Structural insights into substrate recognition and product expulsion in CTX-M enzymes

Journal of Molecular Biology

Volumn 400, Issue 1, 2010, Pages 108-120

  Delmas, Julien ^a,b   Leyssene, David ^a   Dubois, Damien ^a,b   Birck, Catherine ^c   Vazeille, Emilie ^b   Robin, Frédéric ^a,b   Bonnet Richard, R ^a,b  

^a UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

^b UNIVERSITÉ CLERMONT AUVERGNE   (France)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Antibiotic resistance; Catalytic reaction; Extended spectrum cephalosporins; X ray crystallography; lactamases

Indexed keywords

ARGININE; BETA LACTAM ANTIBIOTIC; BETA LACTAMASE; BETA LACTAMASE CTX M; CARBOXYPEPTIDASE; CEFOTAXIME; CEPHALOSPORIN; PENICILLIN G;

ARTICLE; BINDING SITE; CATALYSIS; CONTROLLED STUDY; DRUG HYDROLYSIS; DRUG STRUCTURE; ENZYME ACTIVE SITE; ENZYME STRUCTURE; ENZYME SUBSTRATE; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; PHENOTYPE; PRIORITY JOURNAL; STATIC ELECTRICITY; STEREOSPECIFICITY; X RAY DIFFRACTION;

EID: 77953729075     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.04.062     Document Type: Article

References (75)

1. Ambler R.P., Coulson A.F., Frere J.M., Ghuysen J.M., Joris B., Forsman M., et al. A standard numbering scheme for the class A beta-lactamases. Biochem. J. 1991, 276:269-270.
2. Rawlings N.D., Morton F.R., Kok C.Y., Kong J., Barrett A.J. MEROPS: the peptidase database. Nucleic Acids Res. 2008, 36:320-325.
3. Beadle B.M., Trehan I., Focia P.J., Shoichet B.K. Structural milestones in the reaction pathway of an amide hydrolase: substrate, acyl, and product complexes of cephalothin with AmpC beta-lactamase. Structure 2002, 10:413-424.
4. Chen Y., Bonnet R., Shoichet B.K. The acylation mechanism of CTX-M beta-lactamase at 0.88 Å resolution. J. Am. Chem. Soc. 2007, 129:5378-5380.
5. Chen Y., Minasov G., Roth T.A., Prati F., Shoichet B.K. The deacylation mechanism of AmpC beta-lactamase at ultrahigh resolution. J. Am. Chem. Soc. 2006, 128:2970-2976.
6. Chen Y., Shoichet B., Bonnet R. Structure, function, and inhibition along the reaction coordinate of CTX-M beta-lactamases. J. Am. Chem. Soc. 2005, 127:5423-5434.
7. Curley C.P., Pratt R.F. Effectiveness of tetrahedral adducts as transition-state analogs and inhibitors of the class C β-lactamase of Enterobacter cloacae P99. J. Am. Chem. Soc. 1997, 119:1529-1538.
8. Minasov G., Wang X., Shoichet B.K. An ultrahigh resolution structure of TEM-1 beta-lactamase suggests a role for Glu166 as the general base in acylation. J. Am. Chem. Soc. 2002, 124:5333-5340.
9. Nukaga M., Mayama K., Crichlow G.V., Knox J.R. Structure of an extended-spectrum class A beta-lactamase from Proteus vulgaris K1. J. Mol. Biol. 2002, 317:109-117.
10. Oefner C., D'Arcy A., Daly J.J., Gubernator K., Charnas R.L., Heinze I., et al. Refined crystal structure of beta-lactamase from Citrobacter freundii indicates a mechanism for beta-lactam hydrolysis. Nature 1990, 343:284-288.
11. Schneider K.D., Karpen M.E., Bonomo R.A., Leonard D.A., Powers R.A. The 1.4 Å crystal structure of the class D beta-lactamase OXA-1 complexed with doripenem. Biochemistry 2009, 48:11480-11487.
12. Galleni M., Lamotte-Brasseur J., Raquet X, Dubus A., Monnaie D., Knox J.R., Frère J.M. The enigmatic catalytic mechanism of active-site serine beta-lactamases. Biochem. Pharmacol. 1995, 49:1171-1178.
13. Matagne A., Lamotte-Brasseur J., Frere J.M. Catalytic properties of class A beta-lactamases: efficiency and diversity. Biochem. J. 1998, 330:581-598.
14. Matagne A., Dubus A., Galleni M., Frère J.M. The beta-lactamase cycle: a tale of selective pressure and bacterial ingenuity. Nat. Prod. Rep. 1999, 19:1-19.
15. Wang X., Minasov G., Blazquez J., Caselli E., Prati F., Shoichet B.K. Recognition and resistance in TEM beta-lactamase. Biochemistry 2003, 42:8434-8444.
16. Bonnet R. Growing group of extended-spectrum beta-lactamases: the CTX-M enzymes. Antimicrob. Agents Chemother. 2004, 48:1-14.
17. Bradford P.A. Extended-spectrum β-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin. Microbiol. Rev. 2001, 14:933-951.
18. Bush K. Beta-lactamases of increasing clinical importance. Curr. Pharm. Des. 1999, 5:839-845.
19. Jacoby G.A. Extended-spectrum beta-lactamases and other enzymes providing resistance to oxyimino-beta-lactams. Infect. Dis. Clin. North Am. 1997, 11:875-887.
20. 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.
21. Tzouvelekis L.S., Bonomo R.A. SHV-type beta-lactamases. Curr. Pharm. Des. 1999, 5:847-864.
22. Paterson D.L., Ko W.C., Von Gottberg A., Mohapatra S., Casellas J.M., Goossens H., et al. Antibiotic therapy for Klebsiella pneumoniae bacteremia: implications of production of extended-spectrum beta-lactamases. Clin. Infect. Dis. 2004, 39:31-37.
23. Brown N.G., Shanker S., Prasad B.V., Palzkill T. Structural and biochemical evidence that a TEM-1 beta-lactamase N170G active site mutant acts via substrate-assisted catalysis. J. Biol. Chem. 2009, 284:33703-33712.
24. Cantu C., Huang W., Palzkill T. Selection and characterization of amino acid substitutions at residues 237-240 of TEM-1 beta-lactamase with altered substrate specificity for aztreonam and ceftazidime. J. Biol. Chem. 1996, 271:22538-22545.
25. Cantu C., Palzkill T. The role of residue 238 of TEM-1 beta-lactamase in the hydrolysis of extended-spectrum antibiotics. J. Biol. Chem. 1998, 273:26603-26609.
26. Huang W., Petrosino J., Hirsch M., Shenkin P.S., Palzkill T. Amino acid sequence determinants of beta-lactamase structure and activity. J. Mol. Biol. 1996, 258:688-703.
27. Majiduddin F.K., Materon I.C., Palzkill T.G. Molecular analysis of beta-lactamase structure and function. Int. J. Med. Microbiol. 2002, 292:127-137.
28. Petrosino J.F., Palzkill T. Systematic mutagenesis of the active site omega loop of TEM-1 beta-lactamase. J. Bacteriol. 1996, 178:1821-1828.
29. Huletsky A., Knox J.R., Levesque R.C. Role of Ser-238 and Lys-240 in the hydrolysis of third-generation cephalosporins by SHV-type beta-lactamases probed by site-directed mutagenesis and three-dimensional modeling. J. Biol. Chem. 1993, 268:3690-3697.
30. Wang X., Minasov G., Shoichet B.K. The structural bases of antibiotic resistance in the clinically derived mutant beta-lactamases TEM-30, TEM-32, and TEM-34. J. Biol. Chem. 2002, 277:32149-32156.
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, 320:85-95.
32. Canton R., Coque T.M. The CTX-M beta-lactamase pandemic. Curr. Opin. Microbiol. 2006, 9:466-475.
33. Arpin C., Dubois V., Coulange L., Andre C., Fischer I., Noury P., et al. Extended-spectrum beta-lactamase-producing Enterobacteriaceae in community and private health care centers. Antimicrob. Agents Chemother. 2003, 47:3506-3514.
34. Kassis-Chikhani N., Vimont S., Asselat K., Trivalle C., Minassian B., Sengelin C., et al. CTX-M beta-lactamase-producing Escherichia coli in long-term care facilities, France. Emerg. Infect. Dis. 2004, 10:1697-1698.
35. Leflon-Guibout V., Jurand C., Bonacorsi S., Espinasse F., Guelfi M.C., Duportail F., et al. Emergence and spread of three clonally related virulent isolates of CTX-M-15-producing Escherichia coli with variable resistance to aminoglycosides and tetracycline in a French geriatric hospital. Antimicrob. Agents Chemother. 2004, 48:3736-3742.
36. Dubois D., Prasadarao N.V., Mittal R., Bret L., Roujou-Gris M., Bonnet R. CTX-M beta-lactamase production and virulence of Escherichia coli K1. Emerg. Infect. Dis. 2009, 15:1988-1990.
37. Walther-Rasmussen J., Hoiby N. Cefotaximases (CTX-M-ases), an expanding family of extended-spectrum beta-lactamases. Can. J. Microbiol. 2004, 50:137-165.
38. Gazouli M., Legakis N.J., Tzouvelekis L.S. Effect of substitution of Asn for Arg-276 in the cefotaxime-hydrolyzing class A beta-lactamase CTX-M-4. FEMS Microbiol. Lett. 1998, 169:289-293.
39. Gazouli M., Tzelepi E., Sidorenko S.V., Tzouvelekis L.S. Sequence of the gene encoding a plasmid-mediated cefotaxime-hydrolyzing class A beta-lactamase (CTX-M-4): involvement of serine 237 in cephalosporin hydrolysis. Antimicrob. Agents Chemother. 1998, 42:1259-1262.
40. Ibuka A.S., Ishii Y., Galleni M., Ishiguro M., Yamaguchi K., Frere J.M., et al. Crystal structure of extended-spectrum beta-lactamase Toho-1: insights into the molecular mechanism for catalytic reaction and substrate specificity expansion. Biochemistry 2003, 42:10634-10643.
41. Perez-Llarena F.J., Cartelle M., Mallo S., Beceiro A., Perez A., Villanueva R., et al. Structure-function studies of arginine at position 276 in CTX-M beta-lactamases. J. Antimicrob. Chemother. 2008, 61:792-797.
42. Delmas J., Robin F., Carvalho F., Mongaret C., Bonnet R. Prediction of the evolution of ceftazidime resistance in extended-spectrum beta-lactamase CTX-M-9. Antimicrob. Agents Chemother. 2006, 50:731-738.
43. Novais A., Canton R., Coque T.M., Moya A., Baquero F., Galan J.C. Mutational events in cefotaximase extended-spectrum beta-lactamases of the CTX-M-1 cluster involved in ceftazidime resistance. Antimicrob. Agents Chemother. 2008, 52:2377-2382.
44. Chen Y., Delmas J., Sirot J., Shoichet B., Bonnet R. Atomic resolution structures of CTX-M beta-lactamases: extended spectrum activities from increased mobility and decreased stability. J. Mol. Biol. 2005, 348:349-362.
45. Delmas J., Chen Y., Prati F., Robin F., Shoichet B.K., Bonnet R. Structure and dynamics of CTX-M enzymes reveal insights into substrate accommodation by extended-spectrum beta-lactamases. J. Mol. Biol. 2008, 375:192-201.
46. Shimamura T., Ibuka A., Fushinobu S., Wakagi T., Ishiguro M., Ishii Y., Matsuzawa H. Acyl-intermediate structures of the extended-spectrum class A beta-lactamase, Toho-1, in complex with cefotaxime, cephalothin, and benzylpenicillin. J. Biol. Chem. 2002, 277:46601-46608.
47. Christensen H., Martin M.T., Waley S.G. Beta-lactamases as fully efficient enzymes. Determination of all the rate constants in the acyl-enzyme mechanism. Biochem. J. 1990, 266:853-861.
48. Beadle B.M., Shoichet B.K. Structural basis for imipenem inhibition of class C beta-lactamases. Antimicrob. Agents Chemother. 2002, 46:3978-3980.
49. McDonough M.A., Anderson J.W., Silvaggi N.R., Pratt R.F., Knox J.R., Kelly J.A. Structures of two kinetic intermediates reveal species specificity of penicillin-binding proteins. J. Mol. Biol. 2002, 322:111-122.
50. Rose M., Entian K.D. New genes in the 170 degrees region of the Bacillus subtilis genome encode DNA gyrase subunits, a thioredoxin, a xylanase and an amino acid transporter. Microbiology 1996, 142:3097-3101.
51. Sadasivan C., Yee V.C. Interaction of the factor XIII activation peptide with alpha-thrombin. Crystal structure of its enzyme-substrate analog complex. J. Biol. Chem. 2000, 275:36942-36948.
52. Binning G., Quate C.F., Gerber C. Atomic force microscope. Phys. Rev. Lett. 1986, 56:930-933.
53. Florin E.L., Moy V.T., Gaub H.E. Adhesion forces between individual ligand-receptor pairs. Science 1994, 264:415-417.
54. Craig D., Gao M., Schulten K., Vogel V. Structural insights into how the MIDAS ion stabilizes integrin binding to an RGD peptide under force. Structure 2004, 12:2049-2058.
55. Grubmuller H., Heymann B., Tavan P. Ligand binding: molecular mechanics calculation of the streptavidin-biotin rupture force. Science 1996, 271:997-999.
56. Isralewitz B., Gao M., Schulten K. Steered molecular dynamics and mechanical functions of proteins. Curr. Opin. Struct. Biol. 2001, 11:224-230.
57. Li W., Liu H., Scott E.E., Grater F., Halpert J.R., Luo X., et al. Possible pathway(s) of testosterone egress from the active site of cytochrome P450 2B1: a steered molecular dynamics simulation. Drug Metab. Dispos. 2005, 33:910-919.
58. Morfill J., Neumann J., Blank K., Steinbach U., Puchner E.M., Gottschalk K.E., Gaub H.E. Force-based analysis of multidimensional energy landscapes: application of dynamic force spectroscopy and steered molecular dynamics simulations to an antibody fragment-peptide complex. J. Mol. Biol. 2008, 381:1253-1266.
59. Xu Y., Shen J., Luo X., Silman I., Sussman J.L., Chen K., Jiang H. How does huperzine A enter and leave the binding gorge of acetylcholinesterase? Steered molecular dynamics simulations. J. Am. Chem. Soc. 2003, 125:11340-11349.
60. Ibuka A., Taguchi A., Ishiguro M., Fushinobu S., Ishii Y., Kamitori S., et al. Crystal structure of the E166A mutant of extended-spectrum beta-lactamase Toho-1 at 1.8 Å resolution. J. Mol. Biol. 1999, 285:2079-2087.
61. Desiraju G.R. C-H...O and other weak hydrogen bonds. From crystal engineering to virtual screening. Chem. Commun. 2005, 28:2995-3001.
62. Silvaggi N.R., Josephine H.R., Kuzin A.P., Nagarajan R., Pratt R.F., Kelly J.A. Crystal structures of complexes between the R61 DD-peptidase and peptidoglycan-mimetic beta-lactams: a non-covalent complex with a "perfect penicillin". J. Mol. Biol. 2005, 345:521-533.
63. Molla G., Porrini D., Job V., Motteran L., Vegezzi C., Campaner S., et al. Role of arginine 285 in the active site of Rhodotorula gracilis d-amino acid oxidase. A site-directed mutagenesis study. J. Biol. Chem. 2000, 275:24715-24721.
64. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 276:307-326.
65. Vagin A., Teplyakov A. An approach to multi-copy search in molecular replacement. Acta Crystallogr. Sect. D 2000, 56:1622-1624.
66. Potterton E., McNicholas S., Krissinel E., Cowtan K., Noble M. The CCP4 molecular-graphics project. Acta Crystallogr. Sect. D 2002, 58:1955-1957.
67. Steiner R.A., Lebedev A.A., Murshudov G.N. Fisher's information in maximum-likelihood macromolecular crystallographic refinement. Acta Crystallogr. Sect. D 2003, 59:2114-2124.
68. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D 2004, 60:2126-2132.
69. Laskowski R.A., Moss D.S., Thornton J.M. Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 1993, 231:1049-1067.
70. Delano, W. L. (2002). The PyMOL Molecular Graphics System, Delano Scientific LLC, Palo Alto, CA, USA. http://www.pymol.org.
71. Lovell S.C., Davis I.W., Arendall W.B., de Bakker P.I., Word J.M., Prisant M.G., et al. Structure validation by Calpha geometry: phi,psi and Cbeta deviation. Proteins 2003, 50:437-450.
72. Lindahl E., Hess B., van der Spoel D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 2001, 7:306-317.
73. Cornell W.D., Cieplak P., Bayly C.I., Kollman P.A. Application of RESP charges to calculate conformational energies, hydrogen bond energies, and free energies of solvation. J. Am. Chem. Soc. 1993, 115:9620-9631.
74. Schmidt M.W., Baldridge K.K., Boatz J.A., Elbert S.T., Gordon M.S., Jensen J.H., et al. General atomic and molecular electronic structure system. J. Comput. Chem. 2004, 14:1347-1363.
75. Humphrey W., Dalke A., Schulten K. VMD: Visual Molecular Dynamic. J. Mol. Graphics 1996, 14:33-38.