Simple few-state models reveal hidden complexity in protein folding

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 44, 2012, Pages 17807-17813

  Beauchamp, Kyle A ^a   McGibbon, Robert ^a   Lin, Yu Shan ^a   Pande, Vijay S ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VILLIN;

ACCURACY; ARTICLE; FLOW KINETICS; FLUX PCCA; FUNCTIONAL PROTEOMICS; PREDICTIVE VALUE; PRIORITY JOURNAL; PROCESS MODEL; PROTEIN FOLDING; PROTEIN PROCESSING; QUANTITATIVE ANALYSIS; SLIDING CONSTRAINT RATE ESTIMATION;

KINETICS; MICROFILAMENT PROTEINS; MODELS, MOLECULAR; MODELS, THEORETICAL; PROTEIN FOLDING; PROTEINS;

EID: 84868122477     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1201810109     Document Type: Article

References (63)

1. Anfinsen C, Haber E, Sela M, White F, Jr (1961) The kinetics of formation of native ribonuclease during oxidation of the reduced polypeptide chain. Proc Natl Acad Sci USA 47:1309-1314.
2. Kubelka J, Chiu T, Davies D, EatonW, Hofrichter J (2006) Sub-microsecond protein folding. J Mol Biol 359:546-553.
3. Kim P, Baldwin R (1990) Intermediates in the folding reactions of small proteins. Annu Rev Biochem 59:631-660.
4. Dyson H, Wright P (2002) Coupling of folding and binding for unstructured proteins. Curr Opin Struct Biol 12:54-60.
5. Hardy J, Selkoe D (2002) The amyloid hypothesis of alzheimer's disease: progress and problems on the road to therapeutics. Science 297:353-356.
6. Bai Y, Sosnick T, Mayne L, Englander SW (1995) Protein folding intermediates: nativestate hydrogen exchange. Science 269:192-197.
7. van Kampen N (2007) Stochastic Processes in Physics and Chemistry (North Holland, Amsterdam).
8. Prinz J, et al. (2011) Markov models of molecular kinetics: Generation and validation. J Chem Phys 134:174105-174128.
9. Bowman G, Huang X, Pande V (2009) Using generalized ensemble simulations and markov state models to identify conformational states. Methods 49:197-201.
10. Chodera J, Singhal N, Pande V, Dill K, Swope W (2007) Automatic discovery of metastable states for the construction of markov models of macromolecular conformational dynamics. J Chem Phys 126:155101-155118.
11. Noé F, Schütte C, Vanden-Eijnden E, Reich L, Weikl T (2009) Constructing the equilibrium ensemble of folding pathways from short off-equilibrium simulations. Proc Natl Acad Sci U S A 106:19011-19016.
12. Buchete N, Hummer G (2008) Coarse master equations for peptide folding dynamics. J Phys Chem B 112:6057-6069.
13. Buchner GS, Murphy RD, Buchete NV, Kubelka J (2011) Dynamics of protein folding: Probing the kinetic network of folding-unfolding transitions with experiment and theory. Biochem Biophys Acta 1814:1001-1020.
14. Deuflhard P, Huisinga W, Fischer A, Schütte C (2000) Identification of almost invariant aggregates in reversible nearly uncoupled markov chains. Lin Alg Appl 315:39-59.
15. Deuflhard P,WeberM(2005) Robust perron cluster analysis in conformation dynamics. Lin Alg Appl 398:161-184.
16. Kube S, Weber M (2007) A coarse graining method for the identification of transition rates between molecular conformations. J Chem Phys 126:24103-24113.
17. Sarich M, Noé F, Schütte C (2010) On the approximation quality of markov state models. Multiscale Model Simul 8:1154-1177.
18. Prinz J, Keller B, Noé F (2011) Probing molecular kinetics with markov models: metastable states, transition pathways and spectroscopic observables. Phys Chem Chem Phys 13:16912-16927.
19. Lane T, Bowman G, Beauchamp K, Voelz V, Pande V (2011) Markov state model reveals folding and functional dynamics in ultra-long md trajectories. J Am Chem Soc 133:18413-18419.
20. Beauchamp K, Ensign D, Das R, Pande V (2011) Quantitative comparison of villin headpiece subdomain simulations and triplet-triplet energy transfer experiments. Proc Natl Acad Sci U S A 108:12734-12739.
21. Shaw DE, et al. (2010) Atomic-level characterization of the structural dynamics of proteins. Science 330:341-346.
22. Lindorff-Larsen K, Piana S, Dror R, Shaw D (2011) How fast-folding proteins fold. Science 334:517-520.
23. Shaw D, et al. (2008) Anton, a special-purpose machine for molecular dynamics simulation. Commun ACM 51:91-97.
24. Shirts M, Pande V (2000) Screen savers of the world unite! Science 290: 1903-1904.
25. Best R, Hummer G (2005) Reaction coordinates and rates from transition paths. Proc. Natl. Acad. Sci USA 102:6732-6737.
26. Sarisky C, Mayo S (2001) The beta-beta-alpha fold: explorations in sequence space. J Mol Biol 307:1411-1418.
27. Shen Y, Bax A (2010) Sparta+: a modest improvement in empirical nmr chemical shift prediction by means of an artificial neural network. J Biomol NMR 48:13-22.
28. Han B, Liu Y, Ginzinger S, Wishart D (2011) Shiftx2: significantly improved protein chemical shift prediction. J Biomol NMR 50:43-57.
29. Lindorff-Larsen K, et al. (2010) Improved side-chain torsion potentials for the amber ff99sb protein force field. Proteins: Struct, Funct, Bioinf 78:1950-1958.
30. Piana S, Lindorff-Larsen K, Shaw D (2011) How robust are protein folding simulations with respect to force field parameterization? Biophys J 100: L47-L49.
31. Best R, Buchete N, Hummer G (2008) Are current molecular dynamics force fields too helical? Biophys J 95: L07-L09.
32. Lindorff-Larsen K, et al. (2012) Systematic validation of protein force fields against experimental data. PloS one 7:e32131.
33. Freddolino P, Schulten K (2009) Common structural transitions in explicit-solvent simulations of villin headpiece folding. Biophys J 97:2338-2347.
34. Ensign D, Kasson P, Pande V (2007) Heterogeneity even at the speed limit of folding: large-scale molecular dynamics study of a fast-folding variant of the villin headpiece. J Mol Biol 374:806-816.
35. Jager M, et al. (2006) Structure-function-folding relationship in a ww domain. Proc Natl Acad Sci U S A 103:10648-10653.
36. Wintjens R, et al. (2001) 1 h nmr study on the binding of pin1 trp-trp domain with phosphothreonine peptides. J Biol Chem 276:25150-25156.
37. Krivov S (2011) The free energy landscape analysis of protein (fip35) folding dynamics. J Phys Chem B 115:12315-12324.
38. Nauli S, Kuhlman B, Baker D (2001) Computer-based redesign of a protein folding pathway. Nat Struct Biol 8:602-605.
39. Horng J, Moroz V, Raleigh D (2003) Rapid cooperative two-state folding of a miniature alpha-beta protein and design of a thermostable variant. J Mol Biol 326:1261-1270.
40. Piana S, et al. (2011) Computational design and experimental testing of the fastestfolding β-sheet protein. J Mol Biol 405:43-48.
41. Kührová P, De Simone A, Otyepka M, Best RB (2012) Force-field dependence of chignolin folding and misfolding: Comparison with experiment and redesign. Biophys J 102:1897-1906.
42. Evans MR, Gardner KH (2009) Slow transition between two β-strand registers is dictated by protein unfolding. J Am Chem Soc 131:11306-11307.
43. Chung H, Ganim Z, Jones K, Tokmakoff A (2007) Transient 2d ir spectroscopy of ubiquitin unfolding dynamics. Proc Natl Acad Sci USA 104:14237-14242.
44. Korzhnev D, Kay L (2008) Probing invisible, low-populated states of protein molecules by relaxation dispersion nmr spectroscopy: an application to protein folding. Acc Chem Res 41:442-451.
45. McKnight C, Matsudaira P, Kim P (1997) NMR structure of the 35-residue villin headpiece subdomain. Nat Struct Biol 4:180-184.
46. Chiu T, et al. (2005) High-resolution x-ray crystal structures of the villin headpiece subdomain, an ultrafast folding protein. Proc Natl Acad Sci USA 102:7517-7522.
47. McKnight J, Doering D, Matsudaira P, Kim P (1996) A thermostable 35-residue subdomain within villin headpiece. J Mol Biol 260:126-134.
48. Brewer S, Song B, Daniel P, Dyer R (2007) Residue specific resolution of protein folding dynamics using isotope-edited infrared temperature jump spectroscopy. Biochemistry 46:3279-3285.
49. Wang M, et al. (2003) Dynamic nmr line-shape analysis demonstrates that the villin headpiece subdomain folds on the microsecond time scale. J Am Chem Soc 125:6032-6033.
50. Cellmer T, Buscaglia M, Henry E, Hofrichter J, Eaton W (2011) Making connections between ultrafast protein folding kinetics and molecular dynamics simulations. Proc Natl Acad Sci U S A 108:6103-6108.
51. Kubelka J, EatonW, Hofrichter J (2003) Experimental tests of villin subdomain folding simulations. J Mol Biol 329:625-630.
52. Kubelka J, Henry E, Cellmer T, Hofrichter J, Eaton W (2008) Chemical, physical, and theoretical kinetics of an ultrafast folding protein. Proc Natl Acad Sci USA 105:18655-18662.
53. Reiner A, Henklein P, Kiefhaber T (2010) An unlocking/relocking barrier in conformational fluctuations of villin headpiece subdomain. Proc Natl Acad Sci USA 107:4955-4960.
54. Best R, Hummer G (2009) Optimized molecular dynamics force fields applied to the helix- coil transition of polypeptides. J Phys Chem B 113:9004-9015.
55. Hess B, Kutzner C, Van Der Spoel D, Lindahl E (2008) Gromacs 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput 4:435-447.
56. Rotkiewicz P, Skolnick J (2008) Fast procedure for reconstruction of full-atom protein models from reduced representations. J Comput Chem 29:1460-1465.
57. Beauchamp K, et al. (2011) Msmbuilder2: Modeling conformational dynamics at the picosecond to millisecond scale. J Chem Theory Comput 7:3412-3419.
58. Bowman GR, Beauchamp KA, Boxer G, Pande VS (2009) Progress and challenges in the automated construction of Markov state models for full protein systems. J Chem Phys 131:124101-124112.
59. Noé F, Fischer S (2008) Transition networks for modeling the kinetics of conformational change in macromolecules. Curr Opin Struct Biol 18:154-162.
60. Ward J, Jr (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58:236-244.
61. Mullner D (2011) Modern hierarchical, agglomerative clustering algorithms. Arxiv.
62. Noé F, et al. (2011) Dynamical fingerprints for probing individual relaxation processes in biomolecular dynamics with simulations and kinetic experiments. Proc Natl Acad Sci U S A 108:4822-4827.
63. Schütte C, Noé F, Lu J, Sarich M, Vanden-Eijnden E (2011) Markov state models based on milestoning. J Chem Phys 134:204105-204120.