Overcoming differences: The catalytic mechanism of metallo-β-lactamases

FEBS Letters

Volumn 589, Issue 22, 2015, Pages 3419-3432

  Meini, María Rocío ^a   Llarrull, Leticia I ^a,b   Vila, Alejandro J ^a,b  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

Antibiotic resistance; Drug design; Mechanism; Metallo lactamase; Zinc enzyme

Indexed keywords

AMPICILLIN; BETA LACTAMASE; BIAPENEM; CARBAPENEM DERIVATIVE; CEFALEXIN; CEFUROXIME; CEPHALOSPORIN DERIVATIVE; CLAVULANIC ACID; LATAMOXEF; MEROPENEM; METALLO BETA LACTAMASE; METICILLIN; OXACILLIN; PENICILLIN DERIVATIVE; PENICILLIN G; TAZOBACTAM; ZINC ION;

ACINETOBACTER; AEROMONAS; ANTIBIOTIC RESISTANCE; ARTICLE; BACTEROIDES FRAGILIS; CATALYSIS; CHRYSEOBACTERIUM; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME STRUCTURE; HUMAN; HYDROGEN BOND; NUCLEOPHILICITY; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; RESTING STATE NETWORK; SERRATIA MARCESCENS; STENOTROPHOMONAS MALTOPHILIA; STEREOCHEMISTRY; BACTERIUM; BIOCATALYSIS; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; HYDROLYSIS; METABOLISM; X RAY CRYSTALLOGRAPHY;

BACTERIA; BETA-LACTAMASES; BIOCATALYSIS; CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, MICROBIAL; HUMANS; HYDROLYSIS;

EID: 84946491160     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2015.08.015     Document Type: Review

References (123)

1. J.F. Fisher, S.O. Meroueh, and S. Mobashery Bacterial resistance to beta-lactam antibiotics: compelling opportunism, compelling opportunity Chem. Rev. 105 2005 395 424
2. A.A. Medeiros Evolution and dissemination of beta-lactamases accelerated by generations of beta-lactam antibiotics Clin. Infect. Dis. 24 Suppl. 1 1997 S19-45
3. A.L. Demain, and R.P. Elander The beta-lactam antibiotics: past, present, and future Antonie Van Leeuwenhoek 75 1999 5 19
4. C. Walsh Molecular mechanisms that confer antibacterial drug resistance Nature 406 2000 775 781
5. M.G. Page Cephalosporins in clinical development Expert Opin. Investig. Drugs 13 2004 973 985
6. G.S. Singh Beta-lactams in the new millennium. Part-I: monobactams and carbapenems Mini Rev. Med. Chem. 4 2004 69 92
7. D.L. Paterson, and R.A. Bonomo Extended-spectrum beta-lactamases: a clinical update Clin. Microbiol. Rev. 18 2005 657 686
8. P. Nordmann, T. Naas, and L. Poirel Global Spread of Carbapenemase-producing Enterobacteriaceae Emerg. Infect. Dis. 17 2011 1791 1798
9. H.W. Boucher, G.H. Talbot, D.K. Benjamin Jr., J. Bradley, R.J. Guidos, R.N. Jones, B.E. Murray, R.A. Bonomo, D. Gilbert Infectious Diseases Society of America 10× '20 progress-development of new drugs active against gram-negative bacilli: an update from the Infectious Diseases Society of America Clin. Infect. Dis. 56 2013 1685 1694
10. C. Cain Rediscovering antibiotics SciBX 5 2012
11. K. Hede Antibiotic resistance: an infectious arms race Nature 509 2014 S2 S3
12. T.R. Walsh, M.A. Toleman, L. Poirel, and P. Nordmann Metallo-beta-lactamases: the quiet before the storm? Clin. Microbiol. Rev. 18 2005 306 325
13. M.W. Crowder, J. Spencer, and A.J. Vila Metallo-beta-lactamases: novel weaponry for antibiotic resistance in bacteria Acc. Chem. Res. 39 2006 721 728
14. S.M. Drawz, and R.A. Bonomo Three decades of β-lactamase inhibitors Clin. Microbiol. Rev. 23 2010 160 201
15. L.D. Sabath, and E.P. Abraham Zinc as a cofactor for cephalosporinase from Bacillus cereus 569 Biochem. J. 98 1966 11C 13C
16. R. Bicknell, A. Schäffer, S.G. Waley, and D.S. Auld Changes in the coordination geometry of the active-site metal during catalysis of benzylpenicillin hydrolysis by Bacillus cereus beta-lactamase II Biochemistry 25 1986 7208 7215
17. S. Bounaga, A.P. Laws, M. Galleni, and M.I. Page The mechanism of catalysis and the inhibition of the Bacillus cereus zinc-dependent beta-lactamase Biochem. J. 331 1998 703 711
18. S.M. Fabiane, M.K. Sohi, T. Wan, D.J. Payne, J.H. Bateson, T. Mitchell, and B.J. Sutton Crystal structure of the zinc-dependent beta-lactamase from Bacillus cereus at 1.9 A resolution: binuclear active site with features of a mononuclear enzyme Biochemistry 37 1998 12404 12411
19. D. de Seny, C. Prosperi-Meys, C. Bebrone, G.M. Rossolini, M.I. Page, P. Noel, J.-M. Frère, and M. Galleni Mutational analysis of the two zinc-binding sites of the Bacillus cereus 569/H/9 metallo-beta-lactamase Biochem. J. 363 2002 687 696
20. R.M. Rasia, and A.J. Vila Structural determinants of substrate binding to Bacillus cereus metallo-beta-lactamase J. Biol. Chem. 279 2004 26046 26051
21. A. Badarau, and M.I. Page The variation of catalytic efficiency of Bacillus cereus metallo-beta-lactamase with different active site metal ions Biochemistry 45 2006 10654 10666
22. L.I. Llarrull, M.F. Tioni, and A.J. Vila Metal content and localization during turnover in B. cereus metallo-beta-lactamase J. Am. Chem. Soc. 130 2008 15842 15851
23. M.F. Tioni, L.I. Llarrull, A.A. Poeylaut-Palena, M.A. Martí, M. Saggu, G.R. Periyannan, E.G. Mata, B. Bennett, D.H. Murgida, and A.J. Vila Trapping and characterization of a reaction intermediate in carbapenem hydrolysis by B. cereus metallo-beta-lactamase J. Am. Chem. Soc. 130 2008 15852 15863
24. J.M. González, M.-R. Meini, P.E. Tomatis, F.J. Medrano Martín, J.A. Cricco, and A.J. Vila Metallo-β-lactamases withstand low Zn(II) conditions by tuning metal-ligand interactions Nat. Chem. Biol. 8 2012 698 700
25. G.J. Cuchural, M.H. Malamy, and F.P. Tally Beta-lactamase-mediated imipenem resistance in Bacteroides fragilis Antimicrob. Agents Chemother. 30 1986 645 648
26. T.R. Walsh, L. Hall, S.J. Assinder, W.W. Nichols, S.J. Cartwright, A.P. MacGowan, and P.M. Bennett Sequence analysis of the L1 metallo-beta-lactamase from Xanthomonas maltophilia Biochim. Biophys. Acta 1218 1994 199 201
27. K. Shannon, A. King, and I. Phillips Beta-lactamases with high activity against imipenem and Sch 34343 from Aeromonas hydrophila J. Antimicrob. Chemother. 17 1986 45 50
28. T.R. Walsh, W.A. Neville, M.H. Haran, D. Tolson, D.J. Payne, J.H. Bateson, A.P. MacGowan, and P.M. Bennett Nucleotide and amino acid sequences of the metallo-beta-lactamase, ImiS, from Aeromonas veronii bv. sobria Antimicrob. Agents Chemother. 42 1998 436 439
29. G.M. Rossolini, N. Franceschini, M.L. Riccio, P.S. Mercuri, M. Perilli, M. Galleni, J.M. Frere, and G. Amicosante Characterization and sequence of the Chryseobacterium (Flavobacterium) meningosepticum carbapenemase: a new molecular class B beta-lactamase showing a broad substrate profile Biochem. J. 332 1998 145 152
30. S. Bellais, D. Aubert, T. Naas, and P. Nordmann Molecular and biochemical heterogeneity of class B carbapenem-hydrolyzing beta-lactamases in Chryseobacterium meningosepticum Antimicrob. Agents Chemother. 44 2000 1878 1886
31. J. Morán-Barrio, J.M. González, M.N. Lisa, A.L. Costello, M.D. Peraro, P. Carloni, B. Bennett, D.L. Tierney, A.S. Limansky, A.M. Viale, and A.J. Vila The metallo-beta-lactamase GOB is a mono-Zn(II) enzyme with a novel active site J. Biol. Chem. 282 2007 18286 18293
32. Y. Chen, J. Succi, F.C. Tenover, and T.M. Koehler Beta-lactamase genes of the penicillin-susceptible Bacillus anthracis Sterne strain J. Bacteriol. 185 2003 823 830
33. K. Bush, and J.F. Fisher Epidemiological expansion, structural studies, and clinical challenges of new β-lactamases from gram-negative bacteria Annu. Rev. Microbiol. 65 2011 455 478
34. A.P. Johnson, and N. Woodford Global spread of antibiotic resistance: the example of New Delhi metallo-lactamase (NDM)-mediated carbapenem resistance J. Med. Microbiol. 62 2013 499 513
35. G.M. Rossolini, M.A. Condemi, F. Pantanella, J.-D. Docquier, G. Amicosante, and M.C. Thaller Metallo-β-lactamase producers in environmental microbiota: new molecular class B enzyme in Janthinobacterium lividum Antimicrob. Agents Chemother. 45 2001 837 844
36. M.J. Saavedra, L. Peixe, J.C. Sousa, I. Henriques, A. Alves, and A. Correia Sfh-I, a subclass B2 metallo-β-lactamase from a Serratia fonticola environmental isolate Antimicrob. Agents Chemother. 47 2003 2330 2333
37. M. Stoczko, J.-M. Frère, G.M. Rossolini, and J.-D. Docquier Postgenomic scan of metallo-beta-lactamase homologues in rhizobacteria: identification and characterization of BJP-1, a subclass B3 ortholog from Bradyrhizobium japonicum Antimicrob. Agents Chemother. 50 2006 1973 1981
38. T.R. Walsh, J. Weeks, D.M. Livermore, and M.A. Toleman Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study Lancet Infect. Dis. 11 2011 355 362
39. G. Garau, I. García-Sáez, C. Bebrone, C. Anne, P. Mercuri, M. Galleni, J.-M. Frère, and O. Dideberg Update of the standard numbering scheme for class B β-lactamases Antimicrob. Agents Chemother. 48 2004 2347 2349
40. C. Bebrone Metallo-beta-lactamases (classification, activity, genetic organization, structure, zinc coordination) and their superfamily Biochem. Pharmacol. 74 2007 1686 1701
41. D. de Seny, U. Heinz, S. Wommer, M. Kiefer, W. Meyer-Klaucke, M. Galleni, J.M. Frere, R. Bauer, and H.W. Adolph Metal ion binding and coordination geometry for wild type and mutants of metallo-beta-lactamase from Bacillus cereus 569/H/9 (BcII): a combined thermodynamic, kinetic, and spectroscopic approach J. Biol. Chem. 276 2001 45065 45078
42. N.O. Concha, C.A. Janson, P. Rowling, S. Pearson, C.A. Cheever, B.P. Clarke, C. Lewis, M. Galleni, J.M. Frère, D.J. Payne, J.H. Bateson, and S.S. Abdel-Meguid Crystal structure of the IMP-1 metallo beta-lactamase from Pseudomonas aeruginosa and its complex with a mercaptocarboxylate inhibitor: binding determinants of a potent, broad-spectrum inhibitor Biochemistry 39 2000 4288 4298
43. I. Garcia-Saez, J.-D. Docquier, G.M. Rossolini, and O. Dideberg The three-dimensional structure of VIM-2, a Zn-beta-lactamase from Pseudomonas aeruginosa in its reduced and oxidised form J. Mol. Biol. 375 2008 604 611
44. D.T. King, L.J. Worrall, R. Gruninger, and N.C.J. Strynadka New Delhi metallo-β-lactamase: structural insights into β-lactam recognition and inhibition J. Am. Chem. Soc. 134 2012 11362 11365
45. J.-D. Docquier, M. Benvenuti, V. Calderone, M. Stoczko, N. Menciassi, G.M. Rossolini, and S. Mangani High-resolution crystal structure of the subclass B3 metallo-beta-lactamase BJP-1: rational basis for substrate specificity and interaction with sulfonamides Antimicrob. Agents Chemother. 54 2010 4343 4351
46. B.G. Hall, S.J. Salipante, and M. Barlow The metallo-beta-lactamases fall into two distinct phylogenetic groups J. Mol. Evol. 57 2003 249 254
47. C. Bebrone, H. Delbrück, M.B. Kupper, P. Schlömer, C. Willmann, J.-M. Frère, R. Fischer, M. Galleni, and K.M.V. Hoffmann The structure of the Dizinc subclass B2 metallo-β-lactamase CphA reveals that the second inhibitory zinc ion binds in the histidine site Antimicrob. Agents Chemother. 53 2009 4464 4471
48. D. Yong, M.A. Toleman, C.G. Giske, H.S. Cho, K. Sundman, K. Lee, and T.R. Walsh Characterization of a new metallo-beta-lactamase gene, bla(NDM-1), and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India Antimicrob. Agents Chemother. 53 2009 5046 5054
49. L. Lauretti, M.L. Riccio, A. Mazzariol, G. Cornaglia, G. Amicosante, R. Fontana, and G.M. Rossolini Cloning and characterization of blaVIM, a new integron-borne metallo-beta-lactamase gene from a Pseudomonas aeruginosa clinical isolate Antimicrob. Agents Chemother. 43 1999 1584 1590
50. W.-H. Zhao, and Z.-Q. Hu IMP-type metallo-β-lactamases in gram-negative bacilli: distribution, phylogeny, and association with integrons Crit. Rev. Microbiol. 37 2011 214 226
51. M.A. Toleman, A.M. Simm, T.A. Murphy, A.C. Gales, D.J. Biedenbach, R.N. Jones, and T.R. Walsh Molecular characterization of SPM-1, a novel metallo-β-lactamase isolated in Latin America: report from the SENTRY antimicrobial surveillance programme J. Antimicrob. Chemother. 50 2002 673 679
52. H.M. Lim, J.J. Pène, and R.W. Shaw Cloning, nucleotide sequence, and expression of the Bacillus cereus 5/B/6 beta-lactamase II structural gene J. Bacteriol. 170 1988 2873 2878
53. B.A. Rasmussen, Y. Gluzman, and F.P. Tally Cloning and sequencing of the class B beta-lactamase gene (ccrA) from Bacteroides fragilis TAL3636 Antimicrob. Agents Chemother. 34 1990 1590 1592
54. O. Massidda, G.M. Rossolini, and G. Satta The Aeromonas hydrophila cphA gene: molecular heterogeneity among class B metallo-beta-lactamases J. Bacteriol. 173 1991 4611 4617
55. L. Boschi, P.S. Mercuri, M.L. Riccio, G. Amicosante, M. Galleni, J.M. Frère, and G.M. Rossolini The Legionella (Fluoribacter) gormanii metallo-beta-lactamase: a new member of the highly divergent lineage of molecular-subclass B3 beta-lactamases Antimicrob. Agents Chemother. 44 2000 1538 1543
56. D. Yong, M.A. Toleman, J. Bell, B. Ritchie, R. Pratt, H. Ryley, and T.R. Walsh Genetic and biochemical characterization of an acquired subgroup B3 metallo-β-lactamase Gene, blaAIM-1, and its unique genetic context in Pseudomonas aeruginosa from Australia Antimicrob. Agents Chemother. 56 2012 6154 6159
57. N.O. Concha, B.A. Rasmussen, K. Bush, and O. Herzberg Crystal structure of the wide-spectrum binuclear zinc beta-lactamase from Bacteroides fragilis Structure 4 1996 823 836
58. L. Nauton, R. Kahn, G. Garau, J.F. Hernandez, and O. Dideberg Structural insights into the design of inhibitors for the L1 metallo-beta-lactamase from Stenotrophomonas maltophilia J. Mol. Biol. 375 2008 257 269
59. H. Zhang, and Q. Hao Crystal structure of NDM-1 reveals a common β-lactam hydrolysis mechanism FASEB J. 25 2011 2574 2582
60. J. Spencer, J. Read, R.B. Sessions, S. Howell, G.M. Blackburn, and S.J. Gamblin Antibiotic recognition by binuclear metallo-beta-lactamases revealed by X-ray crystallography J. Am. Chem. Soc. 127 2005 14439 14444
61. G. Garau, C. Bebrone, C. Anne, M. Galleni, J.-M. Frère, and O. Dideberg A metallo-beta-lactamase enzyme in action: crystal structures of the monozinc carbapenemase CphA and its complex with biapenem J. Mol. Biol. 345 2005 785 795
62. F. Fonseca, E.H.C. Bromley, M.J. Saavedra, A. Correia, and J. Spencer Crystal structure of Serratia fonticola Sfh-I: activation of the nucleophile in mono-zinc metallo-β-lactamases J. Mol. Biol. 411 2011 951 959
63. C. Bebrone, C. Anne, F. Kerff, G. Garau, K. De Vriendt, R. Lantin, B. Devreese, J. Van Beeumen, O. Dideberg, J.-M. Frère, and M. Galleni Mutational analysis of the zinc- and substrate-binding sites in the CphA metallo-beta-lactamase from Aeromonas hydrophila Biochem. J. 414 2008 151 159
64. T. Dudev, Dudev M. Lin, and C. Lim First-Second shell interactions in metal binding sites in proteins: a PDB survey and DFT/CDM calculations J. Am. Chem. Soc. 125 2003 3168 3180
65. G. Estiu, D. Suárez, and K.M. Merz Quantum mechanical and molecular dynamics simulations of ureases and Zn beta-lactamases J. Comput. Chem. 27 2006 1240 1262
66. Z. Wang, W. Fast, and S.J. Benkovic On the mechanism of the metallo-beta-lactamase from Bacteroides fragilis Biochemistry 38 1999 10013 10023
67. S. Lindskog, and J.E. Coleman The catalytic mechanism of carbonic anhydrase Proc. Natl. Acad. Sci. USA 70 1973 2505 2508
68. G. Chen, T. Edwards, V.M. D' Souza, and R.C. Holz Mechanistic studies on the aminopeptidase from Aeromonas proteolytica: a two-metal ion mechanism for peptide hydrolysis Biochemistry 36 1997 4278 4286
69. W.L. Mock, and J.T. Tsay PK values for active site residues of carboxypeptidase A J. Biol. Chem. 263 1988 8635
70. A.N. Bigley, and F.M. Raushel Catalytic mechanisms for phosphotriesterases Biochim. Biophys. Acta 1834 2013 443 453
71. R.-Z. Liao, J.-G. Yu, and F. Himo Reaction mechanism of the trinuclear zinc enzyme phospholipase C: a density functional theory study J. Phys. Chem. B 114 2010 2533 2540
72. F.H. Allen The cambridge structural database: a quarter of a million crystal structures and rising Acta Crystallogr. B 58 2002 380 388
73. A. Badarau, and M.I. Page Enzyme deactivation due to metal-ion dissociation during turnover of the cobalt-beta-lactamase catalyzed hydrolysis of beta-lactams Biochemistry 45 2006 11012 11020
74. A. Badarau, and M.I. Page Loss of enzyme activity during turnover of the Bacillus cereus beta-lactamase catalysed hydrolysis of beta-lactams due to loss of zinc ion J. Biol. Inorg. Chem. 13 2008 919 928
75. M.P. Yanchak, R.A. Taylor, and M.W. Crowder Mutational analysis of metallo-beta-lactamase CcrA from Bacteroides fragilis Biochemistry 39 2000 11330 11339
76. J.D. Garrity, A.L. Carenbauer, L.R. Herron, and M.W. Crowder Metal binding Asp-120 in metallo-β-lactamase L1 from Stenotrophomonas maltophilia plays a crucial role in catalysis J. Biol. Chem. 279 2004 920 927
77. Y. Yamaguchi, T. Kuroki, H. Yasuzawa, T. Higashi, W. Jin, A. Kawanami, Y. Yamagata, Y. Arakawa, M. Goto, and H. Kurosaki Probing the role of Asp-120(81) of metallo-beta-lactamase (IMP-1) by site-directed mutagenesis, kinetic studies, and X-ray crystallography J. Biol. Chem. 280 2005 20824 20832
78. L.I. Llarrull, S.M. Fabiane, J.M. Kowalski, B. Bennett, B.J. Sutton, and A.J. Vila Asp-120 locates Zn2 for optimal metallo-beta-lactamase activity J. Biol. Chem. 282 2007 18276 18285
79. H. Feng, J. Ding, D. Zhu, X. Liu, X. Xu, Y. Zhang, S. Zang, D.-C. Wang, and W. Liu Structural and mechanistic insights into NDM-1 catalyzed hydrolysis of cephalosporins J. Am. Chem. Soc. 2014
80. M. Dal Peraro, A.J. Vila, and P. Carloni Protonation state of Asp120 in the binuclear active site of the metallo-β-lactamase from Bacteroides fragilis Inorg. Chem. 42 2003 4245 4247
81. J. Crisp, R. Conners, J.D. Garrity, A.L. Carenbauer, M.W. Crowder, and J. Spencer Structural basis for the role of Asp-120 in metallo-beta-lactamases Biochemistry 46 2007 10664 10674
82. R.M. Rasia, and A.J. Vila Exploring the role and the binding affinity of a second zinc equivalent in B. cereus metallo-beta-lactamase Biochemistry 41 2002 1853 1860
83. A.M. Davies, R.M. Rasia, A.J. Vila, B.J. Sutton, and S.M. Fabiane Effect of pH on the active site of an Arg121Cys mutant of the metallo-beta-lactamase from Bacillus cereus: implications for the enzyme mechanism Biochemistry 44 2005 4841 4849
84. L.I. Llarrull, M.F. Tioni, J. Kowalski, B. Bennett, and A.J. Vila Evidence for a dinuclear active site in the metallo-beta-lactamase BcII with substoichiometric Co(II). A new model for metal uptake J. Biol. Chem. 282 2007 30586 30595
85. M. Aitha, A.R. Marts, A. Bergstrom, A.J. Møller, L. Moritz, L. Turner, J.C. Nix, R.A. Bonomo, R.C. Page, D.L. Tierney, and M.W. Crowder Biochemical, mechanistic, and spectroscopic characterization of metallo-β-lactamase VIM-2 Biochemistry 53 2014 7321 7331
86. H. Yang, M. Aitha, A.R. Marts, A. Hetrick, B. Bennett, M.W. Crowder, and D.L. Tierney Spectroscopic and mechanistic studies of heterodimetallic forms of metallo-β-lactamase NDM-1 J. Am. Chem. Soc. 136 2014 7273 7285
87. R. Bicknell, and S.G. Waley Cryoenzymology of Bacillus cereus beta-lactamase II Biochemistry 24 1985 6876 6887
88. M.J. Hawk, R.M. Breece, C.E. Hajdin, K.M. Bender, Z. Hu, A.L. Costello, B. Bennett, D.L. Tierney, and M.W. Crowder Differential binding of Co(II) and Zn(II) to metallo-β-lactamase Bla2 from Bacillus anthracis J. Am. Chem. Soc. 131 2009 10753 10762
89. Z. Hu, G. Periyannan, B. Bennett, and M.W. Crowder Role of the Zn1 and Zn2 sites in metallo-beta-lactamase L1 J. Am. Chem. Soc. 130 2008 14207 14216
90. M. Dal Peraro, L.I. Llarrull, U. Rothlisberger, A.J. Vila, and P. Carloni Water-assisted reaction mechanism of monozinc beta-lactamases J. Am. Chem. Soc. 126 2004 12661 12668
91. Z. Wang, W. Fast, and S.J. Benkovic Direct observation of an enzyme-bound intermediate in the catalytic cycle of the metallo-β-lactamase from Bacteroides fragilis J. Am. Chem. Soc. 120 1998 10788 10789
92. H. Yang, M. Aitha, A.M. Hetrick, T.K. Richmond, D.L. Tierney, and M.W. Crowder Mechanistic and spectroscopic studies of metallo-β-lactamase NDM-1 Biochemistry 51 2012 3839 3847
93. S. McManus-Munoz, and M.W. Crowder Kinetic mechanism of metallo-beta-lactamase L1 from Stenotrophomonas maltophilia Biochemistry 38 1999 1547 1553
94. J.D. Garrity, B. Bennett, and M.W. Crowder Direct evidence that the reaction intermediate of metallo-beta-lactamase L1 is metal bound Biochemistry 44 2005 1078 1087
95. R.M. Breece, Z. Hu, B. Bennett, M.W. Crowder, and D.L. Tierney Motion of the zinc ions in catalysis by a di-zinc metallo-β-lactamase J. Am. Chem. Soc. 131 2009 11642 11643
96. H. Park, E.N. Brothers, and K.M. Merz Hybrid QM/MM and DFT investigations of the catalytic mechanism and inhibition of the dinuclear zinc metallo-beta-lactamase CcrA from Bacteroides fragilis J. Am. Chem. Soc. 127 2005 4232 4241
97. N.V. Kaminskaia, B. Spingler, and S.J. Lippard Intermediate in beta-lactam hydrolysis catalyzed by a dinuclear zinc(II) complex: relevance to the mechanism of metallo-beta-lactamase J. Am. Chem. Soc. 123 2001 6555 6563
98. Z. Wang, and S.J. Benkovic Purification, characterization, and kinetic studies of a soluble Bacteroides fragilis metallo-beta-lactamase that provides multiple antibiotic resistance J. Biol. Chem. 273 1998 22402 22408
99. M. Dal Peraro, A.J. Vila, P. Carloni, and M.L. Klein Role of zinc content on the catalytic efficiency of B1 metallo beta-lactamases J. Am. Chem. Soc. 129 2007 2808 2816
100. P.F. Cook Enzyme Mechanism from Isotope Effects 1991 CRC Press
101. M.-N. Lisa, L. Hemmingsen, and A.J. Vila Catalytic role of the metal ion in the metallo-beta-lactamase GOB J. Biol. Chem. 285 2010 4570 4577
102. R.M. Rasia, A.J. Vila others Mechanistic study of the hydrolysis of nitrocefin mediated by B. cereus metallo-β-lactamase Arkivoc 3 2003 507 516
103. C. Moali, C. Anne, J. Lamotte-Brasseur, S. Groslambert, B. Devreese, J. Van Beeumen, M. Galleni, and J.-M. Frère Analysis of the importance of the metallo-β-lactamase active site loop in substrate binding and catalysis Chem. Biol. 10 2003 319 329
104. D.H. Griffin, T.K. Richmond, C. Sanchez, A.J. Moller, R.M. Breece, D.L. Tierney, B. Bennett, and M.W. Crowder Structural and kinetic studies on metallo-β-lactamase IMP-1 Biochemistry 50 2011 9125 9134
105. P.E. Tomatis, S.M. Fabiane, F. Simona, P. Carloni, B.J. Sutton, and A.J. Vila Adaptive protein evolution grants organismal fitness by improving catalysis and flexibility Proc. Natl. Acad. Sci. USA 105 2008 20605 20610
106. S.D. Scrofani, J. Chung, J.J. Huntley, S.J. Benkovic, P.E. Wright, and H.J. Dyson NMR characterization of the metallo-beta-lactamase from Bacteroides fragilis and its interaction with a tight-binding inhibitor: role of an active-site loop Biochemistry 38 1999 14507 14514
107. J.J. Huntley, S.D. Scrofani, M.J. Osborne, P.E. Wright, and H.J. Dyson Dynamics of the metallo-beta-lactamase from Bacteroides fragilis in the presence and absence of a tight-binding inhibitor Biochemistry 39 2000 13356 13364
108. J.J.A. Huntley, W. Fast, S.J. Benkovic, P.E. Wright, and H.J. Dyson Role of a solvent-exposed tryptophan in the recognition and binding of antibiotic substrates for a metallo-beta-lactamase Protein Sci. 12 2003 1368 1375
109. A.I. Karsisiotis, C.F. Damblon, and G.C.K. Roberts Solution structures of the Bacillus cereus metallo-β-lactamase BcII and its complex with the broad spectrum inhibitor R -thiomandelic acid Biochem. J. 456 2013 397 407
110. A.L. Carenbauer, J.D. Garrity, G. Periyannan, R.B. Yates, and M.W. Crowder Probing substrate binding to metallo-beta-lactamase L1 from Stenotrophomonas maltophilia by using site-directed mutagenesis BMC Biochem. 3 2002 4
111. M. Aitha, T.K. Richmond, Z. Hu, A. Hetrick, R. Reese, A. Gunther, R. McCarrick, B. Bennett, and M.W. Crowder Dilution of dipolar interactions in a spin-labeled, multimeric metalloenzyme for DEER studies J. Inorg. Biochem. 136 2014 40 46
112. M. Aitha, L. Moritz, I.D. Sahu, O. Sanyurah, Z. Roche, R. McCarrick, G.A. Lorigan, B. Bennett, and M.W. Crowder Conformational dynamics of metallo-β-lactamase CcrA during catalysis investigated by using DEER spectroscopy J. Biol. Inorg. Chem. 20 2015 585 594
113. J. Fisher, R.L. Charnas, S.M. Bradley, and J.R. Knowles Inactivation of the RTEM beta-lactamase from Escherichia coli. Interaction of penam sulfones with enzyme Biochemistry 20 1981 2726 2731
114. G. Zafaralla, and S. Mobashery Evidence for a new enzyme-catalyzed reaction other than. beta-lactam hydrolysis in turnover of a penem by the TEM-1 beta.-lactamase J. Am. Chem. Soc. 115 1993 4962 4965
115. R. Tripathi, and N.N. Nair Mechanism of meropenem hydrolysis by New Delhi metallo β-lactamase ACS Catal. 5 2015 2577 2586
116. J. Brem, W.B. Struwe, A.M. Rydzik, H. Tarhonskaya, I. Pfeffer, E. Flashman, S.S. van Berkel, J. Spencer, T.D.W. Claridge, M.A. McDonough, J.L.P. Benesch, and C.J. Schofield Studying the active-site loop movement of the São Paolo metallo-β-lactamase-1 Chem. Sci. 6 2015 956 963
117. M. Hernandez Valladares, A. Felici, G. Weber, H.W. Adolph, M. Zeppezauer, G.M. Rossolini, G. Amicosante, J.M. Frère, and M. Galleni Zn(II) dependence of the Aeromonas hydrophila AE036 metallo-beta-lactamase activity and stability Biochemistry 36 1997 11534 11541
118. P.A. Crawford, N. Sharma, S. Chandrasekar, T. Sigdel, T.R. Walsh, J. Spencer, and M.W. Crowder Over-expression, purification, and characterization of metallo-beta-lactamase ImiS from Aeromonas veronii bv. sobria Protein Expr. Purif. 36 2004 272 279
119. F. Fonseca, C.J. Arthur, E.H.C. Bromley, B. Samyn, P. Moerman, M.J. Saavedra, A. Correia, and J. Spencer Biochemical characterization of Sfh-I, a subclass B2 metallo-beta-lactamase from Serratia fonticola UTAD54 Antimicrob. Agents Chemother. 55 2011 5392 5395
120. N.P. Sharma, C. Hajdin, S. Chandrasekar, B. Bennett, K.-W. Yang, and M.W. Crowder Mechanistic studies on the mononuclear ZnII-containing metallo-beta-lactamase ImiS from Aeromonas sobria Biochemistry 45 2006 10729 10738
121. J. Spencer, A.R. Clarke, and T.R. Walsh Novel mechanism of hydrolysis of therapeutic β-lactams by Stenotrophomonas maltophilia L1 metallo-β-lactamase J. Biol. Chem. 276 2001 33638 33644
122. S. Haruta, E.T. Yamamoto, Y. Eriguchi, and T. Sawai Characterization of the active-site residues asparagine 167 and lysine 161 of the IMP-1 metallo beta-lactamase FEMS Microbiol. Lett. 197 2001 85 89
123. D. King, and N. Strynadka Crystal structure of New Delhi metallo-β-lactamase reveals molecular basis for antibiotic resistance Protein Sci. 20 2011 1484 1491