Crystal structure of OXA-58 with the substrate-binding cleft in a closed state: Insights into the mobility and stability of the OXA-58 structure

PLoS ONE

Volumn 10, Issue 12, 2015, Pages

  Saino, Hiromichi ^a   Sugiyabu, Tomohiro ^a   Ueno, Go ^b   Yamamoto, Masaki ^b   Ishii, Yoshikazu ^c   Miyano, Masashi ^a  

^a AOYAMA GAKUIN UNIVERSITY   (Japan)

^b RIKEN SPring 8 Center   (Japan)

^c TOHO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAMASE; BETA LACTAMASE OXA 58; BICARBONATE; CARBAMIC ACID; HYDROGEN; LYSINE; METHIONINE; PHENYLALANINE; SERINE; TRYPTOPHAN; UNCLASSIFIED DRUG; BETA LACTAM; BETA-LACTAMASE OXA-58, ACINETOBACTER BAUMANNII;

ACINETOBACTER BAUMANNII; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME PURIFICATION; ENZYME STABILITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; HYDROGEN BOND; HYDROLYSIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INTERACTION; BINDING SITE; CATALYSIS; CHEMISTRY; ENZYME ACTIVE SITE; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

BETA-LACTAMASES; BETA-LACTAMS; BINDING SITES; CATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HYDROGEN BONDING; HYDROLYSIS; MODELS, MOLECULAR; PROTEIN CONFORMATION;

EID: 84957054428     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0145869     Document Type: Article

References (42)

1. Verma V, Testero SA, Amini K, Wei W, Liu J, Balachandran N, et al. Hydrolytic mechanism of OXA-58 enzyme, a carbapenem-hydrolyzing class D β-lactamase from Acinetobacter baumannii. J Biol Chem. 2011; 286: 37292-37303. doi: 10.1074/jbc.M111.280115 PMID: 21880707
2. Poirel L, Marqué S, Héritier C, Segonds C, Chabanon G, Nordmann P. OXA-58, a novel class D β-lactamase involved in resistance to carbapenems in Acinetobacter baumannii. Antimicrob Agents Chemother. 2005; 49: 202-208. PMID: 15616297
3. Queenan AM, Bush K. Carbapenemases: The versatile β-lactamases. Clin Microbiol Rev. 2007; 20: 440-458 PMID: 17630334
4. El Garch F, Bogaerts P, Bebrone C, Galleni M, Glupczynski Y. OXA-198, an acquired carbapenem-hydrolyzing class D β-lactamase from Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2011; 55: 4828-4833. doi: 10.1128/AAC.00522-11 PMID: 21788473
5. Antunes NT, Lamoureaux TL, Toth M, Stewart NK, Frase H, Vakulenko SB. Class D β-lactamases: Are they all carbapenemases? Antimicrob Agents Chemother. 2014; 58: 2119-2125. doi: 10.1128/AAC.02522-13 PMID: 24468778
6. Walsh TR Emerging carbapenemases: A global perspective. Int J Antimicrob Agents. 2010; 36 Suppl 3: S8-S14. doi: 10.1016/S0924-8579(10)70004-2 PMID: 21129630
7. Higgins PG, Dammhayn C, Hackel M, Seifert H. Global spread of carbapenem-resistant Acinetobacter baumannii. J Antimicrob Chemother. 2010; 65: 233-238. doi: 10.1093/jac/dkp428 PMID: 19996144
8. Ehmann DE, Jahic H, Ross PL, Gu RF, Hu J, Durand-Re´ville TF, et al. Kinetics of avibactam inhibition against class A, C, and D β-lactamases. J Biol Chem. 2013; 288: 27960-27971. doi: 10.1074/jbc.M113.485979 PMID: 23913691
9. Ehmann DE, Jahić H, Ross PL, Gu RF, Hu J, Kern G, et al. Avibactam is a covalent, reversible, non-β-lactam β-lactamase inhibitor. Proc Natl Acad Sci U S A. 2012; 109: 11663-11668. doi: 10.1073/pnas.1205073109 PMID: 22753474
10. Banerjee S, Pieper U, Kapadia G, Pannell LK, Herzberg O. Role of the omega-loop in the activity, substrate specificity, and structure of class A β-lactamase. Biochemistry. 1998; 37: 3286-3296. PMID: 9521648
11. Nukaga M, Taniguchi K, Washio Y, Sawai T. Effect of an amino acid insertion into the omega loop region of a class C β-lactamase on its substrate specificity. Biochemistry. 1998; 37: 10461-10468. PMID: 9671516
12. Thomas VL, McReynolds AC, Shoichet BK. Structural bases for stability-function tradeoffs in antibiotic resistance. J Mol Biol. 2010; 396: 47-59. doi: 10.1016/j.jmb.2009.11.005 PMID: 19913034
13. Shimamura T, Ibuka A, Fushinobu S, Wakagi T, Ishiguro M, Ishii Y, et al. Acyl-intermediate structures of the extended-spectrum class A β-lactamase, toho-1, in complex with cefotaxime, cephalothin, and benzylpenicillin. J Biol Chem. 2002; 277: 46601-46608. PMID: 12221102
14. m) of the class A β-lactamase toho-1 correlates with the thermal stability of its catalytic intermediate analog. Biochim Biophys Acta. 2010; 1804: 684-691. doi: 10.1016/j.bbapap.2009.10.023 PMID: 19883800
15. Ibuka AS, Ishii Y, Galleni M, Ishiguro M, Yamaguchi K, Frère JM, et al. Crystal structure of extended-spectrum β-lactamase toho-1: Insights into the molecular mechanism for catalytic reaction and substrate specificity expansion. Biochemistry. 2003; 42: 10634-10643. PMID: 12962487
16. Schneider KD, Ortega CJ, Renck NA, Bonomo RA, Powers RA, Leonard DA. Structures of the class D carbapenemase OXA-24 from Acinetobacter baumannii in complex with doripenem. J Mol Biol. 2011; 406: 583-594. doi: 10.1016/j.jmb.2010.12.042 PMID: 21215758
17. Docquier JD, Benvenuti M, Calderone V, Giuliani F, Kapetis D, De Luca F, et al. Crystal structure of the narrow-spectrum OXA-46 class D β-lactamase: Relationship between active-site lysine carbamylation and inhibition by polycarboxylates. Antimicrob Agents Chemother. 2010; 54: 2167-2174. doi: 10.1128/AAC.01517-09 PMID: 20145076
18. Docquier JD, Calderone V, De Luca F, Benvenuti M, Giuliani F, Bellucci L, et al. Crystal structure of the OXA-48 β-lactamase reveals mechanistic diversity among class D carbapenemases. Chem Biol. 2009; 16: 540-547. doi: 10.1016/j.chembiol.2009.04.010 PMID: 19477418
19. Santillana E, Beceiro A, Bou G, Romero A. Crystal structure of the carbapenemase OXA-24 reveals insights into the mechanism of carbapenem hydrolysis. Proc Natl Acad Sci U S A. 2007; 104: 5354-5359. PMID: 17374723
20. Paetzel M, Danel F, de Castro L, Mosimann SC, Page MG, Strynadka NC. Crystal structure of the class D β-lactamase OXA-10. Nat Struct Mol Biol. 2000; 7: 918-925.
21. Smith CA, Antunes NT, Toth M, Vakulenko SB. Crystal structure of carbapenemase OXA-58 from acinetobacter baumannii. Antimicrob Agents Chemother. 2014; 58: 2135-2143. doi: 10.1128/AAC.01983-13 PMID: 24468777
22. Golemi D, Maveyraud L, Vakulenko S, Samama JP, Mobashery S. Critical involvement of a carbamylated lysine in catalytic function of class D β-lactamases. Proc Natl Acad Sci U S A. 2001; 98: 14280-14285. PMID: 11724923
23. Sun T, Nukaga M, Mayama K, Braswell EH, Knox JR. Comparison of β-lactamases of classes A and D: 1.5-Å crystallographic structure of the class D OXA-1 oxacillinase. Protein Sci. 2003; 12: 82-91. PMID: 12493831
24. Buchman JS, Schneider KD, Lloyd AR, Pavlish SL, Leonard DA. Site-Saturation mutagenesis of position V117 in OXA-1 β-lactamase: Effect of side chain polarity on enzyme carboxylation and substrate turnover. Biochemistry. 2012; 51: 3143-3150. doi: 10.1021/bi201896k PMID: 22429123
25. Baurin S, Vercheval L, Bouillenne F, Falzone C, Brans A, Jacquamet L, et al. Critical role of tryptophan 154 for the activity and stability of class D β-lactamases. Biochemistry. 2009; 48: 11252-11263. doi: 10.1021/bi901548c PMID: 19860471
26. Beaver WL, Wasserman K, Whipp BJ. A new method for detecting anaerobic threshold by gas exchange. J Appl Physiol. 1986; 60: 2020-2027. PMID: 3087938
27. Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB. Nosocomial bloodstream infections in US hospitals: Analysis of 24,179 cases from a prospective nationwide surveillance study. Clinical Infectious Diseases. 2004; 39: 309-317. PMID: 15306996
28. Yoshizumi A, Ishii Y, Aoki K, Testa R, Nichols WW, Tateda K. In vitro susceptibility of characterized β-lactamase-producing gram-negative bacteria isolated in japan to ceftazidime-, ceftaroline-, and aztreonam-avibactam combinations. J Infect Chemother. 2015; 21: 148-151. doi: 10.1016/j.jiac.2014.08.028 PMID: 25444674
29. Okazaki N, Hasegawa K, Ueno G, Murakami H, Kumasaka T, Yamamoto M. Mail-in data collection at spring-8 protein crystallography beamlines. J Synchrotron Radiat. 2008; 15: 288-291. doi: 10.1107/S0909049507064679 PMID: 18421161
30. Powell HR The rossmann fourier autoindexing algorithm in MOSFLM. Acta Crystallogr D Biol Crystallogr. 1999; 55: 1690-1695. PMID: 10531518
31. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, et al. Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr. 2011; 67: 235-242. doi: 10.1107/S0907444910045749 PMID: 21460441
32. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. Phaser crystallographic software. J Appl Crystallogr. 2007; 40: 658-674. PMID: 19461840
33. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, et al. PHENIX: A comprehensive python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr. 2010; 66: 213-221. doi: 10.1107/S0907444909052925 PMID: 20124702
34. Afonine PV, Grosse-Kunstleve RW, Adams PD, Urzhumtsev A. Bulk-solvent and overall scaling revisited: Faster calculations, improved results. Acta Crystallogr D Biol Crystallogr. 2013; 69: 625-634. doi:10.1107/S0907444913000462 PMID: 23519671
35. Afonine PV, Grosse-Kunstleve RW, Echols N, Headd JJ, Moriarty NW, Mustyakimov M, et al. Towards automated crystallographic structure refinement with phenix.Refine. Acta Crystallogr D Biol Crystallogr. 2012; 68: 352-367. doi: 10.1107/S0907444912001308 PMID: 22505256
36. Afonine PV, Grosse-Kunstleve RW, Urzhumtsev A, Adams PD. Automatic multiple-zone rigid-body refinement with a large convergence radius. J Appl Crystallogr. 2009; 42: 607-615. PMID: 19649324
37. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of coot. Acta Crystallogr D Biol Crystallogr. 2010; 66: 486-501. doi: 10.1107/S0907444910007493 PMID: 20383002
38. DeLano WL Pymol: An open-source molecular graphics tool. CCP4 Newsletter On Protein Crystallography. 2002; 40.
39. The Pymol Molecular Graphics System, Version 1.7 Schrödinger, LLC. 2014;.
40. Thomas W, Colin K, Gnuplot 5.0 an interactive plotting program. 2015; Available: http://www.gnuplot.info/.
41. Smith CA, Antunes NT, Stewart NK, Toth M, Kumarasiri M, Chang M, et al. Structural basis for carbapenemase activity of the OXA-23 β-lactamase from acinetobacter baumannii. Chem Biol. 2013; 20: 1107-1115. doi: 10.1016/j.chembiol.2013.07.015 PMID: 24012371
42. June CM, Vallier BC, Bonomo RA, Leonard DA, Powers RA. Structural origins of oxacillinase specificity in class D β-lactamases. Antimicrob Agents Chemother. 2014; 58: 333-341. doi: 10.1128/AAC.01483-13 PMID: 24165180