Energy landscapes and solved protein-folding problems

Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences

Volumn 363, Issue 1827, 2005, Pages 453-467

  Wolynes, Peter G ^a   Karplus, M ^b   Dobson, C M ^c   Zewail, A H ^d   Clarke, J ^c   Schon J C ^e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITÉ LOUIS PASTEUR   (France)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^e MAX PLANCK INSTITUT FÜR FESTKÖRPERFORSCHUNG   (Germany)

Author keywords

Energy landscape theory; Funnel; Protein folding

Indexed keywords

EID: 12944327750     PISSN: 1364503X     EISSN: None     Source Type: Journal    
DOI: 10.1098/rsta.2004.1502     Document Type: Article

References (77)

1. Aloy, P., Stark, A., Hadley, C. & Russell, R. 2003 Predictions without templates: new folds secondary structure and contents in CASP V. Proteins 53, 436-456.
2. Bryngelson, J. D. & Wolynes, P. G. 1987 Spin glasses and the statistical mechanics of protein folding. Proc. Natl Acad. Sci. USA 84, 7524-7528.
3. Bryngelson, J., Onuchic, J., Socci, N. & Wolynes, P. G. 1995 Funnels, pathways, and the energy landscape of protein folding: a synthesis. Proteins 21, 167-195.
4. Calhoun, J. R., Kono, H., Lahr, S., Wang, W., deGrado, W. & Saven, J. 2003 Computational design and characterization of a mononumeric helical dinuclear metalloprotein. J. Mol. Biol. 334, 1101-1115.
5. Clementi, C., Jennings, P. A. & Onuchic, J. N. 2000 How native state topology affects the folding of dihydrofolate reductase and interleukin-beta. Proc. Natl Acad. Sci. USA 97, 5871-5876.
6. Clementi, C., Jennings, P. A. & Onuchic, J. N. 2001 Prediction of folding mechanism for circular permuted proteins. J. Mol. Biol. 311, 879-890.
7. Dobson, C. 2004 Principles of protein folding, misfolding and aggregation. Sem. Cell. Dev. Biol. 15, 3-16.
8. Eastwood, M. E., Wolynes, P. G. 2001 Role of explicitly cooperative interactions in protein folding funnels: a simulation study. J. Chem. Phys. 114, 4702-4716.
9. Eastwood, M., Hardin, C., Luthey-Schulten, Z. & Wolynes, P. G. 2002 Evaluating protein structure prediction schemes using energy landscape theory. IBM J. Res. Develop. 45, 475-497.
10. England, J., Shakhnovich, B. E. & Shakhnovich, E. I. 2003 Natural selection for more designable folds: a mechanism of thermophilic adaption. Proc. Natl Acad. Sci. USA 100, 8727-8731.
11. Fain, B. & Levitt, M. 2003 Funnel sculpting for in silico assembly of secondary structure elements of protein. Proc. Natl Acad. Sci. USA 100, 10 700-10 705.
12. Fersht, A. R. 1997 Nucleation mechanisms in protein folding. Curr. Opin. Struct. Biol. 7, 3-9.
13. Fujitsuka, Y., Takada, S., Luthey - Schulten, Z. A. & Wolynes, P. G. 2004 Optimizing physical energy functions for protein folding. Proteins 54, 88-103.
14. Garcia, A. E. & Onuchic, J. N. 2003 Folding a protein in a computer an atomic description of the folding/unfolding of a protein A. Proc. Natl Acad. Sci. USA 100, 13898-13903.
15. Goldstein, R., Luthey-Schulten, Z. & Wolynes, P. G. 1992a Optimal protein-folding codes from spin-glass theory. Proc. Natl Acad. Sci. USA 89, 4918-4922.
16. Goldstein, R. A., Luthey-Schulten, Z. A. & Wolynes, P. G. 1992b Protein tertiary structure recognition using optimized hamiltonians with local interactions. Proc. Natl Acad. Sci. USA 89, 9029-9033.
17. Hardin, C., Eastwood, M., Luthey-Schulten, Z. & Wolynes, P. G. 2000 Associative memory hamiltonians for structure prediction without homology: alpha-helical proteins. Proc. Natl Acad. Sci. USA 97, 14 235-14 240.
18. Hardin, C., Eastwood, M. P., Prentiss, M., Luthey-Schulten, Z. & Wolynes, P. G. 2001 Folding funnels: the key to robust protein structure prediction. J. Computat. Chem. 23, 138-146.
19. Hardin, C., Eastwood, M. P., Prentiss, M. C., Luthey-Schulten, Z. & Wolynes, P. G. 2003 Associative memory hamiltonians for protein structure prediction without homology: alpha/beta proteins. Proc. Natl Acad. Sci. USA 100, 1679-1684.
20. Jin, W. Z., Kambara, O., Sasakawa, H., Tamura, A. & Takada, S. 2003 De novo design of foldable proteins with smooth folding funnel: automated negative design and experimental verification. Structure 11, 581-590.
21. Karanicolas, J. & Brooks, C. L. 2003 Imported Go-like models demonstrate the robustness of protein folding mechanisms towards non-native interactions. J. Mol. Biol. 334, 309-325.
22. Kauzmann, W. 1959 Factors in the interpretation of protein denaturation. Adv. Protein Chem. 14, 1-53.
23. Koga, N. & Takada, S. 2001 Roles of native topology and chain-length scaling in protein folding: a simulation study with a Go-like model. J. Mol. Biol. 313, 171-180.
24. Kono, H. &; Saven, J. 2001 Statistical theory for protein combinational libraries, packing interactions backbone flexibility and the sequence variability of a main-chain structure. J. Mol. Biol. 306, 607-628.
25. Leopold, P. E., Montal, M. & Onuchic, J. N. 1992 Protein folding funnels:kinetic pathways through a compact conformation space. Proc. Natl Acad. Sci. USA 89, 8721-8725.
26. Levy, Y., Onuchic, J. N. & Wolynes, P. G. 2004 Protein topology determines binding mechanism. Proc. Natl Acad. Sci. USA 101, 511-516.
27. Lu, H. & Skolnick, J. 2001 A distance dependant atomic knowledge based potential for improved protein structure prediction. Proteins 44, 223-232.
28. Mirsky, A. E. & Pauling, L. 1936 On the structure of nature, denatured and coagulated proteins. Proc. Natl Acad. Sci. USA 22, 439-447.
29. Miyashita, O. M., Onuchic, J. N. & Wolynes, P. G. 2003 Nonlinear elasticity, protein quakes and the energy lantdscapes of functional transitions in proteins. Proc. Natl Acad. Sci. USA 100, 12570-12575.
30. Moult, J. 1989 Comparative modeling of protein structure-progress and prospects. J. Res. Natl Bur. Stand. 94, 79-84.
31. Nelson, E. D. & Onuchic, J. N. 1998 Proposed mechanism for stability of proteins of evolutionary mutations. Proc. Natl Acad. Sci. USA 95, 10 682-10 686.
32. Nymeyer, H., Soci, N. D. & Onuchic, J. N. 2000 Landscape approaches for determining the ensemble of folding transition states: success and failure hinge on the degree of frustration. Proc. Natl Acad. Sci. USA 97, 634-639.
33. Onuchic, J. N. & Wolynes, P. G. 2004 Theory of protein folding. Curr. Opin. Struct. Biol. 14, 70-75.
34. Onuchic, J. N., Socci, N. D., Luthey-Schulten, Z. & Wolynes, P. G. 1996 Protein folding funnels: the nature of the transition state ensemble. Fold. Design 1(6), 441-450.
35. Onuchic, J. N., Luthey-Schulten, Z. & Wolynes, P. G. 1997 Theory of protein folding: the energy landscape perspective. A. Rev. Phys. Chem. 48, 545-600.
36. Otlesen, J. J. & Imperiali, B. 2001 Design of a discretely folded mini protein motif with pre-dominantly beta-structure. Nat. Struct. Biol. 8, 535-539.
37. Papoian, G. A., Ulander, J. & Wolynes, P. G. 2003 The role of water mediated interactions in protein-protein recognition landscapes. J. Am. Chem. Soc. 125, 9170-9178.
38. Papoian, G. A., Ulander, J., Eastwood, M. P., Luthey-Schulten, Z. & Wolynes, P. G. 2004 water in protein structure prediction. Proc. Natl Acad. Sci. USA 101, 3352-3357.
39. Pillardy, A. (and 12 others) 2001 Recent improvements in prediction of protein structure by global optimization of a potential energy function. Proc. Natl Acad. Sci. USA 98, 2329-2333.
40. Plotkin, S. S., Wang, J. & Wolynes, P. G. 1996 A correlated energy landscape model for finite, random heteropolymers. Phys. Rev. E 53(6), 6271-6296.
41. Plotkin, S. S., Wang, J. & Wolynes, P. G. 1997 Statistical mechanics of a correlated energy landscape model for protein folding funnels. J. Chem. Phys. 106(7), 2932-2948.
42. Portman, J. J., Takada, S. & Wolynes, P. G. 1998 Variational theory for site resolved protein folding free energy surfaces. Phys. Rev. Lett. 81, 5237-5240.
43. Sasai, M. & Wolynes, P. G. 1990 Molecular theory of associative memory Hamiltonian models of protein folding. Phys. Rev. Lett. 65(21), 2740-2743.
44. Schlunnegger, M. P., Bennett, M. J. & Eisenberg, D. 1997 Oligomer formation by 3D domain swaping: a model for protein assembly and disassembly. Adv. Protein Chem. 50, 61-122.
45. Shakhnovich, E. I. & Gutin, A. M. 1989 The nonergodic (spin glass like) phase of heteropolymer with quenched disordered sequence. Europhys. Lett. 8, 327.
46. Shea, J. E., Onuchic, J. N. & Brooks, C. L. 2000 Energetic frustration and the nature of the transition state in protein folding. J. Chem. Phys. 113, 7663-7671.
47. Shen, T., Huffman, C. & Wolynes, P. G. 2005 (In preparation.)
48. Shoemaker, B. A., Wang, J. & Wolynes, P. G. 1997 Structural correlations in protein folding funnels. Proc. Natl Acad. Sci. USA 94, 5237-5240.
49. Shoemaker, B. A., Wang, J. & Wolynes, P. G. 1999 Exploring structures in protein folding funnels with free energy functionals: the transition state ensemble. J. Mol. Biol. 287, 675-694.
50. Silow, M. & Oliveberg, M. 1997 Transient aggregates in protein folding are easily mistaken for folding intermediates. Proc. Natl Acad. Sci. USA 94, 6084-6086.
51. Snow, C. D., Nguyen, N., Pande, V. S. & Gruebele, M. 2002 Absolute comparison of simulated and experimental protein-folding dynamics. Nature 420, 102-106.
52. Taverna, D. M. & Goldstein, R. A. 2002 Why are proteins so robust to site mutations? J. Mol. Biol. 315, 479-484.
53. Ueda, Y., Taketomi, H. & Go, N. 1978 Studies of protein folding, unfolding, and fluctuations by computer simulation. 2. Three-dimensional lattice model for lysozyme. Biopolymers 17, 1531-1548.
54. Verkhivker, G. M., Bouzida, D. & Gelhaar, D. K. 2003 Simulating disorder-order transitions in molecular recognition of unstructured proteins: where folding meets binding. Proc. Natl Acad. Sci. USA 100, 5148-5153.
55. Vuceti, S., Brown, C. J., Dunker, A. K. & Obradovic, Z. 2003 Flavors of protein disorder. Proteins 52, 573-584.
56. Wei, Y. N., Kim, S., Fela, D., Baum, J. & Hecht, M. H. 2003 Solution structure of a de Novo protein from a designed combinational library. Proc. Natl Acad. Sci. USA 100, 13 270-13 273.
57. Wolynes, P. G. 1996 Symmetry and the energy landscapes of biomolecules. Proc. Natl Acad. Sci. USA 93, 14 249-14 255.
58. Wolynes, P. G. 1997 folding funnels and energy landscapes of larger proteins within the capillarity approximation. Proc. Natl Acad. Sci. USA 94, 6170-6175.
59. Yang, S., Cho, S. S., Levy, Y., Cheung, M. S., Levine, H., Wolynes, P. G. & Onuchic, J. N. 2004 Domain swapping is a consequence of minimal frustration. Proc. Natl Acad. Sci. USA 101, 13786-13791.
60. Zhang, Y. & Skolnick, J. 2004 Automated structure prediction of weakly homologous proteins on a genomic scale. Proc. Natl Acad. Sci. USA 101, 7594-7599.
61. Bruenger, A. T., Brooks III, C. L. & Karplus, M. 1985 Active site dynamics of ribonuclease. Proc. Natl Acad. Sci. USA 82, 8458-8462.
62. Cheung, M. S., Garcia, A. & Onuchic, J. N. 2002 Protein folding mediated by solvation: water expulsion and formation of the hydrophobic core occur after the structural collapse. Proc. Natl Acad. Sci. USA 99, 685-690.
63. Dobson, C. M. 2003 Protein folding and misfolding. Nature 426, 884-890.
64. Hilson, N., Onuchic, J. N. & Garcia, A. E. 1999 Pressure-induced protein folding/unfolding kinetics. Proc. Natl Acad. Sci. USA 96, 14 848-14 853.
65. Luscombe, N. M., Laskowski, R. A., & Thornton, J. M., 2001 Amino acid base interactions: a three-dimensional analysis of protein-DNA interactions at the atomic level. Nucl. Acids Res. 29, 2860-2874.
66. Nooren, I. M. A., & Thornton, J. M., 2003 Structural characterization and functional significance of transient protein-protein interactions. J. Mol. Biol. 325, 991-1018.
67. Plotkin, S., Wang, J. & Wolynes, P. G. 1997 Configurational diffusion on a locally connected correlated energy landscape: application to finite random heteropolymers. J. Phys. Paris 7, 395-421.
68. Portman, J., Takada, S. & Wolynes, P. G. 2001 Microscopic theory of protein folding rates. II. Local reaction coordinates and chain dynamics. J. Chem. Phys. 114, 5082-5096.
69. Schlunegger, M. P., Bennett, M. J. & Eisenberg, D. 1997 Oligomer formation by 3D domain swapping: a model for protein assembly and misassembly. Adv. Protein Chem. 50, 61-122.
70. Schön, J. C. 1997 Preferential trapping on energy landscapes in regions containing deep-lying minima: the reason for the success of simulated annealing? J. Phys. A 30, 2367-2389.
71. Schön. J. C. & Sibani, P. 1998 Properties of the energy landscape of network models for covalent glasses. J. Phys. A 31, 8165-8178.
72. Schön, J. C. & Sibani, P. 2000 Energy and entropy of metastable states in glassy systems. Europhys. Lett. 49, 196-202.
73. Sibani, P., Schön, J. C., Salamon, P. & Andersson, J. O. 1993 Emergent hierarchical structures in complex system dynamics. Europhys. Lett. 22, 479-485.
74. ten Wolde, P. R. & Chandler, D. 2002 Drying-induced hydrophobic polymer collapse. Proc. Natl Acad. Sci. USA 99, 6539-6543.
75. Vendruscolo, M., Paci, E., Karplus, M. & Dobson, C. M. 2003 Structure and relative free energies of partially folded states of proteins. Proc. Natl Acad. Sci. USA 100, 14 817-14 821.
76. Williams, M. A., Thornton, J. M. & Goodfellow, J. M. 1997 Modelling protein unfolding: hen egg-white lysozyme. Protein Engng 10, 895-903.
77. Zhou, R., Huang, X., Margulis, C. J. & Berne, B. J. 2004 Hydrophobic collapse in multidomain protein folding. Science 305, 1605-1609.