Hierarchical conformational analysis of native lysozyme based on sub-millisecond molecular dynamics simulations

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Wang, Kai ^a   Long, Shiyang ^a   Tian, Pu ^a  

^a JILIN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HEN EGG WHITE LYSOZYME; LYSOZYME; UNCLASSIFIED DRUG; HEN EGG LYSOZYME;

ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; HIERARCHICAL CONFORMATIONAL ANALYSIS; HIERARCHICAL ORGANIZATION OF FREE ENERGY LANDSCAPE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PROTEIN ANALYSIS; ANIMAL; CHEMISTRY; MOLECULAR WEIGHT; PROBABILITY; PROTEIN CONFORMATION; TIME FACTOR; X RAY CRYSTALLOGRAPHY;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; MOLECULAR DYNAMICS SIMULATION; MOLECULAR WEIGHT; MURAMIDASE; PROBABILITY; PROTEIN CONFORMATION; TIME FACTORS;

EID: 84936751115     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0129846     Document Type: Article

References (57)

1. Boehr DD, McElheny D, Dyson HJ, Wright PE. The dynamic energy landscape of dihydrofolate reductase catalysis. Science. 2006; 313:1638-42. PMID: 16973882
2. Tang C, Schwieters CD, Clore GM. Open-to-closed transition in apo maltose-binding protein observed by paramagnetic NMR. Nature. 2007; 449:1078-1082. doi: 10.1038/nature06232 PMID: 17960247
3. Henzler-Wildman KA, Thai V, Lei M, Ott M, Wolf-Watz M, Fenn T, et al. Intrinsic motions along an enzymatic reaction trajectory. nature. 2007 12; 450:838-44. doi: 10.1038/nature06410 PMID: 18026086
4. Biehl R, Hoffmann B, Monkenbusch M, Falus P, Préost S, Merkel R, et al. Direct Observation of Correlated Interdomain Motion in Alcohol Dehydrogenase. Phys Rev Lett. 2008 Sep; 101:138102. doi: 10.1103/PhysRevLett.101.138102 PMID: 18851497
5. Hodges C, Bintu L, Lubkowska L, Kashlev M, Bustamante C. Nucleosomal fluctuations govern the transcription dynamics of RNA polymerase II. Science. 2009; 325:626-8. doi: 10.1126/science.1172926 PMID: 19644123
6. Dong M, Husale S, Sahin O. Determination of protein structural flexibility by microsecond force spectroscopy. Nat Nanotechnol. 2009; 4:514-7. doi: 10.1038/nnano.2009.156 PMID: 19662014
7. Vreede J, Juraszek J, Bolhuis PG. Predicting the reaction coordinates of millisecond light-induced conformational changes in photoactive yellow protein. Proc Natl Acad Sci USA. 2010; 107:2391-6. doi: 10.1073/pnas.0908754107
8. Inoue R, Biehl R, Rosenkranz T, Fitter J, Monkenbusch M, Radulescu a, et al. Large domain fluctuations on 50-ns timescale enable catalytic activity in phosphoglycerate kinase. Biophysical journal. 2010 Oct; 99(7):2309-17. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3042550&tool = pmcentrez&rendertype = abstract. doi: 10.1016/j.bpj.2010.08.017 PMID: 20923666
9. Shaw DE, Maragakis P, Lindorff-Larsen K, Piana S, Dror RO, Eastwood MP, et al. Atomic-level characterization of the structural dynamics of proteins. Science (New York, NY). 2010 Oct; 330(6002):341-6. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20947758. doi: 10.1126/science.1187409
10. Wang Y, Tang C, Wang E, Wang J. Exploration of multi-state conformational dynamics and underlying global functional landscape of maltose binding protein. PLoS computational biology. 2012 Jan; 8(4):e1002471. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3330084&tool =pmcentrez&rendertype = abstract. doi: 10.1371/journal.pcbi.1002471 PMID: 22532792
11. Tirion MM. Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys Rev Lett. 1996; 77:1905-08. doi: 10.1103/PhysRevLett.77.1905 PMID: 10063201
12. Gur M, Zomot E, Bahar I. Global motions exhibited by proteins in micro- to milliseconds simulations concur with anisotropic network model predictions. The Journal of chemical physics. 2013 Sep; 139(12):121912. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3739829&tool = pmcentrez&rendertype = abstract. doi: 10.1063/1.4816375 PMID: 24089724
13. Sinko W, Lindert S, McCammon JA. Accounting for Receptor Flexibility and Enhanced Sampling Methods in Computer-Aided Drug Design. Chemical Biology & Drug Design. 2013; 81(1):41-49. doi: 10.1111/cbdd.12051
14. Austin RH, Beeson KW, Eisenstein L, Frauenfelder H, Gunsalus IC. Dynamics of ligand binding to myoglobin. Biochemistry. 1975 Dec; 14(24):5355-73. Available from: http://www.ncbi.nlm.nih.gov/pubmed/1191643. doi: 10.1021/bi00695a021 PMID: 1191643
15. Frauenfelder H, Sligar S, Wolynes P. The energy landscapes and motions of proteins. Science. 1991; 254(5038):1598-1603. Available from: http://www.sciencemag.org/content/254/5038/1598.abstract. doi: 10.1126/science.1749933 PMID: 1749933
16. Zhuravlev PI, Papoian Ga. Functional versus folding landscapes: the same yet different. Current opinion in structural biology. 2010 Feb; 20(1):16-22. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20102791. doi: 10.1016/j.sbi.2009.12.010 PMID: 20102791
17. Lensink MF, Wodak SJ. Docking and scoring protein interactions: CAPRI 2009. Proteins: Structure, Function, and Bioinformatics. 2010; 78(15):3073-3084. doi: 10.1002/prot.22818
18. Gallicchio E, Levy RM. Prediction of SAMPL3 host-guest affinities with the binding energy distribution analysis method (BEDAM). Journal of computer-aided molecular design. 2012 May;(5:) :505-516. doi: 10.1007/s10822-012-9552-3 PMID: 22354755
19. Pons C, Fenwick RB, Esteban-Martín S, Salvatella X, Fernandez-Recio J. Validated Conformational Ensembles Are Key for the Successful Prediction of Protein Complexes. Journal of Chemical Theory and Computation. 2013; 9(3):1830-1837. doi: 10.1021/ct300990h
20. Lexa KW, Carlson HA. Protein flexibility in docking and surface mapping. Quarterly Reviews of Biophysics. 2012 8; 45:301-343. doi: 10.1017/S0033583512000066 PMID: 22569329
21. Lindorff-larsen K, Piana S, Dror RO, Shaw DE. How fast-folding proteins fold. Science. 2011; 334:517-520. doi: 10.1126/science.1208351 PMID: 22034434
22. Lane TJ, Bowman GR, Beauchamp K, Voelz Va, Pande VS. Markov state model reveals folding and functional dynamics in ultra-long MD trajectories. Journal of the American Chemical Society. 2011 Nov; 133(45):18413-9. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3227799&tool = pmcentrez&rendertype = abstract. doi: 10.1021/ja207470h PMID: 21988563
23. Dickson A, Brooks CL. Native states of fast-folding proteins are kinetic traps. Journal of the American Chemical Society. 2013 Mar; 135(12):4729-34. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23458553. doi: 10.1021/ja311077u PMID: 23458553
24. Lane TJ, Shukla D, Beauchamp Ka, Pande VS. To milliseconds and beyond: challenges in the simulation of protein folding. Current opinion in structural biology. 2013 Feb; 23(1):58-65. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23237705. doi: 10.1016/j.sbi.2012.11.002 PMID: 23237705
25. Sosnick TR, Hinshaw JR. Biochemistry. How proteins fold. Science (New York, NY). 2011 Oct; 334(6055):464-5. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22034424. doi: 10.1126/science.1214018
26. Chung HS, McHale K, Louis JM, Eaton Wa. Single-molecule fluorescence experiments determine protein folding transition path times. Science (New York, NY). 2012 Feb; 335(6071):981-4. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22363011. doi: 10.1126/science.1215768
27. Vymětal J, Vondrášek J. Critical Assessment of Current Force Fields. Short Peptide Test Case. Journal of Chemical Theory and Computation. 2013; 9(1):441-451. doi: 10.1021/ct300794a
28. Lindorff-Larsen K, Maragakis P, Piana S, Eastwood MP, Dror RO, Shaw DE. Systematic validation of protein force fields against experimental data. PloS one. 2012 Jan; 7(2):e32131. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3285199&tool = pmcentrez&rendertype=abstract. doi: 10.1371/journal.pone.0032131 PMID: 22384157
29. Gunasekaran K, Ma B, Nussinov R. Is allostery an intrinsic property of all dynamic proteins? Proteins: Structure, Function, and Bioinformatics. 2004; 57(3):433-443. Available from: http://dx.doi.org/10. 1002/prot.20232.
30. Csermely P, Palotai R, Nussinov R. Induced fit, conformational selection and independent dynamic segments: an extended view of binding events. Trends in Biochemical Sciences. 2010; 35(10):539-546. Available from: http://www.sciencedirect.com/science/article/pii/S0968000410000885. doi: 10.1016/j.tibs.2010.04.009 PMID: 20541943
31. Bolhuis PG, Chandler D, Dellago C, Geissler PL. TRANSITION PATH SAMPLING: Throwing Ropes Over Rough Mountain Passes, in the Dark. Annual Review of Physical Chemistry. 2002; 53(1):291-318. doi: 10.1146/annurev.physchem.53.082301.113146 PMID: 11972010
32. Best RB, Hummer G. Diffusive Model of Protein Folding Dynamics with Kramers Turnover in Rate. Phys Rev Lett. 2006 Jun; 96:228104. doi: 10.1103/PhysRevLett.96.228104 PMID: 16803349
33. Chung HS, Louis JM, Eaton WA. Experimental determination of upper bound for transition path times in protein folding from single-molecule photon-by-photon trajectories. Proceedings of the National Academy of Sciences. 2009; 106(29):11837-11844. Available from: http://www.pnas.org/content/106/29/11837.abstract. doi: 10.1073/pnas.0901178106
34. Best RB, Mittal J. Microscopic events in -hairpin folding from alternative unfolded ensembles. Proceedings of the National Academy of Sciences. 2011; 108(27):11087-11092. Available from: http://www.pnas.org/content/108/27/11087.abstract. doi: 10.1073/pnas.1016685108
35. Li DW, Brüschweiler R. In silico relationship between configurational entropy and soft degrees of freedom in proteins and peptides. Phys Rev Lett. 2009 Mar; 102:118108. doi: 10.1103/PhysRevLett.102.118108 PMID: 19392246
36. Fenwick RB, Esteban-Martín S, Richter B, Lee D, Walter KFA, Milovanovic D, et al. Weak Long-Range Correlated Motions in a Surface Patch of Ubiquitin Involved in Molecular Recognition. Journal of the American Chemical Society. 2011; 133(27):10336-10339. doi: 10.1021/ja200461n PMID: 21634390
37. Lindorff-Larsen K, Best RB, DePristo MA, Dobson CM, Vendruscolo M. Simultaneous determination of protein structure and dynamics. Nature. 2005; 433:128-132. Available from: http://www.nature.com/nature/journal/v433/n7022/suppinfo/nature03199-S1.html. doi: 10.1038/nature03199 PMID: 15650731
38. Winn PJ, Lüdemann SK, Gauges R, Lounnas V, Wade RC. Comparison of the dynamics of substrate access channels in three cytochrome P450s reveals different opening mechanisms and a novel functional role for a buried arginine. Proceedings of the National Academy of Sciences. 2002; 99(8):5361-5366. Available from: http://www.pnas.org/content/99/8/5361.abstract. doi: 10.1073/pnas.082522999
39. Gora A, Brezovsky J, Damborsky J. Gates of Enzymes. Chemical Reviews. 2013; 113(8):5871-5923. doi: 10.1021/cr300384w PMID: 23617803
40. Hildebrandt AK, Dietzen M, Lengauer T, Lenhof HP, Althaus E, Hildebrandt A. Efficient computation of root mean square deviations under rigid transformations. Journal of Computational Chemistry. 2014; 35(10):765-771. doi: 10.1002/jcc.23513
41. Magis C, Di Tommaso P, Notredame C. T-RMSD: a web server for automated fine-grained protein structural classification. Nucleic Acids Research. 2013; 41(W1):W358-W362. Available from: http://nar.oxfordjournals.org/content/41/W1/W358.abstract. doi: 10.1093/nar/gkt383 PMID: 23716642
42. Hung LH, Guerquin M, Samudrala R. GPU-Q-J, a fast method for calculating root mean square deviation (RMSD) after optimal superposition. BMC Research Notes. 2011; 4(1):97. doi: 10.1186/1756-0500-4-97 PMID: 21453553
43. Zhou X, Chou J, Wong S. Protein structure similarity from principle component correlation analysis. BMC Bioinformatics. 2006; 7(1):40. doi: 10.1186/1471-2105-7-40 PMID: 16436213
44. Chodera JD, Noé F. Markov state models of biomolecular conformational dynamics. Current Opinion in Structural Biology. 2014; 25(0):135-144. Theory and simulation / Macromolecular machines. Available from: http://www.sciencedirect.com/science/article/pii/S0959440X14000426. doi: 10.1016/j.sbi.2014.04.002 PMID: 24836551
45. Huang X, Yao Y, Bowman GR, Sun J, Guibas LJ, Carlsson G, et al. Constructing multi-resolution markov state models (msms) to elucidate RNA hairpin folding mechanisms. Pacific Symposium on Biocomputing Pacific Symposium on Biocomputing. 2010;p. 228-239. PMID: 19908375
46. Yao Y, Cui RZ, Bowman GR, Silva DA, Sun J, Huang X. Hierarchical Nystrm methods for constructing Markov state models for conformational dynamics. The Journal of Chemical Physics. 2013; 138(17):-. doi: 10.1063/1.4802007
47. Chodera JD, Singhal N, Pande VS, Dill KA, Swope WC. Automatic discovery of metastable states for the construction of Markov models of macromolecular conformational dynamics. The Journal of Chemical Physics. 2007; 126(15):-. doi: 10.1063/1.2714538 PMID: 17461665
48. rd ed. MIT Press and McGraw-Hill; 2009.
49. Sbreveali A, Shakhnovich E, Karplus M. How does a protein fold? nature. 1995 5; 369:248-251. Available from: http://dx.doi.org/10.1038/369248a0.
50. Mirny L, Shakhnovich E. PROTEIN FOLDING THEORY: From Lattice to All-Atom Models. Annual Review of Biophysics and Biomolecular Structure. 2001; 30(1):361-396. doi: 10.1146/annurev.biophys.30.1.361 PMID: 11340064
51. Bonneau R, Baker D. AB INITIO PROTEIN STRUCTURE PREDICTION: Progress and Prospects. Annual Review of Biophysics and Biomolecular Structure. 2001; 30(1):173-189. doi: 10.1146/annurev.biophys.30.1.173 PMID: 11340057
52. Nobuhiro GO¯, Abe H. Noninteracting local-structure model of folding and unfolding transition in globular proteins. I. Formulation. Biopolymers. 1981; 20(5):991-1011. doi: 10.1002/bip.1981.360200511
53. Abe H, Nobuhiro GO¯. Noninteracting local-structure model of folding and unfolding transition in globular proteins. II. Application to two-dimensional lattice proteins. Biopolymers. 1981; 20(5):1013-1031. doi: 10.1002/bip.1981.360200512 PMID: 7225529
54. Humphrey W, Dalke A, Schulten K. VMD: Visual molecular dynamics. Journal of Molecular Graphics. 1996; 14(1):33-38. doi: 10.1016/0263-7855(96)00018-5 PMID: 8744570
55. Stone JE, Phillips JC, Freddolino PL, Hardy DJ, Trabuco LG, Schulten K. Accelerating molecular modeling applications with graphics processors. J Comput Chem. 2007; 28:2618-2640. doi: 10.1002/jcc.20829 PMID: 17894371
56. Harvey MJ, Giupponi G, Gabritiis GD. ACEMD: Accelerating biomolecular dynamics in the microsecond time scale. J Chem Theory Comput. 2009; 5:1632-9. doi: 10.1021/ct9000685
57. Mu Y, Nguyen PH, Stock G. Energy landscape of a small peptide revealed by dihedral angle principal component analysis. Proteins: Structure, Function, and Bioinformatics. 2005; 58(1):45-52. doi: 10.1002/prot.20310