Structural origins of oxacillinase specificity in class D β-lactamases

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 1, 2014, Pages 333-341

  June, Cynthia M ^a   Vallier, Beth C ^a   Bonomo, Robert A ^b,c   Leonard, David A ^a   Powers, Rachel A ^a  

^a GRAND VALLEY STATE UNIVERSITY   (United States)

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

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

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; BETA LACTAMASE; CARBAPENEMASE; CEPHALOSPORINASE; LEUCINE; LYSINE; METHIONINE; OXACILLIN; OXACILLINASE 1; OXACILLINASE 24; OXACILLINASE 40; PHENYLALANINE; TRYPTOPHAN; TYROSINE; UNCLASSIFIED DRUG;

ACINETOBACTER BAUMANNII; ARTICLE; COMPARATIVE STUDY; CRYSTAL STRUCTURE; DEACYLATION; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; HYDROGEN BOND; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; PSEUDOMONAS AERUGINOSA; X RAY;

BACTERIAL PROTEINS; BETA-LACTAMASES; CATALYTIC DOMAIN; CEPHALOSPORINASE; CRYSTALLOGRAPHY, X-RAY; OXACILLIN; SUBSTRATE SPECIFICITY;

EID: 84891539971     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01483-13     Document Type: Article

References (38)

1. Neu HC. 1992. The crisis in antibiotic resistance. Science 257:1064-1073. http://dx.doi.org/10.1126/science.257.5073.1064.
2. Davies J. 1994. Inactivation of antibiotics and the dissemination of resistance genes. Science 264:375-382. http://dx.doi.org/10.1126/science. 8153624.
3. Fisher JF, Meroueh SO, Mobashery S. 2005. Bacterial resistance to β-lactam antibiotics: Compelling opportunism, compelling opportunity. Chem. Rev. 105:395-424. http://dx.doi.org/10.1021/cr030102i.
4. Bush K, Jacoby GA. 2010. Updated functional classification of β-lactamases. Antimicrob. Agents Chemother. 54:969-976. http://dx.doi.org/10 .1128/AAC.01009-09.
5. Bush K, Jacoby GA, Medeiros AA. 1995. A functional classification scheme for β-lactamases and its correlation with molecular structure. Antimicrob. Agents Chemother. 39:1211-1233. http://dx.doi.org/10.1128 /AAC.39.6.1211.
6. Perez F, Hujer AM, Hujer KM, Decker BK, Rather PN, Bonomo RA. 2007. Global challenge of multidrug-resistant Acinetobacter baumannii. Antimicrob. Agents Chemother. 51:3471-3484. http://dx.doi.org/10.1128 /AAC.01464-06.
7. Hedges RW, Datta N, Kontomichalou P, Smith JT. 1974. Molecular specificities of R factor-determined β-lactamases: Correlation with plasmid compatibility. J. Bacteriol. 117:56-62.
8. Ledent P, Raquet X, Joris B, Van Beeumen J, Frere JM. 1993. A comparative study of class D β-lactamases. Biochem. J. 292:555-562.
9. Bush K. 2013. Proliferation and significance of clinically relevant β-lactamases. Ann. N. Y. Acad. Sci. 1277:84-90. http://dx.doi.org/10.1111 /nyas.12023.
10. Drawz SM, Bethel CR, Doppalapudi VR, Sheri A, Pagadala SR, Hujer AM, Skalweit MJ, Anderson VE, Chen SG, Buynak JD, Bonomo RA. 2010. Penicillin sulfone inhibitors of classDβ-lactamases. Antimicrob. Agents Chemother. 54:1414-1424. http://dx.doi.org/10.1128/AAC.00743-09.
11. Santillana E, Beceiro A, Bou G, Romero A. 2007. Crystal structure of the carbapenemase OXA-24 reveals insights into the mechanism of carbapenem hydrolysis. Proc. Natl. Acad. Sci. U. S. A. 104:5354-5359. http://dx doi.org/10.1073/pnas.0607557104.
12. Docquier JD, Calderone V, De Luca F, Benvenuti M, Giuliani F, Bellucci L, Tafi A, Nordmann P, Botta M, Rossolini GM, Mangani S. 2009. Crystal structure of the OXA-48 β-lactamase reveals mechanistic diversity among class D carbapenemases. Chem. Biol. 16:540-547. http: //dx.doi.org/10.1016/j.chembiol. 2009.04.010.
13. De Luca F, Benvenuti M, Carboni F, Pozzi C, Rossolini GM, Mangani S, Docquier JD. 2011. Evolution to carbapenem-hydrolyzing activity in noncarbapenemase class D β-lactamase OXA-10 by rational protein design. Proc. Natl. Acad. Sci. U. S. A. 108:18424-18429. http://dx.doi.org/10 .1073/pnas.1110530108.
14. Schneider KD, Bethel CR, Distler AM, Hujer AM, Bonomo RA, Leonard DA. 2009. Mutation of the active site carboxy-lysine (K70) of OXA-1 β-lactamase results in a deacylation-deficient enzyme. Biochemistry 48: 6136-6145. http://dx.doi.org/10.1021/bi900448u.
15. Schneider KD, Ortega CJ, Renck NA, Bonomo RA, Powers RA, Leonard DA. 2011. Structures of the class D carbapenemase OXA-24 from Acinetobacter baumannii in complex with doripenem. J. Mol. Biol. 406:583- 594. http://dx.doi.org/10.1016/j.jmb.2010.12.042.
16. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326. http://dx .doi.org/10.1016/S0076-6879(97)76066-X.
17. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J. Appl. Crystallogr. 40: 658-674. http://dx.doi.org/10.1107/S0021889807021206.
18. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr.DBiol. Crystallogr. 53:240-255. http://dx.doi.org/10.1107/S0907444996012255.
19. Collaborative Computational Project N. 1994. The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760-763. http://dx.doi.org/10.1107/S0907444994003112.
20. Emsley P, Cowtan K. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132. http://dxdoi.org/10.1107/S0907444904019158.
21. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66:486-501. http: //dx.doi.org/10.1107/S0907444910007493.
22. Chen VB, Arendall WB, 3, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. Mol- Probity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66:12-21. http://dx.doi.org/10.1107/S0907444909042073.
23. Baurin S, Vercheval L, Bouillenne F, Falzone C, Brans A, Jacquamet L, Ferrer JL, Sauvage E, Dehareng D, Frere JM, Charlier P, Galleni M, Kerff F. 2009. Critical role of tryptophan 154 for the activity and stability of class D β-lactamases. Biochemistry 48:11252-11263. http://dx.doi.org/10.1021/ bi901548c.
24. Vercheval L, Bauvois C, di Paolo A, Borel F, Ferrer JL, Sauvage E, Matagne A, Frere JM, Charlier P, Galleni M, Kerff F. 2010. Three factors that modulate the activity of class D β-lactamases and interfere with the post-translational carboxylation of Lys70. Biochem. J. 432:495-504. http://dx.doi.org/10.1042/BJ20101122.
25. Strynadka NC, Adachi H, Jensen SE, Johns K, Sielecki A, Betzel C, Sutoh K, James MN. 1992. Molecular structure of the acyl-enzyme intermediate in β-lactam hydrolysis at 1.7 Å resolution. Nature 359:700-705. http://dx.doi.org/10.1038/359700a0.
26. Beadle BM, Trehan I, Focia PJ, Shoichet BK. 2002. Structural milestones in the reaction pathway of an amide hydrolase: Substrate, acyl, and prod- uct complexes of cephalothin with AmpC β-lactamase. Structure 10:413- 442. http://dx.doi.org/10.1016/S0969-2126(02)00725-6.
27. Patera A, Blaszczak LC, Shoichet BK. 2000. Crystal structures of substrate and inhibitor complexes with AmpC β-lactamase: Possible implications for substrate-assisted catalysis. J. Am. Chem. Soc. 122:10504-10512. http://dx.doi.org/10.1021/ja001676x.
28. Pernot L, Frenois F, Rybkine T, L'Hermite G, Petrella S, Delettre J, Jarlier V, Collatz E, Sougakoff W. 2001. Crystal structures of the class D β-lactamase OXA-13 in the native form and in complex with meropenem. J. Mol. Biol. 310:859-874. http://dx.doi.org/10.1006/jmbi.2001.4805.
29. Docquier JD, Benvenuti M, Calderone V, Giuliani F, Kapetis D, De Luca F, Rossolini GM, Mangani S. 2010. Crystal structure of the narrow-spectrum OXA-46classDβ-lactamase: relationship between active-site lysine carbamylation and inhibition by polycarboxylates. Antimicrob. Agents Chemother. 54:2167-2174. http://dx.doi.org/10.1128/AAC.01517-09.
30. Golemi D, Maveyraud L, Vakulenko S, Samama JP, Mobashery S. 2001. Critical involvement of a carbamylated lysine in catalytic function of class D β-lactamases. Proc. Natl. Acad. Sci. U. S. A. 98:14280-14285. http://dx doi.org/10.1073/pnas.241442898.
31. Maveyraud L, Golemi D, Kotra LP, Tranier S, Vakulenko S, Mobashery S, Samama JP. 2000. Insights into class D β-lactamases are revealed by the crystal structure of the OXA-10 enzyme from Pseudomonas aeruginosa. Structure 8:1289-1298. http://dx.doi.org/10.1016/S0969-2126(00)00534-7.
32. Bethel CR, Distler AM, Ruszczycky MW, Carey MP, Carey PR, Hujer AM, Taracila M, Helfand MS, Thomson JM, Kalp M, Anderson VE, Leonard DA, Hujer KM, Abe T, Venkatesan AM, Mansour TS, Bonomo RA. 2008. Inhibition of OXA-1 β-lactamase by penems. Antimicrob. Agents Chemother. 52:3135-3143. http://dx.doi.org/10.1128/AAC.01677-07.
33. Leonard DA, Bonomo RA, Powers RA. 31 July 2013. Class D β-lactamases: A reappraisal after five decades. Acc. Chem. Res. http://dx.doi.org/10 .1021/ar300327a.
34. Sun T, Nukaga M, Mayama K, Braswell EH, Knox Jr. 2003. Comparison of β-lactamases of classes A and D: 1.5 Å crystallographic structure of the classDOXA-1 oxacillinase. Protein Sci. 12:82-91. http://dx.doi.org/10 .1110/ps.0224303.
35. Kaitany KC, Klinger NV, June CM, Ramey ME, Bonomo RA, Powers RA, Leonard DA. 2013. Structures of the class D carbapenemases OXA-23 and OXA-146: Mechanistic basis of activity against carbapenems, extendedspectrum cephalosporins and aztreonam. Antimicrob. Agents Chemother. 57:4848-4855. http://dx.doi.org/10.1128/AAC.00762-13.
36. Poirel L, Naas T, Nordmann P. 2010. Diversity, epidemiology, and genetics of class D β-lactamases. Antimicrob. Agents Chemother. 54:24- 38. http://dx.doi.org/10.1128/AAC.01512-08.
37. Saves I, Burlet-Schiltz O, Maveyraud L, Samama JP, Prome JC, Masson JM. 1995. Mass spectral kinetic study of acylation and deacylation during the hydrolysis of penicillins and cefotaxime by β-lactamase TEM-1 and the G238S mutant. Biochemistry 34:11660-11667. http://dx.doi.org/10 .1021/bi00037a003.
38. DeLano WL. 2002. The PyMOL molecular graphics system. Schrodinger, LLC, Cambridge, MA.