Structural and kinetic studies on metallo-β-lactamase IMP-1

Biochemistry

Volumn 50, Issue 42, 2011, Pages 9125-9134

  Griffin, Dionne H ^a   Richmond, Timothy K ^a   Sanchez, Carlo ^a   Moller, Abraham Jon ^a   Breece, Robert M ^a   Tierney, David L ^a   Bennett, Brian ^b   Crowder, Michael W ^a  

^a MIAMI UNIVERSITY   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTALLOGRAPHIC DATA; EPR SPECTRA; EXAFS; KINETIC STUDY; LACTAMASES; METAL BINDING; METAL-METAL INTERACTIONS; NITROCEFIN; SPECTROSCOPIC STUDIES; STEADY-STATE KINETICS; UV-VIS STUDIES;

CATALYST ACTIVITY; DIALYSIS; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYMES; KINETIC THEORY; KINETICS; METAL IONS; REACTION INTERMEDIATES; SPECTROSCOPIC ANALYSIS; ZINC COMPOUNDS;

METALS;

COBALT; EDETIC ACID; METAL ION; METALLO BETA LACTAMASE; METALLO BETA LACTAMASE IMP 1; NITROCEFIN; UNCLASSIFIED DRUG; ZINC ION;

ARTICLE; CATALYSIS; CHEMICAL INTERACTION; CHEMICAL REACTION; CRYSTALLOGRAPHY; DIALYSIS; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME KINETICS; ENZYME PURIFICATION; ENZYME STABILITY; ENZYME STRUCTURE; GENE OVEREXPRESSION; HYDROLYSIS; METAL BINDING; PRIORITY JOURNAL; SPECTROSCOPY; STEADY STATE; ULTRAVIOLET RADIATION;

BETA-LACTAMASES; CATIONS, DIVALENT; COBALT; ELECTRON SPIN RESONANCE SPECTROSCOPY; ESCHERICHIA COLI; HYDROLYSIS; SERRATIA MARCESCENS; SPECTROPHOTOMETRY, ULTRAVIOLET; X-RAY ABSORPTION SPECTROSCOPY; ZINC;

EID: 80054999128     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200839h     Document Type: Article

References (72)

1. Gupta, V. (2008) Metallo β-lactamases in Pseudomonas aeruginosa and Acinetobacter species Expert Opin. Invest. Drugs 17, 131-143 (Pubitemid 351578196)
2. Perez, F., Endimiani, A., Hujer, K. M., and Bonomo, R. A. (2007) The continuing challenge of ESBLs Curr. Opin. Pharmacol. 7, 459-469 (Pubitemid 47560222)
3. Walsh, T. R., Toleman, M. A., Poirel, L., and Nordmann, P. (2005) Metallo-β-lactamases: the quiet before the storm? Clin. Microbiol. Rev. 18, 306-325
4. Yong, D., Toleman, M. A., Giske, C. G., Cho, H. S., Sundman, K., Lee, K., and Walsh, T. R. (2009) Characterization of a new metallo-β-lactamase gene, blaNDM-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, 5046-5054
5. Osano, E., Arakawa, Y., Wacharotayankun, R., Ohta, M., Horii, T., Ito, H., Yoshimura, F., and Kato, N. (1994) Molecular Characterization of an Enterobacterial Metallo-β-Lactamase Found in a Clinical Isolate of Serratia marcescens That Shows Imipenem Resistance Antimicrob. Agents Chemother. 38, 71-78 (Pubitemid 24018160)
6. Watanabe, M., Iyobe, S., Inoue, M., and Mitsuhashi, S. (1991) Transferable Imipenem Resistance in Pseudomonas aeruginosa Antimicrob. Agents Chemother. 35, 147-151
7. Laraki, N., Galleni, M., Thamm, I., Riccio, M. L., Amicosante, G., Frere, J. M., and Rossolini, G. M. (1999) Structure of In31, a blaIMP-containing Pseudomonas aeruginosa integron phyletically related to In5, which carries an unusual array of gene cassettes Antimicrob. Agents Chemother. 43, 890-901 (Pubitemid 29165754)
8. Oelschlaeger, P., Ai, N., DuPrez, K. T., Welsh, K. J., and Toney, J. H. (2010) Evolving carbapenemases: Can medicinal chemists advance one step ahead of the coming storm? J. Med. Chem. 53, 3013-3027
9. Iyobe, S., Kushadokoro, H., Ozaki, J., Matsumura, N., Minami, S., Haruta, S., Sawai, T., and O'Hara, K. (2000) Amino Acid Substitutions in a Variant of IMP-1 Metallo-β-Lactamase Antimicrob. Agents Chemother. 44, 2023-2027 (Pubitemid 30484421)
10. Yano, H., Kuga, A., Okamoto, R., Kitasato, H., Kobayashi, T., and Inoue, M. (2001) Plasmid-Encoded Metallo-β-Lactamase (IMP-6) Conferring Resistance to Carbapenems, Especially Meropenem Antimicrob. Agents Chemother. 45, 1343-1348 (Pubitemid 32374100)
11. Iyobe, S., Kusadokoro, H., Takahashi, A., Yomoda, S., Okubo, T., Nakamura, A., and O'Hara, K. (2002) Detection of a Variant Metallo-β- Lactamase, IMP-10, from Two Unrelated Strains of Pseudomonas aeruginosa and an Alcaligenes xylosoxidans Strain Antimicrob. Agents Chemother. 46, 2014-2016 (Pubitemid 34535235)
12. Docquier, J. D., Riccio, M. L., Mugnaioli, C., Luzzaro, F., Endimiani, A., Toniolo, A., Amicosante, G., and Rossolini, G. M. (2003) IMP-12, a new plasmid-encoded metallo-β-lactamase from a Pseudomonas putida clinical isolate Antimicrob. Agents Chemother. 47, 1522-1528 (Pubitemid 36548532)
13. Crowder, M. W., Spencer, J., and Vila, A. J. (2006) Metallo-β- lactamases: Novel weaponry for antibiotic resistance in bacteria Acc. Chem. Res. 39, 721-728
14. 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., and Abdel-Meguid, S. S. (2000) 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 39, 4288-4298 (Pubitemid 30212644)
15. 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., and Gao, Y.-D. (2001) Succinic Acids as Potent Inhibitors of Plasmid-borne IMP-1 Metallo-β-lactamase J. Biol. Chem. 276, 31913-31501
16. Yamaguchi, Y., Kuroki, T., Yasuzawa, H., Higashi, T., Jin, W., Kawanami, A., Yamagata, Y., Arakawa, Y., Goto, M., and Kurosaki, H. (2005) 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. 280, 20824-20832 (Pubitemid 40776787)
17. Costello, A., Periyannan, G., Yang, K. W., Crowder, M. W., and Tierney, D. L. (2006) Site-selective binding of Zn(II) to metallo-β-lactamase L1 from Stenotrophomonas maltophilia J. Biol. Inorg. Chem. 11, 351-358
18. Costello, A. L., Sharma, N. P., Yang, K. W., Crowder, M. W., and Tierney, D. L. (2006) X-ray absorption spectroscopy of the zinc bnding sites in the class B2 metallo-β-lactamase ImiS from Aeromonas veronii bv. sobria Biochemistry 45, 13650-13658 (Pubitemid 44748511)
19. Hawk, M. J., Breece, R. M., Hajdin, C. E., Bender, K. M., Hu, Z., Costello, A. L., Bennett, B., Tierney, D. L., and Crowder, M. W. (2009) Differential binding of Co(II) and Zn(II) to metallo-β-lactamase Bla2 from Bacillus anthracis J. Am. Chem. Soc. 131, 10753-10762
20. 2 sites in metallo-β-lactamase L1 J. Am. Chem. Soc. 130, 14207-14216
21. Periyannan, G., Costello, A. L., Tierney, D. L., Yang, K. W., Bennett, B., and Crowder, M. W. (2006) Sequential binding of cobalt(II) to metallo-β-lactamase CcrA Biochemistry 45, 1313-1320 (Pubitemid 43168394)
22. 2 position in metallo-β-lactamases is critical for activity: a study on chimeric metal sites on a conserved protein scaffold J. Mol. Biol. 373, 1141-1156 (Pubitemid 47539476)
23. Orellano, E. G., Girardini, J. E., Cricco, J. A., Ceccarelli, E. A., and Vila, A. J. (1998) Spectroscopic characterization of a binuclear metal site in Bacillus cereus β-lactamase II Biochemistry 37, 10173-10180 (Pubitemid 28366372)
24. Crowder, M. W., Walsh, T. R., Banovic, L., Pettit, M., and Spencer, J. (1998) Overexpression, Purification, and Characterization of the Cloned Metallo-β-Lactamase L1 from Stenotrophomonas maltophilia Antimicrob. Agents Chemother. 42, 921-926 (Pubitemid 28216380)
25. McManus-Munoz, S. and Crowder, M. W. (1999) Kinetic mechanism of metallo-β-lactamase L1 from Stenotrophomonas maltophilia Biochemistry 38, 1547-1553
26. Segel, I. H. (1993) Enzyme Kinetics, John Wiley and Sons, Inc., New York.
27. Thomas, P. W., Stone, E. M., Costello, A., Tierney, D. L., and Fast, W. (2005) The quorum-quenching lactonase from Bacillus thuringiensis is a metalloprotein Biochemistry 44, 7559-7569 (Pubitemid 40696009)
28. Newville, M. (2001) IFEFFIT: interactive XAFS analysis and FEFF fitting J. Synchrotron Radiat. 8, 322-324 (Pubitemid 33661380)
29. Ankudinov, A. L., Ravel, B., Rehr, J. J., and Conradson, S. D. (1998) Real-space multiple-scattering calculation and interpretation of x-ray-absorption near-edge structure Phys. Rev. B 58, 7565-7576 (Pubitemid 128486524)
30. Laraki, N., Franceschini, N., Rossolini, G. M., Santucci, P., Meunier, C., dePauw, E., Amicosante, G., Frere, J. M., and Galleni, M. (1999) Biochemical Characterization of the Pseudomonas aeruginosa 101/1477 Metallo-β- Lactamase IMP-1 Produced by Escherichia coli Antimicrob. Agents Chemother. 43, 902-906 (Pubitemid 29165755)
31. Moali, C., Anne, C., Lamotte-Brasseur, J., Groslambert, S., Devreese, B., Van Beeumen, J., Galleni, M., and Frere, J. M. (2003) Analysis of the importance of the metallo-β-lactamase active site loop in substrate binding and catalysis Chem. Biol. 10, 319-329 (Pubitemid 36516650)
32. Wang, Z. and Benkovic, S. J. (1998) Purification, Characterization, and Kinetic Studies of Soluble Bacteroides fragilis Metallo-β-Lactamase J. Biol. Chem. 273, 22402-22408 (Pubitemid 28399803)
33. Rasia, R. M. and Vila, A. J. (2003) Mechanistic study of the hydrolysis of nitrocefin mediated by B. cereus metallo-β-lactamase ARKIVOC 3, 507-516 (Pubitemid 38957065)
34. Crowder, M. W., Yang, K. W., Carenbauer, A. L., Periyannan, G., Seifert, M. A., Rude, N. E., and Walsh, T. R. (2001) The Problem of a Solvent Exposable Disulfide when Preparing Co(II)-Substituted Metallo-β-Lactamase L1 from Stenotrophomonas maltophilia J. Biol. Inorg. Chem. 6, 91-99 (Pubitemid 32825475)
35. Garmer, D. R. and Krauss, M. (1993) Ab Initio Quantum Chemical Study of the Cobalt d-d Spectroscopy of Several Substituted Zinc Enzymes J. Am. Chem. Soc. 115, 10247-10257
36. Bennett, B. (2010) EPR of cobalt-substituted zinc enzymes, in Metals in Biology-Applications of high-resolution EPR to metalloenzymes (Hanson, G. R., Ed.) pp 345-370, Springer, Berlin.
37. Bennett, B., Antholine, W. E., D'Souza, V. M., Chen, G. J., Ustinyuk, L., and Holz, R. C. (2002) Structurally distinct active sites in the copper(II)- substituted aminopeptidases from Aeromonas proteolytica and Escherichia coli J. Am. Chem. Soc. 124, 13025-13034 (Pubitemid 35247114)
38. Wright, G. D. (2011) Molecular mechanisms of antibiotic resistance Chem. Commun. 47, 4055-4061
39. Walsh, C. T. and Wright, G. D. (2005) Introduction: Antibiotic resistance Chem. Rev. 105, 391-393 (Pubitemid 40351627)
40. Drawz, S. M. and Bonomo, R. A. (2010) Three decades of β-lactamase inhibitors Clin. Microbiol. Rev. 23, 160-201
41. Hammond, G. G., Huber, J. L., Greenlee, M. L., Laub, J. B., Young, K., Silver, L. L., Balkovec, J. M., Pryor, K. D., Wu, J. K., Leiting, B., Pompliano, D. L., and Toney, J. H. (1999) Inhibition of IMP-1 Metallo-β-Lactamase and Sensitization of IMP-1 Producing Bacteria by Thioester Derivatives FEMS Microbiol. Lett. 459, 289-296 (Pubitemid 29460690)
42. Kurosaki, H., Yamaguchi, Y., Higashi, T., Soga, K., Matsueda, S., Yumoto, H., Misumi, S., Yamagata, Y., Arakawa, Y., and Goto, M. (2005) Irreversible inhibition of metallo-β-lactamase (IMP-1) by 3-(3- mercaptopropionylsulfanyl)-propionic acid pentafluorophenyl ester Angew. Chem., Int. Ed. 44, 3861-3864 (Pubitemid 40885694)
43. Lassaux, P., Hamel, M., Gulea, M., Delbruck, H., Mercuri, P. S., Horsfall, L., Dehareng, D., Kupper, M., Frere, J. M., Hoffmann, K., Galleni, M., and Bebrone, C. (2010) Mercaptophosphonate compounds as broad-spectrum inhibitors of the metallo-β-lactamases J. Med. Chem. 53, 4862-4876
44. Moloughney, J. G., Thomas, J. D., and Toney, J. H. (2005) Novel IMP-1 metallo-β-lactamase inhibitors can reverse Meropenem resistance in Escherichia coli expressing IMP-1 FEMS Microbiol. Lett. 243, 65-71 (Pubitemid 40164390)
45. Siemann, S., Brewer, D., Clarke, A. J., Dmitrienko, G. I., Lajoie, G., and Viswanatha, T. (2002) IMP-1 metallo-β-lactamase: effect of chelators and assessment of metal requirement by electrospray mass spectrometry Biochim. Biophys. Acta, Gen. Subj. 1571, 190-200 (Pubitemid 34686921)
46. Toney, J. H. and Moloughney, J. G. (2004) Metallo-β-lactamase inhibitors: promise for the future? Curr. Opin. Invest. Drugs 5, 823-826
47. Wang, C. and Guo, H. (2007) Inhibitor binding by metallo-β-lactamase IMP-1 from Pseudomonas aeruginosa: Quantum mechanical/molecular mechanical simulations J. Phys. Chem. B 111, 9986-9992 (Pubitemid 47387883)
48. Garrity, J. D., Bennett, B., and Crowder, M. W. (2005) Direct evidence that reaction intermediate in metallo-β-lactamase is metal bound Biochemistry 44, 1078-1087 (Pubitemid 40129667)
49. Sharma, N. P., Hajdin, C., Chandrasekar, S., Bennett, B., Yang, K. W., and Crowder, M. W. (2006) Mechanistic studies on the mononuclear Zn(II)-containing metallo-β-lactamase ImiS from Aeromonas sobria Biochemistry 45, 10729-10738 (Pubitemid 44320488)
50. Goto, M., Takahashi, T., Yamashita, F., Koreeda, A., Mori, H., Ohta, M., and Arakawa, Y. (1997) Inhibition of the Metallo-b-Lactamase Produced from Serratia marcescens by Thiol Compounds Biol. Pharm. Bull. 20, 1136-1140 (Pubitemid 28543258)
51. Materon, I. C. and Palzkill, T. (2001) Identification of residues critical for metallo-β-lactamase function by codon randomization and selection Protein Sci. 10, 2556-2565 (Pubitemid 33091580)
52. Oelschlaeger, P., Mayo, S. L., and Pleiss, J. (2005) Impact of remote mutations on metallo-β-lactamase substrate specificity: implications for the evolution of antibiotic resistance Protein Sci. 14, 765-774 (Pubitemid 40283915)
53. Bounaga, S., Laws, A. P., Galleni, M., and Page, M. I. (1998) The Mechanism of Catalysis and the Inhibition of the Bacillus cereus Zinc-Dependent β-Lactamase Biochem. J. 331, 703-711 (Pubitemid 28211890)
54. Wang, Z., Fast, W., and Benkovic, S. J. (1998) Direct Observation of an Enzyme-Bound Intermediate in the Catalytic Cycle of the Metallo-β-Lactamase from Bacteroides fragilis J. Am. Chem. Soc. 120, 10788
55. Carfi, A., Duee, E., Galleni, M., Frere, J. M., and Dideberg, O. (1998) 1.85 A Resolution Structure of the ZincII β-Lactamase II from Bacillus cereus Acta Crystallogr. D54, 313-323
56. Gonzales, J. M., Buschiazzo, A., and Vila, A. J. (2010) Evidence of Adaptability in metal coordination geometry and active-site loop conformation among B1 metallo-β-lactamases Biochemistry 49, 7930-7938
57. Gardonio, D. and Siemann, S. (2009) Chelator-facilitated chemical modification of IMP-1 metallo-β-lactamase and its consequences on metal binding Biochem. Biophys. Res. Commun. 381, 107-111
58. Wommer, S., Rival, S., Heinz, U., Galleni, M., Frere, J. M., Franceschini, N., Amicosante, G., Rasmussen, B., Bauer, R., and Adolph, H. W. (2002) Substrate-activated zinc binding of metallo-β-lactamases- Physiological importance of the mononuclear enzymes J. Biol. Chem. 277, 24142-24147 (Pubitemid 34951928)
59. Heinz, U. and Adolph, H. W. (2004) Metallo-β-lactamases: two binding sites for one catalytic metal ion? Cell. Mol. Life Sci. 61, 2827-2839 (Pubitemid 40064330)
60. Fast, W., Wang, Z., and Benkovic, S. J. (2001) Familial Mutations and Zinc Stoichiometry Determine the Rate-Limiting Step of Nitrocefin Hydrolysis by Metallo-β-Lactamase from Bacteroides fragilis Biochemistry 40, 1640-1650 (Pubitemid 32144033)
61. Paul-Soto, R., Hernandez-Valladares, M., Galleni, M., Bauer, R., Zeppezauer, M., Frere, J. M., and Adolph, H. W. (1998) Mono- and Binuclear Zn-β-Lactamase from Bacteroides fragilis: Catalytic and Structural Roles of the Zinc Ions FEBS Lett. 438, 137-140 (Pubitemid 28517851)
62. Dal Peraro, M., Vila, A. J., and Carloni, P. (2004) Substrate binding to Mononuclear metallo-β-lactamase from Bacillus cereus Proteins: Struct., Funct., Bioinf. 54, 412-423 (Pubitemid 38202184)
63. de Seny, D., Heinz, U., Wommer, S., Kiefer, M., Meyer-Klaucke, W., Galleni, M., Frere, J. M., Bauer, R., and Adolph, H. W. (2001) Metal ion binding and coordination geometry for wild type and mutants of metallo-β-lactamase from Bacillus cereus 569/H/9 (BcII)-A combined thermodynamic, kinetic, and spectroscopic approach J. Biol. Chem. 276, 45065-45078
64. Estiu, G. L., Rasia, R. M., Cricco, J. A., Vila, A. J., and Zerner, M. C. (2002) Is there a bridging ligand in metal-substituted zinc β-lactamases? A spectroscopic and theoretical answer Int. J. Quantum Chem. 88, 118-132 (Pubitemid 34495328)
65. Paul-Soto, R., Bauer, R., Frere, J. M., Galleni, M., Meyer-Klaucke, W., Nolting, H., Rossolini, G. M., de Seny, D., Hernandez-Villadares, M., Zeppezauer, M., and Adolph, H. W. (1999) Mono- and Binuclear Zn2+ β-Lactamase J. Biol. Chem. 274, 13242-13249
66. Rasia, R. M. and Vila, A. J. (2002) Exploring the role and the binding affinity of a second zinc equivalent in B. cereus metallo-β-lactamase Biochemistry 41, 1853-1860 (Pubitemid 34132260)
67. Selevsek, N., Rival, S., Tholey, A., Heinzle, E., Heinz, U., Hemmingsen, L., and Adolph, H. W. (2009) Zinc ion-induced domain organization in metallo-β-lactamases. A flexible "zinc arm" for rapid metal ion transfer J. Biol. Chem. 284, 16419-16431
68. Jacquin, O., Balbeur, D., Damblon, C., Marchot, P., dePauw, E., Roberts, G. C. K., Frere, J. M., and Matagne, A. (2009) Positively cooperative binding of zinc ions to Bacillus cereus 569/H/9 β-lactamase II suggests that the binuclear enzyme is the only relevant form for catalysis J. Mol. Biol. 392, 1278-1291
69. Badarau, A., Damblon, C., and Page, M. I. (2007) The activity of the dinuclear cobalt-β-lactamase from Bacillus cereus in catalysing the hydrolysis of β-lactams Biochem. J. 401, 197-203 (Pubitemid 46114613)
70. Badarau, A. and Page, M. I. (2006) Enzyme deactivation due to metal ion dissociation during turnover of the cobalt-β-lactamase catalyzed hydrolysis of β-lactams Biochemistry 45, 11012-11020 (Pubitemid 44360172)
71. Badarau, A. and Page, M. I. (2008) Loss of enzyme activity during turnover of the Bacillus cereus β-lactamase catalysed hydrolysis of β-lactams due to loss of zinc ions J. Biol. Inorg. Chem. 13, 919-928
72. Llarrull, L. I., Tioni, M. F., Kowalski, J., Bennett, B., and Vila, A. J. (2007) Evidence for a Dinuclear Active Site in the Metallo-β-lactamase BcII with Substoichiometric Co(II): A new model for metal uptake J. Biol. Chem. 282, 30586-30595 (Pubitemid 350035178)