Event detection and sub-state discovery from biomolecular simulations using higher-order statistics: Application to enzyme adenylate kinase

Proteins: Structure, Function and Bioinformatics

Volumn 80, Issue 11, 2012, Pages 2536-2551

  Ramanathan, Arvind ^a   Savol, Andrej J ^b,c   Agarwal, Pratul K ^a   Chennubhotla, Chakra S ^c  

^a OAK RIDGE NATIONAL LABORATORY   (United States)

^b CARNEGIE MELLON UNIVERSITY   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Adenylate kinase; Anharmonic motions; Molecular dynamics; Principal component analysis; Quasi anharmonic analysis

Indexed keywords

ADENYLATE KINASE;

ARTICLE; BINDING SITE; CONFORMATION; HYDROGEN BOND; HYDROPHOBICITY; MOLECULAR DYNAMICS; ONLINE ANALYSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; QUASI ANHARMONIC ANALYSIS; SIMULATION; STATISTICAL ANALYSIS; STRUCTURE ANALYSIS;

ADENYLATE KINASE; BINDING SITES; ESCHERICHIA COLI; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY;

EID: 84867216105     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24135     Document Type: Article

References (75)

1. Karplus M, McCammon JA. Molecular dynamics simulations of biomolecules. Nat Struct Biol 2002; 9: 646-652.
2. Bowers KJ, Chow E, Xu H, Dror RO, Eastwood MP, Gregersen BA, Klepeis JL, Kolossvary I, Moraes MA, Sacerdoti FD, Salmon JK, Shan Y, Shaw DE. Scalable algorithms for molecular dynamics simulations on commodity clusters. In SC '06: Proceedings of the 2006 ACM/IEEE Conference on Supercomputing, New York, NY; 2006. p 43.
3. Shaw DE, Deneroff MM, Dror RO, Kuskin JS, Larson RH, Salmon JK, Young C, Batson B, Bowers KJ, Chao JC, Eastwood MP, Gagliardo J, Grossman JP, Ho CR, Ierardi DJ, Kolossva ́ry I, Klepeis JL, Layman T, McLeavey C, Moraes MA, Mueller R, Priest EC, Shan Y, Spengler J, Theobald M, Towles B, Wang SC. Anton, a special-purpose machine for molecular dynamics simulation. SIGARCH Comp Arch News 2007; 35: 1-12.
4. Elsen E, Houston M, Vishal V, Darve E, Hanrahan P, Pande V. N-body simulation on gpus. In SC '06: Proceedings of the 2006 ACM/IEEE Conference on Supercomputing, New York, NY; 2006. p 188.
5. Hampton S, Agarwal PK, Alam SR, Crozier PS. Towards microsecond biological molecular dynamics simulations on hybrid processors. Presented at the International Conference on High Performance Computing and Simulation (HPCS), Caen, France; 2010. pp 98-107.
6. van der Kamp MW, Schaeffer RD, Jonsson AL, Scouras AD, Simms AM, Toofanny RD, Benson NC, Anderson PC, Merkley ED, Rysavy S, Bromley D, Beck DA, Daggett V. Dynameomics: a comprehensive database of protein dynamics. Structure 2010; 18: 423-435.
7. Pande VS, Baker I, Chapman J, Elmer SP, Khaliq S, Larson SM, Rhee YM, Shirts MR, Snow C, Sorin EJ, Zagrovic B. Atomistic protein folding simulations on the submillisecond time scale using worldwide distributed computing. Biopolymers 2003; 68: 91-109.
8. van Gunsteren W, Bakowies D, Baron R, Chandrasekhar I, Christen M, Daura X, Gee P, Geerke D, Glattli A, Hunenberger P, Kastenholz M, Oostenbrink C, Schenk M, Trzesniak D, van der Vegt N, Yu H. Biomolecular modeling: goals, problems, perspectives. Angew Chem Int Ed Engl 2006; 45: 4064-4092.
9. Amadei A, Lissen ABM, Berendsen HJC. Essential dynamics of proteins. Proteins 1993; 17: 412-425.
10. Karplus M, Kushick JN. Method for estimating the configurational entropy of macro-molecules. Macromolecules 1981; 14: 325-332.
11. Maisuradze GG, Liwo A, Scheraga HA. Principal component analysis for protein folding dynamics. J Mol Biol 2009; 385: 312-329.
12. Ramanathan A, Agarwal PK. Evolutionarily conserved linkage between enzyme fold, flexibility, and catalysis. PLoS Biol 2011; 9: e1001193.
13. Chang CA, Chen W, Gilson MK. Ligand configurational entropy and protein binding. Proc Natl Acad Sci USA 2007; 104: 1534-1539.
14. Das P, Moll M, Stamati H, Kavraki LE, Clementi C. Low-dimensional free-energy landscapes of protein-folding reactions by nonlinear dimensionality reduction. Proc Natl Acad Sci USA 2006; 103: 9885-9890.
15. Shao J, Tanner S, Thompson N, Cheatham T. Clustering molecular dynamics trajectories. I. Characterizing the performance of different clustering algorithms. J Chem Theory Comput 2007; 3: 2312-2334.
16. Noe F, Horenko I, Schutte C, Smith J. Hierarchical analysis of conformational dynamics in biomolecules: transition networks of metastable states. J Chem Phys 2007; 126: 155102.
17. Muff S, Caflisch A. Kinetic analysis of molecular dynamics simulations reveals changes in the denatured state and switch of folding pathways upon single-point mutation of a b-sheet miniprotein. Proteins 2008; 70: 1185-1195.
18. Deng N-J, Zheng W, Gallicchio E, Levy RM. Insights into the dynamics of hiv-1 protease: a kinetic network model constructed from atomistic simulations. J Am Chem Soc 2011; 133: 9387-9394.
19. Bowman GR, Beauchamp KA, Boxer G, Pande VS. Progress and challenges in the automated construction of Markov state models for full protein systems. J Chem Phys 2009; 131: 124101.
20. Wriggers W, Stafford KA, Shan Y, Piana S, Maragakis P, Lindorff-Larsen K, Miller PJ, Gullingsrud J, Rendleman CA, Eastwood MP, Dror RO, Shaw DE. Automated event detection and activity monitoring in long molecular dynamics simulations. J Chem Theory Comput 2009; 5: 2595-2605.
21. Ramanathan A, Yoo JO, Langmead CJ. On-the-fly identification of conformational sub-states from molecular dynamics simulations. J Chem Theory Comput 1011; 7: 778-789.
22. Frauenfelder H, Parak F, Young RD. Conformational sub-states in proteins. Annu Rev Biophys Biophys Chem 1988; 17: 451-479.
23. Northrup SH, Pearl MR, Morgan JD, McCammon JA, Karplus M. Molecular dynamics of ferrocytochrome c: magnitude and anisotropy of atomic displacements. J Mol Biol 1981; 153: 1087-1111.
24. Doster W, Cusack S, Petry W. Dynamical transition of myoglobin revealed by inelastic neutron scattering. Nature 1989; 337: 754-756.
25. Hayward S, Kitao A, Go N. Harmonicity and anharmonicity in protein dynamics: a normal mode analysis and principal component analysis. Proteins 1995; 23: 177-186.
26. Rasmussen BF, Stock AM, Ringe D, Petsko GA. Crystalline ribonuclease a loses function below the dynamical transition at 220 k. Nature 1992; 357: 423-424.
27. Ferrand M, Dianoux AJ, Petry W, Zaccaï G. Thermal motions and function of bacteriorhodopsin in purple membranes: effects of temperature and hydration studied by neutron scattering. Proc Natl Acad Sci USA 1993; 90: 9668-9672.
28. Ichiye T, Karplus M. Anisotropy and anharmonicity of atomic fluctuations in proteins: analysis of a molecular dynamics simulation. Proteins 1987; 2: 236-259.
29. Ichiye T, Karplus M. Anisotropy and anharmonicity of atomic fluctuations in proteins: implications for x-ray analysis. Biochemistry 1988; 27: 3487-3497.
30. Frauenfelder H, Petsko GA, Tsernoglou D. Temperature-dependent x-ray diffraction as a probe of protein structural dynamics. Nature 1979; 280: 558-563.
31. Frauenfelder H, Sligar S, Wolynes P. The energy landscapes and motions of proteins. Science 1991; 254: 1598-1603.
32. Ramanathan A, Savol AJ, Langmead CJ, Agarwal PK, Chennubhotla CS. Discovering conformational sub-states relevant to protein function. PLoS One 2011; 6: e15827.
33. Henzler-Wildman KA, Lei M, Thai V, Kerns SJ, Karplus M, Kern D. A hierarchy of time-scales in protein dynamics is linked to enzyme catalysis. Nature 2007; 450: 913-916.
34. Temiz NA, Meirovitch E, Bahar I. Escherichia coli adenylate kinase dynamics: comparison of elastic network model modes with mode-coupling (15)N-NMR relaxation data. Proteins 2004; 57: 468-480.
35. Schlauderer G, Reinstein J, Schulz G. Adenylate kinase motions during catalysis: an energetic counterweight balancing substrate binding. Structure 1996; 4: 147-156.
36. Reinstein J, Vetter IR, Schlichting I, Roesch P, Wittinghofer A, Goody RS. Fluorescence and NMR investigations on the ligand binding properties of adenylate kinases. Biochemistry 1990; 29: 7440-7450.
37. Pontiggia F, Zen A, Micheletti C. Small- and large-scale conformational changes of adenylate kinase: a molecular dynamics study of the subdomain motion and mechanics. Biophys J 2008; 95: 5901-5912.
38. Maragakis P, Karplus M. Large amplitude conformational change in proteins explored with a plastic network model: adenylate kinase. J Mol Biol 2005; 352: 807-822.
39. Korkut A, Hendrickson W. Computation of conformational transitions in proteins by virtual atom molecular mechanics as validated in application to adenylate kinase. Proc Natl Acad Sci USA 2009; 106: 15673.
40. Hanson JA, Duderstadt K, Watkins LP, Bhattacharyya S, Brokaw J, Chu J-W, Yang H. Illuminating the mechanistic roles of enzyme conformational dynamics. Proc Natl Acad Sci USA 2007; 104: 18055-18060.
41. Daily MD, Phillips GN, Cui Q. Many local motions cooperate to produce the adenylate kinase conformational transition. J Mol Biol 2010; 400: 618-631.
42. Cukier R. Apo adenylate kinase encodes its holo form: a principal component and varimax analysis. J Phys Chem B 2009; 113: 1662-1672.
43. Beckstein O, Denning EJ, Perilla JR, Woolf TB. Zipping and unzipping of adenylate kinase: atomistic insights into the ensemble of open< -- >closed transitions. J Mol Biol 2009; 394: 160-176.
44. Adén J, Wolf-Watz M. NMR identification of transient complexes critical to adenylate kinase catalysis. J Am Chem Soc 2007; 129: 14003-14012.
45. Whitford PC, Gosavi S, Onuchic JN. Conformational transitions inadenylate kinase. Allosteric communication reduces misligation. J Biol Chem 2008; 283: 2042-2048.
46. Kaminski GA, Friesner RA, Tirado-Rives J, Jorgensen WL. Evaluation and reparametrization of the opls-aa force field for proteins via comparison with accurate quantum chemical calculations on peptides. J Phys Chem B 2001; 105: 6474-6487.
47. Muller CW, Schulz GE. Structure of the complex between adenylate kinase from Escherichia coli and the inhibitor ap5a refined at 1.9 resolution: a model for a catalytic transition state. J Mol Biol 1992; 224: 159-177.
48. Muller C, Schlauderer G, Reinstein J, Schulz G. Adenylate kinase motions during catalysis: an energetic counterweight balancing substrate binding. Structure 1996; 4: 147-156.
49. Berweger CD, van Gunsteren WF, Müller-Plathe F. Force field parametrization by weak coupling. Re-engineering spc water. Chem Phys Lett 1995; 232: 429-436.
50. Ramanathan A, Agarwal PK. Computational identification of slow conformational fluctuations in proteins. J Phys Chem B 2009; 113: 11169-11180.
51. Krautler V, van Gunsteren WF, Hünenberger P. A fast shake algorithm to solve distance constraint equations for small molecules in molecular dynamics simulations. J Comput Chem 2001; 22: 501-508.
52. Plimpton S, Pollock R, Stevens M. Particle-mesh Ewald and rRESPA for parallel molecular dynamics simulations. In: Proceedings of the 8th SIAM Conference on Parallel Processing for Scientific Computing, Minneapolis, MN; 1997.
53. Kong Y, Karplus M. Signaling pathways of pdz2 domain: a molecular dynamics interaction correlation analysis. Proteins 2009; 74: 145-154.
54. Kabsch W. A solution for the best rotation to relate two sets of vectors. Acta Crystallogr 1976; 32: 922-923.
55. Hample FR, Ronchetti EM, Rousseeuw PJ, Stahel WA. Robust statistics: the approach based on influence functions. New York: Wiley; 1986.
56. Zemla A. Lga: a method for finding 3d similarities in protein structures. Nucleic Acids Res 2003; 31: 3370-3374.
57. Theobald D, Wuttke D. Empirical Bayes hierarchical models for regularizing maximum likelihood estimation in the matrix Gaussian Procrustes problem. Proc Natl Acad Sci USA 2006; 103: 18521-18527.
58. Wu D, Wu Z. Superimposition of protein structures with dynamically weighted rmsd. J Mol Model 2009; 16: 211-222.
59. Liu Y, Fang Y, Ramani K. Using least median of squares for structural superposition of flexible proteins. BMC Bioinformatics 2009; 10: 29.
60. Mechelke M, Habeck M. Robust probabilistic superposition and comparison of protein structures. BMC Bioinformatics 2010; 11: 363.
61. Damm KL, Carlson HA. Gaussian-weighted rmsd superposition of proteins: a structural comparison for flexible proteins and predicted protein structures. Biophys J 2006; 90: 4558-4573.
62. Jepson AD, Fleet DJ, El-Maraghi TF. Robust online appearance models for visual tracking. IEEE Trans PAMI 2003; 25: 1296-1311.
63. Cardoso J-F. High-order contrasts for independent component analysis. Neural Comput 1999; 11: 157-192.
64. Oja E, Hyvarinen A. Independent component analysis: algorithms and applications. Neural Netw 2000; 13: 411-430.
65. McLachlan G, Basford K. Mixture models: inference and applications to clustering, Vol. 84 (Statistics: A Series of Textbooks and Monographs). New York: Marcel Dekker; 1988.
66. Brokaw JB, Chu J-W. On the roles of substrate binding and hinge unfolding in conformational changes of adenylate kinase. Biophys J 2010; 99: 3420-3429.
67. Müller CW, Schulz GE. Crystal structures of two mutants of adenylate kinase from Escherichia coli that modify the gly-loop. Proteins 1993; 15: 42-49.
68. Berry MB, Bae E, Bilderback TR, Glaser M, Phillips GN. Crystal structure of adp/amp complex of Escherichia coli adenylate kinase. Proteins 2006; 62: 555-556.
69. Wolf-Watz M, Thai V, Henzler-Wildman K, Hadjipavlou G, Eisenmesser EZ, Kern D. Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair. Nat Struct Mol Biol 2004; 11: 945-949.
70. Henzler-Wildman K, Kern D. Dynamic personalities of proteins. Nature 2007; 450: 964-972.
71. Olsson U, Wolf-Watz M. Overlap between folding and functional energy landscapes for adenylate kinase conformational change. Nat Commun 2010; 1: 11.
72. Miyashita O, Onuchic JN, Wolynes PG. Nonlinear elasticity, proteinquakes, and the energy landscapes of functional transitions in proteins. Proc Natl Acad Sci USA 2003; 100: 12570-12575.
73. Rundqvist L, Adén J, Sparrman T, Wallgren M, Olsson U, Wolf-Watz M. Noncooperative folding of subdomains in adenylate kinase. Biochemistry 2009; 48: 1911-1927.
74. Berry MB, Phillips GN, Jr. Crystal structures of bacillus stearothermophilus adenylate kinase with bound ap5a, mg2+ ap5a, and mn2+ ap5a reveal an intermediate lid position and six coordinate octahedral geometry for bound mg2+ and mn2+. Proteins 1998; 32: 276-288.
75. Savol AJ, Burger VM, Agarwal PK, Ramanathan A, Chennubhotla CS. QAARM: quasi-anharmonic autoregressive model reveals molecular recognition pathways in ubiquitin. Bioinformatics 2011; 27: i52-i60.