Neutron diffraction studies of a class A β-lactamase Toho-1 e166a/r274n/r276n triple mutant

Journal of Molecular Biology

Volumn 396, Issue 4, 2010, Pages 1070-1080

  Tomanicek, Stephen J ^a   Blakeley, Matthew P ^b   Cooper, Jonathan ^c   Chen, Yu ^d   Afonine, Pavel V ^e   Coates, Leighton ^a  

^a OAK RIDGE NATIONAL LABORATORY   (United States)

^b INSTITUT LAUE LANGEVIN   (France)

^c ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^d UNIVERSITY OF SOUTH FLORIDA   (United States)

^e LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Extended spectrum lactamases (ESBLs); Neutron diffraction; Neutron structure; Toho 1; lactamase

Indexed keywords

ALANINE; ARGININE; ASPARAGINE; BETA LACTAMASE CTX M; BETA LACTAMASE TOHO 1; EXTENDED SPECTRUM BETA LACTAMASE; GLUTAMIC ACID; LYSINE; MUTANT PROTEIN; SERINE; UNCLASSIFIED DRUG;

ACYLATION; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME CONFORMATION; ENZYME MECHANISM; ENZYME STRUCTURE; ENZYME SUBSTRATE; HYDROGEN BOND; NEUTRON DIFFRACTION; NONHUMAN; PRIORITY JOURNAL; PROTON TRANSPORT;

BACTERIA (MICROORGANISMS);

EID: 77649270363     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.12.036     Document Type: Article

References (46)

1. Matagne A., Dubus A., Galleni M., Frere J.M. The β-lactamase cycle: a tale of selective pressure and bacterial ingenuity. Nat. Prod. Rep. 1999, 16(1):1-19.
2. Ambler R.P., Coulson A.F.W., Frère J.-M., Ghuysen J.-M., Joris B., Forsman M., et al. A standard numbering scheme for the class A β-lactamases. Biochem. J. 1991, 276:269-272.
3. Matagne A., Lamotte-Brasseur J., Frère J.M. Catalytic properties of class A β-lactamases: efficiency and diversity. Biochem. J. 1998, 330:581-598.
4. Knox J.R. Extended-spectrum and inhibitor-resistant TEM-type β lactamases: mutations, specificity, and three-dimensional structure. Antimicrob. Agents Chemother. 1995, 39:2593-2601.
5. Bradford P.A. Extended-spectrum β-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin. Microbiol. Rev. 2001, 14(4):933-951.
6. Chaibi E.B., Farzaneh S., Morand A., Peduzzi J., Barthelemy M., Sirot D., Labia R. Problems encountered in the characterization of IRT β-lactamase-producing clinical Escherichia coli isolates intermediate-resistant to cephalothin. J. Antimicrob. Chemother. 1996, 37(1):190-191.
7. Du B.S., Marriott M.S., Amyes S.G. TEM- and SHV-derived extended spectrum β-lactamases: relationship between selection, structure and function. J. Antimicrob. Chemother. 1995, 35:7-22.
8. Bonnet R. Growing group of extended-spectrum β-lactamases: the CTX-M enzymes. Antimicrob. Agents Chemother. 2004, 48(1):1-14.
9. Tzouvelekis L.S., Tzelepi E., Tassios P.T., Legakis N.J. CTX-M-type β-lactamases: an emerging group of extended-spectrum enzymes. Int. J. Antimicrob. Agents 2000, 14:137-142.
10. Ishii Y., Ohno A., Taguchi H., Imajo S., Ishiguro M., Matsuzawa H. Cloning and sequence of the gene encoding a cefotaxime-hydrolyzing class A β-lactamase isolated from Escherichia coli. Antimicrob. Agents Chemother. 1995, 39:2269-2275.
11. Ibuka A.S., Ishii Y., Galleni M., Ishiguro M., Yamaguchi K., Frere J.M., 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(36):10634-10643.
12. Ibuka A., Taguchi A., Ishiguro M., Fushinobu S., Ishii Y., Kamitori S., et al. Crystal structure of the E166A mutant of extended-spectrum β-lactamase toho-1 at 1.8 Å resolution. J. Mol. Biol. 1999, 285:2079-2087.
13. Shimamura T., Nitanai Y., Uchiyama T., Matsuzawa H. Improvement of crystal quality by surface mutations of β-lactamase Toho-1. Acta Crystallogr., Sect. F: Struct. Biol. Cryst. Commun. 2009, 65:379-382.
14. Shimamura T., Ibuka A., Fushinobu S., Wakagi T., Ishiguro M., Ishii Y., Matsuzawa H. 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(48):46601-46608.
15. Nitanai, Y., Shimamura, T., Uchiyama, T., Ishii, Y., Takehira, M., Yutan, K., Matsuzawa, H., Miyano, M. (2009). The catalytic efficiency (k(cat)/K(m)) of the class A β-lactamase Toho-1 correlates with the thermal stability of its catalytic intermediate analog. Biochim. Biophys. Acta, in press. doi:10.1016/j.bbapap.2009.10.023.
16. Strynadka N.C., Adachi H., Jensen S.E., Johns K., Sielecki A., Betzel C., et al. Molecular structure of the acyl-enzyme intermediate in β-lactam hydrolysis at 1.7 Å resolution. Nature 1992, 359(6397):700-705.
17. Chen Y., Bonnet R., Shoichet B.K. The acylation mechanism of CTX-M β-lactamase at 0.88 A Resolution. J. Am. Chem. Soc. 2007, 129(17):5378-5380.
18. Nukaga M., Mayama K., Hujer A.M., Bonomo R.A., Knox J.R. Ultrahigh resolution structure of a class A β-lactamase: on the mechanism and specificity of the extended-spectrum SHV-2 enzyme. J. Mol. Biol. 2003, 328:289-301.
19. Maveyraud L., Pratt R.F., Samama J.P. Crystal structure of an acylation transition-state analog of the TEM-1 β-lactamase. Mechanistic implications for class A β-lactamases. Biochemistry 1998, 37:2622-2628.
20. Minasov G., Wang X., Shoichet B.K. An ultrahigh resolution structure of TEM-1 β-lactamase suggests a role for Glu166 as the general base in acylation. J. Am. Chem. Soc. 2002, 124:5333-5340.
21. Chen Y., Shoichet B., Bonnet R. Structure, function, and inhibition along the reaction coordinate of CTX-M β-lactamases. J. Am. Chem. Soc. 2005, 127:5423-5434.
22. Chen Y., Delmas J., Sirot J., Shoichet B., Bonnet R. Atomic resolution structures of CTX-M β-lactamases: extended spectrum activities from increased mobility and decreased stability. J. Mol. Biol. 2005, 348:349-362.
23. Lamotte-Brasseur J., Dive G., Dideberg O., Charlier P., Frere J.M., Ghuysen J.M. Mechanism of acyl transfer by the class A serine β-lactamase of Streptomyces albus G. Biochem. J. 1991, 279:213-221.
24. Meroueh S.O., Fisher J.F., Schlegel H.B., Mobashery S. Ab initio QM/MM study of class A β-lactamase acylation: dual participation of Glu166 and Lys73 in a concerted base promotion of Ser70. J. Am. Chem. Soc. 2005, 127:15397-15407.
25. Hermann J.C., Ridder L., Mulholland A.J., Holtje H.D. Identification of Glu166 as the general base in the acylation reaction of class A β-lactamases through QM/MM modeling. J. Am. Chem. Soc. 2003, 125:9590-9591.
26. Gibson R.M., Christensen H., Waley S.G. Site-directed mutagenesis of β-lactamase I. Single and double mutants of Glu-166 and Lys-73. Biochem. J. 1990, 272(6):13-619.
27. Golemi-Kotra D., Meroueh S.O., Kim C., Vakulenko S.B., Bulychev A., Stemmler A.J., et al. The importance of a critical protonation state and the fate of the catalytic steps in class A β-lactamases and penicillin-binding proteins. J. Biol. Chem. 2004, 279:34665-34673.
28. Escobar W.A., Tan A.K., Lewis E.R., Fink A.L. Role of residues 104, 164, 166, 238 and 240 in the substrate profile of PER-1 β-lactamase hydrolysing third-generation cephalosporins. Biochemistry 1994, 33:7619-7626.
29. Lietz E.J., Truher H, Kahn D, Hokenson M.J., Fink A.L. Lysine-73 is involved in the acylation and deacylation of β-lactamase. Biochemistry 2000, 39:4971-4981.
30. Praznikar J., Afonine P.V., Guncar G., Adams P.D., Turk D. Averaged kick maps: less noise, more signal...and probably less bias. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2009, 65:921-931.
31. Wang X., Minasov G., Shoichet B.K. Evolution of an antibiotic resistance enzyme constrained by stability and activity trade-offs. J. Mol. Biol. 2002, 320(1):85-95.
32. Atanasov B.P., Mustafi D., Makinen M.W. Protonation of the β-lactam nitrogen is the trigger event in the catalytic action of class A β-lactamases. Proc. Natl Acad. Sci. USA 2000, 97:3160-3165.
33. Thomas V.L., Golemi-Kotra D., Kim C., Vakulenko S.B., Mobashery S., Shoichet B.K. Structural consequences of the inhibitor-resistant Ser130Gly substitution in TEM β-lactamase. Biochemistry 2005, 44:9330-9338.
34. Hermann J.C., Hensen C., Ridder L., Mulholland A.J., Holtje H.D. Mechanisms of antibiotic resistance: QM/MM modeling of the acylation reaction of a class A β-lactamase with benzylpenicillin. J. Am. Chem. Soc. 2005, 127:4454-4465.
35. Wilkinson C., Lehmann M.S., Meilleur F., Blakeley M.P., Myles D.A.A., Vogelmeier S., et al. Characterization of image plates for neutron diffraction. J. Appl. Crystallogr. 2009, 42:749-757.
36. Blakeley M.P. Neutron macromolecular crystallography. Crystallogr. Rev. 2009, 15(3):157-218.
37. Helliwell J.R., Habash J., Cruickshank D.W.J., Harding M.M., Greenhough T.J., Campbell J.W., et al. The recording and analysis of synchrotron X-radiation Laue diffraction photographs. J. Appl. Crystallogr. 1989, 22:483-497.
38. Campbell J.W. LAUEGEN, an X-windows-based program for the processing of Laue X-ray diffraction data. J. Appl. Crystallogr. 1995, 28:228-236.
39. Campbell J.W., Hao Q., Harding M.M., Nguti N.D., Wilkinson C. LAUEGEN version 6.0 and INTLDM. J. Appl. Crystallogr. 1998, 31:496-502.
40. Arzt S., Campbell J.W., Harding M.M., Hao Q., Helliwell J.R. LSCALE-the new normalization, scaling and absorption correction program in the Daresbury Laue software suite. J. Appl. Crystallogr. 1999, 32:554-562.
41. The CCP4 Suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 1994, 50:760-763. Collaborative Computational Project, Number 4.
42. Adams P.D., Grosse-Kunstleve R.W., Hung L.-W., Ioerger T.R., McCoy A.J., Moriarty N.W., et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2002, 58:1948-1954.
43. Afonine, P. V., Grosse-Kunstleve, R. W. & Adams, P. D. (2005). CCP4 Newsl.42, contribution 8.
44. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60:2126-2132.
45. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., Wang X., et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 2007, 35:W375-383.
46. DeLano, W.L. (2008). The PyMOL molecular graphics system. DeLano Scientific LLC, Palo Alto, CA, USA. http://www.pymol.org.