A frustrated binding interface for intrinsically disordered proteins

Journal of Biological Chemistry

Volumn 289, Issue 9, 2014, Pages 5528-5533

  Jemth, Per ^a   Mu, Xin ^a   Engström, Åke ^a   Dogan, Jakob ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING INTERFACE; BINDING PARTNERS; DISORDERED DOMAINS; DISORDERED PROTEINS; ENERGY LANDSCAPE; FOLDING REACTIONS; INTERACTION FREE ENERGIES; INTRINSICALLY DISORDERED PROTEINS;

PROTEINS;

BINDING ENERGY;

INTRINSICALLY DISORDERED PROTEIN; MUTANT PROTEIN; NUCLEAR COACTIVATOR BINDING DOMAIN; PEPTIDES AND PROTEINS; RETINOIC ACID RECEPTOR; THYROID HORMONE RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; CELL CYCLE REGULATION; ENERGY TRANSFER; HUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION;

INTRINSICALLY DISORDERED PROTEINS; KINETICS; PROTEIN DOMAINS; PROTEIN ENGINEERING; PROTEIN-PROTEIN INTERACTIONS;

HUMANS; MODELS, MOLECULAR; MUTATION; NUCLEAR RECEPTOR COACTIVATOR 3; PROTEIN FOLDING; RECOMBINANT PROTEINS;

EID: 84896886700     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.537068     Document Type: Article

References (39)

1. Dyson, H. J., and Wright, P. E. (2005) Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6, 197-208 (Pubitemid 40314921)
2. Uversky, V. N., Oldfield, C. J., and Dunker, A. K. (2008) Intrinsically disordered proteins in human diseases: introducing the D2 concept. Annu. Rev. Biophys. 37, 215-246
3. Kjaergaard, M., Teilum, K., and Poulsen, F. M. (2010) Conformational selection in the molten globule state of the nuclear coactivator binding domain of CBP. Proc. Natl. Acad. Sci. U.S.A. 107, 12535-12540
4. Demarest, S. J., Martinez-Yamout, M., Chung, J., Chen, H., Xu, W., Dyson, H. J., Evans, R. M., and Wright, P. E. (2002) Mutual synergistic folding in recruitment of CBP/p300 by p160 nuclear receptor coactivators. Nature 415, 549-553 (Pubitemid 34130612)
5. Demarest, S. J., Deechongkit, S., Dyson, H. J., Evans, R. M., and Wright, P. E. (2004) Packing, specificity, and mutability at the binding interface between the p160 coactivator and CREB-binding protein. Protein Sci. 13, 203-210 (Pubitemid 38021154)
6. Ebert, M. O., Bae, S. H., Dyson, H. J., and Wright, P. E. (2008) NMR relaxation study of the complex formed between CBP and the activation domain of the nuclear hormone receptor coactivator ACTR. Biochemistry 47, 1299-1308 (Pubitemid 351198706)
7. Dogan, J., Schmidt, T., Mu, X., Engström, Å., and Jemth, P. (2012) Fast association and slow transitions in the interaction between two intrinsically disordered protein domains. J. Biol. Chem. 287, 34316-34324
8. Dogan, J., Mu, X., Engström, Å., and Jemth, P. (2013) The transition state structure for coupled binding and folding of disordered protein domains. Sci. Rep. 3, 2076
9. Iešmantavičius, V., Dogan, J., Jemth, P., Teilum, K., and Kjaergaard, M. (2014) Helical propensity in an intrinsically disordered protein accelerates ligand binding. Angew. Chem. Int. Ed. Engl. 10.1002/anie.201307712
10. Itzhaki, L. S., Otzen, D. E., and Fersht, A. R. (1995) The structure of the transition state for folding of chymotrypsin inhibitor 2 analysed by protein engineering methods: evidence for a nucleation-condensation mechanism for protein folding. J. Mol. Biol. 254, 260-288
11. Carter, P. J., Winter, G., Wilkinson, A. J., and Fersht, A. R. (1984) The use of double mutants to detect structural changes in the active site of the tyrosyl-tRNA synthetase (Bacillus stearothermophilus). Cell 38, 835-840
12. Malatesta, F. (2005) The study of bimolecular reactions under non-pseudo-first order conditions. Biophys. Chem. 116, 251-256
13. Gianni, S., Haq, S. R., Montemiglio, L. C., Jürgens, M. C., Engström, Å., Chi, C. N., Brunori, M., and Jemth, P. (2011) Sequence-specific long range networks in PSD-95/Discs large/ZO-1 (PDZ) domains tune their binding selectivity. J. Biol. Chem. 286, 27167-27175
14. Hultqvist, G., Haq, S. R., Punekar, A. S., Chi, C. N., Engström, Å., Bach, A., Strømgaard, K., Selmer, M., Gianni, S., and Jemth, P. (2013) Energetic pathway sampling in a protein interaction domain. Structure 21, 1193-1202
15. Schreiber, G., and Fersht, A. R. (1995) Energetics of protein-protein interactions: analysis of the Barnase-Barstar interface by single mutations and double mutant cycles. J. Mol. Biol. 248, 478-486
16. Goldman, E. R., Dall'Acqua, W., Braden, B. C., and Mariuzza, R. A. (1997) Analysis of binding interactions in an idiotope-antiidiotope protein-protein complex by double mutant cycles. Biochemistry 36, 49-56 (Pubitemid 27024677)
17. Dall'Acqua, W., Goldman, E. R., Lin, W., Teng, C., Tsuchiya, D., Li, H., Ysern, X., Braden, B. C., Li, Y., Smith-Gill, S. J., and Mariuzza, R. A. (1998) A mutational analysis of binding interactions in an antigen-antibody protein-protein complex. Biochemistry 37, 7981-7991 (Pubitemid 28307057)
18. Pons, J., Rajpal, A., and Kirsch, J. F. (1999) Energetic analysis of an antigen/antibody interface: alanine scanning mutagenesis and double mutant cycles on the HyHEL-10/lysozyme interaction. Protein Sci. 8, 958-968 (Pubitemid 29211733)
19. Kiel, C., Serrano, L., and Herrmann, C. (2004) A detailed thermodynamic analysis of Ras/effector complex interfaces. J. Mol. Biol. 340, 1039-1058 (Pubitemid 38968701)
20. Reichmann, D., Cohen, M., Abramovich, R., Dym, O., Lim, D., Strynadka, N. C., and Schreiber, G. (2007) Binding hot spots in the TEM1-BLIP interface in light of its modular architecture. J. Mol. Biol. 365, 663-679 (Pubitemid 44960349)
21. Bryngelson, J. D., and Wolynes, P. G. (1987) Spin glasses and the statistical mechanics of protein folding. Proc. Natl. Acad. Sci. U.S.A. 84, 7524-7528
22. Qin, B. Y., Liu, C., Srinath, H., Lam, S. S., Correia, J. J., Derynck, R., and Lin, K. (2005) Crystal structure of IRF-3 in complex with CBP. Structure 13, 1269-1277 (Pubitemid 41262094)
23. Oldfield, C. J., Meng, J., Yang, J. Y., Yang, M. Q., Uversky, V. N., and Dunker, A. K. (2008) Flexible nets: disorder and induced fit in the associations of p53 and 14-3-3 with their partners. BMCGenomics 9, Suppl. 1, S1
24. Vacic, V., Oldfield, C. J., Mohan, A., Radivojac, P., Cortese, M. S., Uversky, V. N., and Dunker, A. K. (2007) Characterization of molecular recognition features, MoRFs, and their binding partners. J. Proteome Res. 6, 2351-2366 (Pubitemid 46985123)
25. Lee, C. W., Martinez-Yamout, M. A., Dyson, H. J., and Wright, P. E. (2010) Structure of the p53 transactivation domain in complex with the nuclear receptor coactivator binding domain of CREB binding protein. Biochemistry 49, 9964-9971
26. Matsuda, S., Harries, J. C., Viskaduraki, M., Troke, P. J., Kindle, K. B., Ryan, C., and Heery, D. M. (2004) A conserved α-helical motif mediates the binding of diverse nuclear proteins to the SRC1 interaction domain of CBP. J. Biol. Chem. 279, 14055-14064 (Pubitemid 38468941)
27. Lin, C. H., Hare, B. J., Wagner, G., Harrison, S. C., Maniatis, T., and Fraenkel, E. (2001) A small domain of CBP/p300 binds diverse proteins: solution structure and functional studies. Mol. Cell 8, 581-590 (Pubitemid 32946935)
28. Waters, L., Yue, B., Veverka, V., Renshaw, P., Bramham, J., Matsuda, S., Frenkiel, T., Kelly, G., Muskett, F., Carr, M., and Heery, D. M. (2006) Structural diversity in p160/CREB-binding protein coactivator complexes. J. Biol. Chem. 281, 14787-14795 (Pubitemid 43855184)
29. Ryan, C. M., Harries, J. C., Kindle, K. B., Collins, H. M., and Heery, D. M. (2006) Functional interaction of CREB binding protein (CBP) with nuclear transport proteins and modulation by HDAC inhibitors. Cell Cycle 5, 2146-2152 (Pubitemid 44553750)
30. Mas, C., Lussier-Price, M., Soni, S., Morse, T., Arseneault, G., Di Lello, P., Lafrance-Vanasse, J., Bieker, J. J., and Omichinski, J. G. (2011) Structural and functional characterization of an atypical activation domain in erythroid Krüppel-like factor (EKLF). Proc. Natl. Acad. Sci. U.S.A. 108, 10484-10489
31. Huang, Y., and Liu, Z. (2009) Kinetic advantage of intrinsically disordered proteins in coupled folding-binding process: a critical assessment of the "fly-casting" mechanism. J. Mol. Biol. 393, 1143-1159
32. Shammas, S. L., Rogers, J. M., Hill, S. A., and Clarke, J. (2012) Slow, reversible, coupled folding and binding of the spectrin tetramerization domain. Biophys. J. 103, 2203-2214
33. Zhou, H. X. (2012) Intrinsic disorder: signaling via highly specific but short-lived association. Trends Biochem. Sci. 37, 43-48
34. Drobnak, I., De Jonge, N., Haesaerts, S., Vesnaver, G., Loris, R., and Lah, J. (2013) Energetic basis of uncoupling folding from binding for an intrinsically disordered protein. J. Am. Chem. Soc. 135, 1288-1294
35. Sugase, K., Dyson, H. J., and Wright, P. E. (2007) Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 447, 1021-1025 (Pubitemid 46975749)
36. Rogers, J. M., Steward, A., and Clarke, J. (2013) Folding and binding of an intrinsically disordered protein: fast, but not 'diffusion-limited.' J. Am. Chem. Soc. 135, 1415-1422
37. Gianni, S., Morrone, A., Giri, R., and Brunori, M. (2012) A folding-after-binding mechanism describes the recognition between the transactivation domain of c-Myb and the KIX domain of the CREB-binding protein. Biochem. Biophys. Res. Commun. 428, 205-209
38. del Sol, A., Tsai, C. J., Ma, B., and Nussinov, R. (2009) The origin of allosteric functional modulation: multiple pre-existing pathways. Structure 17, 1042-1050
39. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific LLC, San Carlos, CA