Biochemical, mechanistic, and spectroscopic characterization of metallo-β-lactamase VIM-2

Biochemistry

Volumn 53, Issue 46, 2014, Pages 7321-7331

  Aitha, Mahesh ^a   Marts, Amy R ^a   Bergstrom, Alex ^a   Møller, Abraham Jon ^a   Moritz, Lindsay ^a   Turner, Lucien ^a   Nix, Jay C ^b   Bonomo, Robert A ^c,d   Page, Richard C ^a   Tierney, David L ^a   Crowder, Michael W ^a  

^a MIAMI UNIVERSITY   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^d CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYES; ENZYMES; SPECTROSCOPIC ANALYSIS; ZINC COMPOUNDS;

ANIONIC INTERMEDIATES; LACTAMASES; METAL BINDING; SPECTROSCOPIC CHARACTERIZATION; SPECTROSCOPIC STUDIES;

ZINC;

COBALT; HISTIDINE; METALLO BETA LACTAMASE; METALLO BETA LACTAMASE VIM 2; UNCLASSIFIED DRUG; ZINC; BETA LACTAMASE; VIM-2 BETA-LACTAMASE;

ARTICLE; BIOCHEMISTRY; CRYSTAL STRUCTURE; ELECTRON SPIN RESONANCE; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME MECHANISM; ENZYME PURIFICATION; ENZYME STRUCTURE; EXAFS SPECTROSCOPY; GEL FILTRATION CHROMATOGRAPHY; METAL BINDING; OXIDATION; PH; PROTEIN EXPRESSION; SPECTROSCOPY; STEADY STATE; STOICHIOMETRY; ULTRAVIOLET SPECTROSCOPY; X RAY ABSORPTION SPECTROSCOPY; X RAY CRYSTALLOGRAPHY; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; METABOLISM; MOLECULAR CLONING; PSEUDOMONAS AERUGINOSA; UPREGULATION;

BETA-LACTAMASES; BINDING SITES; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; MODELS, MOLECULAR; PSEUDOMONAS AERUGINOSA; SPECTRUM ANALYSIS; UP-REGULATION; ZINC;

EID: 84913546091     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500916y     Document Type: Article

References (76)

1. CDC (2013) Antibiotic resistance threats in the United States, http://www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf.
2. Nordmann, P., Naas, T., and Poirel, L. (2011) Global spread of carbapenemase-producing Enterobacteriaceae Emerging Infect. Dis. 17, 1791-1798
3. Watanabe, M., Iyobe, S., Inoue, M., and Mitsuhashi, S. (1991) Transferable imipenem resistance in Pseudomonas aeruginosa Antimicrob. Agents Chemother. 35, 147-151
4. 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
5. Bush, K. (2013) The ABCD's of β-lactamase nomenclature J. Infect. Chemother. 19, 549-559
6. Osano, E., Arakawa, Y., Wacharotayankun, R., Ohta, M., Horii, T., Ito, H., Yoshimura, F., and Kato, N. (1994) Molecular characterization of an enterobacterial metallo-b-lactamase found in a clinical isolate of Serratia marcescens that shows imipenem resistance Antimicrob. Agents Chemother. 38, 71-78
7. Nordmann, P., Poirel, L., Walsh, T. R., and Livermore, D. M. (2011) The emerging NDM carbapenemases Trends Microbiol. 19, 588-595
8. Jacoby, G. and Bush, K., β-Lactamase classification and amino acid sequences for TEM, SHV and OXA extended-spectrum and inhibitor resistant enzymes, http://www.lahey.org/Studies/ (accessed July 13, 2014).
9. Johnson, A. P. and Woodford, N. (2013) Global spread of antibiotic resistance: the example of New Delhi metallo-β-lactamase (NDM)-mediated carbapenem resistance J. Med. Microbiol. 62, 499-513
10. Lauretti, L., Riccio, M. L., Mazzariol, A., Cornaglia, G., Amicosante, G., Fontana, R., and Rossolini, G. M. (1999) Cloning and characterization of blaVIM, a new integron-borne metallo-β-lactamase gene from a Pseudomonas aeruginosa clinical isolate Antimicrob. Agents Chemother. 43, 1584-1590
11. Yang, Y., Keeney, D., Tang, X. J., Canfield, N., and Rasmussen, B. A. (1999) Kinetic properties and metal content of the metallo-β-lactamase CcrA harboring selective amino acid substitutions J. Biol. Chem. 274, 15706-15711
12. Frasson, I., Biasolo, M. A., Bartolini, A., Cavallaro, A., Richter, S. N., and Palu, G. (2013) Rapid detection of blaVIM-1-37 and blaKPC1/2-12 alleles from clinical samples by multiplex PCR-based assays Int. J. Antimicrob. Agents 42, 68-71
13. Cornaglia, G., Giamarellou, H., and Rossolini, G. M. (2011) Metallo-β-lactamases: a last frontier for β-lactams? Lancet Infect. Dis. 11, 381-393
14. Poirel, L., Naas, T., Nicolas, D., Collet, L., Bellais, S., Cavallo, J. D., and Nordmann, P. (2000) Characterization of VIM-2, a carbapenem-hydrolyzing metallo-β-lactamase and its plasmid- and integron-borne gene from a Pseudomonas aeruginosa clinical isolate in France Antimicrob. Agents Chemother. 44, 891-897
15. Yan, J. J., Hsueh, P. R., Ko, W. C., Luh, K. T., Tsai, S. H., Wu, H. M., and Wu, J. J. (2001) Metallo-β-lactamases in clinical Pseudomonas isolates in Taiwan and identification of VIM-3, a novel variant of the VIM-2 enzyme Antimicrob. Agents Chemother. 45, 2224-2228
16. Mavroidi, A., Tsakris, A., Tzelepi, E., Pournaras, S., Loukova, V., and Tzouvelekis, L. S. (2000) Carbapenem-hydrolysing VIM-2 metallo-β-lactamase in Pseudomonas aeruginosa from Greece J. Antimicrob. Chemother. 46, 1041-1042
17. Pallecchi, L., Riccio, M. L., Docquier, J. D., Fontana, R., and Rossolini, G. M. (2001) Molecular heterogeneity of bla(VIM-2)-containing integrons from Pseudomonas aeruginosa plasmids encoding the VIM-2 metallo-β-lactamase FEMS Microbiol. Lett. 195, 145-150
18. Lolans, K., Queenan, A. M., Bush, K., Sahud, A., and Quinn, J. P. (2005) First nosocomial outbreak of Pseudomonas aeruginosa producing an integron-borne metallo-β-lactamase (VIM-2) in the United States Antimicrob. Agents Chemother. 49, 3538-3540
19. Yu, Y. S., Qu, T. T., Zhou, J. Y., Wang, J., Li, H. Y., and Walsh, T. R. (2006) Integrons containing the VIM-2 metallo-β-lactamase gene among imipenem-resistant Pseudomonas aeruginosa strains from different Chinese hospitals J. Clin. Microbiol. 44, 4242-4245
20. Duljasz, W., Gniadkowski, M., Sitter, S., Wojna, A., and Jebelean, C. (2009) First organisms with acquired metallo-β-lactamases (IMP-13, IMP-22, and VIM-2) reported in Austria Antimicrob. Agents Chemother. 53, 2221-2222
21. Pournaras, S., Maniati, M., Petinaki, E., Tzouvelekis, L. S., Tsakris, A., Legakis, N. J., and Maniatis, A. N. (2003) Hospital outbreak of multiple clones of Pseudomonas aeruginosa carrying the unrelated metallo-β-lactamase gene variants blaVIM-2 and blaVIM-4 J. Antimicrob. Chemother. 51, 1409-1414
22. Cardoso, O., Alves, A. F., and Leitao, R. (2008) Metallo-β-lactamase VIM-2 in Pseudomonas aeruginosa isolates from a cystic fibrosis patient Int. J. Antimicrob. Agents 31, 375-379
23. Castanheira, M., Bell, J. M., Turnidge, J. D., Mathai, D., and Jones, R. N. (2009) Carbapenem resistance among Pseudomonas aeruginosa strains from India: evidence for nationwide endemicity of multiple metallo-β-lactamase clones (VIM-2, -5, -6, and -11 and the newly characterized VIM-18) Antimicrob. Agents Chemother. 53, 1225-1227
24. Griffin, D. H., Richmond, T. K., Sanchez, C., M?ller, A. J., Breece, R. M., Tierney, D. L., Bennett, B., and Crowder, M. W. (2011) Structural and kinetic studies on metallo-β-lactamase IMP-1 Biochemistry 50, 9125-9134
25. Thomas, P. W., Zheng, M., Wu, S., Guo, H., Liu, D., Xu, D., and Fast, W. (2011) Characterization of purified New Delhi metallo-β-lactamase-1 Biochemistry 50, 10102-10113
26. Yang, H., Aitha, M., Hetrick, A. M., Richmond, T. K., Tierney, D. L., and Crowder, M. W. (2012) Mechanistic and spectroscopic studies of metallo-β-lactamase NDM-1 Biochemistry 51, 3839-3847
27. Yang, H., Aitha, M., Marts, A. R., Hetrick, A., Bennett, B., Crowder, M. W., and Tierney, D. L. (2014) Spectroscopic and mechanistic studies of heterodimetallic forms of metallo-β-lactamase NDM-1 J. Am. Chem. Soc. 136, 7273-7285
28. Yamaguchi, Y., Jin, W., Matsunaga, K., Ikemizu, S., Yamagata, Y., Wachino, J. I., Shibata, N., Arakawa, Y., and Kurosaki, H. (2007) Crystallographic investigation of the inhibition mode of a VIM-2 metallo-β-lactamase from Pseudomonas aeruginosa by a mercaptocarboxylate inhibitor J. Med. Chem. 50, 6647-6653
29. Garcia-Saez, I., Docquier, J. D., Rossolini, G. M., and Dideberg, O. (2008) The three-dimensional structure of VIM-2, a Zn-β-lactamase from Pseudomonas aeruginosa in its reduced and oxidised form J. Mol. Biol. 375, 604-611
30. Borgianni, L., Vandenameele, J., Matagne, A., Bini, L., Bonomo, R. A., Frere, J. M., Rossolini, G. M., and Docquier, J. D. (2010) Mutational analysis of VIM-2 reveals an essential determinant for metallo-β-lactamase stability and folding Antimicrob. Agents Chemother. 54, 3197-3204
31. Rajagopalan, P. T. R., Grimme, S., and Pei, D. H. (2000) Characterization of cobalt(II)-substituted peptide deformylase: Function of the metal ion and the catalytic residue Glu-133 Biochemistry 39, 779-790
32. Docquier, J. D., Lamotte-Brasseur, J., Galleni, M., Amicosante, G., Frere, J. M., and Rossolini, G. M. (2003) On functional and structural heterogeneity of VIM-type metallo-β-lactamases J. Antimicrob. Chem. 51, 257-266
33. Hu, Z. X., Periyannan, G. R., and Crowder, M. W. (2008) Folding strategy to prepare Co(II)-substituted metallo-β-lactamase L1 Anal. Biochem. 378, 177-183
34. Segel, I. H. (1993) Enzyme Kinetics, John Wiley and Sons, Inc., New York.
35. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674
36. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D 66, 213-221
37. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot Acta Cryst. D 66, 486-501
38. The PyMOL Molecular Graphics System, Version 1.6.0.0 (2013), Schrödinger, LLC.
39. Chen, V. B., Arendall, W. B., Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. D 66, 12-21
40. Thomas, P. W., Stone, E. M., Costello, A. L., Tierney, D. L., and Fast, W. (2005) The quorum-quenching lactonase from Bacillus thuringiensis is a metalloprotein Biochemistry 44, 7559-7565
41. 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
42. McManus-Munoz, S. and Crowder, M. W. (1999) Kinetic mechanism of metallo-β-lactamase L1 from Stenotrophomonas maltophilia Biochemistry 38, 1547-1553
43. Garrity, J. D., Bennett, B., and Crowder, M. W. (2005) Direct evidence that the reaction intermediate of metallo-β-lactamase L1 is metal bound Biochemistry 44, 1078-1087
44. 2 sites in metallo-β-lactamase L1 J. Am. Chem. Soc. 130, 14207-14216
45. Hu, Z., Spadafora, L. J., Hajdin, C. E., Bennett, B., and Crowder, M. W. (2009) Structure and mechanism of copper- and nickel-substituted analogues of metallo-β-lactamase L1 Biochemistry 48, 2981-2989
46. Borra, P. S., Leiros, H. K. S., Ahmad, R., Spencer, J., Leiros, I., Walsh, T. R., Sundsfjord, A., and Samuelsen, O. (2011) Structural and computational investigations of VIM-7: insights into the substrate specificity of vim metallo-β-lactamases J. Mol. Biol. 411, 174-189
47. 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
48. 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
49. Wang, Z. G. and Benkovic, S. J. (1998) Purification, characterization, and kinetic studies of a soluble Bacteroides fragilis metallo-β-lactamase that provides multiple antibiotic resistance J. Biol. Chem. 273, 22402-22408
50. Crowder, M. W., Yang, K. W., Carenbauer, A. L., Periyannan, G., Seifert, M. E., 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. Chem. 6, 91-99
51. 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
52. Bennett, B. (2010) in EPR of cobalt-substituted zinc enzymes, Metals in Biology (Hanson, G. and Berliner, L., Eds.) pp 345-370, Springer, Berlin.
53. Wang, Z. G., 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, 10788-10789
54. Hawk, M. J., Breece, R. M., Hajdin, C. E., Bender, K. M., Hu, Z. X., 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
55. 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
56. Sharma, N. P., Hajdin, C., Chandrasekar, S., Bennett, B., Yang, K. W., and Crowder, M. W. (2006) Mechanistic studies on the mononuclear ZnII-containing metallo-β-lactamase ImiS from Aeromonas sobria Biochemistry 45, 10729-10738
57. Periyannan, G. R., 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
58. Breece, R. M., Llarrull, L. I., Tioni, M. F., Vila, A. J., and Tierney, D. L. (2012) X-ray absorption spectroscopy of metal site speciation in the metallo-β-lactamase BcII from Bacillus cereus J. Inorg. Biochem. 111, 182-186
59. 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
60. Llarrull, L. I., Tioni, M. F., and Vila, A. J. (2008) Metal content and localization during turnover in B. cereus metallo-β-lactamase J. Am. Chem. Soc. 130, 15842-15851
61. 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 Asp-120(81) of metallo-β-lactamase (IMP-1) by site-directed mutagenesis, kinetic studies, and X-ray crystallography J. Biol. Chem. 280, 20824-20832
62. 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
63. 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
64. Kurosaki, H., Yamaguchi, Y., Yasuzawa, H., Jin, W., Yamagata, Y., and Arakawa, Y. (2006) Probing, inhibition, and crystallographic characterization of metallo-β-lactamase (IMP-1) with fluorescent agents containing dansyl and thiol groups ChemMedChem 1, 969-972
65. Toney, J. H., Hammond, G. G., Fitzgerald, P. M., 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, 31913-31918
66. Llarrull, L. I., Fabiane, S. M., Kowalski, J. M., Bennett, B., Sutton, B. J., and Vila, A. J. (2007) Asp-120 locates Zn2 for optimal metallo-β-lactamase activity J. Biol. Chem. 282, 18276-18285
67. Davies, A. M., Rasia, R. M., Vila, A. J., Sutton, B. J., and Fabiane, S. M. (2005) 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 44, 4841-4849
68. King, D. T., Worrall, L. J., Gruninger, R., and Strynadka, N. C. (2012) New Delhi metallo-β-lactamase: structural insights into β-lactam recognition and inhibition J. Am. Chem. Soc. 134, 11362-11365
69. King, D. and Strynadka, N. (2011) Crystal structure of New Delhi metallo-β-lactamase reveals molecular basis for antibiotic resistance Protein Sci. 20, 1484-1491
70. Zhang, H. and Hao, Q. (2011) Crystal structure of NDM-1 reveals a common β-lactam hydrolysis mechanism FASEB J. 25, 2574-2582
71. Toney, J. H., Fitzgerald, P. M., 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., and Hammond, G. G. (1998) Antibiotic sensitization using biphenyl tetrazoles as potent inhibitors of Bacteroides fragilis metallo-β-lactamase Chem. Biol. 5, 185-196
72. Carfi, A., Duee, E., Paul-Soto, R., Galleni, M., Frere, J. M., and Dideberg, O. (1998) X-ray structure of the ZnII β-lactamase from Bacteroides fragilis in an orthorhombic crystal form Acta Crystallogr. D 54, 45-57
73. Fitzgerald, P. M., Wu, J. K., and Toney, J. H. (1998) Unanticipated inhibition of the metallo-β-lactamase from Bacteroides fragilis by 4-morpholineethanesulfonic acid (MES): a crystallographic study at 1.85-Å resolution Biochemistry 37, 6791-6800
74. Concha, N. O., Rasmussen, B. A., Bush, K., and Herzberg, O. (1996) Crystal structure of the wide-spectrum binuclear zinc β-lactamase from Bacteroides fragilis Structure 4, 823-836
75. 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
76. Gonzalez, J. M., Meini, M. R., Tomatis, P. E., Medrano Martin, F. J., Cricco, J. A., and Vila, A. J. (2012) Metallo-β-lactamases withstand low Zn(II) conditions by tuning metal-ligand interactions Nat. Chem. Biol. 8, 698-700