Ensemble modeling of protein disordered states: Experimental restraint contributions and validation

Proteins: Structure, Function and Bioinformatics

Volumn 80, Issue 2, 2012, Pages 556-572

  Marsh, Joseph A ^a,b,c   Forman Kay, Julie D ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Drk SH3; Inhibitor 2; Intrinsically disordered; NMR; SAXS; Sic1; Unfolded state

Indexed keywords

ARTICLE; CONTROLLED STUDY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; RADIATION SCATTERING; VALIDATION PROCESS; ALGORITHM; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER PROGRAM; MONTE CARLO METHOD; NUCLEAR MAGNETIC RESONANCE; PROCEDURES; PROTEIN CONFORMATION; PROTEIN FOLDING; REPRODUCIBILITY; SMALL ANGLE SCATTERING; SRC HOMOLOGY DOMAIN; X RAY DIFFRACTION;

CYCLIN DEPENDENT KINASE INHIBITOR; PROTEIN; PROTEIN PHOSPHATASE INHIBITOR-2; SACCHAROMYCES CEREVISIAE PROTEIN; SIC1 PROTEIN, S CEREVISIAE; TRYPTOPHAN;

ALGORITHMS; COMPUTATIONAL BIOLOGY; CYCLIN-DEPENDENT KINASE INHIBITOR PROTEINS; MODELS, MOLECULAR; MONTE CARLO METHOD; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEINS; REPRODUCIBILITY OF RESULTS; SACCHAROMYCES CEREVISIAE PROTEINS; SCATTERING, SMALL ANGLE; SOFTWARE; SRC HOMOLOGY DOMAINS; TRYPTOPHAN; X-RAY DIFFRACTION;

EID: 84855711579     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.23220     Document Type: Article

References (64)

1. Wright PE, Dyson HJ. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J Mol Biol 1999; 293: 321-331.
2. Gsponer J, Babu MM. The rules of disorder or why disorder rules. Prog Biophys Mol Biol 2009; 99: 94-103.
3. Uversky VN, Gillespie JR, Fink AL. Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 2000; 41: 415-427.
4. Dunker AK, Lawson JD, Brown CJ, Williams RM, Romero P, Oh JS, Oldfield CJ, Campen AM, Ratliff CM, Hipps KW, Ausio J, Nissen MS, Reeves R, Kang C, Kissinger CR, Bailey RW, Griswold MD, Chiu W, Garner EC, Obradovic Z. Intrinsically disordered protein. J Mol Graph Model 2001; 19: 26-59.
5. Wright PE, Dyson HJ. Linking folding and binding. Curr Opin Struct Biol 2009; 19: 31-38.
6. Mittag T, Kay LE, Forman-Kay JD. Protein dynamics and conformational disorder in molecular recognition. J Mol Recognit 2010; 23: 105-116.
7. Bienkiewicz EA, Adkins JN, Lumb KJ. Functional consequences of preorganized helical structure in the intrinsically disordered cell-cycle inhibitor p27(kip1). Biochemistry 2002; 41: 752-759.
8. Baker JMR, Hudson RP, Kanelis V, Choy WY, Thibodeau PH, Thomas PJ, Forman-Kay JD. Cftr regulatory region interacts with nbd1 predominantly via multiple transient helices. Nat Struct Mol Biol 2007; 14: 738-745.
9. Eliezer D. Biophysical characterization of intrinsically disordered proteins. Curr Opin Struct Biol 2009; 19: 23-30.
10. Sugase K, Dyson HJ, Wright PE. Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 2007; 447: 1021-1025.
11. Mittag T, Forman-Kay JD. Atomic-level characterization of disordered protein ensembles. Curr Opin Struct Biol 2007; 17: 3-14.
12. Fisher CK, Stultz CM. Constructing ensembles for intrinsically disordered proteins. Curr Opin Struct Biol 2011; 21: 426-431.
13. Jensen MR, Markwick PR, Meier S, Griesinger C, Zweckstetter M, Grzesiek S, Bernadó P, Blackledge M. Quantitative determination of the conformational properties of partially folded and intrinsically disordered proteins using nmr dipolar couplings. Structure 2009; 17: 1169-1185.
14. Allison JR, Varnai P, Dobson CM, Vendruscolo M. Determination of the free energy landscape of alpha-synuclein using spin label nuclear magnetic resonance measurements. J Am Chem Soc 2009; 131: 18314-18326.
15. Dedmon MM, Lindorff-Larsen K, Christodoulou J, Vendruscolo M, Dobson CM. Mapping long-range interactions in alpha-synuclein using spin-label NMR and ensemble molecular dynamics simulations. J Am Chem Soc 2005; 127: 476-477.
16. Francis CJ, Lindorff-Larsen K, Best RB, Vendruscolo M. Characterization of the residual structure in the unfolded state of the delta131delta fragment of staphylococcal nuclease. Proteins 2006; 65: 145-152.
17. Lowry DF, Stancik A, Shrestha RM, Daughdrill GW. Modeling the accessible conformations of the intrinsically unstructured transactivation domain of p53. Proteins 2008; 71: 587-598.
18. Esteban-Martín S, Fenwick RB, Salvatella X. Refinement of ensembles describing unstructured proteins using NMR residual dipolar couplings. J Am Chem Soc 2010; 132: 4626-4632.
19. Huang JR, Grzesiek S. Ensemble calculations of unstructured proteins constrained by rdc and pre data: a case study of urea-denatured ubiquitin. J Am Chem Soc 2010; 132: 694-705.
20. Jha AK, Colubri A, Freed KF, Sosnick TR. Statistical coil model of the unfolded state: resolving the reconciliation problem. Proc Natl Acad Sci USA 2005; 102: 13099-13104.
21. Bernadó P, Blanchard L, Timmins P, Marion D, Ruigrok RW, Blackledge M. A structural model for unfolded proteins from residual dipolar couplings and small-angle x-ray scattering. Proc Natl Acad Sci USA 2005; 102: 17002-17007.
22. Nodet G, Salmon L, Ozenne V, Meier S, Jensen MR, Blackledge M. Quantitative description of backbone conformational sampling of unfolded proteins at amino acid resolution from NMR residual dipolar couplings. J Am Chem Soc 2009; 131: 17908-17918.
23. Salmon L, Nodet G, Ozenne V, Yin G, Jensen MR, Zweckstetter M, Blackledge M. NMR characterization of long-range order in intrinsically disordered proteins. J Am Chem Soc 2010; 132: 8407-8418.
24. Jensen MR, Salmon L, Nodet G, Blackledge M. Defining conformational ensembles of intrinsically disordered and partially folded proteins directly from chemical shifts. J Am Chem Soc 2010; 132: 1270-1272.
25. Fisher CK, Huang A, Stultz CM. Modeling intrinsically disordered proteins with bayesian statistics. J Am Chem Soc 2010; 132: 14919-14927.
26. Krzeminski M, Fuentes G, Boelens R, Bonvin AMJJ. Minoes: a new approach to select a representative ensemble of structures in NMR studies of (partially) unfolded states. application to delta25-pyp. Proteins 2009; 74: 895-904.
27. Marsh JA, Neale C, Jack FE, Choy WY, Lee AY, Crowhurst KA, Forman-Kay JD. Improved structural characterizations of the drkn sh3 domain unfolded state suggest a compact ensemble with native-like and non-native structure. J Mol Biol 2007; 367: 1494-1510.
28. Marsh JA, Forman-Kay JD. Structure and disorder in an unfolded state under nondenaturing conditions from ensemble models consistent with a large number of experimental restraints. J Mol Biol 2009; 391: 359-374.
29. Choy WY, Forman-Kay JD. Calculation of ensembles of structures representing the unfolded state of an sh3 domain. J Mol Biol 2001; 308: 1011-1032.
30. Pinheiro AS, Marsh JA, Forman-Kay JD, Peti W. Structural signature of the mypt1-pp1 interaction. J Am Chem Soc 2011; 133: 73-80.
31. Marsh JA, Dancheck B, Ragusa MJ, Allaire M, Forman-Kay JD, Peti W. Structural diversity in free and bound states of intrinsically disordered protein phosphatase 1 regulators. Structure 2010; 18: 1094-1103.
32. Mittag T, Marsh J, Grishaev A, Orlicky S, Lin H, Sicheri F, Tyers M, Forman-Kay JD. Structure/function implications in a dynamic complex of the intrinsically disordered sic1 with the cdc4 subunit of an scf ubiquitin ligase. Structure 2010; 18: 494-506.
33. Crowhurst KA, Tollinger M, Forman-Kay JD. Cooperative interactions and a non-native buried trp in the unfolded state of an sh3 domain. J Mol Biol 2002; 322: 163-178.
34. Bezsonova I, Evanics F, Marsh JA, Forman-Kay JD, Prosser RS. Oxygen as a paramagnetic probe of clustering and solvent exposure in folded and unfolded states of an sh3 domain. J Am Chem Soc 2007; 129: 1826-1835.
35. Bezsonova I, Singer A, Choy W-Y, Tollinger M, Forman-Kay JD. Structural comparison of the unstable drkn sh3 domain and a stable mutant. Biochemistry 2005; 44: 15550-15560.
36. Evanics F, Bezsonova I, Marsh J, Kitevski JL, Forman-Kay JD, Prosser RS. Tryptophan solvent exposure in folded and unfolded states of an sh3 domain by 19f and 1h NMR. Biochemistry 2006; 45: 14120-14128.
37. Crowhurst KA, Forman-Kay JD. Aromatic and methyl noes highlight hydrophobic clustering in the unfolded state of an sh3 domain. Biochemistry 2003; 42: 8687-8695.
38. Choy WY, Mulder FA, Crowhurst KA, Muhandiram DR, Millett IS, Doniach S, Forman-Kay JD, Kay LE. Distribution of molecular size within an unfolded state ensemble using small-angle x-ray scattering and pulse field gradient NMR techniques. J Mol Biol 2002; 316: 101-112.
39. Zhang O, Forman-Kay JD. Structural characterization of folded and unfolded states of an sh3 domain in equilibrium in aqueous buffer. Biochemistry 1995; 34: 6784-6794.
40. Chevelkov V, Xue Y, Rao DK, Forman-Kay JD, Skrynnikov NR. 15n h/d-solexsy experiment for accurate measurement of amide solvent exchange rates: application to denatured drkn sh3. J Biomol NMR 2010; 46: 227-244.
41. Nash P, Tang X, Orlicky S, Chen Q, Gertler FB, Mendenhall MD, Sicheri F, Pawson T, Tyers M. Multisite phosphorylation of a cdk inhibitor sets a threshold for the onset of DNA replication. Nature 2001; 414: 514-521.
42. Mittag T, Orlicky S, Choy WY, Tang X, Lin H, Sicheri F, Kay LE, Tyers M, Forman-Kay JD. Dynamic equilibrium engagement of a polyvalent ligand with a single-site receptor. Proc Natl Acad Sci USA 2008; 105: 17772-17777.
43. Dancheck B, Nairn AC, Peti W. Detailed structural characterization of unbound protein phosphatase 1 inhibitors. Biochemistry 2008; 47: 12346-12356.
44. Marsh JA, Singh VK, Jia Z, Forman-Kay JD. Sensitivity of secondary structure propensities to sequence differences between alpha- and gamma-synuclein: implications for fibrillation. Protein Sci 2006; 15: 2795-2804.
45. Wishart DS, Sykes BD, Richards FM. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J Mol Biol 1991; 222: 311-333.
46. Neal S, Nip AM, Zhang H, Wishart DS. Rapid and accurate calculation of protein 1h, 13c and 15n chemical shifts. J Biomol NMR 2003; 26: 215-240.
47. Vuister GW, Bax A. Quantitative j correlation: a new approach for measuring homonuclear three-bond j(hnh.alpha.) coupling constants in 15n-enriched proteins. J Am Chem Soc 1993; 115: 7772-7777.
48. Marsh JA, Baker JMR, Tollinger M, Forman-Kay JD. Calculation of residual dipolar couplings from disordered state ensembles using local alignment. J Am Chem Soc 2008; 130: 7804-7805.
49. Klein-Seetharaman J, Oikawa M, Grimshaw SB, Wirmer J, Duchardt E, Ueda T, Imoto T, Smith LJ, Dobson CM, Schwalbe H. Long-range interactions within a nonnative protein. Science 2002; 295: 1719-1722.
50. Zhang F, Brüschweiler R. Contact model for the prediction of NMR n-h order parameters in globular proteins. J Am Chem Soc 2002; 124: 12654-12655.
51. Battiste JL, Wagner G. Utilization of site-directed spin labeling and high-resolution heteronuclear nuclear magnetic resonance for global fold determination of large proteins with limited nuclear overhauser effect data. Biochemistry 2000; 39: 5355-5365.
52. Xue Y, Podkorytov IS, Rao DK, Benjamin N, Sun H, Skrynnikov NR. Paramagnetic relaxation enhancements in unfolded proteins: theory and application to drkn sh3 domain. Protein Sci 2009; 18: 1401-1424.
53. Donaldson LW, Skrynnikov NR, Choy WY, Muhandiram DR, Sarkar B, Forman-Kay JD, Kay LE. Structural characterization of proteins with an attached atcun motif by paramagnetic relaxation enhancement NMR spectroscopy. J Am Chem Soc 2001; 123: 9843-9847.
54. Mok YK, Kay CM, Kay LE, Forman-Kay J. Noe data demonstrating a compact unfolded state for an sh3 domain under non-denaturing conditions. J Mol Biol 1999; 289: 619-638.
55. García De La Torre J, Huertas ML, Carrasco B. Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophys J 2000; 78: 719-730.
56. Svergun D, Barberato C, Koch MHJ. Crysol-a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J Appl Crystallogr 1995; 28: 768-773.
57. Frishman D, Argos P. Knowledge-based protein secondary structure assignment. Proteins 1995; 23: 566-579.
58. Fedyukina DV, Rajagopalan S, Sekhar A, Fulmer EC, Eun YJ, Cavagnero S. Contribution of long-range interactions to the secondary structure of an unfolded globin. Biophys J 2010; 99: L37-L39.
59. Sosnick TR, Shtilerman MD, Mayne L, Englander SW. Ultrafast signals in protein folding and the polypeptide contracted state. Proc Natl Acad Sci USA 1997; 94: 8545-8550.
60. Qi PX, Sosnick TR, Englander SW. The burst phase in ribonuclease a folding and solvent dependence of the unfolded state. Nat Struct Biol 1998; 5: 882-884.
61. Marsh JA, Forman-Kay JD. Sequence determinants of compaction in intrinsically disordered proteins. Biophys J 2010; 98: 2383-2390.
62. Feldman HJ, Hogue CW. A fast method to sample real protein conformational space. Proteins 2000; 39: 112-131.
63. Ganguly D, Chen J. Structural interpretation of paramagnetic relaxation enhancement-derived distances for disordered protein states. J Mol Biol 2009; 390: 467-477.
64. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr Sect D Biol Crystallogr 1998; 54 (Part 5): 905-921.