Metallo-β-lactamases: Novel weaponry for antibiotic resistance in bacteria

Accounts of Chemical Research

Volumn 39, Issue 10, 2006, Pages 721-728

  Crowder, Michael W ^a   Spencer, James ^b   Vila, Alejandro J ^c  

^a MIAMI UNIVERSITY   (United States)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAMASE; METAL;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIUM; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECT; ENZYME SPECIFICITY; GENETICS; PHYSIOLOGY;

BACTERIA; BETA-LACTAMASES; DRUG RESISTANCE, BACTERIAL; METALS; MODELS, MOLECULAR; SUBSTRATE SPECIFICITY;

EID: 33750624074     PISSN: 00014842     EISSN: None     Source Type: Journal    
DOI: 10.1021/ar0400241     Document Type: Article

References (69)

1. Fisher, J. F.; Meroueh, S. O.; Mobashery, S. Bacterial resistance to β-lactam antibiotics: Compelling opportunism, compelling opportunity. Chem. Rev. 2005, 105, 395-424.
2. Galleni, M.; Lamotte-Brasseur, J.; Rossolini, G. M.; Spencer, J.; Dideberg, O.; Frere, J. M. Standard numbering scheme for class B β-lactamases. Antimicrob. Agents Chemother. 2001, 45, 660-663.
3. Walsh, T. R.; Toleman, M. A.; Poirel, L.; Nordmann, P. Metallo-β-lactamases: The quiet before the storm? Clin. Microbiol. Rev. 2005, 18, 306-325.
4. Heinz, U.; Adolph, H. W. Metallo-β-lactamases: Two binding sites for one catalytic metal ion? Cell. Mol. Life Sci. 2004, 61, 2827-2839.
5. Toney, J. H.; Moloughney, J. G. Metallo-β-lactamase inhibitors: Promise for the future? Curr. Opin. Invest. Drugs 2004, 5, 823-826.
6. Daiyasu, H.; Osaka, K.; Ishino, Y.; Toh, H. Expansion of the zinc metallo-hydrolase family of the β-lactamase fold. FEBS Lett. 2001, 503, 1-6.
7. Carfi, A.; Pares, S.; Duee, E.; Galleni, M.; Duez, C.; Frere, J. M.; Dideberg, O. The 3-D structure of a zinc metallo-β-lactamase from Bacillus cereus reveals a new type of protein fold. EMBO J. 1995, 14, 4914-4921.
8. Fabiane, S. M.; Sohi, M. K.; Wan, T.; Payne, D. J.; Bateson, J. H.; Mitchell, T.; Sutton, B. J. Crystal structure of the zinc-dependent β-lactamase from Bacillus cereus at 1.9 Å resolution: Binuclear active site with features of a mononuclear enzyme. Biochemistry 1998, 37, 12404-12411.
9. Concha, N. O.; Rasmussen, B. A.; Bush, K.; Herzberg, O. Crystal structure of the wide-spectrum binuclear zinc β-lactamase from Bacteroides fragilis. Structure 1996, 4, 823-836.
10. Ullah, J. H.; Walsh, T. R.; Taylor, I. A.; Emery, D. C.; Verma, C. S.; Gamblin, S. J.; Spencer, J. The crystal structure of the L1 metallo-β- lactamase from Stenotrophomonas maltophilia at 1.7 Å resolution. J. Mol. Biol. 1998, 284, 125-136.
11. Auld, D. S. In Handbook of Metalloproteins; Messerschmidt, A., Ed.; John Wiley and Sons: New York, 2004; Vol. 3, pp 416-431.
12. Liaw, S. H.; Shen, J. C.; Ko, T. P.; Hsu, C. S.; Chen, C. J.; Wang, A. H. J.; Tsai, Y. C. Crystal structure of D-aminoacylase from Alcaligenes faecalis DA1. J. Biol. Chem. 2003, 278, 4957-4962.
13. Dal Peraro, M.; Llarrull, L. I.; Rothlisberger, U.; Vila, A. J.; Carloni, P. Water-assisted reaction mechanism of monozinc β-lactamases. J. Am. Chem. Soc. 2004, 126, 12661-12668.
14. Dal Peraro, M.; Vila, A. J.; Carloni, P. Structural determinants and hydrogen bond network of the mononuclear zinc(II)-β-lactamase active site. J. Biol. Inorg. Chem. 2002, 7, 704-712.
15. Davies, A. M.; Rasia, R. M.; Vila, A. J.; Sutton, B. J.; Fabiane, S. M. Effect of pH on the active site of an Arg121Cys mutant of the metallo-β-lactamase from Bacillus cereus: Implications for the enzyme mechanism. Biochemistry 2005, 44, 4841-4849.
16. de Seny, D.; Heinz, U.; Wommer, S.; Kiefer, M.; Meyer-Klaucke, W.; Galleni, M.; Frere, J. M.; Bauer, R.; Adolph, H. W. Metal ion binding and coordination geometry for wild type and mutants of metallo-β-lactamase from Bacillus cereus 569/H/9 (Bcll). J. Biol. Chem. 2001, 276, 45065-45078.
17. Garau, G.; Bebrone, C.; Anne, C.; Galleni, M.; Frere, J. M.; Dideberg, O. A metallo-β-lactamase enzyme in action: Crystal structure of the monozinc carbapenemase CphA and its complex with biapenem. J. Mol. Biol. 2005, 345, 785-795.
18. Valladares, M. H.; Kiefer, M.; Heinz, U.; Soto, R. P.; Meyer-Klaucke, W.; Nolting, H. F.; Zeppezauer, M.; Galleni, M.; Frere, J. M.; Rossolini, G. M.; Amicosante, G.; Adolph, H. W. Kinetic and spectroscopic characterization of native and metal-substituted β-lactamase from Aeromonas hydrophila AE036. FEBS Lett. 2000, 467, 221-225.
19. Crawford, P. A.; Yang, K. W.; Sharma, N.; Bennett, B.; Crowder, M. W. Spectroscopic studies on cobalt(II)-substituted metallo-β-lactamase ImiS from Aeromonas veronii bv. sobria. Biochemistry 2005, 44, 5168-5176.
20. Valladares, M. H.; Felici, A.; Weber, G.; Adolph, H. W.; Zeppezauer, M.; Rossolini, G. M.; Amicosante, G.; Frere, J. M.; Galleni, M. Zn(II) depedence of the Aeromonas hydrophila AE036 metallo-β-lactamase activity and stability. Biochemistry 1997, 36, 11534-11541.
21. Vanhove, M.; Zakhem, M.; Devreese, B.; Franceschini, N.; Anne, C.; Bebrone, C.; Amicosante, G.; Rossolini, G. M.; van Beeumen, J.; Frere, J. M.; Galleni, M. Role of Cys221 and Asn116 in the zinc-binding sites of the Aeromonas hydrophile metallo-β-lactamase. Cell. Mol. Life Sci. 2003, 60, 2501-2509.
22. Bellais, S.; Aubert, D.; Naas, T.; Nordmann, P. Molecular and biochemical heterogeneity of class B carbapenem-hydrolyzing β-lactamases in Chryseobacterium meningosepticum. Antimicrob. Agents Chemother. 2000, 44, 1878-1886.
23. Oelschlaeger, P.; Mayo, S. L.; Pleiss, J. Impact of remote mutations on metallo-β-lactamase substrate specificity: Implications for the evolution of antibiotic resistance. Protein Sci. 2005, 14, 765-774.
24. Materon, I. C.; Beharry, Z.; Huang, W.; Perez, C.; Palzkill, T. Analysis of the context dependent sequence requirements of active site residues in the metallo-β-lactamase IMP-1. J. Mol. Biol. 2004, 344, 653-663.
25. Tomatis, P. E.; Rasia, R. M.; Segovia, L.; Vila, A. J. Mimicking natural evolution in metallo-β-lactamases through second-shell ligand mutations. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 13761-13766.
26. Wommer, S.; Rival, S.; Heinz, U.; Galleni, M.; Frere, J. M.; Franceschini, N.; Amicosante, G.; Rasmussen, B.; Bauer, R.; Adolph, H. W. Substrate-activated zinc binding of metallo-β-lactamases - Physiological importance of the mononuclear enzymes. J. Biol. Chem. 2002, 277, 24142-24147.
27. Periyannan, G.; Shaw, P. J.; Sigdel, T.; Crowder, M. W. In vivo folding of recombinant metallo-β-lactamase L1 requires the presence of Zn(II). Protein Sci. 2004, 13, 2236-2243.
28. Rasia, R. M.; Vila, A. J. Structural determinants of substrate binding to Bacillus cereus metallo-β-lactamase. J. Biol. Chem. 2004, 279, 26046-26051.
29. Yanchak, M. P.; Taylor, R. A.; Crowder, M. W. Mutational analysis of metallo-β-lactamase CcrA from Bacteroides fragilis. Biochemistry 2000, 39, 11330-11339.
30. Carenbauer, A. L.; Garrity, J. A.; Periyannan, G.; Yates, R. B.; Crowder, M. W. Probing substrate binding to metallo-β-lactamase L1 from Stenotrophomonas maltophilia by using site-directed mutagenesis. BMC Biochem. 2002, 3, 4-10.
31. Mercuri, P. S.; Garcia-Saez, I.; DeVriendt, K.; Thamm, I.; Devresse, B.; van Beeumen, J.; Dideberg, O.; Rossolini, G. M.; Frere, J. M.; Galleni, M. Probing the specificity of the subclass B3 FEZ-1 metallo-β-lactamase by site-directed mutagenesis. J. Biol. Chem. 2004, 279, 33630-33638.
32. Felici, A.; Amicosante, G.; Oratore, A.; Strom, R.; Ledent, P.; Joris, B.; Fanuel, L.; Frere, J. M. An overview of the kinetic parameters of class B β-lactamases. Biochem. J. 1993, 291, 151-155.
33. Kaminshaia, N. V.; He, C.; Lippard, S. J. Reactivity of m-hydroxodizinc(II) centers in enzymatic catalysis through model studies. Inorg. Chem. 2000, 39, 3365-3373.
34. Toney, J. H.; Hammond, G. G.; Fitzgerald, P. M. D.; Sharma, N.; Balkovec, J. M.; Rouen, G. P.; Olson, S. H.; Hammond, M. L.; Greenlee, M. L.; Gao, Y. D. Succinic acids as potent inhibitors of plasmid-borne IMP-1 metallo-β- lactamase. J. Biol. Chem. 2001, 276, 31913-31918.
35. Kaminskaia, N. V.; Spingler, B.; Lippard, S. J. Intermediate in β-lactam hydrolysis catalyzed by a dinuclear zinc(II) complex: Relevance to the mechanism of metallo-β-lactamase. J. Am. Chem. Soc. 2001, 123, 6555-6563.
36. Spencer, J.; Read, J.; Sessions, R. B.; Howell, S.; Blackburn, G. M.; Gamblin, S. J. Antibiotic recognition by binuclear metallo-β-lactamases revealed by X-ray crystallography. J. Am. Chem. Soc. 2005, 127, 14439-14444.
37. Garrity, J. D.; Pauff, J. M.; Crowder, M. W. Probing the dynamics of a mobile loop above the active site of L1, a metallo-β-lactamase from Stenotrophomonas maltophilia, via site-directed mutagenesis and stopped-flow fluorescence spectroscopy. J. Biol. Chem. 2004, 279, 39663-39670.
38. Park, H.; Brothers, E. N.; Merz, K. M. Hybrid QM/MM and DFT investigations of the catalytic mechanism and inhibition of the dinuclear zinc metallo-β-lactamase CcrA from Bacteroides fragilis. J. Am. Chem. Soc. 2005, 127, 4232-4241.
39. Toney, J. H.; Fitzgerald, P. M. D.; Grover-Sharma, N.; Olson, S. H.; May, W. J.; Sundelof, J. G.; Vanderwall, D. E.; Cleary, K. A.; Grant, S. K.; Wu, J. K.; Kozarich, J. W.; Pompliano, D. L.; Hammond, G. G. Antibiotic sensitization using biphenyl tetrazoles as potent inhibitors of Bacteroides fragilis metallo-β-lactamase. Chem. Biol. 1998, 5, 185-196.
40. Concha, N. O.; Janson, C. A.; Rowling, P.; Pearson, S.; Cheever, C. A.; Clarke, B. P.; Lewis, C.; Galleni, M.; Frere, J. M.; Payne, D. J.; Bateson, J. H.; Abdel-Meguid, S. S. Crystal structure of the IMP-1 metallo-β-lactamase from Pseudomonas aeruginosa and its complex with a mercaptocarboxylate inhibitor: Binding determinants of a potent, broad-spectrum inhibitor. Biochemistry 2000, 39, 4288-4298.
41. Scrofani, S. D. B.; Chung, J.; Huntley, J. J. A.; Benkovic, S. J.; Wright, P. E.; Dyson, H. J. NMR Characterization of the metallo-β-lactamase from Bacteroides fragilis and its interaction with a tight-binding inhibitor: Role of an active-site loop. Biochemistry 1999, 38, 14507-14514.
42. Salsbury, F. R.; Crowley, M. F.; Brooks, C. L. Modeling of the metallo-β-lactamase from B. fragilis: Structural and dynamic effects of inhibitor binding. Proteins 2001, 44, 448-459.
43. Moali, C.; Anne, C.; Lamotte-Brasseur, J.; Groslambert, S.; Devreese, B.; van Beeumen, J.; Galleni, M.; Frere, J. M. Analysis of the importance of the metallo-β-lactamase active site loop in substrate binding and catalysis. Chem. Biol. 2003, 10, 319-329.
44. Dal Peraro, M.; Vila, A. J.; Carloni, P. Substrate binding to mononuclear metallo-β-lactamase from Bacillus cereus. Proteins 2004, 54, 412-423.
45. de Seny, D.; Prosperi-Meys, C.; Bebrone, C.; Rossolini, G. M.; Page, M. I.; Noel, P.; Frere, J. M.; Galleni, M. Mutational analysis of the two zinc-binding sites of the Bacillus cereus 569/H/9 metallo-β-lactamase. Biochem. J. 2002, 363, 687-696.
46. Bounaga, S.; Laws, A. P.; Galleni, M.; Page, M. I. The mechanism of catalysis and the inhibition of the Bacillus cereus zinc-dependent β-lactamase. Biochem. J. 1998, 331, 703-711.
47. Wang, Z.; Fast, W.; Benkovic, S. J. On the mechanism of the metallo-β-lactamase from Bacteroides fragilis. Biochemistry 1999, 38, 10013-10023.
48. Wang, Z.; Fast, W.; Benkovic, S. J. Direct observation of an enzyme-bound intermediate in the catalytic cycle of the metallo-β-lactamase from Bacteroides fragilis. J. Am. Chem. Soc. 1998, 120, 10788-10789.
49. McMannus-Munoz, S.; Crowder, M. W. Kinetic mechanism of metallo-β-lactamase L1 from Stenotrophomonas maltophilia. Biochemistry 1999, 38, 1547-1553.
50. Garrity, J. D.; Bennett, B.; Crowder, M. W. Direct evidence that reaction intermediate in metallo-β-lactamase is metal bound. Biochemistry 2005, 44, 1078-1087.
51. Spencer, J.; Clark, A. R.; Walsh, T. R. Novel mechanism of hydrolysis of therapeutic β-lactams by Stenotrophomonas maltophilia L1 metallo-β-lactamase. J. Biol. Chem. 2001, 276, 33638-33644.
52. Suarez, D.; Brothers, E. N.; Merz, K. M. Insights into the structure and dynamics of the dinuclear zinc β-lactamase site from Bacteroides fragilis. Biochemistry 2002, 41, 6615-6630.
53. Suarez, D.; Diaz, N.; Merz, K. M. Molecular dynamics simulations of the dinuclear zinc-β-lactamase from Bacteroides fragilis complexed with imipenem. J. Comput. Chem. 2002, 23, 1587-1600.
54. Dal Peraro, M.; Vila, A. J.; Carloni, P. Protonation state of Asp120 in the binuclear active site of the metallo-β-lactamase from Bacteroides fragilis. Inorg. Chem. 2003, 42, 4245-4247.
55. Garrity, J. D.; Carenbauer, A. L.; Herron, L. R.; Crowder, M. W. Metal binding Asp-120 in metallo-β-lactamase L1 from Stenotrophomonas maltophilia plays a crucial role in catalysis. J. Biol. Chem. 2004, 279, 920-927.
56. Wang, Z.; Benkovic, S. J. Purification, characterization, and kinetic studies of soluble Bacteroides fragilis metallo-β-lactamase. J. Biol. Chem. 1998, 273, 22402-22408.
57. Fast, W.; Wang, Z.; Benkovic, S. J. Familial mutations and zinc stoichiometry determine the rate-limiting step of nitrocefin hydrolysis by metallo-β-lactamase from Bacteroides fragilis. Biochemistry 2001, 40, 1640-1650.
58. Yamaguchi, Y.; Kuroki, T.; Yasuzawa, H.; Higashi, T.; Jin, W.; Kawanami, A.; Yamagata, Y.; Arakawa, Y.; Goto, M.; Kurosaki, H. Probing the role of Asp120(81) of metallo-β-lactamase (IMP-1) by site-directed mutagenesis, kinetic studies, and X-ray crystallography. J. Biol. Chem. 2005, 280, 20824-20832.
59. Suarez, D.; Merz, K. M. Molecular dynamics simulations of the mononuclear zinc-β-lactamase from Bacillus cereus. J. Am. Chem. Soc. 2001, 123, 3759-3770.
60. Diaz, N.; Suarez, D.; Merz, K. M. Molecular dynamics simulations of the mononuclear zinc-β-lactamase from Bacillus cereus complexed with benzylpenicillin and a quantum chemical study of the reaction mechanism. J. Am. Chem. Soc. 2001, 123, 9867-9879.
61. Orellano, E. G.; Girardini, J. E.; Cricco, J. A.; Ceccarelli, E. A.; Vila, A. J. Spectroscopic characterization of a binuclear metal site in Bacillus cereus β-lactamase II. Biochemistry 1998, 37, 10173-10180.
62. Rasia, R. M.; Vila, A. J. Exploring the role and the binding affinity of a second zinc equivalent in B. cereus metallo-β-lactamase. Biochemistry 2002, 41, 1853-1860.
63. Bicknell, R.; Waley, S. G. Cryoenzymology of Bacillus cereus β-lactamase II. Biochemistry 1985, 24, 6876-6887.
64. Bicknell, R.; Schaffer, A.; Waley, S. G.; Auld, D. S. Changes in the coordination geometry of the active site metal during catalysis of benzylpenicillin hydrolysis by Bacillus cereus β-lactamase II. Biochemistry 1986, 25, 7208-7215.
65. Lim, H. M.; Pene, J. J. Mutations affecting the catalytic activity of Bacillus cereus 5/B/6 β-lactamase II. J. Biol. Chem. 1989, 264, 11682-11687.
66. Rasia, R. M.; Vila, A. J. Mechanistic study of the hydrolysis of nitrocefin mediated by B. cereus metallo-β-lactamase. ARKIVOC 2003, 3, 507-516.
67. Xu, D.; Xie, D.; Guo, H. Catalytic mechanism of class B2 metallo-β-lactamase. J. Biol. Chem. 2006, 281, 8740-8747.
68. Murphy, T. A.: Catto, L. E.; Halford, S. E.; Hadfield, A. T.; Minor, W.; Walsh, T. R.; Spencer J. Crystal structure of Pseudomonas aeruginosa SPM-1 provides insights into variable zinc affinity of metallo-β-lactamases. J. Mol. Biol. 2006, 357, 890-903.
69. Park, H. S.; Nam, S. H.; Lee, J. K. M.; Yoon, C. N.; Mannervik, B.; Benkovic, S. J.; Kim, H. S. Design and evolution of new catalytic activity with an existing protein scaffold. Science 2006, 311, 535-538.