Relative free enthalpies for point mutations in two proteins with highly similar sequences but different folds

Biochemistry

Volumn 52, Issue 29, 2013, Pages 4962-4970

  Hansen, Niels ^a   Allison, Jane R ^b   Hodel, Florian H ^a   Van Gunsteren, Wilfred F ^a  

^a ETH ZURICH   (Switzerland)

^b MASSEY UNIVERSITY   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

BUNDLE STRUCTURES; DIFFERENT STRUCTURE; FREE ENTHALPY; NON-NATIVE; POINT MUTATIONS; SEQUENCE IDENTITY; STABLE FORM;

AMINO ACIDS; PROTEINS;

ENTHALPY;

AMINO ACID SEQUENCE; ARTICLE; ENTHALPY; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; THERMODYNAMICS;

AMINO ACIDS; POINT MUTATION; PROTEIN FOLDING; PROTEINS; THERMODYNAMICS;

EID: 84880624394     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400272q     Document Type: Article

References (82)

1. Anfinsen, C. B. (1973) Principles that govern folding of protein chains Science 181, 223-330
2. Kidera, A., Konishi, Y., Ooi, T., and Scheraga, H. A. (1985) Relation between sequence similarity and structural similarity in proteins. Role of important properties of amino acids J. Protein Sci. 4, 265-297
3. Zwanzig, R., Szabo, A., and Bagchi, B. (1992) Levinthal's paradox Proc. Natl. Acad. Sci. U.S.A. 89, 20-22
4. Ambroggio, X. I. and Kuhlmann, B. (2006) Design of protein conformational switches Curr. Opin. Struct. Biol. 16, 525-530
5. Harano, Y. (2012) Application of hydration thermodynamics to the evaluation of protein structures and protein-ligand binding Entropy 14, 1443-1468
6. Ben-Naim, A. (2013) The Protein Folding Problem and Its Solutions, World Scientific, New York.
7. Rosato, A., Bagaria, A., Baker, D., Bardiaux, B., Cavalli, A., Doreleijers, J. F., Giachetti, A., Guerry, P., Güntert, P., Herrmann, T., Huang, Y. J., Jonker, H. R. A., Mao, B., Malliavin, T. E., Montelione, G. T., Nilges, M., Raman, S., van der Schot, G., Vranken, W. F., Vuister, G. W., and Bonvin, A. M. J. J. (2009) CASD-NMR: Critical assessment of automated structure determination by NMR Nat. Methods 6, 625-626
8. Guerry, P. and Herrmann, T. (2011) Advances in automated NMR protein structure determination Q. Rev. Biophys. 44, 257-309
9. Khatib, F., DiMaio, F., Cooper, S., Kazmierczyk, M., Gilski, M., Krzywda, S., Zabranska, H., Pichova, I., Thompson, J., Popovic, Z., Jaskolski, M., and Baker, D. (2011) Crystal structure of a monomeric retroviral protease solved by protein folding game players Nat. Struct. Mol. Biol. 18, 1175-1177
10. Schlick, T., Collepardo-Guevara, R., Halvorsen, L. A., Jung, S., and Xiao, X. (2011) Biomolecular modeling and simulation: A field coming of age Q. Rev. Biophys. 44, 191-228
11. Zhou, Y., Duan, Y., Yang, Y., Faraggi, E., and Lei, H. (2011) Trends in template/fragment-free protein structure prediction Theor. Chem. Acc. 128, 3-16
12. Alexander, P. A., He, Y., Chen, Y., Orban, J., and Bryan, P. N. (2007) The design and characterization of two proteins with 88% sequence identity but different structure and function Proc. Natl. Acad. Sci. U.S.A. 104, 11963-11968
13. He, Y., Chen, Y., Alexander, P., Bryan, P. N., and Orban, J. (2008) NMR structures of two designed proteins with high sequence identity but different fold and function Proc. Natl. Acad. Sci. U.S.A. 105, 14412-14417
14. Alexander, P. A., He, Y., Chen, Y., Orban, J., and Bryan, P. N. (2009) A minimal sequence code for switching protein structure and function Proc. Natl. Acad. Sci. U.S.A. 106, 21149-21154
15. Bryan, P. N. and Orban, J. (2013) Implications of protein fold switching Curr. Opin. Struct. Biol. 23, 314-316
16. Horst, J. and Samudrala, R. (2009) Diversity of protein structures and difficulties in fold recognition: The curious case of protein G F1000 Biology Reports 1, 69
17. Shen, Y., Bryan, P. N., He, Y., Orban, J., Baker, D., and Bax, A. (2010) De novo structure generation using chemical shifts for proteins with high-sequence identity but different folds Protein Sci. 19, 349-356
18. Bryan, P. N. and Orban, J. (2010) Proteins that switch folds Curr. Opin. Struct. Biol. 20, 482-488
19. Rackovsky, S. (2011) Spectral analysis of a protein conformational switch Phys. Rev. Lett. 106, 248101
20. Shao, Q., Zhu, W., and Gao, Y. Q. (2012) Robustness in protein folding revealed by thermodynamics calculations J. Phys. Chem. B 116, 13848-13856
21. König, G. and Boresch, S. (2009) Hydration free energies of amino acids: Why side chain analog data are not enough J. Phys. Chem. B 113, 8967-8974
22. van Gunsteren, W. F. (1988) The role of computer simulation techniques in protein engineering Protein Eng. 2, 5-13
23. Levy, R. M. and Gallicchio, E. (1998) Computer simulations with explicit solvent: Recent progress in the thermodynamic decomposition of free energies and in modelling of electrostatic effects Annu. Rev. Phys. Chem. 49, 531-567
24. König, G., Bruckner, S., and Boresch, S. (2013) Absolute hydration free energies of blocked amino acids: Implications for protein solvation and stability Biophys. J. 104, 453-462
25. Meinke, J. H., Mohanty, S., Nadler, W., Zimmermann, O., and Hansmann, U. H. E. (2009) Computer simulation of proteins: Thermodynamics and structure prediction Eur. Phys. J. D51, 33-40
26. Schulz, R., Lindner, B., Petridis, L., and Smith, J. C. (2009) Scaling of multimillion-atom biological molecular dynamics simulation on a petascale supercomputer J. Chem. Theory Comput. 5, 2798-2808
27. Shaw, D. E., Maragakis, P., Lindorff-Larsen, K., Piana, S., Dror, R. O., Eastwood, M. P., Bank, J. A., Jumper, J. M., Salmon, J. K., Shan, Y., and Wriggers, W. (2010) Atomic-level characterization of the structural dynamics of proteins Science 330, 341-346
28. IUPAP (1978) Symbols, Units and Nomenclature in Physics, Vol. 93A, pp 1-60, Physica, Amsterdam.
29. IUPAC (1988) Quantities, Units and Symbols in Physical Chemistry, Blackwell Scientific Publications, Oxford, U.K.
30. Freddolino, P. L., Park, S., Roux, B., and Schulten, K. (2009) Force field bias in protein folding simulations Biophys. J. 96, 3772-3780
31. Faver, J. C., Benson, M. L., He, X., Roberts, B. P., Wang, B., Marshall, M. S., Sherrill, C. D., and Merz, K. M. (2011) The energy computation paradox and ab initio protein folding PLoS One 6, e18868
32. Allison, J. R., Bergeler, M., Hansen, N., and van Gunsteren, W. F. (2011) Current computer modeling cannot explain why two highly similar sequences fold into different structures Biochemistry 50, 10965-10973
33. Christ, C. D. and van Gunsteren, W. F. (2007) Enveloping distribution sampling: A method to calculate free energy differences from a single simulation J. Chem. Phys. 126, 184110
34. Christ, C. D. and van Gunsteren, W. F. (2008) Multiple free energies from a single simulation: Extending enveloping distribution sampling to nonoverlapping phase-space distributions J. Chem. Phys. 128, 174112
35. Christ, C. D. and van Gunsteren, W. F. (2009) Simple, efficient, and reliable computation of multiple free energy differences from a single simulation: A reference Hamiltonian parameter update scheme for enveloping distribution sampling J. Chem. Theory Comput. 5, 276-286
36. Christ, C. D. and van Gunsteren, W. F. (2009) Comparison of three enveloping distribution sampling Hamiltonians for the estimation of multiple free energy differences from a single simulation J. Comput. Chem. 30, 1664-1679
37. Berg, B. A. and Neuhaus, T. (1992) Multicanonical ensemble: A new approach to simulate first-order phase transitions Phys. Rev. Lett. 68, 9-12
38. Han, K. K. (1992) A new Monte Carlo method for estimating free energy and chemical potential Phys. Lett. A 165, 28-32
39. Lyubartsev, A. P., Martsinovski, A. A., Shevkunov, S. V., and Vorontsov-Velyaminov, P. N. (1992) New approach to Monte Carlo calculations of the free energy: Method of expanded ensembles J. Chem. Phys. 96, 1776-1783
40. Marinari, E. and Parisi, G. (1992) Simulated tempering: A new Monte Carlo scheme Europhys. Lett. 19, 451-458
41. Escobedo, F. A. and de Pablo, J. J. (1995) Monte Carlo simulation of the chemical potential of polymers in an expanded ensemble J. Chem. Phys. 103, 2703-2710
42. Smith, G. R. and Bruce, A. D. (1995) A study of the multi-canonical Monte Carlo method J. Phys. A: Math. Gen. 28, 6623-6643
43. Geyer, C. J. and Thompson, E. A. (1995) Annealing Markov chain Monte Carlo with applications to ancestral inference J. Am. Stat. Assoc. 90, 909-920
44. Han, K. K. (1996) Multiensemble sampling: An alternative efficient Monte Carlo technique Phys. Rev. E 54, 6906-6910
45. Wu, D. (2010) An efficient umbrella potential for the accurate calculation of free energies by molecular simulation J. Chem. Phys. 133, 044115
46. Kong, X. and Brooks, C. L., III (1996) λ-dynamics: A new approach to free energy calculations J. Chem. Phys. 105, 2414-2423
47. Mitsutake, A., Sugita, Y., and Okamoto, Y. (2001) Generalized-ensemble algorithms for molecular simulations of biopolymers Biopolymers 60, 96-123
48. Bitetti-Putzer, R., Yang, W., and Karplus, M. (2003) Generalized ensembles serve to improve the convergence of free energy simulations Chem. Phys. Lett. 377, 633-641
49. Chen, Y. G. and Hummer, G. (2007) Slow conformational dynamics and unfolding of the calmodulin C-terminal domain J. Am. Chem. Soc. 129, 2414-2415
50. Li, H., Fajer, M., and Yang, W. (2007) Simulated scaling method for localized enhanced sampling and simultaneous "alchemical" free energy simulations: A general method for molecular mechanical, quantum mechanical, and quantum mechanical/molecular mechanical simulations J. Chem. Phys. 126, 024106
51. Paluch, A. S., Shah, J. K., and Maginn, E. J. (2011) Efficient solvation free energy calculations of amino acid analogs by expanded ensemble molecular dynamics simulation J. Chem. Theory Comput. 7, 1394-1403
52. Okamoto, Y. (2012) Molecular simulations in generalised ensemble Mol. Simul. 38, 1282-1296
53. Riniker, S., Christ, C. D., Hansen, N., Mark, A. E., Nair, P. C., and van Gunsteren, W. F. (2011) Comparison of enveloping distribution sampling and thermodynamic integration to calculate binding free energies of phenylethanolamine N-methyltransferase J. Chem. Phys. 135, 024105
54. Hansen, N., Dolenc, J., Knecht, M., Riniker, S., and van Gunsteren, W. F. (2012) Assessment of enveloping distribution sampling to calculate relative free enthalpies of binding for eight netropsin-DNA duplex complexes in aqueous solution J. Comput. Chem. 33, 640-651
55. 10-, α-, and π-helices J. Chem. Theory Comput. 7, 3884-3897
56. Kirkwood, J. G. (1935) Statistical mechanics of fluid mixtures J. Chem. Phys. 3, 300-313
57. Torrie, G. M. and Valleau, J. P. (1977) Nonphysical sampling distributions in Monte Carlo free-energy estimation: Umbrella sampling J. Comput. Phys. 23, 187-199
58. Jacucci, G. and Quirke, N. (1982) Free energy calculations for crystals Lect. Notes Phys. 166, 38-57
59. Powles, J. G., Evans, W. A. B., and Quirke, N. (1982) Non-destructive molecular-dynamics simulation of the chemical potential of a fluid Mol. Phys. 46, 1347-1370
60. Salsburg, Z. W., Jacobson, J. D., Fickett, W., and Wood, W. W. (1959) Application of the Monte Carlo method to the lattice-gas model. I. Two-dimensional triangular lattice J. Chem. Phys. 30, 65-72
61. Ferrenberg, A. M. and Swendsen, R. H. (1988) New Monte Carlo technique for studying phase transitions Phys. Rev. Lett. 61, 2635-2638
62. Wu, D. and Kofke, D. A. (2005) Phase-space overlap measures. I. Fail-safe bias detection in free energies calculated by molecular simulation J. Chem. Phys. 123, 054103
63. Christen, M., Hünenberger, P. H., Bakowies, D., Baron, R., Bürgi, R., Geerke, D. P., Heinz, T. N., Kastenholz, M. A., Kräutler, V., Oostenbrink, C., Peter, C., Trzesniak, D., and van Gunsteren, W. F. (2005) The GROMOS software for biomolecular simulation: GROMOS05 J. Comput. Chem. 26, 1719-1751
64. Poger, D., van Gunsteren, W. F., and Mark, A. E. (2010) A new force field for simulating phosphatidylcholine bilayers J. Comput. Chem. 31, 1117-1125
65. Schmid, N., Eichenberger, A., Choutko, A., Riniker, S., Winger, M., Mark, A. E., and van Gunsteren, W. F. (2011) Definition and testing of the GROMOS force-field versions: 54A7 and 54B7 Eur. Biophys. J. 40, 843-856
66. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., and Hermans, J. ((1981) in Intermolecular Forces Pullmann, B., Ed.) pp 331-342, Reidel, Dordrecht, The Netherlands.
67. Hockney, R. W. (1970) The potential calculation and some applications Methods Comput. Phys. 9, 136-211
68. Ryckaert, J.-P., Ciccotti, G., and Berendsen, H. J. C. (1977) Numerical integration of the Cartesian equations of motion of a system with constraints: Molecular dynamics of n -alkanes J. Comput. Phys. 23, 327-341
69. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath J. Chem. Phys. 81, 3684-3690
70. Berendsen, H. J. C. (1985) in Molecular Dynamics and Protein Structure (Hermans, J., Ed.) pp 18-22, Polycrystal Book Service, Western Springs, IL.
71. Barker, J. A. and Watts, R. O. (1973) Monte Carlo studies of the dielectric properties of water-like models Mol. Phys. 26, 789-792
72. Tironi, I. G., Sperb, R., Smith, P. E., and van Gunsteren, W. F. (1995) A generalized reaction field method for molecular dynamics simulations J. Chem. Phys. 102, 5451-5459
73. Heinz, T. N., van Gunsteren, W. F., and Hünenberger, P. H. (2001) Comparison of four methods to compute the dielectric permittivity of liquids from molecular dynamics simulations J. Chem. Phys. 115, 1125-1136
74. van Gunsteren, W. F., Billeter, S. R., Eising, A. A., Hünenberger, P. H., Krüger, P., Mark, A. E., Scott, W. R. P., and Tironi, I. G. (1996) Biomolecular Simulation: The GROMOS96 Manual and User Guide, Vdf Hochschulverlag AG an der ETH Zürich, Zürich.
75. Pearlman, D. A. (1994) A comparison of alternative approaches to free energy calculations J. Phys. Chem. 98, 1487-1493
76. Eichenberger, A. P., Allison, J. R., Dolenc, J., Geerke, D. P., Horta, B. A. C., Meier, K., Oostenbrink, C., Schmid, N., Steiner, D., Wang, D., and van Gunsteren, W. F. (2011) The GROMOS++ software for the analysis of biomolecular simulation trajectories J. Chem. Theory Comput. 7, 3379-3390
77. Kabsch, W. and Sander, C. (1983) Dictionary of protein secondary structure: Pattern-recognition of hydrogen-bonded and geometrical features Biopolymers 22, 2577-2637
78. Yu, H.-A. and Karplus, M. (1988) A thermodynamic analysis of solvation J. Chem. Phys. 89, 2366-2379
79. Peter, C., Oostenbrink, C., van Dorp, A., and van Gunsteren, W. F. (2004) Estimating entropies from molecular dynamics simulations J. Chem. Phys. 120, 2652-2661
80. van Gunsteren, W. F., Geerke, D. P., Trzesniak, D., Oostenbrink, C., and van der Vegt, N. F. A. ((2007) in Protein Folding and Drug Design, Proceedings of the International School of Physics "Enrico Fermi", course CLXV (Broglia, R. A., Serrano, L., and Tiana, G., Eds.) pp 177-191, IOS Press, Amsterdam.
81. Wang, L., Deng, Y., Knight, J. L., Wu, Y., Kim, B., Sherman, W., Shelley, J. C., Lin, T., and Abel, R. (2013) Modeling local structural rearrangements using FEP/REST: Application to relative binding affinity predictions of CDK2 inhibitors J. Chem. Theory Comput. 9, 1282-1293
82. He, Y., Chen, Y., Alexander, P., Bryan, P. N., and Orban, J. (2012) Mutational tipping points for switching protein folds and functions Structure 20, 283-291