NMR dynamics of PSE-4 β-lactamase: An interplay of ps-ns order and μs-ms motions in the active site

Biophysical Journal

Volumn 96, Issue 11, 2009, Pages 4681-4691

  Morin, Sébastien ^a   Gagné, Stéphane M ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; BETA LACTAM ANTIBIOTIC; BETA LACTAMASE; BETA LACTAMASE TEM 1; NITROGEN 15; PSE 4 ENZYME; UNCLASSIFIED DRUG; AMIDE; BETA LACTAMASE PSE 4; BETA-LACTAMASE PSE-4; BETA-LACTAMASE TEM-1;

ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; DIFFUSION; ELASTICITY; MOTION; PROTEIN CONFORMATION; THERMODYNAMICS; TIME;

AMIDES; BETA-LACTAMASES; COMPUTER SIMULATION; DIFFUSION; ELASTICITY; MODELS, CHEMICAL; MODELS, MOLECULAR; MOTION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; THERMODYNAMICS; TIME FACTORS;

EID: 68949086333     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.02.068     Document Type: Article

References (52)

1. Fisher, J. F., S. O. Meroueh, and S. Mobashery. 2005. Bacterial resistance to β-lactam antibiotics: compelling opportunism, compelling opportunity. Chem. Rev. 105:395-424.
2. Matagne, A., J. Lamotte-Brasseur, and J. M. Frère. 1998. Catalytic properties of class A β-lactamases: efficiency and diversity. Biochem. J. 330:581-598.
3. Christensen, H., M. T. Martin, and S. G. Waley. 1990. β-lactamases as fully efficient enzymes. Determination of all the rate constants in the acyl-enzyme mechanism. Biochem. J. 266:853-861.
4. Hedstrom, L. 2002. Serine protease mechanism and specificity. Chem. Rev. 102:4501-4524.
5. Oefner, C., A. D'Arcy, J. J. Daly, K. Gubernator, R. L. Charnas, et al. 1990. Refined crystal structure of β-lactamase from Citrobacter freundii indicates a mechanism for β-lactam hydrolysis. Nature. 343:284-288.
6. 70. J. Am. Chem. Soc. 127:15397-15407.
7. Allerhand, A., D. Doddrell, V. Glushko, D. W. Cochran, E. Wenkert, et al. 1971. Conformation and segmental motion of native and denatured ribonuclease A in solution. Application of natural-abundance carbon-13 partially relaxed Fourier transform nuclear magnetic resonance. J. Am. Chem. Soc. 93:544-546.
8. Wand, A. J. 2001. Dynamic activation of protein function: a view emerging from NMR spectroscopy. Nat. Struct. Biol. 8:926-931.
9. Yon, J. M., D. Perahia, and C. Ghélis. 1998. Conformational dynamics and enzyme activity. Biochimie. 80:33-42.
10. Savard, P.-Y., and S. M. Gagné. 2006. Backbone dynamics of TEM-1 determined by NMR: evidence for a highly ordered protein. Biochemistry. 45:11414-11424.
11. 105 mutants in TEM-1 β-lactamase: dynamics are correlated with function. J. Biol. Chem. 282:21448-21459.
12. Newsom, S. W. 1969. Carbenicillin-resistant Pseudomonas. Lancet. 2:1141.
13. Reid, A. J., I. N. Simpson, P. B. Harper, and S. G. Amyes. 1988. The differential expression of genes for the PSE-4 β-lactamase in Pseudomonas aeruginosa and the Enterobacteriaceae. J. Antimicrob. Chemother. 21:525-533.
14. Lim, D., F. Sanschagrin, L. Passmore, L. D. Castro, R. C. Levesque, et al. 2001. Insights into the molecular basis for the carbenicillinase activity of PSE-4 β-lactamase from crystallographic and kinetic studies. Biochemistry. 40:395-402.
15. Lipari, G., and A. Szabo. 1982. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104:4546-4559.
16. Lipari, G., and A. Szabo. 1982. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104:4559-4570.
17. 15N backbone resonance assignments for PSE-4, a 29.5 kDa class A β-lactamase from Pseudomonas aeruginosa. J. Biomol. NMR. 36 (Suppl 1):11.
18. Kay, L. E., P. Keifer, and T. Saarinen. 1992. Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 114:10663-10665.
19. 15N NMR relaxation. Biochemistry. 33:5984-6003.
20. 15N NMR relaxation measurements at two magnetic fields. J. Biomol. NMR. 8:273-284.
21. Delaglio, F., S. Grzesiek, G. W. Vuister, G. Zhu, J. Pfeifer, et al. 1995. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR. 6:277-293.
22. 15N relaxation data exclusively. J. Biomol. NMR. 6:153-162.
23. d'Auvergne, E. J., and P. R. Gooley. 2008. Optimization of NMR dynamic models. I. Minimization algorithms and their performance within the model-free and Brownian rotational diffusion spaces. J. Biomol. NMR. 40:107-119.
24. d'Auvergne, E. J., and P. R. Gooley. 2008. Optimization of NMR dynamic models. II. A new methodology for the dual optimization of the model-free parameters and the Brownian rotational diffusion tensor. J. Biomol. NMR. 40:121-133.
25. Kabsch, W., and C. Sander. 1983. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 22:2577-2637.
26. Akaike, H.1973. Information theory and an extension of the maximum likelihood principle. In Proceedings of the 2nd International Symposium on Information Theory, Budapest, Hungary. B.N. Petrov and F. Csaki, editors.
27. Hurvich, C., and C.-L. Tsai. 1989. Regression and time series model selection in small samples. Biometrika. 76:297-307.
28. Ambler, R. P., A. F. Coulson, J. M. Frère, J. M. Ghuysen, B. Joris, et al. 1991. A standard numbering scheme for the class A β-lactamases. Biochem. J. 276:269-270.
29. Clore, G. M., A. Szabo, A. Bax, L. E. Kay, P. C. Driscoll, et al. 1990. Deviations from the simple two-parameter model-free approach to the interpretation of Nitrogen-15 nuclear magnetic-relaxation of proteins. J. Am. Chem. Soc. 112:4989-4991.
30. 13C heteronuclear NMR spectroscopy. J. Am. Chem. Soc. 113:4371-4380.
31. Mandel, A. M., M. Akke, and A. G. Palmer. 1995. Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme. J. Mol. Biol. 246:144-163.
32. García de la Torre, J., M. L. Huertas, and B. Carrasco. 2000. HYDRONMR: prediction of NMR relaxation of globular proteins from atomic-level structures and hydrodynamic calculations. J. Magn. Reson. 147:138-146.
33. Hall, J. B., and D. Fushman. 2003. Characterization of the overall and local dynamics of a protein with intermediate rotational anisotropy: differentiating between conformational exchange and anisotropic diffusion in the B3 domain of protein G. J. Biomol. NMR. 27:261-275.
34. Lee, A. L., S. A. Kinnear, and A. J. Wand. 2000. Redistribution and loss of side chain entropy upon formation of a calmodulin-peptide complex. Nat. Struct. Biol. 7:72-77.
35. Roccatano, D., G. Sbardella, M. Aschi, G. Amicosante, C. Bossa, et al. 2005. Dynamical aspects of TEM-1 β-lactamase probed by molecular dynamics. J. Comput. Aided Mol. Des. 19:329-340.
36. Jelsch, C., L. Mourey, J. M. Masson, and J. P. Samama. 1993. Crystal structure of Escherichia coli TEM1 β-lactamase at 1.8 Å resolution. Proteins. 16:364-383.
37. Millet, O., J. Loria, C. Kroenke, M. Pons, and A. Palmer. 2000. The static magnetic field dependence of chemical exchange linebroadening defines the NMR chemical shift time scale. J. Am. Chem. Soc. 122:2867-2877.
38. Doucet, N., P.-Y. De Wals, and J. N. Pelletier. 2004. Site-saturation mutagenesis of Tyr-105 reveals its importance in substrate stabilization and discrimination in TEM-1 β-lactamase. J. Biol. Chem. 279:46295-46303.
39. Doucet, N., and J. N. Pelletier. 2007. Simulated annealing exploration of an active-site tyrosine in TEM-1 β-lactamase suggests the existence of alternate conformations. Proteins. 69:340-348.
40. 13C′ chemical shifts in proteins using a density functional database. J. Biomol. NMR. 21:321-333.
41. Lahey Clinic. TEM extended-spectrum and inhibitor resistant β-lactamases. www.lahey.org/Studies/temtable.asp.
42. Fetrow, J. S. 1995. Omega loops: nonregular secondary structures significant in protein function and stability. FASEB J. 9:708-717.
43. Vijayakumar, S., G. Ravishanker, R. F. Pratt, and D. L. Beveridge. 1995. Molecular dynamics simulation of a class A β-lactamase: structural and mechanistic implications. J. Am. Chem. Soc. 117:1722-1730.
44. Díaz, N., T. L. Sordo, K. M. Merz, Jr., and D. Suárez. 2003. Insights into the acylation mechanism of class A β-lactamases from molecular dynamics simulations of the TEM-1 enzyme complexed with benzylpenicillin. J. Am. Chem. Soc. 125:672-684.
45. Krishna, M. M. G., L. Hoang, Y. Lin, and S. W. Englander. 2004. Hydrogen exchange methods to study protein folding. Methods. 34:51-64.
46. Bai, Y., J. S. Milne, L. Mayne, and S. W. Englander. 1993. Primary structure effects on peptide group hydrogen exchange. Proteins. 17:75-86.
47. Connelly, G. P., Y. Bai, M. F. Jeng, and S. W. Englander. 1993. Isotope effects in peptide group hydrogen exchange. Proteins. 17:87-92.
48. Vanhove, M., G. Guillaume, P. Ledent, J. H. Richards, R. H. Pain, et al. 1997. Kinetic and thermodynamic consequences of the removal of the Cys-77-Cys-123 disulphide bond for the folding of TEM-1 β-lactamase. Biochem. J. 321:413-417.
49. 13C NMR chemical shifts can predict disulfide bond formation. J. Biomol. NMR. 18:165-171.
50. Willard, L., A. Ranjan, H. Zhang, H. Monzavi, R. F. Boyko, et al. 2003. VADAR: a web server for quantitative evaluation of protein structure quality. Nucleic Acids Res. 31:3316-3319.
51. Jarymowycz, V. A., and M. J. Stone. 2006. Fast time scale dynamics of protein backbones: NMR relaxation methods, applications, and functional consequences. Chem. Rev. 106:1624-1671.
52. Sabbagh, Y., E. Thériault, F. Sanschagrin, N. Voyer, T. Palzkill, et al. 1998. Characterization of a PSE-4 mutant with different properties in relation to penicillanic acid sulfones: importance of residues 216 to 218 in class A β-lactamases. Antimicrob. Agents Chemother. 42:2319-2325.