The Zn2 Position in Metallo-β-Lactamases is Critical for Activity: A Study on Chimeric Metal Sites on a Conserved Protein Scaffold

Journal of Molecular Biology

Volumn 373, Issue 5, 2007, Pages 1141-1156

  González, Javier M ^a   Medrano Martín, Francisco J ^b   Costello, Alison L ^c   Tierney, David L ^c   Vila, Alejandro J ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

antibiotic resistance; catalytic mechanism; metallo lactamases; mutants; Zn2 site

Indexed keywords

APOENZYME; BETA LACTAM ANTIBIOTIC; CEFALORIDINE; CEFOTAXIME; HYDROLASE; IMIPENEM; METALLO BETA LACTAMASE; NITROCEFIN; PENICILLIN G; ZINC ION;

AEROMONAS HYDROPHILA; AEROMONAS VERONII; ANTIBIOTIC RESISTANCE; ARTICLE; BACILLUS CEREUS; BACILLUS THURINGIENSIS; BACTEROIDES FRAGILIS; CRYSTAL STRUCTURE; DESULFOVIBRIO GIGAS; DRUG BINDING SITE; DRUG HYDROLYSIS; ENZYME ACTIVITY; ENZYME KINETICS; FOURIER TRANSFORMATION; LEGIONELLA; MOLECULAR CLONING; MUTANT; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SEQUENCE ALIGNMENT; SERRATIA; STEADY STATE; STENOTROPHOMONAS MALTOPHILIA; STREPTOCOCCUS PNEUMONIAE; X RAY CRYSTALLOGRAPHY;

BACILLUS CEREUS; BACTERIA (MICROORGANISMS);

EID: 35148836146     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.08.031     Document Type: Article

References (62)

1. Fisher J.F., Meroueh S.O., and Mobashery S. Bacterial resistance to beta-lactam antibiotics: compelling opportunism, compelling opportunity. Chem. Rev. 105 (2005) 395-424
2. Frere J.M. Beta lactamases and bacterial resstance to antibiotics. Mol. Microbiol. 16 (1995) 385-395
3. Wilke M.S., Lovering A.L., and Strynadka N.C. beta-Lactam antibiotic resistance: a current structural perspective. Curr. Opin. Microbiol. 8 (2005) 525-533
4. Page M.I., and Laws A.P. The mechanism of catalysis and the inhibition of beta-lactamases. J. Chem. Soc. Chem. Commun. 1998 (1998) 1609-1617
5. Strynadka N.C., Adachi H., Jensen S.E., Johns K., Sielecki A., Betzel C., et al. Molecular structure of the acyl-enzyme intermediate in beta-lactam hydrolysis at 1.7 Å resolution. Nature 359 (1992) 700-705
6. Sulton D., Pagan-Roderiguez D., Zhou X., Liu Y., Hujer A.M., Bethel C.R., et al. Clavulanic acid inactivation of SHV-1 and the inhibitor resistant SER130GLY SHV-1 beta-lactamase: insights into the mechanism of inhibition. J. Biol. Chem. 280 (2005) 35528-35536
7. Crowder M.W., Spencer J., and Vila A.J. Metallo-beta-lactamases: novel weaponry for antibiotic resistance in bacteria. Acc. Chem. Res. 39 (2006) 721-728
8. Wang Z., Fast W., Valentine A.M., and Benkovic S.J. Metallo-β-lactamase: structure and mechanism. Curr. Opin. Chem. Biol. 3 (1999) 614-622
9. Walsh T.R., Toleman M.A., Poirel L., and Nordmann P. Metallo-beta-lactamases: the quiet before the storm?. Clin. Microbiol. Rev. 18 (2005) 306-325
10. Heinz U., and Adolph H.W. Metallo-beta-lactamases: two binding sites for one catalytic metal ion?. Cell Mol. Life Sci. 61 (2004) 2827-2839
11. Toney J.H., and Moloughney J.G. Metallo-beta-lactamase inhibitors: promise for the future?. Curr. Opin. Investig. Drugs 5 (2004) 823-826
12. Daiyasu H., Osaka K., Ishino Y., and Toh H. Expansion of the zinc metallo-hydrolase family of the beta-lactamase fold. FEBS Letters 503 (2001) 1-6
13. Carfi A., Pares S., Duee E., Galleni M., Duez C., Frère J.M., and Dideberg O. The 3-D structure of a zinc metallo-beta-lactamase from Bacillus cereus reveals a new type of protein fold. EMBO J. 14 (1995) 4914-4921
14. Galleni M., Lamotte-Brasseur J., Rossolini G.M., Spencer J., Dideberg O., and Frere J.M. Standard numbering scheme for class B beta-lactamases. Antimicrob. Agents Chemother. 45 (2001) 660-663
15. Garau G., Di Guilmi A.M., and Hall B.G. Structure-based phylogeny of the metallo-beta-lactamases. Antimicrob. Agents Chemother. 49 (2005) 2778-2784
16. Fabiane S.M., Sohi M.K., Wan T., Payne D.J., Bateson J.H., Mitchell T., and Sutton B.J. Crystal structure of the zinc-dependent beta lactamase from Bacillus cereus at 1.9 Å resolution: binuclear active site with features of a mononuclear enzime. Biochemistry 37 (1998) 12404-12411
17. Toney J.H., Hammond G.G., Fitzgerald P.M., Sharma N., Balkovec J.M., Rouen G.P., et al. Succinic acids as potent inhibitors of plasmid-borne IMP-1 metallo-beta-lactamase. J. Biol. Chem. 276 (2001) 31913-31918
18. Ullah J.H., Walsh T.R., Taylor I.A., Emery D.C., Verma C.S., Gamblin S.J., and Spencer J. The crystal strucuture of the L1 metallo-beta-lactamase from Stenotrophomonas maltophilia at 1.7 Å resolution. J. Mol. Biol. 284 (1998) 125-136
19. Garcia-Saez I., Mercuri P.S., Papamicael C., Kahn R., Frere J.M., Galleni M., et al. Three-dimensional structure of FEZ-1, a monomeric subclass B3 metallo-beta-lactamase from Fluoribacter gormanii, in native form and in complex with D-captopril. J. Mol. Biol. 325 (2003) 651-660
20. Murphy T.A., Catto L.E., Halford S.E., Hadfield A. T., Minor W., Walsh T.R., and Spencer J. Crystal structure of Pseudomonas aeruginosa SPM-1 provides insights into variable zinc affinity of metallo-beta-lactamases. J. Mol. Biol. 357 (2006) 890-903
21. Garau G., Bebrone C., Anne C., Galleni M., Frere J.M., and Dideberg O. 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
22. Sharma N.P., Hajdin C., Chandrasekar S., Bennett B., Yang K.W., and Crowder M.W. Mechanistic studies on the mononuclear Zn(II)-containing metallo-beta-lactamase ImiS from Aeromonas sobria. Biochemistry 45 (2006) 10729-10738
23. Crawford P.A., Yang K.W., Sharma N., Bennett B., and Crowder M.W. Spectroscopic studies on cobalt(II)-substituted metallo-beta-lactamase ImiS from Aeromonas veronii bv. sobria. Biochemistry 44 (2005) 5168-5176
24. Bebrone C., Anne C., De Vriendt K., Devreese B., Rossolini G.M., van Beeumen J., et al. Dramatic broadening of the substrate profile of the Aeromonas hydrophila CphA metallo-beta-lactamase by site-directed mutagenesis. J. Biol. Chem. 280 (2005) 28195-28202
25. Bounaga S., Laws A.P., Galleni M., and Page M.I. The mechanism of catalysis and the inhibition of the Bacillus cereus zinc-dependent beta-lactamase. Biochem. J. 31 (1998) 703-711
26. Wang Z., Fast W., and Benkovic S.J. On the mechanism of the metallo-β-lactamase from Bacteroides fragilis. Biochemistry 38 (1999) 10013-10023
27. Spencer J., Read J., Sessions R.B., Howell S., Blackburn G.M., and Gamblin S.J. Antibiotic recognition by binuclear metallo-beta-lactamases revealed by X-ray crystallography. J. Am. Chem. Soc. 127 (2005) 14439-14444
28. Xu D., Xie D., and Guo H. Catalytic mechanism of class B2 metallo-beta-lactamase. J. Biol. Chem. 281 (2006) 8740-8747
29. Rasia R.M., and Vila A.J. Exploring the role and the binding affinity of a second zinc equivalent in B. cereus metallo-beta-lactamase. Biochemistry 41 (2002) 1853-1860
30. Morán-Barrio J., González J.M., Lisa M.N., Costello A.L., Peraro M.D., Carloni P., et al. The metallo-beta-lactamase GOB is a mono-Zn(II) enzyme with a novel active site. J. Biol. Chem. 282 25 (2007) 18286-18293
31. Cameron A.D., Ridderstrom M., Olin B., and Mannervik B. Crystal structure of human glyoxalase II and its complex with a glutathione thiolester substrate analogue. Structure Fold. Des. 7 (1999) 1067-1078
32. Thomas P.W., Stone E.M., Costello A.L., Tierney D.L., and Fast W. The quorum-quenching lactonase from Bacillus thuringiensis is a metalloprotein. Biochemistry 44 (2005) 7559-7569
33. Hagelueken G., Adams T.M., Wiehlmann L., Widow U., Kolmar H., Tummler B., et al. The crystal structure of SdsA1, an alkylsulfatase from Pseudomonas aeruginosa, defines a third class of sulfatases. Proc. Natl. Acad. Sci. USA 103 (2006) 7631-7636
34. Park H.S., Nam S.H., Lee J.K., Yoon C.N., Mannervik B., Benkovic S.J., and Kim H.S. Design and evolution of new catalytic activity with an existing protein scaffold. Science 311 (2006) 535-538
35. Seny D., Prosperi-Meys C., Bebrone C., Rossolini G.M., Page M.I., Noel P., et al. Mutational analysis of the two zinc-binding sites of the Bacillus cereus 569/H/9 metallo-beta-lactamase. Biochem. J. 363 (2002) 687-696
36. 2+-beta-lactamase. Role of the conserved cysteine in the catalytic mechanism. J. Biol. Chem. 274 (1999) 13242-13249
37. Garrity J.D., Carenbauer A.L., Herron L.R., and Crowder M.W. Metal binding Asp-120 in metallo-beta-lactamase L1 from Stenotrophomonas maltophilia plays a crucial role in catalysis. J. Biol. Chem. 279 (2004) 920-927
38. Yanchak M.P., Taylor R.A., and Crowder M.W. Mutational analysis of metallo-beta-lactamase CcrA from Bacteroides fragilis. Biochemistry 39 (2000) 11330-11339
39. Vanhove M., Zakhem M., Devreese B., Franceschini N., Anne C., Bebrone C., et al. Role of Cys221 and Asn116 in the zinc-binding sites of the Aeromonas hydrophila metallo-beta-lactamase. Cell Mol. Life Sci. 60 (2003) 2501-2509
40. Rasia R.M., Ceolin M., and Vila A.J. Grafting a new metal ligand in the cocatalytic site of B. cereus metallo-beta-lactamase: structural flexibility without loss of activity. Protein Sci. 12 (2003) 1538-1546
41. de Seny D., Heinz U., Wommer S., Kiefer M., Meyer-Klaucke W., Galleni M., et al. 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. Davies A.M., Rasia R.M., Vila A.J., Sutton B.J., and Fabiane S.M. 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
43. Costello A., Periyannan G., Yang K.W., Crowder M.W., and Tierney D.L. Site-selective binding of Zn(II) to metallo-beta-lactamase L1 from Stenotrophomonas maltophilia. J. Biol. Inorg. Chem. 11 (2006) 351-358
44. Yang Y., Keeney D., Tang X., Canfield N., and Rasmussen B.A. Kinetic properties and metal content of the metallo-β-lacatamase CcrA harboring selective amino acid substitutions. J. Biol. Chem. 274 (1999) 15706-15711
45. Llarrull L.I., Fabiane S.M., Kowalski J.M., Bennett B., Sutton B.J., and Vila A.J. Asp-120 locates Zn2 for optimal metallo-beta-lactamase activity. J. Biol. Chem. 282 25 (2007) 18276-18285
46. Liu D., Lepore B.W., Petsko G.A., Thomas P.W., Stone E.M., Fast W., and Ringe D. Three-dimensional structure of the quorum-quenching N-acyl homoserine lactone hydrolase from Bacillus thuringiensis. Proc. Natl. Acad. Sci. USA 102 (2005) 11882-11887
47. Dal Peraro M., Vila A.J., Carloni P., and Klein M.L. Role of zinc content on the catalytic efficiency of B1 metallo-beta-lactamases. J. Am. Chem Soc. 129 (2007) 2808-2812
48. Dal Peraro M., Vila A.J., and Carloni P. Substrate binding to mononuclear metallo-beta-lactamase from Bacillus cereus. Proteins: Struct. Funct. Genet. 54 (2004) 412-423
49. Dal Peraro M., Llarrull L.I., Rothlisberger U., Vila A.J., and Carloni P. Water-assisted reaction mechanism of monozinc beta-lactamases. J. Am. Chem. Soc. 126 (2004) 12661-12668
50. Chantalat L., Duee E., Galleni M., Frere J.M., and Dideberg O. Structural effects of the active site mutation cysteine to serine in Bacillus cereus zinc-beta-lactamase. Protein Sci. 9 (2000) 1402-1406
51. Hall B.G., Salipante S.J., and Barlow M. Independent origins of subgroup Bl+ B2 and subgroup B3 metallo-beta-lactamases. J. Mol. Evol. 59 (2004) 133-141
52. Orellano E.G., Girardini J.E., Cricco J.A., Ceccarelli E.A., and Vila A.J. Spectroscopic characterization of a binuclear metal site in Bacillus cereus beta-lactamase II. Biochemistry 37 (1998) 10173-10180
53. Hunt J.B., Neece S.H., and Ginsburg A. The use of 4-(2-pyridylazo)resorcinol in studies of zinc release from Escherichia coli aspartate transcarbamoylase. Anal. Biochem. 146 (1985) 150-157
54. Kuzmic P. Program DYNAFIT for the analysis of enzyme kinetic data: application to HIV proteinase. Anal. Biochem. 237 (1996) 260-273
55. Shulz A.R. A closer look to the basic assumptions. Enzyme Kinetics, from Diastase to Multi-enzyme Systems (1994), Cambridge University Press, Cambridge 22-48
56. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-325
57. Collaborative Computational Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D, Biol. Crystallogr. 50 (1994) 760-763
58. Navaza J. AMoRe: an automated package for molecular replacement. Acta Crystallog. sect. D Bi55 (1994) 247-255
59. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallog. sect. D 53 (1997) 240-255
60. Laskowski R.A., Mac Arthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26 (1993) 283-291
61. Ankudinov A.L., Ravel B., Rehr J.J., and Conradson S.D. Real-space multiple-scattering calculation and interpretation of x-ray-absorption near-edge structure. Phys. Rev. ser. B 58 (1998) 7565-7576
62. McClure C.P., Rusche K.M., Peariso K., Jackman J.E., Fierke C.A., and Penner-Hahn J.E. EXAFS studies of the zinc sites of UDP-(3-O-acyl)-N-acetylglucosamine deacetylase (LpxC). J. Inorg. Biochem. 94 (2003) 78-85