Structural insights into the TLA-3 extended-spectrum β-lactamase and its inhibition by avibactam and OP0595

Antimicrobial Agents and Chemotherapy

Volumn 61, Issue 10, 2017, Pages

  Jin, Wanchun ^a   Wachino, Jun Ichi ^a   Yamaguchi, Yoshihiro ^b   Kimura, Kouji ^a   Kumar, Anupriya ^a   Yamada, Mototsugu ^c   Morinaka, Akihiro ^c   Sakamaki, Yoshiaki ^c   Yonezawa, Minoru ^c   Kurosaki, Hiromasa ^d   Arakawa, Yoshichika ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

^c MEIJI SEIKA KAISHA LTD   (Japan)

^d KINJO GAKUIN UNIVERSITY   (Japan)

Author keywords

Avibactam; Crystal structure; Diazabicyclooctane; ESBL; Extended spectrum lactamase; OP0595; TLA 3

Indexed keywords

AMINO ACID; AVIBACTAM; CEPHALOSPORIN DERIVATIVE; NACUBACTAM; PENICILLINASE; SULFATE; TLA 3 EXTENDED SPECTRUM BETA LACTAMASE; UNCLASSIFIED DRUG; AZABICYCLO DERIVATIVE; BETA LACTAMASE; BETA LACTAMASE INHIBITOR; LACTAM;

ACYLATION; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; COVALENT BOND; DRUG EFFECT; DRUG INHIBITION; ENZYME INHIBITION; EQUILIBRIUM CONSTANT; ESCHERICHIA COLI; EXTENDED SPECTRUM BETA LACTAMASE PRODUCING ENTEROBACTERIACEAE; NONHUMAN; PRIORITY JOURNAL; RATE CONSTANT; ENZYME ACTIVE SITE; HUMAN; METABOLISM; MICROBIAL SENSITIVITY TEST; X RAY CRYSTALLOGRAPHY;

AZABICYCLO COMPOUNDS; BETA-LACTAMASE INHIBITORS; BETA-LACTAMASES; CATALYTIC DOMAIN; CEPHALOSPORINS; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; HUMANS; LACTAMS; MICROBIAL SENSITIVITY TESTS;

EID: 85029766785     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00501-17     Document Type: Article

References (37)

1. Lukac PJ, Bonomo RA, Logan LK. 2015. Extended-spectrum β-lactamase-producing Enterobacteriaceae in children: old foe, emerging threat. Clin Infect Dis 60:1389–1397. https://doi.org/10.1093/cid/civ020.
2. Oteo J, Perez-Vazquez M, Campos J. 2010. Extended-spectrum β-lactamase producing Escherichia coli: changing epidemiology and clinical impact. Curr Opin Infect Dis 23:320–326. https://doi.org/10.1097/QCO.0b013e3283398dc1.
3. Michael GB, Kaspar H, Siqueira AK, de Freitas Costa E, Corbellini LG, Kadlec K, Schwarz S. 2017. Extended-spectrum β-lactamase (ESBL)producing Escherichia coli isolates collected from diseased food-producing animals in the GERM-Vet monitoring program 2008-2014. Vet Microbiol 200:142–150. https://doi.org/10.1016/j.vetmic.2016.08.023.
4. Canton R, Gonzalez-Alba JM, Galan JC. 2012. CTX-M enzymes: origin and diffusion. Front Microbiol 3:110. https://doi.org/10.3389/fmicb.2012.00110.
5. Naas T, Poirel L, Nordmann P. 2008. Minor extended-spectrum β-lactamases. Clin Microbiol Infect 14(Suppl 1):42–52. https://doi.org/10.1111/j.1469-0691.2007.01861.x.
6. Silva J, Aguilar C, Ayala G, Estrada MA, Garza-Ramos U, Lara-Lemus R, Ledezma L. 2000. TLA-1: a new plasmid-mediated extended-spectrum β-lactamase from Escherichia coli. Antimicrob Agents Chemother 44: 997–1003. https://doi.org/10.1128/AAC.44.4.997-1003.2000.
7. Girlich D, Poirel L, Schluter A, Nordmann P. 2005. TLA-2, a novel Ambler class A expanded-spectrum β-lactamase. Antimicrob Agents Chemother 49:4767–4770. https://doi.org/10.1128/AAC.49.11.4767-4770.2005.
8. Jin W, Wachino J, Kimura K, Yamada K, Arakawa Y. 2015. New plasmid-mediated aminoglycoside 6=-N-acetyltransferase, AAC(6=)-Ian, and ESBL, TLA-3, from a Serratia marcescens clinical isolate. J Antimicrob Chemother 70:1331–1337. https://doi.org/10.1093/jac/dku537.
9. Bush K. 2015. A resurgence of β-lactamase inhibitor combinations effective against multidrug-resistant Gram-negative pathogens. Int J Antimicrob Agents 46:483–493. https://doi.org/10.1016/j.ijantimicag.2015.08.011.
10. 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-β-lactam β-lactamase inhibitor. J Antimicrob Chemother 54:410 – 417. https://doi.org/10.1093/jac/dkh358.
11. Blizzard TA, Chen H, Kim S, Wu J, Bodner R, Gude C, Imbriglio J, Young K, Park YW, Ogawa A, Raghoobar S, Hairston N, Painter RE, Wisniewski D, Scapin G, Fitzgerald P, Sharma N, Lu J, Ha S, Hermes J, Hammond ML. 2014. Discovery of MK-7655, a β-lactamase inhibitor for combination with Primaxin(R). Bioorg Med Chem Lett 24:780–785. https://doi.org/10.1016/j.bmcl.2013.12.101.
12. Morinaka A, Tsutsumi Y, Yamada M, Suzuki K, Watanabe T, Abe T, Furuuchi T, Inamura S, Sakamaki Y, Mitsuhashi N, Ida T, Livermore DM. 2015. OP0595, a new diazabicyclooctane: mode of action as a serine β-lactamase inhibitor, antibiotic and β-lactam ‘enhancer.’ J Antimicrob Chemother 70:2779–2786. https://doi.org/10.1093/jac/dkv166.
13. Falcone M, Paterson D. 2016. Spotlight on ceftazidime/avibactam: a new option for MDR Gram-negative infections. J Antimicrob Chemother 71: 2713–2722. https://doi.org/10.1093/jac/dkw239.
14. Morinaka A, Tsutsumi Y, Yamada K, Takayama Y, Sakakibara S, Takata T, Abe T, Furuuchi T, Inamura S, Sakamaki Y, Tsujii N, Ida T. 2016. In vitro and in vivo activities of OP0595, a new diazabicyclooctane, against CTX-M-15-positive Escherichia coli and KPC-positive Klebsiella pneumoniae. Antimicrob Agents Chemother 60:3001–3006. https://doi.org/10.1128/AAC.02704-15.
15. Krishnan NP, Nguyen NQ, Papp-Wallace KM, Bonomo RA, van den Akker F. 2015. Inhibition of Klebsiella β-lactamases (SHV-1 and KPC-2) by avibactam: a structural study. PLoS One 10:e0136813. https://doi.org/10.1371/journal.pone.0136813.
16. Lahiri SD, Mangani S, Durand-Reville T, Benvenuti M, De Luca F, Sanyal G, Docquier JD. 2013. Structural insight into potent broad-spectrum inhibition with reversible recyclization mechanism: avibactam in complex with CTX-M-15 and Pseudomonas aeruginosa AmpC β-lactamases. Antimicrob Agents Chemother 57:2496–2505. https://doi.org/10.1128/AAC.02247-12.
17. Ruggiero M, Papp-Wallace KM, Taracila MA, Mojica MF, Bethel CR, Rudin SD, Zeiser ET, Gutkind G, Bonomo RA, Power P. 2017. Exploring the landscape of diazabicyclooctane inhibition: avibactam inactivation of PER-2 β-lactamase. Antimicrob Agents Chemother 61:e02476-16. https://doi.org/10.1128/AAC.02476-16.
18. Winkler ML, Papp-Wallace KM, Taracila MA, Bonomo RA. 2015. Avibactam and inhibitor-resistant SHV β-lactamases. Antimicrob Agents Chemother 59:3700–3709. https://doi.org/10.1128/AAC.04405-14.
19. Ehmann DE, Jahic H, Ross PL, Gu RF, Hu J, Durand-Reville TF, Lahiri S, Thresher J, Livchak S, Gao N, Palmer T, Walkup GK, Fisher SL. 2013. Kinetics of avibactam inhibition against class A, C, and D β-lactamases. J Biol Chem 288:27960–27971. https://doi.org/10.1074/jbc.M113.485979.
20. Ehmann DE, Jahic H, Ross PL, Gu RF, Hu J, Kern G, Walkup GK, Fisher SL. 2012. Avibactam is a covalent, reversible, non-β-lactam β-lactamase inhibitor. Proc Natl Acad Sci U S A 109:11663–11668. https://doi.org/10.1073/pnas.1205073109.
21. Ruggiero M, Kerff F, Herman R, Sapunaric F, Galleni M, Gutkind G, Charlier P, Sauvage E, Power P. 2014. Crystal structure of the extended-spectrum β-lactamase PER-2 and insights into the role of specific residues in the interaction with β-lactams and β-lactamase inhibitors. Antimicrob Agents Chemother 58:5994 – 6002. https://doi.org/10.1128/AAC.00089-14.
22. Adamski CJ, Cardenas AM, Brown NG, Horton LB, Sankaran B, Prasad BV, Gilbert HF, Palzkill T. 2015. Molecular basis for the catalytic specificity of the CTX-M extended-spectrum β-lactamases. Biochemistry 54:447–457. https://doi.org/10.1021/bi501195g.
23. Bouthors AT, Delettre J, Mugnier P, Jarlier V, Sougakoff W. 1999. Site-directed mutagenesis of residues 164, 170, 171, 179, 220, 237 and 242 in PER-1 β-lactamase hydrolysing expanded-spectrum cephalosporins. Protein Eng 12:313–318. https://doi.org/10.1093/protein/12.4.313.
24. King DT, King AM, Lal SM, Wright GD, Strynadka NC. 2015. Molecular mechanism of avibactam-mediated β-lactamase inhibition. ACS Infect Dis 1:175–184. https://doi.org/10.1021/acsinfecdis.5b00007.
25. Livermore DM, Mushtaq S, Warner M, Woodford N. 2015. Activity of OP0595/β-lactam combinations against Gram-negative bacteria with extended-spectrum, AmpC and carbapenem-hydrolysing β-lactamases. J Antimicrob Chemother 70:3032–3041. https://doi.org/10.1093/jac/dkv239.
26. Karlowsky JA, Biedenbach DJ, Kazmierczak KM, Stone GG, Sahm DF. 2016. Activity of ceftazidime-avibactam against extended-spectrum- and AmpC β-lactamase-producing Enterobacteriaceae collected in the INFORM Global Surveillance Study from 2012 to 2014. Antimicrob Agents Chemother 60:2849 –2857. https://doi.org/10.1128/AAC.02286-15.
27. Papp-Wallace KM, Winkler ML, Gatta JA, Taracila MA, Chilakala S, Xu Y, Johnson JK, Bonomo RA. 2014. Reclaiming the efficacy of β-lactam–β-lactamase inhibitor combinations: avibactam restores the susceptibility of CMY-2-producing Escherichia coli to ceftazidime. Antimicrob Agents Chemother 58:4290–4297. https://doi.org/10.1128/AAC.02625-14.
28. Clinical and Laboratory Standards Institute. 2012. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard, 9th ed. Document M07-A9. Clinical and Laboratory Standards Institute, Wayne, PA.
29. Watanabe N, Nagae T, Yamada Y, Tomita A, Matsugaki N, Tabuchi M. 2017. Protein crystallography beamline BL2S1 at the Aichi Synchrotron. J Synchrotron Radiat 24:338–343. https://doi.org/10.1107/S1600577516018579.
30. Battye TG, Kontogiannis L, Johnson O, Powell HR, Leslie AG. 2011. iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr D Biol Crystallogr 67:271–281. https://doi.org/10.1107/S0907444910048675.
31. Evans P. 2006. Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62:72–82. https://doi.org/10.1107/S0907444905036693.
32. Vagin A, Teplyakov A. 2010. Molecular replacement with MOLREP. Acta Crystallogr D Biol Crystallogr 66:22–25. https://doi.org/10.1107/S0907444909042589.
33. Tranier S, Bouthors AT, Maveyraud L, Guillet V, Sougakoff W, Samama JP. 2000. The high resolution crystal structure for class A β-lactamase PER-1 reveals the bases for its increase in breadth of activity. J Biol Chem 275:28075–28082.
34. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126–2132. https://doi.org/10.1107/S0907444904019158.
35. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53:240 –255. https://doi.org/10.1107/S0907444996012255.
36. Lovell SC, Davis IW, Arendall WB, III, de Bakker PI, Word JM, Prisant MG, Richardson JS, Richardson DC. 2003. Structure validation by Cα geometry: φ, ψ and Cβ deviation. Proteins 50:437–450. https://doi.org/10.1002/prot.10286.
37. Schrödinger. 2016. Schrödinger release 2016-1. Schrödinger, LLC, New York, NY.