Understanding protein unfolding from molecular simulations

Wiley Interdisciplinary Reviews: Computational Molecular Science

Volumn 2, Issue 3, 2012, Pages 405-423

  Toofanny, Rudesh D ^a   Daggett, Valerie ^a  

^a University of Washington   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84859910826     PISSN: 17590876     EISSN: 17590884     Source Type: Journal    
DOI: 10.1002/wcms.1088     Document Type: Article

References (106)

1. Jonsson AL, Scott KA, Daggett V. Dynameomics: a consensus view of the protein unfolding/folding transition state ensemble across a diverse set of protein folds. Biophys J 2009, 97:2958-2966.
2. Mittag T, Forman-Kay JD. Atomic-level characterization of disordered protein ensembles. Curr Opin Struct Biol 2007, 17:3-14.
3. Dar TA, Schaeffer RD, Daggett V, Bowler BE. Manifestations of native topology in the denatured state ensemble of Rhodopseudomonas palustris cytochrome c′. Biochemistry 2011, 50:1029-1041.
4. Kazmirski SL, Wong KB, Freund SM, Tan YJ, Fersht AR, Daggett V. Protein folding from a highly disordered denatured state: the folding pathway of chymotrypsin inhibitor 2 at atomic resolution. Proc Natl Acad Sci USA 2001, 98:4349-4354.
5. Morrone A, McCully ME, Bryan PN, Brunori M, Daggett V, Gianni S, Travaglini-Allocatelli C. The denatured state dictates the topology of two proteins with almost identical sequence but different native structure and function. J Biol Chem 2011, 286:3863-3872.
6. Fersht AR, Leatherbarrow RJ, Wells TN. Structure-activity relationships in engineered proteins: analysis of use of binding energy by linear free energy relationships. Biochemistry 1987, 26:6030-6038.
7. Matouschek A, Kellis JT, Serrano L, Fersht AR. Mapping the transition-state and pathway of protein folding by protein engineering. Nature 1989, 340:122-126.
8. Fersht AR, Leatherbarrow RJ, Wells TNC. Quantitative analysis of structure-activity relationships in engineered proteins by linear free-energy relationships. Nature 1986, 322:284-286.
9. Fersht AR, Matouschek A, Serrano L. The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding. J Mol Biol 1992, 224:771-782.
10. Rief M, Gautel M, Oesterhelt F, Fernandez JM, Gaub HE. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 1997, 276:1109-1112.
11. Freddolino PL, Liu F, Gruebele M, Schulten K. Ten-microsecond molecular dynamics simulation of a fast-folding WW domain. Biophys J 2008, 94:L75-L77.
12. Freddolino PL, Park S, Roux B, Schulten K. Force field bias in protein folding simulations. Biophys J 2009, 96:3772-3780.
13. Shaw DE, Maragakis P, Lindorff-Larsen K, Piana S, Dror RO, Eastwood MP, Bank JA, Jumper JM, Salmon JK, Shan Y, et al. Atomic-level characterization of the structural dynamics of proteins. Science 2010, 330:341-346.
14. Beck DAC, Daggett V. Methods for molecular dynamics simulations of protein folding/unfolding in solution. Methods Enzymol 2004, 34:112-120.
15. Tolman RC. The principle of microscopic reversibility. Proc Natl Acad Sci USA 1925, 11:436-439.
16. Jackson SE, elMasry N, Fersht AR. Structure of the hydrophobic core in the transition state for folding of chymotrypsin inhibitor 2: a critical test of the protein engineering method of analysis. Biochemistry 1993, 32:11270-11278.
17. Li AJ, Daggett V. Characterization of the transition-state of protein unfolding by use of molecular-dynamics-chymotrypsin inhibitor-2. Proc Natl Acad Sci USA 1994, 91:10430-10434.
18. Li AJ, Daggett V. Identification and characterization of the unfolding transition state of chymotrypsin inhibitor 2 by molecular dynamics simulations. J Mol Biol 1996, 257:412-429.
19. McCully ME, Beck DAC, Daggett V. Microscopic reversibility of protein folding in molecular dynamics simulations of the engrailed homeodomain. Biochemistry 2008, 47:7079-7089.
20. McCully ME, Beck DA, Fersht AR, Daggett V. Refolding the engrailed homeodomain: structural basis for the accumulation of a folding intermediate. Biophys J 2010, 99:1628-1636.
21. Dinner AR, Karplus M. Is protein unfolding the reverse of protein folding? A lattice simulation analysis. J Mol Biol 1999, 292:403-419.
22. Shea JE, Brooks CL 3rd. From folding theories to folding proteins: a review and assessment of simulation studies of protein folding and unfolding. Annu Rev Phys Chem 2001, 52:499-535.
23. Cavalli A, Ferrara P, Caflisch A. Weak temperature dependence of the free energy surface and folding pathways of structured peptides. Proteins 2002, 47:305-314.
24. Guo W, Lampoudi S, Shea JE. Temperature dependence of the free energy landscape of the src-SH3 protein domain. Proteins 2004, 55:395-406.
25. Torrent J, Marchal S, Ribo M, Vilanova M, Georges C, Dupont Y, Lange R. Distinct unfolding and refolding pathways of ribonuclease a revealed by heating and cooling temperature jumps. Biophys J 2008, 94:4056-4065.
26. Tirado-Rives J, Orozco M, Jorgensen WL. Molecular dynamics simulations of the unfolding of barnase in water and 8 M aqueous urea. Biochemistry 1997, 36:7313-7329.
27. Caflisch A, Karplus M. Structural details of urea binding to barnase: a molecular dynamics analysis. Structure 1999, 7:477-488.
28. Bennion BJ, Daggett V. The molecular basis for the chemical denaturation of proteins by urea. Proc Natl Acad Sci USA 2003, 100:5142-5147.
29. Day R, Daggett V. Sensitivity of the folding/unfolding transition state ensemble of chymotrypsin inhibitor 2 to changes in temperature and solvent. Protein Sci 2005, 14:1242-1252.
30. Bennion BJ, Daggett V. Counteraction of urea-induced protein denaturation by trimethylamine N-oxide: a chemical chaperone at atomic resolution. Proc Natl Acad Sci USA 2004, 101:6433-6438.
31. Stumpe MC, Grubmuller H. Polar or apolar-the role of polarity for urea-induced protein denaturation. PLoS Comput Biol 2008, 4:e1000221.
32. Rocco AG, Mollica L, Ricchiuto P, Baptista AM, Gianazza E, Eberini I. Characterization of the protein unfolding processes induced by urea and temperature. Biophys J 2008, 94:2241-2251.
33. Camilloni C, Rocco AG, Eberini I, Gianazza E, Broglia RA, Tiana G. Urea and guanidinium chloride denature protein L in different ways in molecular dynamics simulations. Biophys J 2008, 94:4654-4661.
34. Hua L, Zhou R, Thirumalai D, Berne BJ. Urea denaturation by stronger dispersion interactions with proteins than water implies a 2-stage unfolding. Proc Natl Acad Sci USA 2008, 105:16928-16933.
35. Geierhaas CD, Best RB, Paci E, Vendruscolo M, Clarke J. Structural comparison of the two alternative transition states for folding of TI I27. Biophys J 2006, 91:263-275.
36. Geierhaas CD, Paci E, Vendruscolo M, Clarke J. Comparison of the transition states for folding of two Ig-like proteins from different superfamilies. J Mol Biol 2004, 343:1111-1123.
37. Gianni S, Geierhaas CD, Calosci N, Jemth P, Vuister GW, Travaglini-Allocatelli C, Vendruscolo M, Brunori M. A PDZ domain recapitulates a unifying mechanism for protein folding. Proc Natl Acad Sci USA 2007, 104:128-133.
38. Jemth P, Gianni S. PDZ domains: folding and binding. Biochemistry 2007, 46:8701-8708.
39. Lindorff-Larsen K, Vendruscolo M, Paci E, Dobson CM. Transition states for protein folding have native topologies despite high structural variability. Nat Struct Mol Biol 2004, 11:443-449.
40. Paci E, Vendruscolo M, Dobson CM, Karplus M. Determination of a transition state at atomic resolution from protein engineering data. J Mol Biol 2002, 324:151-163.
41. Best RB, Vendruscolo M. Structural interpretation of hydrogen exchange protection factors in proteins: characterization of the native state fluctuations of CI2. Structure 2006, 14:97-106.
42. Gsponer J, Hopearuoho H, Whittaker SB, Spence GR, Moore GR, Paci E, Radford SE, Vendruscolo M. Determination of an ensemble of structures representing the intermediate state of the bacterial immunity protein Im7. Proc Natl Acad Sci USA 2006, 103:99-104.
43. Paci E, Karplus M. Forced unfolding of fibronectin type 3 modules: an analysis by biased molecular dynamics simulations. J Mol Biol 1999, 288:441-459.
44. Lu H, Isralewitz B, Krammer A, Vogel V, Schulten K. Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation. Biophys J 1998, 75:662-671.
45. Lu H, Schulten K. Steered molecular dynamics simulations of force-induced protein domain unfolding. Proteins 1999, 35:453-463.
46. Grubmuller H, Heymann B, Tavan P. Ligand binding: molecular mechanics calculation of the streptavidin-biotin rupture force. Science 1996, 271:997-999.
47. Best RB, Fowler SB, Herrera JL, Steward A, Paci E, Clarke J. Mechanical unfolding of a titin Ig domain: structure of transition state revealed by combining atomic force microscopy, protein engineering and molecular dynamics simulations. J Mol Biol 2003, 330:867-877.
48. Forman JR, Qamar S, Paci E, Sandford RN, Clarke J. The remarkable mechanical strength of polycystin-1 supports a direct role in mechanotransduction. J Mol Biol 2005, 349:861-871.
49. Forman JR, Yew ZT, Qamar S, Sandford RN, Paci E, Clarke J. Non-native interactions are critical for mechanical strength in PKD domains. Structure 2009, 17:1582-1590.
50. Ng SP, Rounsevell RW, Steward A, Geierhaas CD, Williams PM, Paci E, Clarke J. Mechanical unfolding of TNfn3: the unfolding pathway of a fnIII domain probed by protein engineering, AFM and MD simulation. J Mol Biol 2005, 350:776-789.
51. Paci E, Karplus M. Unfolding proteins by external forces and temperature: the importance of topology and energetics. Proc Natl Acad Sci USA 2000, 97:6521-6526.
52. Sheinerman FB, Brooks CL 3rd. Calculations on folding of segment B1 of streptococcal protein G. J Mol Biol 1998, 278:439-456.
53. Sheinerman FB, Brooks CL 3rd. Molecular picture of folding of a small alpha/beta protein. Proc Natl Acad Sci USA 1998, 95:1562-1567.
54. Kazmirski SL, Li A, Daggett V. Analysis methods for comparison of multiple molecular dynamics trajectories: applications to protein unfolding pathways and denatured ensembles. J Mol Biol 1999, 290:283-304.
55. Beck DA, Daggett V. A one-dimensional reaction coordinate for identification of transition states from explicit solvent P(fold)-like calculations. Biophys J 2007, 93:3382-3391.
56. Scott KA, Randles LG, Moran SJ, Daggett V, Clarke J. The folding pathway of spectrin R17 from experiment and simulation: using experimentally validated MD simulations to characterize states hinted at by experiment. J Mol Biol 2006, 359:159-173.
57. Toofanny RD, Jonsson AL, Daggett V. A comprehensive multidimensional-embedded, one-dimensional reaction coordinate for protein unfolding/folding. Biophys J 2010, 98:2671-2681.
58. Daggett V, Li AJ, Itzhaki LS, Otzen DE, Fersht AR. Structure of the transition state for folding of a protein derived from experiment and simulation. J Mol Biol 1996, 257:430-440.
59. Jackson SE, Fersht AR. Folding of chymotrypsin inhibitor-2 .1. Evidence for a 2-state transition. Biochemistry 1991, 30:10428-10435.
60. Otzen DE, Itzhaki LS, Elmasry NF, Jackson SE, Fersht AR. Structure of the transition-state for the folding/unfolding of the barley chymotrypsin inhibitor-2 and its implications for mechanisms of protein-folding. Proc Natl Acad Sci USA 1994, 91:10422-10425.
61. Itzhaki LS, Otzen DE, Fersht AR. The structure of the transition-state for folding of chymotrypsin inhibitor-2 analyzed by protein engineering methods-evidence for a nucleation-condensation mechanism for protein-folding. J Mol Biol 1995, 254:260-288.
62. Ladurner AG, Itzhaki LS, Daggett V, Fersht AR. Synergy between simulation and experiment in describing the energy landscape of protein folding. Proc Natl Acad Sci USA 1998, 95:8473-8478.
63. Lazaridis T, Karplus M. "New view" of protein folding reconciled with the old through multiple unfolding simulations. Science 1997, 278:1928-1931.
64. Day R, Bennion BJ, Ham S, Daggett V. Increasing temperature accelerates protein unfolding without changing the pathway of unfolding. J Mol Biol 2002, 322:189-203.
65. Day R, Daggett V. Direct observation of microscopic reversibility in single-molecule protein folding. J Mol Biol 2007, 366:677-686.
66. Day R, Daggett V. Ensemble versus single-molecule protein unfolding. Proc Natl Acad Sci USA 2005, 102:13445-13450.
67. Mayor U, Johnson CM, Daggett V, Fersht AR. Protein folding and unfolding in microseconds to nanoseconds by experiment and simulation. Proc Natl Acad Sci USA 2000, 97:13518-13522.
68. Gianni S, Guydosh NR, Khan F, Caldas TD, Mayor U, White GWN, DeMarco ML, Daggett V, Fersht AR. Unifying features in protein-folding mechanisms. Proc Natl Acad Sci USA 2003, 100:13286-13291.
69. Mayor U, Guydosh NR, Johnson CM, Grossmann JG, Sato S, Jas GS, Freund SM, Alonso DO, Daggett V, Fersht AR. The complete folding pathway of a protein from nanoseconds to microseconds. Nature 2003, 421:863-867.
70. Religa TL, Markson JS, Mayor U, Freund SM, Fersht AR. Solution structure of a protein denatured state and folding intermediate. Nature 2005, 437:1053-1056.
71. DeMarco ML, Alonso DO, Daggett V. Diffusing and colliding: the atomic level folding/unfolding pathway of a small helical protein. J Mol Biol 2004, 341:1109-1124.
72. Petrovich M, Jonsson AL, Ferguson N, Daggett V, Fersht AR. Phi-analysis at the experimental limits: mechanism of beta-hairpin formation. J Mol Biol 2006, 360:865-881.
73. Macias MJ, Gervais V, Civera C, Oschkinat H. Structural analysis of WW domains and design of a WW prototype. Nat Struct Biol 2000, 7:375-379.
74. Sharpe T, Jonsson AL, Rutherford TJ, Daggett V, Fersht AR. The role of the turn in beta-hairpin formation during WW domain folding. Protein Sci 2007, 16:2233-2239.
75. Jacobs DM, Saxena K, Vogtherr M, Bernado P, Pons M, Fiebig KM. Peptide binding induces large scale changes in inter-domain mobility in human Pin1. J Biol Chem 2003, 278:26174-26182.
76. Kowalski JA, Liu K, Kelly JW. NMR solution structure of the isolated Apo Pin1 WW domain: comparison to the X-ray crystal structures of Pin1. Biopolymers 2002, 63:111-121.
77. Peng T, Zintsmaster JS, Namanja AT, Peng JW. Sequence-specific dynamics modulate recognition specificity in WW domains. Nat Struct Mol Biol 2007, 14:325-331.
78. Ranganathan R, Ross EM. PDZ domain proteins: scaffolds for signaling complexes. Curr Biol 1997, 7:R770-R773.
79. Verdecia MA, Bowman ME, Lu KP, Hunter T, Noel JP. Structural basis for phosphoserine-proline recognition by group IV WW domains. Nat Struct Biol 2000, 7:639-643.
80. Wong KB, Daggett V. Barstar has a highly dynamic hydrophobic core: evidence from molecular dynamics simulations and nuclear magnetic resonance relaxation data. Biochemistry 1998, 37:11182-11192.
81. Liu F, Du D, Fuller AA, Davoren JE, Wipf P, Kelly JW, Gruebele M. An experimental survey of the transition between two-state and downhill protein folding scenarios. Proc Natl Acad Sci USA 2008, 105:2369-2374.
82. Wilson CA, Kreychman J, Gerstein M. Assessing annotation transfer for genomics: quantifying the relations between protein sequence, structure and function through traditional and probabilistic scores. J Mol Biol 2000, 297:233-249.
83. Rose GD, Creamer TP. Protein folding: predicting predicting. Proteins 1994, 19:1-3.
84. Alexander PA, He Y, Chen Y, Orban J, Bryan PN. The design and characterization of two proteins with 88% sequence identity but different structure and function. Proc Natl Acad Sci USA 2007, 104:11963-11968.
85. He Y, Chen Y, Alexander P, Bryan PN, Orban J. NMR structures of two designed proteins with high sequence identity but different fold and function. Proc Natl Acad Sci USA 2008, 105:14412-14417.
86. Rao KS, Tzul FO, Christian AK, Gordon TN, Bowler BE. Thermodynamics of loop formation in the denatured state of rhodopseudomonas palustris cytochrome c′: scaling exponents and the reconciliation problem. J Mol Biol 2009, 392:1315-1325.
87. Munoz V, Serrano L. Elucidating the folding problem of helical peptides using empirical parameters. Nat Struct Biol 1994, 1:399-409.
88. Lee JC, Engman KC, Tezcan FA, Gray HB, Winkler JR. Structural features of cytochrome c′ folding intermediates revealed by fluorescence energy-transfer kinetics. Proc Natl Acad Sci USA 2002, 99:14778-14782.
89. Kimura T, Lee JC, Gray HB, Winkler JR. Site-specific collapse dynamics guide the formation of the cytochrome c′ four-helix bundle. Proc Natl Acad Sci USA 2007, 104:117-122.
90. Kellermayer MS, Smith SB, Granzier HL, Bustamante C. Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science 1997, 276:1112-1116.
91. Tskhovrebova L, Trinick J, Sleep JA, Simmons RM. Elasticity and unfolding of single molecules of the giant muscle protein titin. Nature 1997, 387:308-312.
92. Grater F, Shen J, Jiang H, Gautel M, Grubmuller H. Mechanically induced titin kinase activation studied by force-probe molecular dynamics simulations. Biophys J 2005, 88:790-804.
93. Marszalek PE, Lu H, Li H, Carrion-Vazquez M, Oberhauser AF, Schulten K, Fernandez JM. Mechanical unfolding intermediates in titin modules. Nature 1999, 402:100-103.
94. Fowler SB, Best RB, Toca Herrera JL, Rutherford TJ, Steward A, Paci E, Karplus M, Clarke J. Mechanical unfolding of a titin Ig domain: structure of unfolding intermediate revealed by combining AFM, molecular dynamics simulations, NMR and protein engineering. J Mol Biol 2002, 322:841-849.
95. Williams PM, Fowler SB, Best RB, Toca-Herrera JL, Scott KA, Steward A, Clarke J. Hidden complexity in the mechanical properties of titin. Nature 2003, 422:446-449.
96. Ruoslahti E, Reed JC. Anchorage dependence, integrins, and apoptosis. Cell 1994, 77:477-478.
97. Sottile J, Hocking DC, Swiatek PJ. Fibronectin matrix assembly enhances adhesion-dependent cell growth. J Cell Sci 1998, 111 (Pt 19):2933-2943.
98. Wang JH, Thampatty BP, Lin JS, Im HJ. Mechanoregulation of gene expression in fibroblasts. Gene 2007, 391:1-15.
99. Krammer A, Lu H, Isralewitz B, Schulten K, Vogel V. Forced unfolding of the fibronectin type III module reveals a tensile molecular recognition switch. Proc Natl Acad Sci USA 1999, 96:1351-1356.
100. Craig D, Krammer A, Schulten K, Vogel V. Comparison of the early stages of forced unfolding for fibronectin type III modules. Proc Natl Acad Sci USA 2001, 98:5590-5595.
101. Gao M, Craig D, Vogel V, Schulten K. Identifying unfolding intermediates of FN-III(10) by steered molecular dynamics. J Mol Biol 2002, 323:939-950.
102. Gao M, Craig D, Lequin O, Campbell ID, Vogel V, Schulten K. Structure and functional significance of mechanically unfolded fibronectin type III1 intermediates. Proc Natl Acad Sci USA 2003, 100:14784-14789.
103. Craig D, Gao M, Schulten K, Vogel V. Tuning the mechanical stability of fibronectin type III modules through sequence variations. Structure 2004, 12:21-30.
104. Li L, Huang HH, Badilla CL, Fernandez JM. Mechanical unfolding intermediates observed by single-molecule force spectroscopy in a fibronectin type III module. J Mol Biol 2005, 345:817-826.
105. Qian F, Wei W, Germino G, Oberhauser A. The nanomechanics of polycystin-1 extracellular region. J Biol Chem 2005, 280:40723-40730.
106. Bycroft M, Bateman A, Clarke J, Hamill SJ, Sandford R, Thomas RL, Chothia C. The structure of a PKD domain from polycystin-1: implications for polycystic kidney disease. EMBO J 1999, 18:297-305.