Modeling conformational ensembles of slow functional motions in pin1-WW

PLoS Computational Biology

Volumn 6, Issue 12, 2010, Pages

  Morcos, Faruck ^a,b   Chatterjee, Santanu ^a,b   McClendon, Christopher L ^c   Brenner, Paul R ^d   López Rendón, Roberto ^e   Zintsmaster, John ^d   Ercsey Ravasz, Maria ^a,d   Sweet, Christopher R ^a,d   Jacobson, Matthew P ^c   Peng, Jeffrey W ^d   Izaguirre, Jesús A ^a,b  

^a Interdisciplinary Center for Network Science and Applications   (United States)

^b University of Notre Dame   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF NOTRE DAME   (United States)

^e UNIVERSIDAD AUTÓNOMA DEL ESTADO DE MÉXICO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

FREE ENERGY; NUCLEAR MAGNETIC RESONANCE; PROTEINS;

CONFORMATIONAL DYNAMICS; CONFORMATIONAL ENSEMBLE; FUNCTIONAL MOTIONS; MACROSTATES; MARKOV STATE MODELS; NMR RELAXATION; PROTEIN-PROTEIN INTERACTIONS; RELAXATION STUDIES; TIME-SCALES; WW DOMAIN;

DYNAMICS;

PEPTIDYLPROLYL ISOMERASE PIN1; APOENZYME; NIMA INTERACTING PEPTIDYLPROLYL ISOMERASE; NIMA-INTERACTING PEPTIDYLPROLYL ISOMERASE; PEPTIDYLPROLYL ISOMERASE;

ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME SUBSTRATE COMPLEX; HYDROGEN BOND; MARKOV STATE MODEL; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; NUCLEAR MAGNETIC RESONANCE; PROTEIN PROTEIN INTERACTION; SIMULATION; BIOLOGY; CHEMISTRY; HUMAN; METABOLISM; METHODOLOGY; PROBABILITY; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE;

APOENZYMES; COMPUTATIONAL BIOLOGY; HUMANS; HYDROGEN BONDING; MARKOV CHAINS; MOLECULAR DYNAMICS SIMULATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDYLPROLYL ISOMERASE; PROTEIN CONFORMATION; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY;

EID: 78651242947     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1001015     Document Type: Article

References (52)

1. Pawson T, Nash P (2003) Assembly of cell regulatory systems through protein interaction domains. Science 300: 445-452.
2. Mittermaier A, Kay LE (2006) New tools provide new insights in nmr studies of protein dynamics. Science 312: 224-228.
3. Palmer AG, Massi F (2006) Characterization of the dynamics of biomacromolecules using rotating-frame spin relaxation nmr spectroscopy. Chem Rev 106: 1700-1719.
4. Vallurupalli P, Hansen DF, Kay LE (2008) Structures of invisible, excited protein states by relaxation dispersion nmr spectroscopy. Proc Natl Acad Sci U S A 105: 11766-11771.
5. Bouvignies G, Bernad P, Meier S, Cho K, Grzesiek S, et al. (2005) Identification of slow correlated motions in proteins using residual dipolar and hydrogen-bond scalar couplings. Proc Natl Acad Sci U S A 102: 13885-13890.
6. Früh D, Tolman JR, Bodenhausen G, Zwahlen C (2001) Cross-correlated chemical shift modulation: a signature of slow internal motions in proteins. J Am Chem Soc 123: 4810-4816.
7. Palmer AG (2004) NMR characterization of the dynamics of biomacromolecules. Chem Rev 104: 3623-3640.
8. Kay LE (2005) NMR studies of protein structure and dynamics. J Magn Reson 173: 193-207.
9. Blackledge MJ, Brüschweiler R, Griesinger C, Schmidt JM, Xu P, et al. (1993) Conformational backbone dynamics of the cyclic decapeptide antamanide. Application of a new multiconformational search algorithm based on NMR data. Biochemistry 32: 10960-10974.
10. Grey MJ, Wang C, Palmer AG (2003) Disulfide bond isomerization in basic pancreatic trypsin inhibitor: multisite chemical exchange quantified by CPMG relaxation dispersion and chemical shift modeling. J Am Chem Soc 125: 14324-14335.
11. Lange OF, Grubmüller H, de Groot BL (2005) Molecular dynamics simulations of protein G challenge NMR-derived correlated backbone motions. Angew Chem Int Ed Engl 44: 3394-3399.
12. Lakomek NA, Walter KFA, Farès C, Lange OF, de Groot BL, et al. (2008) Selfconsistent residual dipolar coupling based model-free analysis for the robust determination of nanosecond to microsecond protein dynamics. J Biomol NMR 41: 139-155.
13. Lange OF, Lakomek NA, Fares C, Schröder GF, Walter KFA, et al. (2008) Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science 320: 1471-1475.
14. Markwick PRL, Bouvignies G, Salmon L, McCammon JA, Nilges M, et al. (2009) Toward a unified representation of protein structural dynamics in solution. J Am Chem Soc 131: 16968-16975.
15. Fersht AR (2002) On the simulation of protein folding by short time scale molecular dynamics and distributed computing. Proc Natl Acad Sci U S A 99: 14122-14125.
16. Huang X, Bowman GR, Bacallado S, Pande VS (2009) Rapid equilibrium sampling initiated from nonequilibrium data. Proc Natl Acad Sci U S A 106: 19765-19769.
17. Noé F, Schütte C, Vanden-Eijnden E, Reich L, Weikl TR (2009) Constructing the equilibrium ensemble of folding pathways from short off-equilibrium simulations. Proc Natl Acad Sci U S A 106: 19011-19016.
18. Andrec M, Felts AK, Gallicchio E, Levy RM (2005) Protein folding pathways from replica exchange simulations and a kinetic network model. Proc Natl Acad Sci U S A 102: 6801-6806.
19. Ilsley JL, Sudol M, Winder SJ (2002) The WW domain: linking cell signalling to the membrane cytoskeleton. Cell Signal 14: 183-189.
20. Sudol M, Hunter T (2000) New wrinkles for an old domain. Cell 103: 1001-1004.
21. Jäger M, Zhang Y, Bieschke J, Nguyen H, Dendle M, et al. (2006) Structurefunction- folding relationship in a WW domain. Proc Natl Acad Sci U S A 103: 10648-10653.
22. Peng T, Zintsmaster JS, Namanja AT, Peng JW (2007) Sequence-specific dynamics modulate recognition specificity in WW domains. Nat Struct Mol Biol 14: 325-331.
23. Bakan A, Bahar I (2009) The intrinsic dynamics of enzymes plays a dominant role in determining the structural changes induced upon inhibitor binding. Proc Natl Acad Sci U S A 106: 14349-14354.
24. Lipari G, Szabo A (1982) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J Am Chem Soc 104: 4546-4559.
25. Akke M, Palmer A (1996) Monitoring macromolecular motions on microsecondmillisecond times scales fo R1 - R1 constant-relaxation-time NMR spectroscopy. J Am Chem Soc 118: 911-912.
26. Neal S, Nip AM, Zhang H, Wishart DS (2003) Rapid and accurate calculation of protein 1h, 13c and 15n chemical shifts. J Biomol NMR 26: 215-240.
27. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781-1802.
28. Bowman GR, Huang X, Pande VS (2009) Using generalized ensemble simulations and Markov state models to identify conformational states. Methods 49: 197-201.
29. 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.
30. Chodera JD, Singhal N, Pande VS, Dill KA, Swope WC (2007) Automatic discovery of metastable states for the construction of Markov models of macromolecular conformational dynamics. J Chem Phys 126: 155101.
31. McClendon CL, Friedland G, Mobley DL, Amirkhani H, Jacobson MP (2009) Quantifying correlations between allosteric sites in thermodynamic ensembles. J Chem Theory Comput 9: 2486-2502.
32. Wales DJ, Scheraga HA (1999) Global optimization of clusters, crystals, and biomolecules. Science 285: 1368-1372.
33. Bryngelson JD, Onuchic JN, Socci ND, Wolynes PG (1995) Funnels, pathways, and the energy landscape of protein folding: a synthesis. Proteins 21: 167-195.
34. Ma H, Gruebele M (2006) Low barrier kinetics: dependence on observables and free energy surface. J Comput Chem 27: 125-134.
35. Freeman LC (1977) A set of measures of centrality based on betweenness. Sociometry 40: 35-41.
36. Metzner P, Schütte C, Vanden-Eijnden E (2009) Transition path theory for Markov jump processes. Multiscale Model Simul 7: 1192-1219.
37. Bowman GR, Ensign DL, Pande VS (2010) Enhanced modeling via network theory: Adaptive sampling of Markov State Models. J Chem Theory Comput 6: 787-794.
38. Bowman GR, Pande VS (2010) Protein folded states are kinetic hubs. Proc Natl Acad Sci U S A 107: 10890-10895.
39. Cover T, Thomas J (2006) Elements of Information Theory. New Jersey: John Wiley and Sons. 19 p.
40. Ulrich EL, Akutsu H, Doreleijers JF, Harano Y, Ioannidis YE, et al. (2007) BioMagResBank. Nucleic Acids Res 36: D402-D408.
41. Zagrovic B, Gattin Z, Lau JKC, Huber M, van Gunsteren WF (2008) Structure and dynamics of two beta-peptides in solution from molecular dynamics simulations validated against experiment. Eur Biophys J 37: 903-912.
42. Kony DB, Hnenberger PH, van Gunsteren WF (2007) Molecular dynamics simulations of the native and partially folded states of ubiquitin: influence of methanol cosolvent, pH, and temperature on the protein structure and dynamics. Protein Sci 16: 1101-1118.
43. Merkley ED, Bernard B, Daggett V (2008) Conformational changes below the Tm: molecular dynamics studies of the thermal pretransition of ribonuclease A. Biochemistry 47: 880-892.
44. Agarwal PK, Billeter SR, Rajagopalan PTR, Benkovic SJ, Hammes-Schiffer S (2002) Network of coupled promoting motions in enzyme catalysis. Proc Natl Acad Sci U S A 99: 2794-2799.
45. Rod TH, Radkiewicz JL, Brooks CL (2003) Correlated motion and the effect of distal mutations in dihydrofolate reductase. Proc Natl Acad Sci U S A 100: 6980-6985.
46. Ranganathan R, Lu KP, Hunter T, Noel JP (1997) Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent. Cell 89: 875-886.
47. Wintjens R, Wieruszeski JM, Drobecq H, Rousselot-Pailley P, Bue L, et al. (2001) 1H NMR study on the binding of Pin1 Trp-Trp domain with phosphothreonine peptides. J Biol Chem 276: 25150-25156.
48. Lange OF, Grubmüller H (2006) Generalized correlation for biomolecular dynamics. Proteins: Structure, Function, and Bioinformatics 62: 1053-1061.
49. Namanja AT, Peng T, Zintsmaster JS, Elson AC, Shakour MG, et al. (2007) Substrate recognition reduces side-chain flexibility for conserved hydrophobic residues in human Pin1. Structure 15: 313-327.
50. Jacobs DM, Saxena K, Vogtherr M, Bernado P, Pons M, et al. (2003) Peptide binding induces large scale changes in inter-domain mobility in human Pin1. J Biol Chem 278: 26174-26182.
51. Daum S, Lücke C, Wildemann D, Schiene-Fischer C (2007) On the benefit of bivalency in peptide ligand/Pin1 interactions. J Mol Biol 374: 147-161.
52. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504.