Energy landscape of a peptide consisting of α-helix, 310-helix, β-turn, β-hairpin, and other disordered conformations

Protein Science

Volumn 10, Issue 6, 2001, Pages 1160-1171

  Higo, Junichi ^a,d   Ito, Nobutoshi ^a   Kuroda, Masataka ^b   Ono, Satoshi ^a   Nakajima, Nobuyuki ^c   Nakamura, Haruki ^c  

^a BIOMOL ENG RESEARCH INSTITUTE   (Japan)

^b MITSUBISHI TANABE PHARMA CORPORATION   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

Author keywords

Folding; Force field; Funnel; Multicanonical; Random state; Rugged surface; helix; hairpin

Indexed keywords

ACETYLLYSYLGLUTAMINYLCYSTEINYLARGINYLGLUTAMYLARGINYLALANINE N METHYL ESTER; DNA BINDING PROTEIN; PEPTIDE; PROTEIN C MYB; UNCLASSIFIED DRUG; WATER;

ALPHA HELIX; ARTICLE; BETA SHEET; CIRCULAR DICHROISM; ENERGY; HYDROGEN BOND; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; TEMPERATURE;

EID: 0035008585     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.44901     Document Type: Article

References (91)

1. Alba, E.D., Rico, M., and Jimenez, A. 1999. The turn sequence directs β-strand alignment in designed β-hairpins. Protein Sci. 8: 2234-2244.
2. Andricioaei, I. and Straub, J.E. 1996. Generalized simulated annealing algorithms using Tsallis statistics: Application to conformational optimization of a tetrapeptide. Phys. Rev. E. 53: R3055-R3058.
3. Bartels, C. and Karplus, M. 1997. Multidimensional adaptive umbrella sampling: Application to main chain and side chain peptide conformations. J. Compt. Chem. 18: 1450-462.
4. _. 1998. Probability distributions for complex systems: Adaptive umbrella sampling of the potential energy. J. Phys. Chem. B 102: 865-880.
5. Bartels, C., Stote, R.H., and Karplus, M. 1998. Characterization of flexible molecules in solution: The RGDW peptide. J. Mol. Biol. 284: 1641-1660.
6. Bartels, C., Schaefer, M., and Karplus, M. 1999. Determination of equilibrium properties of biomolecular systems using multidimensional adaptive umbrella sampling. J. Chem. Phys. 111: 8048-8067.
7. Berg, B.A. and Neuhaus, T. 1992. Multicanonical ensemble: A new approach to simulate first order phase transitions. Phys. Rev. Lett. 68: 9-12.
8. Blanco, F.J. and Serrano, L. 1995. Folding of protein G B1 domain studied by the conformational characterization of fragments comprising its secondary structure elements. Eur. J. Biochem. 230: 634-649.
9. Blanco, F.J., Serrano L. and Forman-Kay, J.D. 1998. High populations of non-native structures in the denatured state are compatible with the formations of the native fold state. J. Mol. Biol. 284: 1153-1164.
10. Boczko, E.M. and Brooks, III, C.L. 1995. First-principle calculation of the folding free energy of a three-helix bundle protein. Science 269: 393-396.
11. Bond, C.J., Wong, K.-B., Clarke, J., Fersht, A.R., and Daggett, V. 1997. Characterization of residual structure in the thermally denatured state of barnase by simulation and experiment: Description of the folding pathway. Proc. Natl. Acad. Sci. 94: 13409-13413.
12. Bonvin, A.M.J.J. and van Gunsteren, W.F. 2000. β-hairpin stability and folding: Molecular dynamics studies of the first β-hairpin of tendamistat. J. Mol. Biol. 296: 255-268.
13. Brooks, III, C.L. 1998. Simulations of protein folding and unfolding. Curr. Opin. Struc. Biol. 8: 222-226.
14. Bryngelson, J.D., Onuchic, J.N., Socci, N.D., and Wolynes, P.G. 1995. Funnels, pathways, and the energy landscape of protein folding: A synthesis. Proteins 21: 167-195.
15. Caves, L.S.D., Evanseck, J.D., and Karplus, M. 1998. Locally accessible conformations: Multiple molecular dynamics simulations of crambin. Protein Sci. 7: 649-666.
16. Chan, H.S, and Dill, K.A. 1998. Protein folding in landscape perspective: Chevron plots and non-Arrhenius kinetics. Proteins 30: 2-33.
17. Chikenji, G. and Kikuchi, M. 2000. A lattice model study of α - β transitions in protein folding - the free-energy landscape analysis -. Prog. Theor. Physics Suppl. 138: 406-407
18. Chikenji, G., Kikuchi, M., and Iba, Y. 1999. Multi-self-overlap ensemble for protein folding: Ground state search and thermodynamics. Phys. Rev. Lett. 83: 1886-1889.
19. Cornell, W.D., Cieplak, P., Bayly, C.I., Gould, I.R., Kenneth, J., Merz, M., Ferguson, D.M., Spellmeyer, D.C., Fox, T., Caldwell, J.W., et al. 1995. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117: 5179-5197.
20. Daura, X., van Gunsteren, W.F., and Mark, A.E. 1999. Folding-unfolding thermodynamics of a β-heptapeptide from equiliblium simulations. Proteins 34: 269-280.
21. Dill, K.A. 1999. Polymer principles and protein folding. Protein Sci. 8: 1166-1180.
22. Ding, H-Q., Karasawa, N., and Goddard, III, W.A. 1992. Atomic level simulations on a million particles: The cell multipole method for Coulomb and London nonbond interactions. J. Chem. Phys. 97: 4309-4315.
23. Dinner, A.R., Lazaridis, T., and Karplus, M. 1999. Understanding β-hairpin formation. Proc. Natl. Acad. Sci. 96: 9068-9073.
24. Duan, Y. and Kollman, PA. 1998. Pathways to protein folding intermediate observed in a 1-microseond simulation in aqueous solution. Science 282: 740-744.
25. Evans, D.J. and Morriss, G.P. 1983. The isothermal/isobaric molecular dynamics ensemble. Phys. Lett. A 98: 433-436.
26. Frank, M.K., Clore, G.M., and Gronenborn, A.M. 1995. Structural and dynamic characterization of the urea denatured state of the immunoglobulin binding domain of streptococcal protein G by multidimensional heteronuclear NMR spectroscopy. Protein Sci. 4: 2605-2615.
27. Galzitskaya, O.V., Higo, J., Kuroda, M., and Nakamura, H. 2000. β-hairpin folds by molecular dynamics simulations. Chem. Phys. Lett 325: 421-429.
28. Gillespie, J.R. and Shortle, D. 1997a. Characterization of long-range structure in the denatured state of staphylococcal nuclease. I. Paramagnetic relaxation enhancement by nitroxide spin labels. J. Mol. Biol. 268: 158-169.
29. _. 1997b. Characterization of long-range structure in the denatured state of staphylococcal nuclease. II. Distance restraints from paramagnetic relaxation and calculation of ensemble structures. J. Mol. Biol. 268: 170-184.
30. Hamada, D., Segawa, S., and Goto, Y. 1996. Non-native α-helical intermediate in the refolding of β-lactoglobulin, a predominantly β-sheet protein. Nature Struct. Biol. 3: 868-873.
31. Hansmann, U.H.E, and Okamoto, Y. 1993. Prediction of peptide conformation by multicanonical algorithm: New approach to the multi-minima problem. J. Compt. Chem. 14: 1333-1338.
32. _. 1997a. Generalized-ensemble Monte Carlo method for systems with rough energy landscape. Phys. Rev. E 56: 2228-2233.
33. _. 1997b. Numerical comparison of three recently proposed algorithms in the protein folding problem. J. Comp. Chem. 18: 920-933.
34. Hansmann, U.H.E., Okamoto, Y., and Eisenmenger, F. 1996. Molecular dynamics, Langevin, and hybrid Monte Carlo simulations in multicanonical ensemble. Chem. Phys. Lett. 259: 321-330.
35. Hesselbo, B. and Stinchcombe, R.B. 1995. Monte Carlo simulation and global optimization without parameters. Phys. Rev. Lett. 74: 2151-2155.
36. Higo, J. and Umeyama, H. 1997. Protein dynamics determined by backbone conformation and atom packing. Protein Eng. 10: 373-380.
37. Higo, J., Nakajima, N., Shirai, H., Kidera, A., and Nakamura, H. 1997. Two-component multicanonical Monte Carlo method for effective conformation sampling. J. Comp. Chem. 18: 2086-2092.
38. Higo, J., Galzitskaya, O.V., Ono, S., and Nakamura, H. 2001. Energy landscape of a β-hairpin peptide in explicit water. Studied by multicanonical molecular dynamics. Chem. Phys. Lett. 337: 169-175.
39. Honda, S., Kobayashi, N., and Munekata, E. 2000. Thermodynamics of a β-hairpin structure: Evidence for cooperative formation of folding nucleus. J. Mol. Biol. 295: 269-278.
40. Hukushima, K. and Nemoto, K. 1996. Exchange Monte Carlo method and application to spin glass simulations. J. Phys. Soc. Jpn. 65: 1604-1608.
41. Iba, Y., Chikenji, G., and Kikuchi, M. 1998. Simulation of lattice polymers with multi-self-overlap ensemble. J. Phys. Soc. Jpn. 67: 3327-3330.
42. Irback, A. and Potthast, F. 1995. Studies of an off-lattice model for protein folding: Sequence dependence and improved sampling at finite temperature. J. Chem. Phys. 103: 10298-10305.
43. Istrail, S., Schwartz, R., and King, J. 1999. Lattice simulation of aggregation funnels for protein folding. J. Comput. Biol. 6: 143-162.
44. Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impley, R.W., and Klein. M.L. 1987. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79: 926-935.
45. Kamatari, Y.O., Ohji, S., Konno, T., Seki, Y., Soda, K., Kataoka, M., and Akasaka, K. 1999. The compact and extended denatured conformations of apomyoglobin in the methanol-water solvent. Protein Sci. 8: 873-882.
46. Kazmirski, S.L. and Daggett, V. 1998. Non-native interactions in protein folding intermediates: Molecular dynamics simulations of hen lysozyme. J. Mol. Biol. 284: 793-806.
47. Kidera, A. 1995. Enhanced conformation sampling in Monte Carlo simulations of proteins: Application to constrained peptide. Proc. Natl. Acad. Sci. 92: 9886-9889.
48. Kikuchi, M., Chikenji, G., and Iba, Y. 2000. Multi-selfoverlap-ensemble Monte Carlo method for lattice proteins and heteropolymears. Prog. Theor. Physics Supp. 138: 404-405.
49. Kim, S.T., Shirai, H., Nakajima, N., Higo, J., and Nakamura, H. 1999. Enhanced conformational diversity search of CDR-H3 in antibodies: Role of the first CRD-H3 residue. Proteins 37: 683-696.
50. Kollman, P.A., Dixon, R.W., Cornell, W.D., Chipot, C., and Pohorille, A. 1997. The development/application of a "minimalist" organic/biochemical molecular mechanic force field using a combination of ab initio calculations and experimental data. In: Computer simulations of biological systems. (ed. W.F. van Gunsteren), ESCOM, Dordrecht, The Netherlands.
51. Lazarids, T. and Karplus, M. 1997. "New view" of protein folding reconciled with the old through multiple unfolding simulations. Science 278: 1928-1931.
52. Lee, J. 1993. New Monte Carlo algorithm: Entropie sampling. Phys. Rev. Lett. 71: 211-214.
53. Li, H., Helling, R., Tang, C., and Wingreen, N. 1996. Emergence of preferred structures in a simple model of protein folding. Science 273: 666-669.
54. Lyubartsev, A.P., Martsinovski, A.A., Shevkunov, S.V., and Vorontsov-Velyaminov, P.N. 1992. New approach to Monte Carlo calculation of the free energy: method of expanded ensembles. J. Chem. Phys. 96: 1776-1783.
55. Morikami, K., Nakai, T., Kidera, A., Saito, M., and Nakamura, H. 1992. PRESTO: A vectorized molecular mechanics program for biopolymers. Comput. Chem. 16: 243-248.
56. Munoz, V., Thompson, P.A., Hofrichter, J., and Eaton, W.A. 1997. Folding dynamics and mechanism of β-hairpin formation. Nature 390: 196-199.
57. Nakajima, N. 1998. A selectively enhanced multicanonical molecular dynamics method for conformational sampling of peptides in realistic water molecules. Chem. Phys. Lett. 288: 319-326.
58. Nakajima, N., Nakamura, H., and Kidera, A. 1997a. Multicanonical ensemble generated by molecular dynamics simulation for enhanced conformational sampling of peptides. J. Phys. Chem. B 101: 817-824.
59. Nakajima, N., Higo, J., Kidera, A., and Nakamura, H. 1997b. Flaxible docking of a ligand peptide to a receptor protein by multicanonical molecular dynamics simulation. Chem. Phys. Lett. 278: 297-301.
60. Nakajima, N., Higo, J., Kidera, A., and Nakamura, H. 2000. Free energy landscape of peptides by enhanced conformational sampling. J. Mol. Biol. 296: 197-216.
61. Nakamura, H., Ono, S., and Higo, J. 1999. A general ab initio approach for free energy landscape of biological molecules around the transition states: Fusion of the classical molecular mechanics simulation and the quantum chemical calculation. Proc. Japan Acad. B75: 291-294.
62. Nakamura, H.K. and Sasai, M. 1999. Hierarchy and connectivity in the folding funnel. In: Old and new views of protein folding. (ed. K. Kuwajima and M. Arai), pp. 125-131. Elsevier, Amsterdam.
63. Neri, D., Billeter, M., Wider, G., and Wuthrich, K. 1992. NMR determination of residual structure in a urea-denatured protein, 434-repressor. Science 257: 1559-1563.
64. Ogata, K., Morikawa, S., Nakamura, H., Hojo, H., Yoshimura, S., Zhang, R., Aimoto, S., Ametani, Y., Hirata, Z., Sarai, A., et al. 1995. Comparison of the free DNA-complexed forms of the DNA-binding domain from c-Myb. Struct. Biol. 2: 309-320.
65. Ono, S., Nakajima, N., Higo, J., and Nakamura, H. 1999. The multicanonical weighted histogram analysis method for the free-energy landscape along structural transition paths. Chem. Phys. Lett. 312: 247-254.
66. _. 2000. Peptide free-energy profile is strongly dependent on the force field: Comparison of C96 and AMBER95. J. Comp. Chem. 21: 748-762.
67. Pande, V.S. and Rokhsar, A.S. 1999. Molecular dynamics simulations of unfolding and refolding of a β-hairpin fragment of protein C. Proc. Natl. Acad. Sci. 96: 9062-9067.
68. Ramirez-Alvarado, M., Blanco, F.J., and Serrano, L. 1996. De novo design and structural analysis of a model β-hairpin peptide system. Nature Struct. Biol. 3: 604-611.
69. Roccatano, D., Amadei, A., Di Nora, A., and Berendsen, H.J.C. 1999. A molecular dynamics study of the 41-56 β-hairpin from B1 domain of protein G. Protein Sci. 8: 2130-2143.
70. Ryckaert, J-P., Ciccotti, G., and Berendsen, H.J.C. 1977. Numerical integration of Cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. J. Comp. Phys. 23: 327-341.
71. Schaefer, M., Bartels, C., and Kurplus, M. 1998. Solution conformations and thermodynamics of structured peptides: Molecular dynamics simulation with an implicit solvation model. J. Mol. Biol. 284: 835-848.
72. Searle, M.S., Zerella, R., Williams, D.H., and Packman, L.C. 1996. Native-like β-hairpin structure in an isolated fragment from ferredoxin: NMR and CD studies of solvent effect on the N-teminal 20 residues. Protein Eng. 9: 559-565.
73. Shirai, H., Nakajima, N., Higo, J., Kidera, A., and Nakamura, H. 1998. Conformational sampling of CDR-H3 in antibodies by multicanonical molecular dynamics simulation. J. Mol. Biol. 278: 481-496.
74. Shortle, D. 1993. Denatured states of proteins and their roles in folding and stability. Curr. Opin. Struct. Biol. 3: 66-74.
75. _. 1996. Structural analysis of non-native states of proteins by NMR methods. Curr. Opin. Struct. Biol. 6: 24-30.
76. Sinclair, J.F. and Shortle, D. 1999. Analysis of long-range interactions in a model denatured state of staphylococcal nuclease based on correlated changes in backbone dynamics. Protein Sci. 8: 991-1000.
77. Sugita, Y. and Okamoto, Y. 1999. Replica-exchange molecular dynamics method for protein folding. Chem. Phys. Lett. 314: 141-151.
78. _. 2000a. An analysis on protein folding problem by replica-exchange method. Prog. Theor. Physics Supp. 138: 402-403.
79. _. 2000b. Replica-exchange multicanonical algorithm and multicanonical replica-exchange method for simulating systems with rough energy landscape. Chem. Phys. Lett. 329: 261-270.
80. Sugita, Y., Kitao, A., and Okamoto, Y. 2000. Multidimensional replica-exchange method for free energy calculations J. Chem. Phys. 113: 5065-5071.
81. Takano, M., Yamato, T., Higo, J., Suyama, A., and Nagayama, K. 1999. Molecular dynamics of a 15-residue poly(L-alanine) in water: Helix formation and energetics. J. Am. Chem. Soc. 121: 605-612.
82. Tatsumi, R. and Chikenji, G. 1999. Origin of the designability of protein structues. Phys. Rev. E 60: 4696-4700.
83. Tsai, J., Levitt, M., and Baker, D. 1999. Hierarchy of structure loss in MD simulations of src SH3 domain unfolding. J. Mol. Biol. 291: 215-225.
84. Tsallis, C. 1988. Possible generalization of Boltzmann-Gibbs statistics. J. Stat. Phys. 52: 479-487.
85. Wang, H., Varady, J., Ng, L., and Sung, S-S. 1999b. Molecular dynamics simulations of β-hairpin folding. Proteins 37: 325-333.
86. Wang, L., Duan, Y., Shortle, R., Imperiali, B., and Kollman, P.A. 1999a. Study of stability and unfolding mechanism of BBA1 by molecular dynamics simulations at different temperatures. Protein Sci. 8: 1292-1304.
87. Wang, Y. and Shortle, D. 1997. Residual helical and turn structure in the denatured state of staphylococcal nuclease: Analysis of peptide fragments. Folding & Design 2: 93-100.
88. Wong, K-B., Clarke, J., Bond, C.J., Neira, J.L., Freund, S.M.V., Fersht, A.R., and Daggett, V. 2000. Towards a complete description of the structural and dynamic properties of the denatured state of barnase and the role of residual structure in folding. J. Mol. Biol. 296: 1257-1282.
89. Wright, P.E. and Dyson, H.J. 1999. Intrinsically unstructured proteins: Reassessing the protein structure-function paradigm. J. Mol. Biol. 293: 321-331.
90. Yong, W.S. and Brooks, III, C.L. 1996. A microscopic view of helix propagation: N and C-terminal helix growth in alanine helices. J. Mol. Biol. 259: 560-572.
91. Zimm, H.B. and Bragg, J.K. 1959. Theory of phase transition between helix and random coil in polypeptide chains. J. Chem. Phys. 31: 526-535.