneumoniae. Antimicrob. Agents Chemother. 55:82-85.
23. Stachyra T, Pechereau MC, Bruneau JM, Claudon M, Frere JM, Miossec C, Coleman K, Black MT. 2010. Mechanistic studies of the inactivation of TEM-1 and P99 by NXL104, a novel non-beta-lactam beta-lactamase inhibitor. Antimicrob. Agents Chemother. 54:5132-5138.
24. Citron DM, Tyrrell KL, Merriam V, Goldstein EJ. 2011. In vitro activity of ceftazidime-NXL104 against 396 strains of beta-lactamase-producing anaerobes. Antimicrob. Agents Chemother. 55:3616-3620.
25. Ehmann DE, Jahic H, Ross PL, Gu RF, Hu J, Kern G, Walkup GK, Fisher SL. 2012. Avibactam is a covalent, reversible, non-beta-lactam beta-lactamase inhibitor. Proc. Natl. Acad. Sci. U. S. A. 109:11663-11668.
26. Drawz SM, Bonomo RA. 2010. Three decades of beta-lactamase inhibitors. Clin. Microbiol. Rev. 23:160-201.
27. Docquier JD, Lamotte-Brasseur J, Galleni M, Amicosante G, Frere JM, Rossolini GM. 2003. On functional and structural heterogeneity of VIMtype metallo-beta-lactamases. J. Antimicrob. Chemother. 51:257-266.
28. Studier FW. 2005. Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41:207-234.
29. Benvenuti M, Mangani S. 2007. Crystallization of soluble proteins in vapor diffusion for X-ray crystallography. Nat. Protoc. 2:1633-1651.
30. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS. 2011. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67:235-242.
31. Smart OS, Womack TO, Flensburg C, Keller P, Paciorek W, Sharff A, Vonrhein C, Bricogne G. 2012. Exploiting structure similarity in refinement: Automated NCS and target-structure restraints in BUSTER. Acta Crystallogr. D Biol. Crystallogr. 68:368-380.
32. Emsley P, Cowtan K. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
33. DeLano WL. 2002. The PyMOL molecular graphics system. DeLano Scientific, San Carlos, CA.
34. Frase H, Smith CA, Toth M, Champion MM, Mobashery S, Vakulenko SB. 2011. Identification of products of inhibition of GES-2 beta-lactamase by tazobactam by X-ray crystallography and spectrometry. J. Biol. Chem. 286:14396-14409.
35. Delmas J, Chen Y, Prati F, Robin F, Shoichet BK, Bonnet R. 2008. Structure and dynamics of CTX-M enzymes reveal insights into substrate accommodation by extended-spectrum beta-lactamases. J. Mol. Biol. 375: 192-201.
36. Minasov G, Wang X, Shoichet BK. 2002. An ultrahigh resolution structure of TEM-1 beta-lactamase suggests a role for Glu166 as the general base in acylation. J. Am. Chem. Soc. 124:5333-5340.
37. Beadle BM, Trehan I, Focia PJ, Shoichet BK. 2002. Structural milestones in the reaction pathway of an amide hydrolase: Substrate, acyl, and product complexes of cephalothin with AmpC beta-lactamase. Structure 10: 413-424.
38. Meroueh SO, Minasov G, Lee W, Shoichet BK, Mobashery S. 2003. Structural aspects for evolution of beta-lactamases from penicillinbinding proteins. J. Am. Chem. Soc. 125:9612-9618.
39. Jacoby GA. 2009. AmpC beta-lactamases. Clin. Microbiol. Rev. 22:161-182.
40. Beadle BM, Shoichet BK. 2002. Structural basis for imipenem inhibition of class C beta-lactamases. Antimicrob. Agents Chemother. 46:3978-3980.
41. Xu H, Hazra S, Blanchard JS. 2012. NXL104 irreversibly inhibits the beta-lactamase from Mycobacterium tuberculosis. Biochemistry 51: 4551-4557.
42. Chen Y, Shoichet B, Bonnet R. 2005. Structure, function, and inhibition along the reaction coordinate of CTX-M beta-lactamases. J. Am. Chem. Soc. 127:5423-5434.
43. Johnson, F. 1968. Allylic strain in six-membered rings. Chem. Rev. 68: 375.
44. Bürgi HB, Dunitz JD, Shefter E. 1973. Geometrical reaction coordinates. II. Nucleophilic addition to a carbonyl group. J. Am. Chem. Soc. 95:5065-5067.
45. Wilmouth RC, Kassamally S, Westwood NJ, Sheppard RJ, Claridge TD, Aplin RT, Wright PA, Pritchard GJ, Schofield CJ. 1999. Mechanistic insights into the inhibition of serine proteases by monocyclic lactams. Biochemistry 38:7989-7998.
46. Kaur K, Lan MJ, Pratt RF. 2001. Mechanism of inhibition of the class C beta-lactamase of Enterobacter cloacae P99 by cyclic acyl phosph(on)ates: Rescue by return. J. Am. Chem. Soc. 123:10436-10443.