The variation of catalytic efficiency of Bacillus cereus metallo-β-lactamase with different active site metal ions

Biochemistry

Volumn 45, Issue 35, 2006, Pages 10654-10666

  Badarau, Adriana ^a   Page, Michael I ^a  

^a UNIVERSITY OF HUDDERSFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; COBALT; HYDROLYSIS; IONS; MANGANESE COMPOUNDS; PH EFFECTS; ZINC;

BACILLUS CEREUS METALLO-Β-LACTAMASE; CATALYTIC EFFICIENCY; CEPHALORIDINE;

ENZYME KINETICS;

BACTERIAL ENZYME; CAPTOPRIL; CARBONYL DERIVATIVE; CEFALEXIN; CEFALORIDINE; CEFOXITIN; COBALT; HYDROXIDE; LEWIS ACID; MANGANESE; METAL ION; METALLO BETA LACTAMASE; PENICILLIN G; WATER; ZINC;

ARTICLE; BACILLUS CEREUS; CATALYSIS; COMPETITIVE INHIBITION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME KINETICS; ENZYME MECHANISM; ENZYME SUBSTRATE; HYDROLYSIS; NONHUMAN; PH; PKA; PRIORITY JOURNAL; STEADY STATE;

BACILLUS CEREUS; BETA-LACTAMASES; BINDING SITES; CATALYSIS; HYDROGEN-ION CONCENTRATION; KINETICS; METALS; MOLECULAR STRUCTURE; PROTEIN BINDING; WATER;

BACILLUS CEREUS;

EID: 33748253736     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060934l     Document Type: Article

References (69)

1. Frère, J. M. (1995) Beta-lactamases and bacterial resistance to antibiotics, Mol. Microbiol. 16, 385-395.
2. Fisher J. D., Meroueh, S. O., and Mobashery, S. (2005) Bacterial resistance to β-lactam antibiotics: compelling opportunism, compelling opportunity, Chem. Rev. 105, 395-424.
3. Galleni, M., Lamotte-Brasseur, J., Rossolini, G. M., Spencer, J., Dideberg, O., and Frère, J. M. (2001) Standard numbering scheme for class B β-lactamases, Antimicrob. Agents Chemother. 45, 660-663.
4. Fabiane, S. M., Sohi, M. K., Wan, T., Payne, D. J., Bateson, J. H., Mitchell, T., and Sutton, B. J. (1998) 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 37, 12404-12411.
5. 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.
6. 2+-β-lactamase. Role of the conserved cysteine in the catalytic mechanism, J. Biol. Chem. 274, 13242-13249.
7. 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.
8. 2+-β-lactamase from Bacteroides fragilis: catalytic and structural roles of the zinc ions, FEBS Lett. 438, 137-140.
9. Yang, Y., Keeney, D., Tang, X., 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.
10. Wang, Z., Fast, W., and Benkovic, S. J. (1999) On the mechanism of the Bacteroides fragilis metallo-β-lactamase, Biochemistry 38, 10013-10023.
11. Laraki, N., Franceschini, N., Rossolini, G. M., Santucci, P., Meunier, C., de Pauw, E., Amicosante, G., Frère, J. M., and Galleni, M. (1999) Biochemical characterisation of the Pseudomonas aeruginosa 101/1477 metallo-β-lactamase IMP-1 produced by Escherichia coli, Antimicrob. Agents Chemother. 43, 902-906.
12. Haruta, S., Yamaguchi, H., Yamamoto, E. T., Eriguchi, Y., Nukaga, M., O'Hara, K., and Sawai, T. (2000) Functional analysis of the active site of a metallo-β-lactamase proliferating in Japan, Antimicrob. Agents Chemother. 44, 2304-2309.
13. Concha, N. O., Janson, C. A., Rowling, P., Pearson, S., Cheever, C. A., Clarke, B. P., Lewis, C., Galleni, M., Frère, 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.
14. Garcia-Saez, I., Hopkins, J., Papamicael, C., Franceschini, N., Amicosante, G., Rossolini, G. M., Galleni, M., Frère, J. M., and Dideberg, O. (2003) The 1.5-A Structure of Chryseobacterium meningosepticum zinc β-Lactamase in complex with the inhibitor, D-Captopril, J. Biol. Chem. 278, 23868-23873.
15. Crowder, M. W., and Walsh, T. R. (1999) Structure and function of metallo-β-lactamases, Recent Res. Dev. Antimicrob. Agents Chemother. 3, 105-132.
16. Hernandez Valladares, M., Felici, A., Weber, G., Adolph, H. W., Zeppezauer, M., Rossolini, G. M., Amicosante, G., Frère, J. M., and Galleni, M. (1997) Zn(II) dependence of the Aeromonas hydrophila AE036 metallo-β-lactamase activity and stability, Biochemistry 36, 11534-11541.
17. Crawford, P. A., Yang, K. W., Sharma, N., Bennett, B., and Crowder, M. W. (2005) Spectroscopic studies on cobalt(II)-substituted metallo-β-lactamase ImiS from Aeromonas veronti bv. sobria, Biochemistry 44, 5168-5176.
18. Rasmussen, B. A., and Bush, K. (1997) Carbapenem hydrolysing β-lactamases, Antimicrob. Agents Chemother. 41, 223-232.
19. Felici, A., Amicosante, G., Oratore, A., Strom, R., Ledent, P., Joris, B., Fanuel, L., and Frère, J. M. (1993) An overview of the kinetic parameters of class B β-lactamases, Biochem. J. 291, 151-155.
20. Felici, A., and Amicosante, G. (1995) Kinetic analysis of extension of substrate specificity with Xanthomonas maltophilia, Aeromonas hydrophila, and Bacillus cereus metallo-β-lactamases, Antimicrob. Agents Chemother. 39, 192-199.
21. 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.
22. T produced in Escherichia coli, Antimicrob. Agents Chemother. 45, 1254-1262.
23. Carfi, A., Duee, E., Galleni, M., Frère, J. M., and Dideberg, O. (1998) 1.85 Å resolution structure of the zinc (II) β-lactamase from Bacillus cereus, Acta Crystallogr., Sect. D: Biol. Crystallogr. D54, 313-323.
24. Carfi, A., Duee, E., Paul-Soto, R., Galleni, M., Frère, J. M., and Dideberg, O. (1998) X-ray structure of the Zn(II) β-lactamase from Bacteroides fragilis in an orthorhombic crystal form, Acta Crystallogr., Sect. D: Biol. Crystallogr. D54, 45-57.
25. Ullah, J. H., Walsh, T. R., Taylor, I. A., Emery, D. C., Verma, C. S., Gamblin, S. J., and Spencer, J. (1998) The crystal structure of the L1 metallo-β-lactamase from Stenotrophomonas maltophilia at 1.7 Å resolution, J. Mol. Biol. 284, 125-136.
26. García-Sáez, P., Mercuri, S., Papamicael, C., Kahn, R., Frère, J. M., Galleni, M., Rossolini, G. M., and Dideberg, O. (2003) Three-dimensional structure of FEZ-1, a monomeric subclass B3 metallo-β-lactamase from Fluoribacter gormanii, in native form and in complex with D-captopril, J. Mol. Biol. 325, 651-660.
27. Garau, G., Bebrone, C., Anne, C., Galleni, M., Frère, J.-M., and Dideberg, O. (2005) A metallo-β-lactamase in action: crystal structure of the monozinc carbapenemase CphA and its complex with biapenem, J. Mol. Biol. 345, 785-795.
28. 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.
29. Concha, N. O., Rasmussen, B. A., Bush, K., and Herzberg, O. (1997) Crystal structure of the cadmium- and mercury-substituted metallo-β- lactamase from Bacteroides fragilis, Protein Sci. 6, 2671-2676.
30. 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.
31. Carfi, A., Pares, S., Duee, E., Galleni, M., Duez, C., Frère, J. M., and Dideberg, O. (1995) The 3-D structure of a zinc metallo-β-lactamase from Bacillus cereus reveals a new type of protein fold, EMBO J. 14, 4914-4921.
32. Paul-Soto, R., Zeppezauer, M., Adolph, H. W., Galleni, M., Frère, J. M., Carfi, A., Dideberg, O., Wouter, J., Hemmingsen, L., and Bauer, R. (1999) Preference of Cd(II) and Zn(II) for the two metal sites in Bacillus cereus β-lactamase II: a perturbed angular correlation of γ-rays (PAC) spectroscopy study, Biochemistry 38, 16500-16506.
33. de Seny, D., Heinz, U., Wommer, S., Kiefer, M., Meyer-Klaucke, W., Galleni, M., Frère, 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.
34. Wommer, S., Rival, S., Heinz, U., Galleni, M., Frère, 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.
35. Crowder, M. W., Wang, Z., Franklin, S. L., Zovinka, E. P., and Benkovic, S. J. (1996) Characterization of the metal-binding sites of the β-lactamase from Bacteroides fragilis, Biochemistry 35, 12126-12132.
36. 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.
37. Matthews, B. W. (1988) Structural basis of the action of thermolysin and related zinc peptidases, Acc. Chem. Res. 21, 333-340.
38. Lipscomb, W. N., and Strater, N. (1996) Recent advances in zinc enzymology, Chem. Rev. 96, 2375-2433.
39. 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.
40. Bounaga, S. (1999) Mechanism of catalysis and inhibition of Bacillus cereus class B β-lactamase, Ph.D. Thesis, University of Huddersfield, Huddersfield, U.K.
41. Gesmantel, N. P., Proctor, P., and Page, M. I. (1980) Metal-ion catalysed hydrolysis of some β-lactam antibiotics, J. Chem. Soc., Perkin Trans. 2, 1725-1732.
42. Kiefer, L. L., and Fierke, C. A. (1994) Functional characterization of human carbonic anhydrase II variants with altered zinc binding sites, Biochemistry 33, 15233-15240.
43. Bicknell, R., Knott-Hunziker, Y., and Waley, S. G. (1983) The pH-dependence of class B and class C β-lactamases, Biochem. J. 213, 61-66.
44. Baldwin, G. S., Edwards, G. F. StL., Kiener, P. A., Tully, M. J., Waley, S. G., and Abraham, E. P. (1980) Production of a variant of beta-lactamase II with selectively decreased cephalosporinase activity by a mutant of Bacillus cereus 569/H/9, Biochem. J. 191, 111-116.
45. Schowen, K. B., and Schowen, R. L. (1982) Solvent isotope effects on enzyme systems, Methods Enzymol. 87, 551-606.
46. Damblon, C., Jensen, M., Ababou, A., Barsukov, I., Papamicael, C., Schofield, C. J., Olsen, L., Bauer, R., and Roberts, G. C. (2003) The inhibitor thiomandelic acid binds to both metal ions in metallo-beta-lactamase and induces positive cooperativity in metal binding, J. Biol. Chem. 31, 29240-29251.
47. Antonaccio, M. J. (1982) Angiotensin Converting Enzyme (ACE) Inhibitors, Annu. Rev. Pharmacol. Toxicol. 22, 57-87.
48. Heinz, U., Bauer, R., Wommer, S., Meyer-Klaucke, Papamichaels, C., Bateson, J., and Adoph, H. W. (2003) Coordination geometries of metal ions in D- or L-captopril-inhibited metallo-β-lactamases, J. Biol. Chem. 278, 20659-20666.
49. Hughes, M. A., Smith, G. L., and Williams, D. R. (1985) The binding of metal ions by captopril (SQ 14225). Part I. complexation of zinc(II), cadmium(II) and lead(II), Inorg. Chim. Acta 107, 247-252.
50. Barnum, D. W. (1983) Hydrolysis of cations. Formation constants and standard free energies of formation of hydroxyl complexes, Inorg. Chem. 22, 2297-2305.
51. Greenwood, N. N., and Earnshaw, A. (1997) Zinc, Cadmium and Mercury, in Chemistry of the Elements, 2nd ed., pp 1201-1226, Elsevier, Amsterdam.
52. Kraus, M., Gilson, H. S. R., and Gresh, N. (2001) Structure of the first-shell active site in metallolactamase: effect of water ligands, J. Phys. Chem. B 105, 8040-8049.
53. Olsen, L., Antony, J., Hemmingsen, L., and Mikkelsen, K. V. (2002) Structure of a metal ion binding site in beta-lactamase: QM study of the influence of hydrogen bonding network and backbone constraints, J. Phys. Chem. A 106, 1046-1053.
54. Lindskog, S. (1982) Carbonic anhydrase, Adv. Inorg. Chem. 4, 115-170.
55. Makinen, M. W., Kuo, L. C., Dymowski, J. J., and Jaffer, S. (1979) Catalytic role of the metal ion of carboxypeptidase A in ester hydrolysis, J. Biol. Chem. 254, 356-366.
56. Omburo, G. A., Kuo, J. M., Mullins, L. S., and Raushel, F. M. (1992) Characterization of the zinc binding site of bacterial phosphotriesterase, J. Biol. Chem. 267, 13278-13283.
57. Zheng, F., Zhan, C. G., and Ornstein, R. L. (2002) Theoretical determination of two structural forms of the active site in cadmium-containing phosphotriesterases, J. Phys. Chem. B 106, 717-722.
58. Hemmingsen, L., Bauer, R., Bjerrum, M. J., Zeppezauer, M., Adolph, H. W., Formicka, G., and Cedegren-Zeppezauer, E. (1995) Cd-substituted horse liver alcohol dehydrogenase: catalytic site metal coordination geometry and protein conformation, Biochemistry 34, 7145-7153.
59. Caldwell, S. R., Newcomb, J. R., Schlecht, K. A., and Raushel, F. M. (1991) Limits of diffusion in the hydrolysis of substrates by the phosphotriesterase from Pseudomonas diminuta, Biochemistry 30, 7438-7444.
60. Bicknell, R., and Waley, S. G. (1985) Cryoenzymology of Bacillus cereus β-lactamase II, Biochemistry 24, 6876-6887.
61. Ash, D. E., Cox, J. D., and Christianson, D. W. (2000) Arginase: a binuclear manganese metalloenzyme, Met. Ions Biol. Syst. 37, 407-428.
62. Coleman, J. E. (1992) Structure and mechanism of alkaline phosphatase, Annu. Rev. Biophys. Biomol. Struct. 21, 441-483.
63. Badarau, A. (2006) Reactivity and inhibition of metallo-β- lactamases, Ph.D. Thesis, University of Huddersfield.
64. Bundgaard, H. (1976) Hydrolysis and intramolecular aminolysis of cephalexin and cephaloglycin in aqueous solution, Arch. Pharm. Chemi. Sci. Ed. 4, 25-43.
65. Faraci, S. W., and Pratt, R. F. (1986) Mechanism of inhibition of RTEM-2 β-lactamase by cephamycins: relative importance of the 7α-methoxy group and the 3′ leaving group, Biochemistry 25, 2934-1941.
66. Indelicato, J. M., and Wilham, W. L. (1974) Effect of 6-α substitution in penicillins and 7-α substitution in cephalosporins upon β-lactam reactivity, J. Med. Chem. 17, 528-529.
67. Heinz, U., Kiefer, M., Tholey, A., and Adolph, H. W. (2005) On the competition for available zinc, J. Biol. Chem. 280, 3197-3207.
68. Page, M. I. (1992) Structure-activity relationship: chemical, in The Chemistry of β-lactams (Page, M. I., Ed.) pp 79-100, University Press, Cambridge.
69. Spencer, J., Read, J., Sessions, R. B., Howell, S., Blackburn, G. M., and Gamblin, S. J. (2005) Antibiotic recognition by binuclear metallo-β- lactamases revealed by X-ray crystallography, J. Am. Chem. Soc. 127, 14439-14444.