Molecular dynamics simulations of class C β-lactamase from Citrobacter freundii: Insights into the base catalyst for acylation

Biochemistry

Volumn 45, Issue 2, 2006, Pages 439-451

  Díaz, Natalia ^a   Suárez, Dimas ^a   Sordo, Tomás L ^a  

^a UNIVERSITY OF OVIEDO   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLATION; CATALYSTS; COMPUTER SIMULATION; ENZYMES; FREE ENERGY; MOLECULAR DYNAMICS; NEGATIVE IONS; SOLUTIONS;

CITROBACTER FREUNDII; ENZYME-AZTREONAM ORIENTATION; MOLECULAR DYNAMICS SIMULATIONS; QUANTUM MECHANICAL ENERGY CALCULATIONS;

ENZYME KINETICS;

AZTREONAM; BETA LACTAMASE; HYDROXYL GROUP; LYSINE; TYROSINE;

ACYLATION; ANIMAL CELL; AQUEOUS SOLUTION; ARTICLE; CALCULATION; CITROBACTER FREUNDII; CONTROLLED STUDY; COVALENT BOND; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME STABILITY; ENZYME STRUCTURE; MICHAELIS CONSTANT; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; ORIENTATION; PRIORITY JOURNAL; QUANTUM MECHANICS; SIMULATION; STRUCTURE ANALYSIS;

ACYLATION; APOENZYMES; AZTREONAM; BETA-LACTAMASES; CATALYSIS; CITROBACTER FREUNDII; COMBINATORIAL CHEMISTRY TECHNIQUES; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; ENZYME INHIBITORS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; QUANTUM THEORY; THERMODYNAMICS;

ANIMALIA; CITROBACTER FREUNDII;

EID: 30744472632     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi051600j     Document Type: Article

References (63)

1. Walsh, C. (2000) Molecular mechanisms that confer antibacterial drug resistance, Nature 406, 775-781.
2. Wright, G. D. (2000) Resisting resistance: New chemical strategies for battling superbugs, Chem. Biol. 7, 127-132.
3. Fisher, J. F., Meroueh, S. O., and Mobashery, S. (2005) Bacterial resistance to β-lactam antibiotics: Compelling opportunism, compelling opportunity, Chem. Rev. 105, 395-424.
4. Bush, K., Jacoby, G. A., and Medeiros, A. A. (1995) A functional classification scheme for β-lactamases and its correlation with molecular structure, Antimicrob. Agents Chemother. 39, 1211-1233.
5. Maiti, S. N., Philips, O. A., Micetich, R. G., and Livermore, D. M. (1998) β-Lactamase inhibitors: Agents to overcome bacterial resistance, Curr. Med. Chem. 5, 441-456.
6. Beceiro, A., and Bou, G. (2004) Class C β-lactamases: An increasing problem worldwide, Rev. Med. Microbiol. 15, 141-152.
7. Oefner, C., D'Arcy, A., Daly, J. J., Gubernator, K., Charnas, R. L., Heinze, I., Hubschwerlen, C., and Winkler, F. K. (1990) Refined crystal structure of β-lactamase from Citrobacter freundii indicates a mechanism for β-lactam hydrolysis, Nature 343, 284-288.
8. Lobkovsky, E., Moews, P. C., Liu, H., Zhao, H., Frere, J. M., and Knox, J. R. (1993) Evolution of an enzyme activity: Crystallographic structure at 2 Å resolution of cephalosporinase from the AmpC gene of Enterobacter cloacae P99 and comparison with a class A penicillinase, Proc. Natl. Acad. Sci. U.S.A. 90, 11257-11261.
9. Usher, K. C., Blaszczak, L. C., Weston, G. S., Shoichet, B. K., and Remington, S. J. (1998) Three-dimensional structure of AmpC β-lactamase from Escherichia coli bound to a transition-state analogue: Possible implications for the oxyanion hypothesis and for inhibitor design, Biochemistry 37, 16082-16092.
10. Crichlow, G. V., Kuzin, A. P., Nukaga, M., Mayama, K., Sawai, T., and Knox, J. R. (1999) Structure of the extended-spectrum class C β-lactamase of Enterobacter cloacae GC1, a natural mutant with a tandem tripeptide insertion, Biochemistry 38, 10256-10261.
11. Patera, A., Blaszczak, L. C., and Shoichet, B. K. (2000) Crystal structures of substrate and inhibitor complexes with AmpC β-lactamase: Possible implications for substrate-assisted catalysis, J. Am. Chem. Soc. 122, 10504-10512.
12. Powers, R. A., Caselli, E., Focia, P. J., Prati, F., and Shoichet, B. K. (2001) Structures of ceftazidime and its transition-state analog in complex with AmpC β-lactamase: Implications for resistance mutations and inhibitor design, Biochemistry 40, 9207-9214.
13. Trehan, I., Beadle, B. M., and Shoichet, B. K. (2001) Inhibition of AmpC β-lactamase through a destabilizing interaction in the active site, Biochemistry 40, 7992-7999.
14. Beadle, B. M., and Shoichet, B. K. (2002) Structural basis for imipenem inhibition of class C β-lactamases, Antimicrob. Agents Chemother. 46, 3978-3980.
15. Beadle, B. M., Trehan, I., Focia, P. J., and Shoichet, B. K. (2002) Structural milestones in the reaction pathway of an amide hydrolase: Substrate, acyl, and product complexes of cephalothin with AmpC β-lactamase, Structure 10, 413-424.
16. Meroueh, S. O., Minasov, G., Lee, W., Shoichet, B. K., and Mobashery, S. (2003) Structural aspects for evolution of β-lactamases from penicillin-binding proteins, J. Am. Chem. Soc. 125, 9612-9618.
17. Nukaga, M., Abe, T., Venkatesan, A. M., Mansour, T. S., Bonomo, R. A., and Knox, J. R. (2003) Inhibition of class A and class C β-lactamases by penems: Crystallographic structures of a novel 1,4-thiazepine intermediate, Biochemistry 42, 13152-13159.
18. Roth, T. A., Minasov, G., Morandi, S., Prati, F., and Shoichet, B. K. (2003) Thermodynamic cycle analysis and inhibitor design against β-lactamase, Biochemistry 42, 14483-14491.
19. Wouters, J., Fonze, E., Frere, J.-M., and Charlier, P. (2003) Crystal structure of Enterobacter cloacae 908R class C β-lactamase bound to iodo-acetamido-phenyl boronic acid, a transition-state analogue, Cell. Mol. Life Sci. 60, 1764.
20. Nukaga, M., Kumar, S., Nukaga, K., Pratt, R. F., and Knox, J. R. (2004) Hydrolysis of third-generation cephalosporins by class C β-lactamases. Structures of a transition state analog of cefotaxime in wild-type and extended spectrum enzymes, J. Biol. Chem. 279, 9344.
21. Tondi, D., Morandi, F., Bonnet, R., Costi, M. P., and Shoichet, B. K. (2005) Structure-based optimization of a non-β-lactam lead results in inhibitors that do not up-regulate β-lactamase expression in cell culture, J. Am. Chem. Soc. 127, 4632-4639.
22. Michaux, C., Charlier, P., Frere, J.-M., and Wouters, J. (2005) Crystal structure of Brl 42715, C6-(N1-methyl-1,2,3-triazolylmethylene)penem, in complex with Enterobacter cloacae 908R β-lactamase: Evidence for a stereoselective mechanism from docking studies, J. Am. Chem. Soc. 127, 3262-3263.
23. Tsukamoto, K., Tachibana, K., Yamazaki, N., Ishii, Y., Ujie, K., Nishida, N., and Sawai, T. (1990) Role of lysine-67 in the active site of class C β-lactamase from Citrobacter freundii GN346, Eur. J. Biochem. 188, 15-22.
24. Monnaie, D., Dubus, A., and Frère, J.-M. (1994) The role of lysine-67 in a class C β-lactamase is mainly electrostatic, Biochem. J. 304, 1-4.
25. Dubus, A., Ledent, P., Lamotte-Brasseur, J., and Frère, J.-M. (1996) The roles of residues Tyr150, Glu272, and His314 in class C β-lactamases, Proteins: Struct., Funct., Genet. 25, 473-485.
26. Goldberg, S. D., Iannuccilli, W., Nguyen, T., Ju, J., and Cornish, V. W. (2003) Identification of residues critical for catalysis in a class C β-lactamase by combinatorial scanning mutagenesis, Protein Sci. 12, 1633-1645.
27. Monnaie, D., Dubus, A., Cooke, D., Marchand-Brynaert, J., Normark, S., and Frère, J.-M. (1994) Role of residue Lys315 in the mechanism of action of the Enterobacter cloacae 908R β-lactamase, Biochemistry 33, 5193-5201.
28. Zhang, Z., Yu, Y., Musser, J. M., and Palzkill, T. (2001) Amino acid sequence determinants of extended spectrum cephalosporin hydrolysis by the class C P99 β-lactamase, J. Biol. Chem. 276, 46568-46574.
29. a measurements from nuclear magnetic resonance of tyrosine-150 in class C β-lactamase, Biochem. J. 371, 175-181.
30. a calculations for class C β-lactamases: The role of Tyr150, Proteins: Struct., Funct., Genet. 40, 23-28.
31. Bulychev, A., Massova, I., Miyashita, K., and Mobashery, S. (1997) Nuances of mechanisms and their implications for evolution of the versatile β-lactamase activity: From biosynthetic enzymes to drug resistance factors, J. Am. Chem. Soc. 119, 7619-7625.
32. Fenollar-Ferrer, C., Donoso, J., Frau, J., and Muñoz, F. (2005) Molecular modeling of the Henry-Michaelis and acyl-enzyme complexes between imipenem and Enterobacter cloacae P99 β-lactamase, Chem. Biodiversity 2, 645-656.
33. Gherman, B. F., Goldberg, S. D., Cornish, V. W., and Friesner, R. A. (2004) Mixed quantum mechanical/molecular mechanical (QM/MM) study of the deacylation reaction in a penicillin binding protein (PBP) versus in a class C β-lactamase, J. Am. Chem. Soc. 126, 7652-7664.
34. Fenollar-Ferrer, C., Frau, J., Donoso, J., and Muñoz, F. (2003) The role of β-lactam carboxyl group on binding of penicillins and cephalosporins to class C β-lactamases, Proteins: Struct., Funct., Genet. 51, 442-452.
35. Wilkinson, A.-S., Bryant, P. K., Meroueh, S. O., Page, M. G. P., Mobashery, S., and Wharton, C. W. (2003) A dynamic structure for the acyl-enzyme species of the antibiotic aztreonam with the Citrobacter freundii β-lactamase revealed by infrared spectroscopy and molecular dynamics simulations, Biochemistry 42, 1950-1957.
36. Sykes, R. B., Bonner, D. P., Bush, K., and Georgopapadakou, N. H. (1982) Aztreonam (SQ 26,776), a synthetic monobactam specifically active against aerobic gram-negative bacteria, Antimicrob. Agents Chemother. 21, 85-92.
37. Jorgensen, W. L., Chandrasekhar, J., Madura, J., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for the simulation of liquid water, J. Chem. Phys. 79, 926-935.
38. Schafmeister, C., Ross, W. S., and Romanovski, V. (1995) LEaP, University of California, San Francisco.
39. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Jr., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules, J. Am. Chem. Soc. 117, 5179-5197.
40. Case, D. A., Darden, T. A., Cheatham, T. E. I., Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Merz, K. M., Wang, B., Pearlman, D. A., Crowley, M., Brozell, S., Tsui, V., Gohlke, H., Mongan, J., Hornak, V., Cui, G., Beroza, P., Schafmeister, C., Caldwell, J. W., Ross, W. S., and Kollman, P. A. (2004), AMBER 8, University of California, San Francisco.
41. Berendsen, H. J. C., Potsma, J. P. M., van Gunsteren, W. F., DiNola, A. D., and Haak, J. R. (1984) Molecular dynamics with coupling to and external bath, J. Chem. Phys. 81, 3684-3690.
42. Essman, V., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., and Pedersen, L. G. (1995) A smooth Particle-Mesh-Ewald method, J. Chem. Phys. 103, 8577-8593.
43. Kraulis, P. J. (1991) Molscript: A program to produce both detailed and schematic plots of protein structures, J. Appl. Crystallogr. 24, 946-950.
44. Merritt, E. A., and Bacon, D. J. (1997) Raster3D: Photorealistic molecular graphics., Methods Enzymol. 277, 505-524.
45. Florey, K. (1988) Aztreonam, in Analytical profiles of drug substances, pp 1-39, Academic Press, New York.
46. ptz18r β-lactamase enhances the effect of serine-164 substitution on hydrolysis or affinity for cephalosporins and the monobactam aztreonam, Biochemistry 30, 3179-3188.
47. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Zakrzewski, V. G., Montgomery, J. A., Stratmann, R. E., Jr., Burant, J. C., Dapprich, S., Millam, J. M., Daniels, A. D., Kudin, K. N., Strain, M. C., Farkas, O., Tomasi, J., Barone, V., Cossi, M., Cammi, R., Mennucci, B., Pomelli, C., Adamo, C., Clifford, S., Ochterski, J., Petersson, G. A., Ayala, P. Y., Cui, Q., Morokuma, K., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Cioslowski, J., Ortiz, J. V., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Gomperts, R., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Gonzalez, C., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Andres, J. L., Gonzalez, C., Head-Gordon, M., Replogle, E. S., and Pople, J. A. (1998) Gaussian98, Gaussian, Inc., Pittsburgh, PA.
48. Kollman, P. A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., Lee, M., Lee, T., Duan, Y., Wang, W., Donini, O., Cieplak, P., Srinivasan, J., Case, D. A., and Cheatham, T. E. (2000) Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models, Acc. Chem. Res. 33, 889-897.
49. Gohlke, H., and Case, D. A. (2003) Converging free energy estimates: MM-PB(GB)SA studies on the protein-protein complex Ras-Raf, J. Comput. Chem. 25, 238-250.
50. Díaz, N., Sordo, T. L., and Suárez, D. (2005) Insights into the base catalysis exerted by the DD-transpeptidase from Streptomyces K15: A molecular dynamics study, Biochemistry 44, 3225-3240.
51. Yang, W., and Lee, T.-S. (1995) A density-matrix form of the divide-and-conquer approach for electronic structure calculations of large molecules, J. Chem. Phys. 103, 5674-5678.
52. Dixon, S. L., and Merz, K. M., Jr. (1997) Fast, accurate semiempirical molecular orbital calculations for macromolecules, J. Chem. Phys. 107, 879-893.
53. Wang, B., Raha, K., Liao, N., Peters, M. B., Kim, H., Westerhoff, L. M., Wollacott, A. M., van der Vaart, A., Gogonea, V., Suarez, D., Dixon, S. L., Vincent, J. J., Brothers, E. N., and Merz, K. M. J. (2005) DIVCON 4.0, QuantumBio Inc., State College, PA.
54. Stewart, J. J. P. (1989) Optimization of parameters for semiempirical methods I. Method, J. Comput. Chem. 10, 209-220.
55. Gogonea, V., and Merz, K. M., Jr. (1999) Fully quantum mechanical description of proteins in solution. Combining linear scaling quantum mechanical methodologies with the Poisson-Boltzmann equation, J. Phys. Chem. A 103, 5171-5178.
56. Orozco, M., and Luque, F. J. (2000) Theoretical methods for the description of the solvent effect in biomolecular systems, Chem. Rev. 100, 4187-4225.
57. Elstner, M., Hobza, P., Frauenheim, T., Suhai, S., and Kaxiras, E. (2001) Hydrogen bonding and stacking interactions of nucleic acid base pairs: A density-functional-theory based treatment, J. Chem. Phys. 114, 5149-5154.
58. Elstner, M., Porezag, D., Jungnickel, G., Elsner, J., Haugk, M., Frauenheim, T., Suhai, S., and Seifert, G. (1998) Self-consistent-charge density-functional tight-binding method for simulations of complex materials properties, Phys. Rev. B 58, 7260-7268.
59. Miller, K. J. (1990) Additivity methods in molecular polarizability, J. Am. Chem. Soc. 112, 8533-8542.
60. Halgren, T. A. (1992) Representation of van der Waals (vdw) interactions in molecular mechanics force fields: Potential form, combination rules, and vdw parameters, J. Am. Chem. Soc. 114, 7827-7843.
61. Vondrásek, J., Bendová, L., Klusák, V., and Hobza, P. (2005) Unexpectedly strong energy stabilization inside the hydrophobic core of small protein rubredoxin mediated by aromatic residues: Correlated ab initio quantum chemical calculations, J. Am. Chem. Soc. 127, 2615-2619.
62. Dubus, A., Normark, S., Kania, M., and Page, M. G. P. (1994) The role of tyrosine 150 in catalysis of β-lactam hydrolysis by AmpC β-lactamase from Escherichia coli investigated by site-directed mutagenesis, Biochemistry 33, 8577-8586.
63. Adediran, S. A., and Pratt, R. F. (1999) β-Secondary and solvent deuterium kinetic isotope effects on catalysis by the Streptomyces R61 DD-peptidadse: Comparison with a structurally similar class C β-lactamase, Biochemistry 38, 1469-1477.