Analysis of sub-τc and supra-τc motions in protein Gβ1 using molecular dynamics simulations

Biophysical Journal

Volumn 97, Issue 9, 2009, Pages 2513-2520

  Bui, Jennifer M ^a   Gsponer, Jörg ^b   Vendruscolo, Michele ^a   Dobson, Christopher M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; BACTERIAL PROTEIN; IGG FC BINDING PROTEIN, STREPTOCOCCUS; IGG FC-BINDING PROTEIN, STREPTOCOCCUS;

ARTICLE; COMPUTER SIMULATION; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PH MEASUREMENT; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; BIOPHYSICS; CHEMISTRY; MAGNETISM; METABOLISM; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PH; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; STATIC ELECTRICITY; STATISTICAL MODEL; STREPTOCOCCUS; TIME;

BACTERIAL PROTEINS; BIOPHYSICS; COMPUTER SIMULATION; HYDROGEN-ION CONCENTRATION; MAGNETIC RESONANCE SPECTROSCOPY; MAGNETICS; MODELS, STATISTICAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; STATIC ELECTRICITY; STREPTOCOCCUS; TIME FACTORS;

EID: 72249116591     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.07.061     Document Type: Article

References (44)

1. Mittermaier, A., and L. E. Kay. 2006. New tools provide new insights in NMR studies of protein dynamics. Science. 312:224-228.
2. Boehr, D. D., H. J. Dyson, and P. E. Wright. 2006. An NMR perspective on enzyme dynamics. Chem. Rev. 106:3055-3079.
3. Palmer, 3rd, A. G. 2004. NMR characterization of the dynamics of biomacromolecules. Chem. Rev. 104:3623-3640.
4. Igumenova, T. I., K. K. Frederick, and A. J. Wand. 2006. Characterization of the fast dynamics of protein amino acid side chains using NMR relaxation in solution. Chem. Rev. 106:1672-1699.
5. Lipari, G., and A. Szabo. 1982. Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules. J. Am. Chem. Soc. 104:4546-4559.
6. Tjandra, N., and A. Bax. 1997. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science. 278:1111-1114. (Pubitemid 27517889)
7. Meiler, J., J. J. Prompers, W. Peti, C. Griesinger, and R. Bruschweiler. 2001. Model-free approach to the dynamic interpretation of residual dipolar couplings in globular proteins. J. Am. Chem. Soc. 123:6098-6107.
8. Tolman, J. R., H. M. Al-Hashimi, L. E. Kay, and J. H. Prestegard. 2001. Structural and dynamic analysis of residual dipolar coupling data for proteins. J. Am. Chem. Soc. 123:1416-1424.
9. Lange, O. F., N. A. Lakomek, C. Fares, G. F. Schroder, K. F. Walter, et al. 2008. Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science. 320:1471-1475.
10. Maragakis, P., K. Lindorff-Larsen, M. P. Eastwood, R. O. Dror, J. L. Klepeis, et al. 2008. Microsecond molecular dynamics simulation shows effect of slow loop dynamics on backbone amide order parameters of proteins. J. Phys. Chem. B. 112:6155-6158.
11. Adcock, S. A., and J. A. McCammon. 2006. Molecular dynamics: survey of methods for simulating the activity of proteins. Chem. Rev. 106:1589-1615.
12. Trbovic, N., B. Kim, R. A. Friesner, and A. G. Palmer, 3rd. 2008. Structural analysis of protein dynamics by MD simulations and NMR spinrelaxation. Proteins. 71:684-694.
13. Showalter, S. A., and R. Bruschweiler. 2007. Quantitative molecular ensemble interpretation of NMR dipolar couplings without restraints. J. Am. Chem. Soc. 129:4158-4159.
14. Markwick, P. R., G. Bouvignies, and M. Blackledge. 2007. Exploring multiple timescale motions in protein GB3 using accelerated molecular dynamics and NMR spectroscopy. J. Am. Chem. Soc. 129:4724-4730.
15. Barchi, Jr., J. J., B. Grasberger, A. M. Gronenborn, and G. M. Clore. 1994. Investigation of the backbone dynamics of the IgG-binding domain of streptococcal protein G by heteronuclear two-dimensional 1H-15N nuclear magnetic resonance spectroscopy. Protein Sci. 3:15-21.
16. Achari, A., S. P. Hale, A. J. Howard, G. M. Clore, A. M. Gronenborn, et al. 1992. 1.67-A x-ray structure of the B2 immunoglobulin-binding domain of streptococcal protein G and comparison to the NMR structure of the B1 domain. Biochemistry. 31:10449-10457.
17. Bouvignies, G., P. Bernado, S. Meier, K. Cho, S. Grzesiek, et al. 2005. Identification of slow correlated motions in proteins using residual dipolar and hydrogen-bond scalar couplings. Proc. Natl. Acad. Sci. USA. 102:13885-13890.
18. Clore, G. M., and C. D. Schwieters. 2004. Amplitudes of protein backbone dynamics and correlated motions in a small alpha/beta protein: correspondence of dipolar coupling and heteronuclear relaxation measurements. Biochemistry. 43:10678-10691.
19. Gronenborn, A. M., D. R. Filpula, N. Z. Essig, A. Achari, M. Whitlow, et al. 1991. A novel, highly stable fold of the immunoglobulin binding domain of streptococcal protein G. Science. 253:657-661.
20. Vriend, G. 1990. WHAT IF: a molecular modeling and drug design program. J. Mol. Graph. 8:52-56.
21. Gilson, M. K., and B. Honig. 1988. Calculation of the total electrostatic energy of a macromolecular system: solvation energies, binding energies, and conformational analysis. Proteins. 4:7-18.
22. Ulmer, T. S., B. E. Ramirez, F. Delaglio, and A. Bax. 2003. Evaluation of backbone proton positions and dynamics in a small protein by liquid crystal NMR spectroscopy. J. Am. Chem. Soc. 125:9179-9191.
23. Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulations liquid water. J. Chem. Phys. 79:926-935.
24. Hornak, V., R. Abel, A. Okur, B. Strockbine, A. Roitberg, et al. 2006. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins. 65:712-725.
25. Hornak, V., A. Okur, R. C. Rizzo, and C. Simmerling. 2006. HIV-1 protease flaps spontaneously open and closed in molecular dynamics simulations. Proc. Natl. Acad. Sci. USA. 103:915-920.
26. Case, D. A., T. E. Cheatham, T. Darden, H. Gohlke, R. Luo, et al. 2005. The Amber biomolecular simulation programs. J. Comput. Chem. 26:1668-1688.
27. Andersen, H. C. 1980. Molecular dynamics simulations at constant pressure and-or temperature. J. Chem. Phys. 72:2384-2393.
28. 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.
29. Ryckaert, J. P. C., G. Ciccotti, and H. 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.
30. Redfield, A. G. 1965. The theory of relaxation processes. Adv. Magn. Reson. 1:1-32.
31. Clore, G. M., P. C. Driscoll, P. T. Wingfield, and A. M. Gronenborn. 1990. Analysis of the backbone dynamics of interleukin-1 beta using two-dimensional inverse detected heteronuclear 15N-1H NMR spectroscopy. Biochemistry. 29:7387-7401.
32. Chen, J., C. L. Brooks, 3rd, and P. E. Wright. 2004. Model-free analysis of protein dynamics: assessment of accuracy and model selection protocols based on molecular dynamics simulation. J. Biomol. NMR. 29:243-257.
33. Showalter, S. A., and R. Bruschweiler. 2007. Validation of molecular dynamics simulations of biomolecules using NMR spin relaxation as benchmarks: application to the AMBER99SB force field. J. Chem. Theory Comput. 3:961-975.
34. Byeon, I. J., J. M. Louis, and A. M. Gronenborn. 2003. A protein contortionist: core mutations of GB1 that induce dimerization and domain swapping. J. Mol. Biol. 333:141-152.
35. Chandrasekhar, I., G. M. Clore, A. Szabo, A. M. Gronenborn, and B. R. Brooks. 1992. A 500 ps molecular dynamics simulation study of interleukin- 1 beta in water. Correlation with nuclear magnetic resonance spectroscopy and crystallography. J. Mol. Biol. 226:239-250.
36. Karplus, M. 1959. Contact electron-spin coupling of nuclear magnetic moments. J. Chem. Phys. 30:11-15.
37. Vogeli, B., J. Ying, A. Grishaev, and A. Bax. 2007. Limits on variations in protein backbone dynamics from precise measurements of scalar couplings. J. Am. Chem. Soc. 129:9377-9385.
38. Bruschweiler, R., and D. A. Case. 1994. Adding harmonic motion to the Karplus relation for spin-spin coupling. J. Am. Chem. Soc. 116:11199-11200.
39. Hu, J. S., and A. Bax. 1998. Measurement of three-bond, 13C0-13C beta J couplings in human ubiquitin by a triple resonance, E. COSY-type NMR technique. J. Biomol. NMR. 11:199-203.
40. Lindorff-Larsen, K., R. B. Best, and M. Vendruscolo. 2005. Interpreting dynamically-averaged scalar couplings in proteins. J. Biomol. NMR. 32:273-280.
41. Clore, G. M. 1999. Structures of B1 domain of streptococcal protein G. J. Am. Chem. Soc. 121:2337-2338.
42. Gronenborn, A. M., and G. M. Clore. 1993. Identification of the contact surface of a streptococcal protein G domain complexed with a human Fc fragment. J. Mol. Biol. 233:331-335.
43. Bouvignies, G., P. Markwick, R. Bruschweiler, and M. Blackledge. 2006. Simultaneous determination of protein backbone structure and dynamics from residual dipolar couplings. J. Am. Chem. Soc. 128:15100-15101.
44. Penengo, L., M. Mapelli, A. G. Murachelli, S. Confalonieri, L. Magri, et al. 2006. Crystal structure of the ubiquitin binding domains of rabex-5 reveals two modes of interaction with ubiquitin. Cell. 124:1183-1195.