Linking folding and binding

Current Opinion in Structural Biology

Volumn 19, Issue 1, 2009, Pages 31-38

  Wright, Peter E ^a   Dyson, H Jane ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LIPOPROTEIN; NUCLEOTIDE; PEPTIDOGLYCAN;

ENZYME KINETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PREDICTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; BINDING SITES; DATABASES, PROTEIN; HUMANS; KINETICS; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEINS; SIGNAL TRANSDUCTION;

EID: 60349101875     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2008.12.003     Document Type: Review

References (65)

1. Dyson H.J., and Wright P.E. Coupling of folding and binding for unstructured proteins. Curr Opin Struct Biol 12 (2002) 54-60
2. Dunker A.K., Cortese M.S., Romero P., Iakoucheva L.M., and Uversky V.N. Flexible nets. The roles of intrinsic disorder in protein interaction networks. FEBS J 272 (2005) 5129-5148
3. Xie H.B., Vucetic S., Iakoucheva L.M., Oldfield C.J., Dunker A.K., Uversky V.N., and Obradovic Z. Functional anthology of intrinsic disorder. 1. Biological processes and functions of proteins with long disordered regions. J Proteome Res 6 (2007) 1882-1898
4. Vucetic S., Xie H.B., Iakoucheva L.M., Oldfield C.J., Dunker A.K., Obradovic Z., and Uversky V.N. Functional anthology of intrinsic disorder. 2. Cellular components, domains, technical terms, developmental processes, and coding sequence diversities correlated with long disordered regions. J Proteome Res 6 (2007) 1899-1916
5. Xie H.B., Vucetic S., Iakoucheva L.M., Oldfield C.J., Dunker A.K., Obradovic Z., and Uversky V.N. Functional anthology of intrinsic disorder. 3. Ligands, post-translational modifications, and diseases associated with intrinsically disordered proteins. J Proteome Res 6 (2007) 1917-1932
6. Lobley A., Swindells M.B., Orengo C.A., and Jones D.T. Inferring function using patterns of native disorder in proteins. PLoS Comput Biol 3 (2007) e162
7. Waf1/Cip1/Sdi1 in the free and Cdk2-bound state: conformational disorder mediates binding diversity. Proc Natl Acad Sci U S A 93 (1996) 11504-11509
8. Romero P., Obradovic Z., Kissinger C.R., Villafranca J.E., and Dunker A.K. Identifying disordered regions in proteins from amino acid sequences. Proc IEEE Int Conf Neural Netw 1997 (1997) 90-95
9. Radivojac P., Iakoucheva L.M., Oldfield C.J., Obradovic Z., Uversky V.N., and Dunker A.K. Intrinsic disorder and functional proteomics. Biophys J 92 (2007) 1439-1456
10. Dyson H.J., and Wright P.E. Elucidation of the protein folding landscape by NMR. Methods Enzymol 394 (2005) 299-321
11. Bernado P., Blanchard L., Timmins P., Marion D., Ruigrok R.W., and Blackledge M. A structural model for unfolded proteins from residual dipolar couplings and small-angle X-ray scattering. Proc Natl Acad Sci U S A 102 (2005) 17002-17007
12. Bernado P., Mylonas E., Petoukhov M.V., Blackledge M., and Svergun D.I. Structural characterization of flexible proteins using small-angle X-ray scattering. J Am Chem Soc 129 (2007) 5656-5664. SAXS is used as the basis for analysis of the conformational ensemble of flexible proteins using an ensemble optimization method.
13. Dedmon M.M., Lindorff-Larsen K., Christodoulou J., Vendruscolo M., and Dobson C.M. Mapping long-range interactions in alpha-synuclein using spin-label NMR and ensemble molecular dynamics simulations. J Am Chem Soc 127 (2005) 476-477
14. Mukhopadhyay S., Krishnan R., Lemke E.A., Lindquist S., and Deniz A.A. A natively unfolded yeast prion monomer adopts an ensemble of collapsed and rapidly fluctuating structures. Proc Natl Acad Sci U S A 104 (2007) 2649-2654. Investigation of the structural ensemble and dynamics of the prion-determining domain of the yeats prion Sup35 using single-molecule fluorescence resonance energy transfer and fluorescence correlation spectroscopy.
15. Miyagi A., Tsunaka Y., Uchihashi T., Mayanagi K., Hirose S., Morikawa K., and Ando T. Visualization of intrinsically disordered regions of proteins by high-speed atomic force microscopy. Chemphyschem 9 (2008) 1859-1866
16. Zhu F., Tranter G.E., Isaacs N.W., Hecht L., and Barron L.D. Delineation of protein structure classes from multivariate analysis of protein Raman optical activity data. J Mol Biol 363 (2006) 19-26
17. •] above) and NMR spectroscopy to characterize the solution structure of the full-length p53 and the ensemble structure of the disordered N-terminal transactivation domain.
18. Jao C.C., Der-Sarkissian A., Chen J., and Langen R. Structure of membrane-bound αsynuclein studied by site-directed spin labeling. Proc Natl Acad Sci U S A 101 (2004) 8331-8336
19. Morin B., Bourhis J.M., Belle V., Woudstra M., Carriere F., Guigliarelli B., Fournel A., and Longhi S. Assessing induced folding of an intrinsically disordered protein by site-directed spin-labeling electron paramagnetic resonance spectroscopy. J Phys Chem B 110 (2006) 20596-20608
20. Wright P.E., and Dyson H.J. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J Mol Biol 293 (1999) 321-331
21. Dyson H.J., and Wright P.E. Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6 (2005) 197-208
22. Mohan A., Oldfield C.J., Radivojac P., Vacic V., Cortese M.S., Dunker A.K., and Uversky V.N. Analysis of molecular recognition features (MoRFs). J Mol Biol 362 (2006) 1043-1059. Describes the identification of sequence motifs within larger intrinsically disordered proteins that exhibit molecular recognition and binding functions.
23. Remaut H., and Waksman G. Protein-protein interaction through β-strand addition. Trends Biochem Sci 31 (2006) 436-444
24. Mészáros B., Tompa P., Simon I., and Dosztanyi Z. Molecular principles of the interactions of disordered proteins. J Mol Biol 372 (2007) 549-561
25. Bonsor D.A., Grishkovskaya I., Dodson E.J., and Kleanthous C. Molecular mimicry enables competitive recruitment by a natively disordered protein. J Am Chem Soc 129 (2007) 4800-4807. This study compares the structures of TolB complexes with the globular target protein Pal and with the intrinsically disordered ligand colicin and reveals a novel binding mechanism.
26. Oldfield C.J., Meng J., Yang J.Y., Yang M.Q., Uversky V.N., and Dunker A.K. Flexible nets: disorder and induced fit in the associations of p53 and 14-3-3 with their partners. BMC Genomics 9 Suppl. 1 (2008) S1
27. Demarest S.J., Deechongkit S., Dyson H.J., Evans R.M., and Wright P.E. Packing, specificity, and mutability at the binding interface between the p160 coactivator and CREB-binding protein. Protein Sci 13 (2004) 203-210
28. Demarest S.J., Martinez-Yamout M., Chung J., Chen H., Xu W., Dyson H.J., Evans R.M., and Wright P.E. Mutual synergistic folding in recruitment of CBP/p300 by p160 nuclear receptor coactivators. Nature 415 (2002) 549-553
29. Qin B.Y., Liu C., Srinath H., Lam S.S., Correia J.J., Derynck R., and Lin K. Crystal structure of IRF-3 in complex with CBP. Structure 13 (2005) 1269-1277
30. Fuxreiter M., Simon I., Friedrich P., and Tompa P. Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. J Mol Biol 338 (2004) 1015-1026
31. Korzhnev D.M., and Kay L.E. Probing invisible, low-populated states of protein molecules by relaxation dispersion NMR spectroscopy: an application to protein folding. Acc Chem Res 41 (2008) 442-451. A comprehensive review of current methods to characterize low-populated protein folding intermediates using NMR relaxation dispersion.
32. Sugase K., Dyson H.J., and Wright P.E. Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 447 (2007) 1021-1025. NMR methods, including chemical shift titration and relaxation dispersion, are used to determine the kinetics and mechanism by which the intrinsically disordered pKID activation domain of CREB folds on binding to the KIX domain of CBP.
33. 133-phosphorylated and non-phosphorylated forms of the kinase inducible transactivation domain of CREB. FEBS Lett 430 (1998) 317-322
34. Radhakrishnan I., Pérez-Alvarado G.C., Parker D., Dyson H.J., Montminy M.R., and Wright P.E. Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: a model for activator: coactivator interactions. Cell 91 (1997) 741-752
35. ••] above). An induced-folding mechanism incorporating non-native initial contacts and a partially folded intermediate is consistent with the experimental results.
36. Shoemaker B.A., Portman J.J., and Wolynes P.G. Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc Natl Acad Sci U S A 97 (2000) 8868-8873
37. Lu Q., Lu H.P., and Wang J. Exploring the mechanism of flexible biomolecular recognition with single molecule dynamics. Phys Rev Lett 98 (2007) 128105
38. Ferreira M.E., Hermann S., Prochasson P., Workman J.L., Berndt K.D., and Wright A.P.H. Mechanism of transcription factor recruitment by acidic activators. J Biol Chem 280 (2005) 21779-21784
39. Onitsuka M., Kamikubo H., Yamazaki Y., and Kataoka M. Mechanism of induced folding: both folding before binding and binding before folding can be realized in staphylococcal nuclease mutants. Proteins Struct Funct Bioinform 72 (2008) 837-847
40. Song J., Guo L.W., Muradov H., Artemyev N.O., Ruoho A.E., and Markley J.L. Intrinsically disordered γ-subunit of cGMP phosphodiesterase encodes functionally relevant transient secondary and tertiary structure. Proc Natl Acad Sci U S A 105 (2008) 1505-1510
41. Bienkiewicz E.A., Adkins J.N., and Lumb K.J. Functional consequences of preorganized helical structure in the intrinsically disordered cell-cycle inhibitor p27(Kip1). Biochemistry 41 (2002) 752-759
42. Zor T., Mayr B.M., Dyson H.J., Montminy M.R., and Wright P.E. Roles of phosphorylation and helix propensity in the binding of the KIX domain of CREB-binding protein by constitutive (c-Myb) and inducible (CREB) activators. J Biol Chem 277 (2002) 42241-42248
43. Verkhivker G.M., Bouzida D., Gehlhaar D.K., Rejto P.A., Freer S.T., and Rose P.W. Simulating disorder-order transitions in molecular recognition of unstructured proteins: where folding meets binding. Proc Natl Acad Sci U S A 100 (2003) 5148-5153
44. Verkhivker G.M. Protein conformational transitions coupled to binding in molecular recognition of unstructured proteins: deciphering the effect of intermolecular interactions on computational structure prediction of the p27Kip1 protein bound to the cyclin A-cyclin-dependent kinase 2 complex. Proteins 58 (2005) 706-716
45. Chong P.A., Ozdamar B., Wrana J.L., and Forman-Kay J.D. Disorder in a target for the Smad2 Mad homology 2 domain and its implications for binding and specificity. J Biol Chem 279 (2004) 40707-40714
46. Baker J.M.R., Hudson R.P., Kanelis V., Choy W.Y., Thibodeau P.H., Thomas P.J., and Forman-Kay J.D. CFTR regulatory region interacts with NBD1 predominantly via multiple transient helices. Nat Struct Mol Biol 14 (2007) 738-745. This paper shows that NBD1 forms dynamic and fluctuating complexes with multiple helical motifs in the intrinsically disordered regulatory region of CFTR.
47. Sivakolundu S.G., Nourse A., Moshiach S., Bothner B., Ashley C., Satumba J., Lahti J., and Kriwacki R.W. Intrinsically unstructured domains of Arf and Hdm2 form bimolecular oligomeric structures in vitro and in vivo. J Mol Biol 384 (2008) 240-254. This paper reports the novel finding that intrinsically disordered regions in Arf and Hdm2 fold together to form amyloid-like structures that function in the regulation of Hdm2 and p53.
48. Pontius B.W. Close encounters: why unstructured, polymeric domains can increase rates of specific macromolecular association. Trends Biochem Sci 18 (1993) 181-186
49. Levy Y., Onuchic J.N., and Wolynes P.G. Fly-casting in protein-DNA binding: frustration between protein folding and electrostatics facilitates target recognition. J Am Chem Soc 129 (2007) 738-739
50. Narayanan R., Ganesh O.K., Edison A.S., and Hagen S.J. Kinetics of folding and binding of an intrinsically disordered protein: the inhibitor of yeast aspartic proteinase YPrA. J Am Chem Soc 130 (2008) 11477-11485
51. Choi H.J., Huber A.H., and Weis W.I. Thermodynamics of β-catenin-ligand Interactions: the roles of the N- and C-terminal tails in modulating binding affinity. J Biol Chem 281 (2006) 1027-1038
52. Sugase K., Lansing J.C., Dyson H.J., and Wright P.E. Tailoring relaxation dispersion experiments for fast-associating protein complexes. J Am Chem Soc 129 (2007) 13406-13407
53. Hilser V.J., and Thompson E.B. Intrinsic disorder as a mechanism to optimize allosteric coupling in proteins. Proc Natl Acad Sci U S A 104 (2007) 8311-8315
54. De Guzman R.N., Goto N.K., Dyson H.J., and Wright P.E. Structural basis for cooperative transcription factor binding to the CBP coactivator. J Mol Biol 355 (2006) 1005-1013
55. Bertagna A., Toptygin D., Brand L., and Barrick D. The effects of conformational heterogeneity on the binding of the Notch intracellular domain to effector proteins: a case of biologically tuned disorder. Biochem Soc Trans 36 (2008) 157-166. A wormlike chain model is used to show that the disordered region between two domains is of appropriate length to promote recruitment and subsequent complex formation.
56. Iakoucheva L.M., Radivojac P., Brown C.J., O'Connor T.R., Sikes J.G., Obradovic Z., and Dunker A.K. The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res 32 (2004) 1037-1049
57. Pufall M.A., Lee G.M., Nelson M.L., Kang H.S., Velyvis A., Kay L.E., McIntosh L.P., and Graves B.J. Variable control of Ets-1 DNA binding by multiple phosphates in an unstructured region. Science 309 (2005) 142-145
58. Solt I., Magyar C., Simon I., Tompa P., and Fuxreiter M. Phosphorylation-induced transient intrinsic structure in the kinase-inducible domain of CREB facilitates its recognition by the KIX domain of CBP. Proteins: Struct, Funct Genet 64 (2006) 749-757
59. Borg M., Mittag T., Pawson T., Tyers M., Forman-Kay J.D., and Chan H.S. Polyelectrostatic interactions of disordered ligands suggest a physical basis for ultrasensitivity. Proc Natl Acad Sci U S A 104 (2007) 9650-9655. A mean-field statistical mechanical model is used to predict the threshold number of phosphorylation sites required for the binding of the cyclin-dependent kinase inhibitor Sic1 to its target protein.
60. Lenz P., and Swain P.S. An entropic mechanism to generate highly cooperative and specific binding from protein phosphorylations. Curr Biol 16 (2006) 2150-2155
61. Li C., Charlton L.M., Lakkavaram A., Seagle C., Wang G., Young G.B., Macdonald J.M., and Pielak G.J. Differential dynamical effects of macromolecular crowding on an intrinsically disordered protein and a globular protein: implications for in-cell NMR spectroscopy. J Am Chem Soc 130 (2008) 6310-6311
62. Dedmon M.M., Patel C.N., Young G.B., and Pielak G.J. FlgM gains structure in living cells. Proc Natl Acad Sci U S A 99 (2002) 12681-12684
63. Tompa P., Prilusky J., Silman I., and Sussman J.L. Structural disorder serves as a weak signal for intracellular protein degradation. Proteins 71 (2008) 903-909. There appears only a very weak correlation between the lifetimes of intrinsically disordered proteins in the cell and the degree of disorder, and many disordered proteins have surprisingly long half-lives in the cell.
64. Hegyi H., and Tompa P. Intrinsically disordered proteins display no preference for chaperone binding in vivo. PLoS Comput Biol 4 (2008) e1000017
65. Eliezer D., and Palmer A.G. III Proteins hunt and gather. Nature 447 (2007) 920-921