Robust Density-Based Clustering to Identify Metastable Conformational States of Proteins

Journal of Chemical Theory and Computation

Volumn 12, Issue 5, 2016, Pages 2426-2435

  Sittel, Florian ^a   Stock, Gerhard ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APROTININ; PROTEIN;

ANIMAL; BOVINE; CHEMISTRY; CLUSTER ANALYSIS; MARKOV CHAIN; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY;

ANIMALS; APROTININ; CATTLE; CLUSTER ANALYSIS; MARKOV CHAINS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEINS;

EID: 84969601898     PISSN: 15499618     EISSN: 15499626     Source Type: Journal    
DOI: 10.1021/acs.jctc.5b01233     Document Type: Article

References (43)

1. Villa, P.; Roebroeks, W. Neandertal demise: an archaeological analysis of the modern human superiority complex PLoS One 2014, 9, e96424 10.1371/journal.pone.0096424
2. Rohrdanz, M. A.; Zheng, W.; Clementi, C. Discovering Mountain Passes via Torchlight: Methods for the Definition of Reaction Coordinates and Pathways in Complex Macromolecular Reactions Annu. Rev. Phys. Chem. 2013, 64, 295-316 10.1146/annurev-physchem-040412-110006
3. Hegger, R.; Altis, A.; Nguyen, P. H.; Stock, G. How Complex is the Dynamics of Peptide Folding? Phys. Rev. Lett. 2007, 98, 028102 10.1103/PhysRevLett.98.028102
4. Krivov, S. V.; Karplus, M. Diffusive reaction dynamics on invariant free energy profiles Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 13841-13846 10.1073/pnas.0800228105
5. Stock, G.; Jain, A.; Riccardi, L.; Nguyen, P. H. In Protein and Peptide Folding, Misfolding and Non-Folding; Schweitzer-Stenner, R., Ed.; Wiley: New York, 2012; p 57.
6. Schaudinnus, N.; Bastian, B.; Hegger, R.; Stock, G. Multidimensional Langevin modeling of nonoverdamped dynamics Phys. Rev. Lett. 2015, 115, 050602 10.1103/PhysRevLett.115.050602
7. Amadei, A.; Linssen, A. B. M.; Berendsen, H. J. C. Essential dynamics of proteins Proteins: Struct., Funct., Genet. 1993, 17, 412-425 10.1002/prot.340170408
8. de Groot, B. L.; Daura, X.; Mark, A. E.; Grubmüller, H. Essential dynamics of reversible peptide folding: Memory-free conformational dynamics governed by internal hydrogen bonds J. Mol. Biol. 2001, 309, 299-313 10.1006/jmbi.2001.4655
9. Altis, A.; Nguyen, P. H.; Hegger, R.; Stock, G. Dihedral angle principal component analysis of molecular dynamics simulations J. Chem. Phys. 2007, 126, 244111 10.1063/1.2746330
10. Blöchliger, N.; Caflisch, A.; Vitalis, A. Weighted Distance Functions Improve Analysis of High-Dimensional Data: Application to Molecular Dynamics Simulations J. Chem. Theory Comput. 2015, 11, 5481-5492 10.1021/acs.jctc.5b00618
11. Perez-Hernandez, G.; Paul, F.; Giorgino, T.; De Fabritiis, G.; Noe, F. Identification of slow molecular order parameters for Markov model construction J. Chem. Phys. 2013, 139, 015102 10.1063/1.4811489
12. Rao, F.; Caflisch, A. The protein folding network J. Mol. Biol. 2004, 342, 299-306 10.1016/j.jmb.2004.06.063
13. Buchete, N.-V.; Hummer, G. Coarse master equations for peptide folding dynamics J. Phys. Chem. B 2008, 112, 6057-6069 10.1021/jp0761665
14. Noe, F.; Schütte, C.; Vanden-Eijnden, E.; Reich, L.; Weikl, T. Constructing the Full Ensemble of Folding Pathways from Short Off-Equilibrium Simulations Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 19011-19016 10.1073/pnas.0905466106
15. Bowman, G. R.; Beauchamp, K. A.; Boxer, G.; Pande, V. S. Progress and challenges in the automated construction of Markov state models for full protein systems J. Chem. Phys. 2009, 131, 124101 10.1063/1.3216567
16. Prinz, J.-H.; Wu, H.; Sarich, M.; Keller, B.; Senne, M.; Held, M.; Chodera, J. D.; Schütte, C.; Noe, F. Markov models of molecular kinetics: generation and validation J. Chem. Phys. 2011, 134, 174105 10.1063/1.3565032
17. Shukla, D.; Hernández, C. X.; Weber, J. K.; Pande, V. S. Markov state models provide insights into dynamic modulation of protein function Acc. Chem. Res. 2015, 48, 414-422 10.1021/ar5002999
18. Ester, M.; Kriegel, H.-P.; Sander, J.; Xu, X. In Proceedings of the Second International Conference on Knowledge Discovery and Data Mining; Simoudis, E.; Han, J.; Fayyad, U. M., Eds.; AAAI Press, 1996; pp 226-231.
19. Keller, B.; Daura, X.; van Gunsteren, W. F. Comparing geometric and kinetic cluster algorithms for molecular simulation data J. Chem. Phys. 2010, 132, 074110 10.1063/1.3301140
20. Campos, S. R.; Baptista, A. M. Conformational analysis in a multidimensional energy landscape: Study of an arginylglutamate repeat J. Phys. Chem. B 2009, 113, 15989-16001 10.1021/jp902991u
21. Rodriguez, A.; Laio, A. Clustering by fast search and find of density peaks Science 2014, 344, 1492-1496 10.1126/science.1242072
22. Hartigan, J. A.; Wong, M. A. A K-means clustering algorithm Applied Statistics 1979, 28, 100-108 10.2307/2346830
23. Röblitz, S.; Weber, M. Fuzzy spectral clustering by PCCA+: application to Markov state models and data classification Adv. Data Analysis and Classification 2013, 7, 147-179 10.1007/s11634-013-0134-6
24. Bowman, G. R.; Meng, L.; Huang, X. Quantitative comparison of alternative methods for coarse-graining biological networks J. Chem. Phys. 2013, 139, 121905 10.1063/1.4812768
25. Jain, A.; Stock, G. Identifying metastable states of folding proteins J. Chem. Theory Comput. 2012, 8, 3810-3819 10.1021/ct300077q
26. Mu, Y.; Nguyen, P. H.; Stock, G. Energy Landscape of a Small Peptide Revealed by Dihedral Angle Principal Component Analysis Proteins: Struct., Funct., Genet. 2005, 58, 45-52 10.1002/prot.20310
27. Altis, A.; Otten, M.; Nguyen, P. H.; Hegger, R.; Stock, G. Construction of the free energy landscape of biomolecules via dihedral angle principal component analysis J. Chem. Phys. 2008, 128, 245102 10.1063/1.2945165
28. Schuler, L. D.; Daura, X.; van Gunsteren, W. F. An improved GROMOS96 force field for aliphatic hydrocarbons in the condensed phase J. Comput. Chem. 2001, 22, 1205-1218 10.1002/jcc.1078
29. Hornak, V.; Abel, R.; Okur, A.; Strockbine, B.; Roitberg, A.; Simmerling, C. Comparison of multiple Amber force fields and development of improved protein backbone parameters Proteins: Struct., Funct., Genet. 2006, 65, 712-725 10.1002/prot.21123
30. Best, R. B.; Hummer, G. Optimized Molecular Dynamics Force Fields Applied to the Helix-Coil Transition of Polypeptides J. Phys. Chem. B 2009, 113, 9004-9015 10.1021/jp901540t
31. Lindorff-Larsen, K.; Piana, S.; Palmo, K.; Maragakis, P.; Klepeis, J. L.; Dror, R. O.; Shaw, D. E. Improved side-chain torsion potentials for the Amber ff99SB protein force field Proteins: Struct., Funct., Genet. 2010, 78, 1950-1958 10.1002/prot.22711
32. Piana, S.; Lindorff-Larsen, K.; Shaw, D. E. Protein folding kinetics and thermodynamics from atomistic simulation Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 17845-17850 10.1073/pnas.1201811109
33. 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.; Wriggers, W. Atomic-Level Characterization of the Structural Dynamics of Proteins Science 2010, 330, 341-346 10.1126/science.1187409
34. Sittel, F.; Jain, A.; Stock, G. Principal component analysis of molecular dynamics: On the use of Cartesian vs. internal coordinates J. Chem. Phys. 2014, 141, 014111 10.1063/1.4885338
35. Jain, A.; Stock, G. Hierarchical folding free energy landscape of HP35 revealed by most probable path clustering J. Phys. Chem. B 2014, 118, 7750-7760 10.1021/jp410398a
36. Epanechnikov, V. A. Non-Parametric Estimation of a Multivariate Probability Density Theory Probab. Its Appl. 1969, 14, 153-158 10.1137/1114019
37. Grubmüller, H. Predicting slow structural transitions in macromolecular systems: Conformational flooding Phys. Rev. E: Stat. Phys., Plasmas, Fluids, Relat. Interdiscip. Top. 1995, 52, 2893-2906 10.1103/PhysRevE.52.2893
38. Laio, A.; Parrinello, M. Escaping free-energy minima Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 12562-12566 10.1073/pnas.202427399
39. Yao, Y.; Cui, R. Z.; Bowman, G. R.; Silva, D.-A.; Sun, J.; Huang, X. Hierarchical Nyström methods for constructing Markov state models for conformational dynamics J. Chem. Phys. 2013, 138, 174106 10.1063/1.4802007
40. Faradjian, A. K.; Elber, R. Computing time scales from reaction coordinates by milestoning J. Chem. Phys. 2004, 120, 10880-10889 10.1063/1.1738640
41. Kabsch, W.; Sander, C. Dictionary of protein secondary structure: Pattern recognition of hydrogen bonded and geometrical features Biopolymers 1983, 22, 2577-2637 10.1002/bip.360221211
42. Frishman, D.; Argos, P. Knowledge-based protein secondary structure assignment Proteins: Struct., Funct., Genet. 1995, 23, 566-79 10.1002/prot.340230412
43. Humphrey, W.; Dalke, A.; Schulten, K. VMD-Visual Molecular Dynamics J. Mol. Graphics 1996, 14, 33-38 10.1016/0263-7855(96)00018-5