Multiple molecular dynamics simulations of TEM β-lactamase: Dynamics and water binding of the Ω-loop

Biophysical Journal

Volumn 97, Issue 9, 2009, Pages 2550-2558

  Bös, Fabian ^a   Pleiss, Jürgen ^a  

^a UNIVERSITY OF STUTTGART   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAMASE TEM 1;

ARTICLE; COMPUTER SIMULATION; ENZYME STABILITY; HYDROPHILICITY; MOLECULAR DYNAMICS; PROTEIN INTERACTION; PROTEIN STRUCTURE;

EID: 72249091122     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.08.031     Document Type: Article

References (52)

1. Bradford, P. A. 2001. Extended-spectrum β-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin. Microbiol. Rev. 14:933-951.
2. Datta, N., and P. Kontomichalou. 1965. Penicillinase synthesis controlled by infectious R factors in Enterobacteriaceae. Nature. 208:239-241.
3. Poole, K. 2004. Resistance to β-lactam antibiotics. Cell. Mol. Life Sci. 61:2200-2223.
4. Jelsch, C., F. Lenfant, J. M. Masson, and J. P. Samama. 1992. Beta-lactamase TEM1 of E. coli crystal structure determination at 2.5 Å resolution. FEBS Lett. 299:135-142.
5. Vakulenko, S. B., M. Toth, P. Taibi, S. Mobashery, and S. A. Lerner. 1995. Effects of Asp-179 mutations in Tem(Puc19) β-lactamase on susceptibility to β-lactams. Antimicrob. Agents Chemother. 39:1878-1880.
6. Vakulenko, S. B., P. Taibi-Tronche, M. Toth, I. Massova, S. A. Lerner, et al. 1999. Effects on substrate profile by mutational substitutions at positions 164 and 179 of the class A TEMpUC19 β-lactamase from Escherichia coli. J. Biol. Chem. 274:23052-23060.
7. Majiduddin, F. K., and T. Palzkill. 2003. An analysis of why highly similar enzymes evolve differently. Genetics. 163:457-466.
8. Matagne, A., J. Lamotte-Brasseur, and J. M. Frere. 1998. Catalytic properties of class A β-lactamases: efficiency and diversity. Biochem. J. 330:581-598. (Pubitemid 28111949)
9. 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.
10. Diaz, N., T. L. Sordo, K. M. Merz, Jr., and D. Suarez. 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.
11. 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.
12. Savard, P. Y., and S. M. Gagne. 2006. Backbone dynamics of TEM-1 determined by NMR: evidence for a highly ordered protein. Biochemistry. 45:11414-11424.
13. Massova, I., and S. Mobashery. 1998. Kinship and diversification of bacterial penicillin-binding proteins and β-lactamases. Antimicrob. Agents Chemother. 42:1-17.
14. Bös, F., and J. Pleiss. 2008.Conservedwatermolecules stabilize the Ω-loop in class A β-lactamases. Antimicrob. Agents Chemother. 52:1072-1079.
15. Hess, B. 2002. Convergence of sampling in protein simulations. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 65:031910.
16. Straub, J. E., and D. Thirumalai. 1993. Theoretical probes of conformational fluctuations in S-peptide and RNase A/3′-UMP enzyme product complex. Proteins. 15:360-373.
17. Caves, L. S., J. D. Evanseck, and M. Karplus. 1998. Locally accessible conformations of proteins: multiple molecular dynamics simulations of crambin. Protein Sci. 7:649-666. (Pubitemid 28130887)
18. Elofsson, A., and L. Nilsson. 1993. How consistent are molecular dynamics simulations? Comparing structure and dynamics in reduced and oxidized Escherichia coli thioredoxin. J. Mol. Biol. 233:766-780.
19. Carlson, M. L., R. M. Regan, and Q. H. Gibson. 1996. Distal cavity fluctuations in myoglobin: protein motion and ligand diffusion. Biochemistry. 35:1125-1136.
20. Daggett, V. 2000. Long timescale simulations. Curr. Opin. Struct. Biol. 10:160-164.
21. a of a model leucine zipper, GCN4 and barnase. Proteins. 46:41-60.
22. Likic, V. A., P. R. Gooley, T. P. Speed, and E. E. Strehler. 2005. A statistical approach to the interpretation of molecular dynamics simulations of calmodulin equilibrium dynamics. Protein Sci. 14:2955-2963. (Pubitemid 41770136)
23. Legge, F. S., A. Budi, H. Treutlein, and I. Yarovsky. 2006. Protein flexibility: multiple molecular dynamics simulations of insulin chain B. Biophys. Chem. 119:146-157.
24. 166 as the general base in acylation. J. Am. Chem. Soc. 124:5333-5340.
25. Dolinsky, T. J., J. E. Nielsen, J. A. McCammon, and N. A. Baker. 2004. PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res. 32:W665-W667.
26. Case, D., T. Darden, T. Cheatham, III, C. Simmerling, J. Wang, et al. 2004. AMBER 8. University of California, San Francisco, CA.
27. Duan, Y., C. Wu, S. Chowdhury, M. C. Lee, G. M. Xiong, et al. 2003. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J. Comput. Chem. 24:1999-2012.
28. Ryckaert, J. P., G. Ciccotti, and H. J. C. Berendsen. 1977. Numerical integration of Cartesian equations of motion of a system with constraints - molecular dynamics of n-alkanes. J. Comput. Phys. 23:327-341.
29. Berendsen, H. J. C., J. P. M. Postma, W. F. Vangunsteren, A. Dinola, and J. R. Haak. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690.
30. Darden, T., D. York, and L. Pedersen. 1993. Particle mesh Ewald: an N $ log(N) method for Ewald sums in large systems. J. Chem. Phys. 98:10089-10092.
31. Berendsen, H. J. C., J. R. Grigera, and T. P. Straatsma. 1987. The missing term in effective pair potentials. J. Phys. Chem. 91:6269-6271.
32. Stone, J.E., J. Gullingsrud, and K. Schulten. 2001. A system for interactive molecular dynamics simulation. In I3D '01: Proceedings of the 2001 Symposium on Interactive 3D Graphics. ACM Press, New York, NY.
33. DeLano, W. 2002. The PyMol Molecular Graphics System. http://www. pymol.org. DeLano Scientific, Palo Alto, CA.
34. Ho, B. K., and F. Gruswitz. 2008. HOLLOW: generating accurate representations of channel and interior surfaces in molecular structures. BMC Struct. Biol. 8:49.
35. 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.
36. Spoel, D. V. D., E. Lindahl, B. Hess, G. Groenhof, A. E. Mark, et al. 2005. GROMACS: fast, flexible, and free. J. Comput. Chem. 26:1701-1718.
37. Amadei, A., A. B. Linssen, and H. J. Berendsen. 1993. Essential dynamics of proteins. Proteins. 17:412-425.
38. Hess, B. 2000. Similarities between principal components of protein dynamics and random diffusion. Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics. 62:8438-8448.
39. Sanjeev, B. 2004. ANKUSH software. Indian Institute of Science, Bangalore.
40. Bidmon, K., S. Grottel, F. Bös, J. Pleiss, and T. Ertl. 2008. Visual abstractions of solvent pathlines near protein cavities. Comput. Graph. Forum. 27:935-942.
41. Philippopoulos, M., A. M. Mandel, A. G. Palmer, and C. Lim. 1997. Accuracy and precision of NMR relaxation experiments and MD simulations for characterizing protein dynamics. Proteins. 28:481-493. (Pubitemid 27328565)
42. Mattos, C. 2002. Protein-water interactions in a dynamic world. Trends Biochem. Sci. 27:203-208.
43. Despa, F. 2005. Biological water: its vital role in macromolecular structure and function. Ann. N.Y. Acad. Sci. 1066:1-11.
44. Prabhu, N., and K. Sharp. 2006. Protein-solvent interactions. Chem. Rev. 106:1616-1623.
45. Helms, V. 2007. Protein dynamics tightly connected to the dynamics of surrounding and internal water molecules. ChemPhysChem. 8:23-33.
46. Loris, R., P. P. G. Stas, and L. Wyns. 1994. Conserved waters in legume lectin crystal structures - the importance of bound water for the sequence-structure relationship within the legume lectin family. J. Biol. Chem. 269:26722-26733.
47. Ogata, K., and S. J. Wodak. 2002. Conserved water molecules in MHC class-1 molecules and their putative structural and functional roles. Protein Eng. 15:697-705. (Pubitemid 35175923)
48. Park, S., and J. G. Saven. 2005. Statistical and molecular dynamics studies of buried waters in globular proteins. Proteins. 60:450-463. (Pubitemid 41061638)
49. Ernst, J. A., R. T. Clubb, H. X. Zhou, A. M. Gronenborn, and G. M. Clore. 1995. Demonstration of positionally disordered water within a protein hydrophobic cavity by NMR. Science. 267:1813-1817.
50. Otting, G., E. Liepinsh, and K. Wüthrich. 1991. Protein hydration in aqueous solution. Science. 254:974-980.
51. Takano, K., Y. Yamagata, and K. Yutani. 2003. Buried water molecules contribute to the conformational stability of a protein. Protein Eng. 16:5-9. (Pubitemid 36407059)
52. Wang, X., G. Minasov, and B. K. Shoichet. 2002. Noncovalent interaction energies in covalent complexes: TEM-1 β-lactamase and β-lactams. Proteins. 47:86-96. (Pubitemid 34195257)