Exploring Free Energy Landscapes of Large Conformational Changes: Molecular Dynamics with Excited Normal Modes

Journal of Chemical Theory and Computation

Volumn 11, Issue 6, 2015, Pages 2755-2767

  Costa, Mauricio G S ^a,b,c   Batista, Paulo R ^a   Bisch, Paulo M ^b   Perahia, David ^c  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HEN EGG LYSOZYME; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE; LYSOZYME; P16 PROTEASE, HUMAN IMMUNODEFICIENCY VIRUS 1;

CHEMISTRY; METABOLISM; MOLECULAR DYNAMICS; PROTEIN CONFORMATION;

HIV PROTEASE; MOLECULAR DYNAMICS SIMULATION; MURAMIDASE; PROTEIN CONFORMATION;

EID: 84931263113     PISSN: 15499618     EISSN: 15499626     Source Type: Journal    
DOI: 10.1021/acs.jctc.5b00003     Document Type: Article

References (50)

1. James, L. C.; Tawfik, D. S. Conformational diversity and protein evolution-a 60-year-old hypothesis revisited Trends Biochem. Sci. 2003, 28, 361-8
2. Mulder, F. A. A.; Mittermaier, A.; Hon, B.; Dahlquist, F. W.; Kay, L. E. Studying excited states of proteins by NMR spectroscopy Nat. Struct. Mol. Biol. 2001, 8, 932-5
3. Korzhnev, D. M.; Kay, L. E. Probing invisible, low-populated states of protein molecules by relaxation dispersion NMR spectroscopy: an application to protein folding Acc. Chem. Res. 2008, 41, 442-51
4. Berendsen, H. J.; Hayward, S. Collective protein dynamics in relation to function Curr. Opin. Struct. Biol. 2000, 10, 165-9
5. Bahar, I.; Lezon, T. R.; Bakan, A.; Shrivastava, I. H. Normal mode analysis of biomolecular structures: functional mechanisms of membrane proteins Chem. Rev. 2010, 110, 1463-97
6. Grant, B. J.; Gorfe, A. A.; McCammon, J. A. Large conformational changes in proteins: signaling and other functions Curr. Opin. Struct. Biol. 2010, 20, 142-7
7. Salomon-Ferrer, R.; Götz, A. W.; Poole, D.; Le Grand, S.; Walker, R. C. Routine microsecond molecular dynamics simulations with AMBER on GPUs. 2. Explicit solvent particle mesh Ewald J. Chem. Theory Comput. 2013, 9, 3878-88
8. Hess, B. Convergence of sampling in protein simulations Phys. Rev. E 2002, 65, 031910
9. Hayward, S.; de Groot, B. L., Normal modes and essential dynamics. In Molecular Modeling of Proteins; Kukol, A., Ed.; Humana Press: Totowa, NJ, 2008; Vol. 443.
10. Skjaerven, L.; Hollup, S. M.; Reuter, N. Normal mode analysis for proteins J. Mol. Struct.: THEOCHEM 2009, 898, 42-8
11. Levy, R. M.; Perahia, D.; Karplus, M. Molecular dynamics of an alpha-helical polypeptide: temperature dependence and deviation from harmonic behavior Proc. Natl. Acad. Sci. U.S.A. 1982, 79, 1346-50
12. Ho, B. K.; Perahia, D.; Buckle, A. M. Hybrid approaches to molecular simulation Curr. Opin. Struct. Biol. 2012, 22, 386-93
13. Schlick, T. Molecular dynamics-based approaches for enhanced sampling of long-time, large-scale conformational changes in biomolecules F1000Prime Rep. 2009, 1, 51
14. Kästner, J. Umbrella sampling Wiley Interdiscip. Rev.: Comput. Mol. Sci. 2011, 1, 932-42
15. Barducci, A.; Bonomi, M.; Parrinello, M. Metadynamics Wiley Interdiscip. Rev.: Comput. Mol. Sci. 2011, 1, 826-43
16. Batista, P. R.; Pandey, G.; Pascutti, P. G.; Bisch, P. M.; Perahia, D.; Robert, C. H. Free energy profiles along consensus normal modes provide insight into HIV-1 protease flap opening J. Chem. Theory Comput. 2011, 7, 2348-52
17. Floquet, N.; Durand, P.; Maigret, B.; Badet, B.; Badet-Denisot, M. A.; Perahia, D. Collective motions in glucosamine-6-phosphate synthase: influence of ligand binding and role in ammonia channelling and opening of the fructose-6-phosphate binding site J. Mol. Biol. 2009, 385, 653-64
18. Floquet, N.; Marechal, J. D.; Badet-Denisot, M. A.; Robert, C. H.; Dauchez, M.; Perahia, D. Normal mode analysis as a prerequisite for drug design: application to matrix metalloproteinases inhibitors FEBS Lett. 2006, 580, 5130-6
19. Bahar, I.; Atilgan, A.; Demirel, M.; Erman, B. Vibrational dynamics of folded proteins: significance of slow and fast motions in relation to function and stability Phys. Rev. Lett. 1998, 80, 2733-6
20. Brooks, B. R.; Brooks, C. L., III; Mackerell, A. D., Jr.; Nilsson, L.; Petrella, R. J.; Roux, B.; Won, Y.; Archontis, G.; Bartels, C.; Boresch, S.; Caflisch, A.; Caves, L.; Cui, Q.; Dinner, A. R.; Feig, M.; Fischer, S.; Gao, J.; Hodoscek, M.; Im, W.; Kuczera, K.; Lazaridis, T.; Ma, J.; Ovchinnikov, V.; Paci, E.; Pastor, R. W.; Post, C. B.; Pu, J. Z.; Schaefer, M.; Tidor, B.; Venable, R. M.; Woodcock, H. L.; Wu, X.; Yang, W.; York, D. M.; Karplus, M. CHARMM: the biomolecular simulation program J. Comput. Chem. 2009, 30, 1545-614
21. Perahia, D.; Levy, R. M.; Karplus, M. Motions of an alpha-helical polypeptide-comparison of molecular and harmonic dynamics Biopolymers 1990, 29, 645-677
22. Im, W.; Lee, M. S.; Brooks, C. L., III Generalized born model with a simple smoothing function J. Comput. Chem. 2003, 24, 1691-702
23. Johnson, L. N. The early history of lysozyme Nat. Struct. Biol. 1998, 5, 942-4
24. Blake, C. C. F.; Koenig, D. F.; Mair, G. A.; North, A. C. T.; Phillips, D. C.; Sarma, V. R. Structure of hen egg-white lysozyme: a three-dimensional Fourier synthesis at 2 Å resolution Nature 1965, 206, 757-61
25. Diehl, M.; Doster, W.; Petry, W.; Schober, H. Water-coupled low-frequency modes of myoglobin and lysozyme observed by inelastic neutron scattering Biophys. J. 1997, 73, 2726-32
26. Yoshida, Y.; Ohkuri, T.; Kino, S.; Ueda, T.; Imoto, T. Elucidation of the relationship between enzyme activity and internal motion using a lysozyme stabilized by cavity-filling mutations Cell. Mol. Life Sci. 2005, 62, 1047-55
27. De Simone, A.; Montalvao, R. W.; Dobson, C. M.; Vendruscolo, M. Characterization of the interdomain motions in hen lysozyme using residual dipolar couplings as replica-averaged structural restraints in molecular dynamics simulations Biochemistry 2013, 52, 6480-6
28. Brooks, B.; Karplus, M. Normal modes for specific motions of macromolecules: application to the hinge-bending mode of lysozyme Proc. Natl. Acad. Sci. U.S.A. 1985, 82, 4995-9
29. Brooks, B.; Karplus, M. Harmonic dynamics of proteins: normal modes and fluctuations in bovine pancreatic trypsin inhibitor Proc. Natl. Acad. Sci. U.S.A. 1983, 80, 6571-5
30. Hinsen, K. Structural flexibility in proteins: impact of the crystal environment Bioinformatics 2008, 24, 521-528
31. Schwalbe, H.; Grimshaw, S. B.; Spencer, A.; Buck, M.; Boyd, J.; Dobson, C. M.; Redfield, C.; Smith, L. J. A refined solution structure of hen lysozyme determined using residual dipolar coupling data Protein Sci. 2001, 10, 677-88
32. Refaee, M.; Tezuka, T.; Akasaka, K.; Williamson, M. P. Pressure-dependent changes in the solution structure of hen egg-white lysozyme J. Mol. Biol. 2003, 327, 857-65
33. Kohl, N. E.; Emini, E. A.; Schleif, W. A.; Davis, L. J.; Heimbach, J. C.; Dixon, R. A.; Scolnick, E. M.; Sigal, I. S. Active human immunodeficiency virus protease is required for viral infectivity Proc. Natl. Acad. Sci. U.S.A. 1988, 85, 4686-90
34. Ishima, R.; Freedberg, D. I.; Wang, Y. X.; Louis, J. M.; Torchia, D. A. Flap opening and dimer-interface flexibility in the free and inhibitor-bound HIV protease, and their implications for function Structure 1999, 7, 1047-55
35. Tozzini, V.; Trylska, J.; Chang, C. E.; McCammon, J. A. Flap opening dynamics in HIV-1 protease explored with a coarse-grained model J. Struct. Biol. 2007, 157, 606-15
36. Batista, P. R.; Robert, C. H.; Marechal, J. D.; Hamida-Rebai, M. B.; Pascutti, P. G.; Bisch, P. M.; Perahia, D. Consensus modes, a robust description of protein collective motions from multiple-minima normal mode analysis-application to the HIV-1 protease Phys. Chem. Chem. Phys. 2010, 12, 2850-9
37. Galiano, L.; Bonora, M.; Fanucci, G. E. Interflap distances in HIV-1 protease determined by pulsed EPR measurements J. Am. Chem. Soc. 2007, 129, 11004-5
38. He, J.; Zhang, Z.; Shi, Y.; Liu, H. Efficiently explore the energy landscape of proteins in molecular dynamics simulations by amplifying collective motions J. Chem. Phys. 2003, 119, 4005-17
39. Gur, M.; Madura, J. D.; Bahar, I. Global transitions of proteins explored by a multiscale hybrid methodology: application to adenylate kinase Biophys. J. 2013, 105, 1643-52
40. Ramanadham, M.; Sieker, L. C.; Jensen, L. H. Refinement of triclinic lysozyme 0.2. The method of stereochemically restrained least-squares Acta Crystallogr., Sect. B: Struct. Sci. 1990, 46, 63-9
41. Spinelli, S.; Liu, Q. Z.; Alzari, P. M.; Hirel, P. H.; Poljak, R. J. The three-dimensional structure of the aspartyl protease from the HIV-1 isolate BRU Biochimie 1991, 73, 1391-6
42. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. Scalable molecular dynamics with NAMD J. Comput. Chem. 2005, 26, 1781-802
43. Brooks, B. R.; Bruccoleri, R. E.; Olafson, B. D.; States, D. J.; Swaminathan, S.; Karplus, M. CHARMM: a program for macromolecular energy,minimization, and dynamics calculations J. Comput. Chem. 1983, 4, 187-217
44. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 1983, 79, 926-35
45. Ulrich, E.; Lalith, P.; Max, L. B.; Tom, D.; Hsing, L.; Lee, G. P. A smooth particle mesh Ewald method J. Chem. Phys. 1995, 103, 8577-93
46. Miyamoto, S.; Kollman, P. A. Settle-an analytical version of the Shake and Rattle algorithm for rigid water models J. Comput. Chem. 1992, 13, 952-62
47. Ryckaert, J.-P.; Ciccotti, G.; Berendsen, H. J. C. Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n -alkanes J. Comput. Phys. 1977, 23, 327-41
48. Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; Hermans, J. Interaction models for water in relation to protein hydration. In Intermolecular Forces; Pullman, B., Ed.; Springer: The Netherlands, 1981; Vol. 14, pp 331-42.
49. Berendsen, H. J. C.; Postma, J. P. M.; Vangunsteren, W. F.; Dinola, A.; Haak, J. R. Molecular dynamics with coupling to an external bath J. Chem. Phys. 1984, 81, 3684-90
50. Tama, F.; Sanejouand, Y. H. Conformational change of proteins arising from normal mode calculations Protein Eng. 2001, 14, 1-6