Protonation state and substrate binding to B2 metallo-β-lactamase CphA from Aeromonas hydrofila

Proteins: Structure, Function and Genetics

Volumn 69, Issue 3, 2007, Pages 595-605

  Simona, F ^a,b   Magistrato, A ^a,b   Vera, D M A ^c   Garau, G ^d   Vila, A J ^e   Carloni, Paolo ^a  

^a SISSA   (Italy)

^b DEMOCRITOS NATIONAL SIMULATION CENTER   (Italy)

^c DEPARTAMENTO DE FISICOQUÍMICA   (Argentina)

^d SAN RAFFAELE HOSPITAL   (Italy)

^e UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

Enzyme catalysis; MD simulations; Metallo lactamases; Protonation state; Substrate binding

Indexed keywords

BETA LACTAM ANTIBIOTIC; METALLO BETA LACTAMASE; PROTEIN CPHA; UNCLASSIFIED DRUG; ZINC;

AEROMONAS HYDROPHILA; AQUEOUS SOLUTION; ARTICLE; COMPLEX FORMATION; DENSITY FUNCTIONAL THEORY; ENZYME ACTIVE SITE; ENZYME SUBSTRATE COMPLEX; HYDROGEN BOND; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTON TRANSPORT; QUANTUM MECHANICS; SIMULATION;

AEROMONAS HYDROPHILA; BACTERIAL PROTEINS; BETA-LACTAMASES; BINDING SITES; COMPUTER SIMULATION; ELECTROSTATICS; HYDROGEN BONDING; HYDROGENATION; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTONS; QUANTUM THEORY; THIENAMYCINS; ZINC;

AEROMONAS; BACTERIA (MICROORGANISMS);

EID: 35448961683     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21476     Document Type: Article

References (74)

1. Walsh TR, Toleman MA, Poirel L, Nordmann P. Metallo-β-lactamases: the quiet before the storm? Clin Microbiol Rev 2005;18:306-325.
2. Walsh TR. The emergence and implications of metallo-β-lactamases in Gram-negative bacteria. Clin Microbiol Infec 2005;11:2-9.
3. Frere JM. Beta-lactamases and bacterial-resistance to antibiotics. Mol Microbiol 1995;16:385-395.
4. Livermore DM, Woodford N. Carbapenemases: a problem in waiting? Curr Opin Microbiol 2000;3:489-495.
5. Crowder WM, Spencer J, Vila AJ. Metallo-β-lactamases: Novel weaponry for antibiotic resistance in bacteria. Acc Chem Rev 2006; 39:721-728.
6. Buynak JD. Understanding the longevity of the β-lactam antibiotics and of antibiotic/β-lactamase inhibitor combinations. Biochem Pharmacol 2006;71:930-940.
7. Buynak JD. The discovery and development of modified penicillin-and cephalosporin-derived β-lactamase inhibitors. Curr Med Chem 2004;11:1951-1964.
8. Bush K, Jacoby GA, Medeiros AA. A functional classification scheme for β-lactamases and its correlation with molecular-structure. Antimicrob Agents Chemother 1995;39:1211-1233.
9. Galleni M, Lamotte-Brasseur J, Rossolini GM, Spencer J, Dideberg O, Frere JM. Standard numbering scheme for class B β-lactamases. Antimicrob Agents Chemother 2001;45:660-663.
10. Garau G, Garcia-Saez I, Bebrone C, Anne C, Mercuri P, Galleni M, Frere JM, Dideberg O. Update of the standard numbering scheme for class B β-lactamases. Antimicrob Agents Chemother 2004;48: 2347-2349.
11. Carfi A, Pares S, Duee E, Galleni M, Duez C, Frere JM, 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.
12. 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.
13. Cricco JA, Orellano EG, Rasia RM, Ceccarelli EA, Vila AJ. Metallo-β-lactamases: does it take two to tango? Coordin Chem Rev 1999;192:519-535.
14. Heinz U, Adolph HW Metallo-β-lactamases: two binding sites for one catalytic metal ion? Cell Mol Life Sci 2004;61:2827-2839.
15. Concha NO, Rasmussen BA, Bush K, Herzberg O. Crystal structure of the wide-spectrum binuclear zinc β-lactamase from Bacteroides fragilis. Structure 1996;4:823-836.
16. Fabiane SM, Sohi MK, Wan T, Payne DJ, Bateson JH, Mitchell T, Sutton BJ. Crystal structure of the zinc-dependent β-lactamase from Bacillus cereus at 1.9 angstrom resolution: Binuclear active site with features of a mononuclear enzyme. Biochemistry 1998;37:12404-12411.
17. Toney JH, Fitzgerald PMD, Grover-Sharma N, Olson SH, May WJ, Sundelof JG, Vanderwall DE, Cleary KA, Grant SK, Wu JK, Kozarich JW, Pompliano DL, Hammond GG. Antibiotic sensitization using biphenyl tetrazoles as potent inhibitors of Bacteroides fragilis metallo-β-lactamase. Chem Biol 1998;5:185-196.
18. Concha NO, Janson CA, Rowling P, Pearson S, Cheever CA, Clarke BP, Lewis C, Galleni M, Frere JM, Payne DJ, Bateson JH, Abdel-Meguid SS. Crystal structure of the IMP-1 metallo β-lactamase from Pseudomonas aeruginosa and its complex with a mercaptocarboxy-late inhibitor: binding determinants of a potent, broad-spectrum inhibitor. Biochem 2000;39:4288-4298.
19. Toney JH, Hammond GG, Fitzgerald PMD, Sharma N, Balkovec JM, Rouen GP, Olson SH, Hammond ML, Greenlee ML, Gao YD. Succinic acids as potent inhibitors of plasmid-borne IMP-1 metallo-β-lactamase. J Biol Chem 2001;276:31913-31918.
20. Ullah JH, Walsh TR, Taylor IA, Emery DC, Verma CS, Gamblin SJ, Spencer J. The crystal structure of the L1 metallo-β-lactamase from Stenotrophomonas maltophilia at 1.7 angstrom resolution. J Mol Biol 1998;284:125-136.
21. Garcia-Saez I, Mercuri PS, Papamicael C, Kahn R, Frere JM, Galleni M, Rossolini GM, Dideberg O. 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 2003;325:651-660.
22. Garau G, Bebrone C, Anne C, Galleni M, Frere JM, Dideberg O. A metallo-β-lactamase enzyme in action: Crystal structures of the monozinc carbapenemase CphA and its complex with biapenem. J Mol Biol 2005;345:785-795.
23. Valladares MH, Felici A, Weber G, Adolph HW, Zeppezauer M, Rossolini GM, Amicosante G, Frere JM, Galleni M. Zn(ii) dependence of the Aeromonas hydrophila AE036 metallo-β-lactamase activity and stability. Biochem 1997;36:11534-11541.
24. Xu DG, Zhou YZ, Xie DQ, Guo H. Antibiotic binding to monozinc CphA β-lactamase from Aeromonas hydropila: quantum mechanical/molecular mechanical and density functional theory studies. J Med Chem 2005;48:6679-6689.
25. Xu DG, Xie DQ, Guo H. Catalytic mechanism of class B2 metallo-β-lactamase. J Biol Chem 2006;281:8740-8747.
26. Dal Peraro M, Vila AJ, 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.
27. Nordmann P, Poirel L. Emerging carbapenemases in Gram-negative aerobes. Clin Microbiol Infec 2002;8:321-331.
28. Wommer S, Rival S, Heinz U, Galleni M, Frere JM, Franceschini N, Amicosante G, Rasmussen B, Bauer R, Adolph HW. Substrate-activated zinc binding of metallo-β-lactamases in physiological importance of the mononuclear enzymes. J Biol Chem 2002;277:24142-24147.
29. Dal Peraro M, Llarrull LI, Rothlisberger U, Vila AJ, Carloni P. Water-assisted reaction mechanism of monozinc beta-lactamases. J Am Chem Soc 2004;126:12661-12668.
30. Gervasio FL, Schettino V, Mangani S, Krack M, Carloni P, Parrinello M. Influence of outer-shell metal ligands on the structural and electronic properties of horse liver alcohol dehydrogenase zinc active site J Phys Chem B 2003;107:6886-6892.
31. Tomatis PE, Rasia RM, Segovia L, Vila AJ. Mimicking natural evolution in metallo-β-lactamases through second-shell ligand mutations. P Natl Acad Sci USA 2005;102:13761-13766.
32. Becke AD. Density-functional exchange-energy approximation with correct asymptotic behavior. Phys Rev A 1988;38:3098-3100.
33. Lee CT, Yang WT, Parr RG. Development of the colle-salvetti correlation-energy formula into a functional of the electron density. Phys Rev B 1988;37:785-789.
34. Troullier N, Martins JL. Efficient pseudopotentials for plane-wave calculations. Phys Rev B 1991;43:1993-2006.
35. Kleinman L, Bylander DM. Efficacious form for model pseudopotentials. Phys Rev Lett 1982;48:1425-1428.
36. Martyna GJ, Tuckerman ME. A reciprocal space based method for treating long range interactions in ab initio and force-field-based calculations in clusters. J Chem Phys 1999;110:2810-2821.
37. Copyright IBM Corp. CPMD, http://www.cpmd.org. CPMD, 1990-2004.
38. Car R, Parrinello M. Unified approach for molecular-dynamics and density-functional theory. Phys Rev Lett 1985;55:2471-2474.
39. Case DA, Pearlman DA, Caldwell JW, Cheatham TE III WS, Wang J, Ross, Simmerling CL, Darden T, Merz KM, Stanton RV, Cheng AL, Vincent JJ, Crowley M, Tsui V, Gohlke H, Radmer RJ, Duan Y, Pittera J, Massova I, Seibel GL, Singh UC, Weiner PK, Kollman PA. AMBER7. University of California, San Francisco, 2002.
40. Jorgensen WL, Chandrasekhar J, Madura J, Klein ML. Comparison of simple potential functions for simulating liquid water. J Chem Phys 1983;79:926-935.
41. Suarez D, Merz KM. Molecular dynamics simulations of the mononuclear zinc-β-lactamase from Bacillus cereus. J Am Chem Soc 2001; 123:3759-3770.
42. Diaz N, Suarez D, Merz KM. 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.
43. Suarez D, Diaz N, Merz KM. Molecular dynamics simulations of the dinuclear zinc-β-lactamase from bacteroides fragilis complexed with imipenem. J Comput Chem 2002;23:1587-1600.
44. Sola M, Lledos A, Duran M, Bertran J. Anion binding and pentacoordination in zinc(ii) complexes. Inorg Chem 1991;30:2523-2527.
45. Mangani S, Carloni P, Orioli P. X-ray diffraction studies on carboxypeptidase-a complexes: the zinc stereochemistry. Coordin Chem Rev 1992;120:309-324.
46. Oelschlaeger P, Schmid RD, Pleiss J. Modeling domino effects in enzymes: molecular basis of the substrate specificity of the bacterial metallo-β-lactamases IMP-1 and imp-6. Biochem 2003;42:8945-8956.
47. Oelschlaeger P, Schmid RD, Pleiss J. Insight into the mechanism of the IMP-1 metallo-β-lactamase by molecular dynamics simulations. Protein Eng Des Sel 2003;16:341-350.
48. Wang JM, Wolf RM, Caldwell JW, Kollman PA, Case DA. Development and testing of a general amber force field. J Comput Chem 2004;25:1157-1174.
49. Bayly CI, Cieplak P, Cornell WD, Kollman PA. A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges - the resp model. J Phys Chem 1993;97:10269-10280.
50. Cornell WD, Cieplak P, Bayly CI, Kollman PA. Application of resp charges to calculate conformational energies, hydrogen-bond energies, and free-energies of solvation. J Am Chem Soc 1993;115:9620-9631.
51. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery JA Jr, Vreven T, Kudin KN, Burant JC, Millam JM, Iyengar SS, Tomasi J, Barone V, Mennucci B, Cossi M, Scalmani G, Rega N, Petersson GA, Nakatsuji H, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Klene M, Li X, Knox JE, Hratchian HP, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Ayala PY, Morokuma K, Voth GA, Salvador P, Dannenberg JJ, Zakrzewski VG, Dapprich S, Daniels AD, Strain MC, Farkas O, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Ortiz JV, Cui Q, Baboul AG, Clifford S, Cioslowski J, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Challacombe M, Gill PMW, Johnson B, Chen W, Wong MW, Gonzalez C, Pople JA. Gaussian 03, Revision C.02. Gaussian, Inc., Wallingford CT, 2004.
52. Darden T, York D, Pedersen L. Particle mesh ewald: an n.log(n) method for ewald sums in large systems. J Chem Phys 1993;98: 10089-10092.
53. Ryckaert JP, Ciccotti G, Berendsen HJC. Numerical-integration of cartesian equations of motion of a system with constraints - molecular-dynamics of n-alkanes. J Comput Phys 1977;23:327-341.
54. Nelson MT, Humphrey W, Gursoy A, Dalke A, Kale LV, Skeel RD, Schulten K. NAMD: a parallel, object oriented molecular dynamics program. Int J High Perform C 1996;10:251-268.
55. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K. Scalable molecular dynamics with namd. J Comput Chem 2005;26:1781-1802.
56. Martyna GJ, Tobias DJ, Klein ML. Constant-pressure molecular dynamics algorithms. J Chem Phys 1994;101:4177-4189.
57. Feller SE, Zhang YH, Pastor RW, Brooks BR. Constant-pressure molecular-dynamics simulation - the langevin piston method. J Chem Phys 1995;103:4613-4621.
58. Nose S. A molecular-dynamics method for simulations in the canonical ensemble. Mol Phys 1984;52:255-268.
59. Hoover WG. Canonical dynamics - equilibrium phase-space distributions. Phys Rev A 1985;31:1695-1697.
60. Leach AR. Molecular modelling, principles and applications. Harlow: Pearson Education; 2001.
61. Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graphics 1996;14:33.
62. Schaftenaar G, Noordik JH. The effect of isodensity surface sampling on ESP derived charges and the effect of adding bondcenters on DMA derived charges. J Comput Aid Mol Des 2000;14:233-242.
63. Crawford PA, Yang KW, Sharma N, Bennett B, Crowder MW. Spectroscopic studies on cobalt(II)-substituted metallo-β-lactamase ImiS from Aeromonas veronii bv. sobria. Biochem 2005;44:5168-5176.
64. Rasia RM, Vila AJ. Exploring the role and the binding affinity of a second zinc equivalent in B. cereus metallo-β-lactamase. Biochem 2002;41:1853-1860.
65. Davies AM, Rasia RM, Vila AJ, Sutton BJ, Fabiane SM. Effect of pH on the active site of an Arg121Cys mutant of the metallo-β-lactamase from Bacillus cereus: implications for the enzyme mechanism. Biochem 2005;44:4841-4849.
66. Scrofani SDB, Chung J, Huntley JJA, Benkovic SJ, Wright PE, Dyson HJ. NMR characterization of the metallo-β-lactamase from Bacteroides fragilis and its interaction with a tight-binding inhibitor: role of an active-site loop. Biochem 1999;38:14507-14514.
67. Huntley JJA, Scrofani SDB, Osborne MJ, Wright PE, Dyson HJ. Dynamics of the metallo-β-lactamase from Bacteroides fragilis in the presence and absence of a tight-binding inhibitor. Biochem 2000;39: 13356-13364.
68. Salsbury FR, Crowley MF, Brooks CL. Modeling of the metallo-β- lactamase from B-fragilis: structural and dynamic effects of inhibitor binding. Proteins Struct Funct Bioinf 2001;44:448-459.
69. Diaz N, Suarez D, Merz KM. 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.
70. Diaz N, Suarez D, Merz KM, Sordo TL. Molecular dynamics simulations of the TEM-1,β-lactamase complexed with cephalothin. J Med Chem 2005;48:780-791.
71. Dal Peraro M, Vila AJ, Carloni P. Protonation state of Asp 120 in the binuclear active site of the metallo-β-lactamase from Bacteroides fragilis. Inorg Chem 2003;42:4245-4247.
72. Dal Peraro M, Vila AJ, Carloni P. Substrate binding to mononuclear metallo-β-lactamase from Bacillus cereus. Proteins Struct Funct Bioinf 2004;54:412-423.
73. Park H, Brothers EN, Merz KM. 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.
74. Estiu G, Suárez D, Merz KM. Quantum mechanical and molecular dynamics simulations of ureases and zn β-lactamases. J Comput Chem 2006;27:1240-1262.