Binding Rate Constants Reveal Distinct Features of Disordered Protein Domains

Biochemistry

Volumn 54, Issue 30, 2015, Pages 4741-4750

  Dogan, Jakob ^a,b   Jonasson, Josefin ^a   Andersson, Eva ^a   Jemth, Per ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ASSOCIATION REACTIONS; BINDING ENERGY; ELECTROSTATICS; IONIC STRENGTH; PROTEINS;

ASSOCIATION RATE CONSTANTS; ENVIRONMENTAL CONDITIONS; INTRINSICALLY DISORDERED PROTEINS; IONIC STRENGTH DEPENDENCE; LOW SALT CONCENTRATION; PHYSIOLOGICAL IONIC STRENGTH; TRANSACTIVATION DOMAIN; TRANSCRIPTIONAL CO-ACTIVATORS;

RATE CONSTANTS;

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTRINSICALLY DISORDERED PROTEIN; PROTEIN P53; SODIUM CHLORIDE; TRANSCRIPTION FACTOR ETS 2; RECOMBINANT PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; ASSOCIATION RATE CONSTANT; BINDING AFFINITY; BINDING KINETICS; CRYSTAL STRUCTURE; DISSOCIATION RATE CONSTANT; IONIC STRENGTH; OBSERVED RATE CONSTANT; PRIORITY JOURNAL; PROTEIN DOMAIN; RATE CONSTANT; SIGNAL NOISE RATIO; STATIC ELECTRICITY; CHEMISTRY; GENETICS; HUMAN; METABOLISM; PROTEIN FOLDING; PROTEIN TERTIARY STRUCTURE;

HUMANS; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; TRANSCRIPTION FACTORS;

EID: 84938629771     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00520     Document Type: Article

References (48)

1. Wright, P. E. and Dyson, H. J. (2015) Intrinsically disordered proteins in cellular signalling and regulation Nat. Rev. Mol. Cell Biol. 16, 18-29 10.1038/nrm3920
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 10.1146/annurev.biophys.37.032807.125924
3. Zhou, H.-X. (2012) Intrinsic disorder: signaling via highly specific but short-lived association Trends Biochem. Sci. 37, 43-48 10.1016/j.tibs.2011.11.002
4. Uversky, V. N., Gillespie, J. R., and Fink, A. L. (2000) Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins: Struct., Funct., Genet. 41, 415-427 10.1002/1097-0134(20001115)41:3<415::AID-PROT130>3.0.CO;2-7
5. Dogan, J., Gianni, S., and Jemth, P. (2014) The binding mechanisms of intrinsically disordered proteins Phys. Chem. Chem. Phys. 16, 6323-6331 10.1039/C3CP54226B
6. 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 10.1016/j.bpj.2012.10.012
7. Shammas, S. L., Travis, A. J., and Clarke, J. (2013) Remarkably fast coupled folding and binding of the intrinsically disordered transactivation domain of cMyb to CBP KIX J. Phys. Chem. B 117, 13346-13356 10.1021/jp404267e
8. 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 10.1021/ja309527h
9. 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 10.1016/j.jmb.2009.09.010
10. Wang, F., Marshall, C. B., and Ikura, M. (2013) Transcriptional/epigenetic regulator CBP/p300 in tumorigenesis: structural and functional versatility in target recognition Cell. Mol. Life Sci. 70, 3989-4008 10.1007/s00018-012-1254-4
11. Xu, J. and Li, Q. (2003) Review of the in vivo functions of the p160 steroid receptor coactivator family Mol. Endocrinol. 17, 1681-1692 10.1210/me.2003-0116
12. Ferreon, J. C., Lee, C. W., Arai, M., Martinez-Yamout, M. A., Dyson, H. J., and Wright, P. E. (2009) Cooperative regulation of p53 by modulation of ternary complex formation with CBP/p300 and HDM2 Proc. Natl. Acad. Sci. U. S. A. 106, 6591-6596 10.1073/pnas.0811023106
13. 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 10.1021/bi1012996
14. 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 10.1016/S1097-2765(01)00333-1
15. Matsuda, S., Harries, J. C., Viskaduraki, M., Troke, P. J. F., Kindle, K. B., Ryan, C., and Heery, D. M. (2004) A Conserved alpha-helical motif mediates the binding of diverse nuclear proteins to the SRC1 interaction domain of CBP J. Biol. Chem. 279, 14055-14064 10.1074/jbc.M310188200
16. 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 10.1016/j.str.2005.06.011
17. 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 10.1038/415549a
18. 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 10.1110/ps.03366504
19. 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 10.1073/pnas.1001693107
20. Kjaergaard, M., Andersen, L., Nielsen, L. D., and Teilum, K. (2013) A folded excited state of ligand-free nuclear coactivator binding domain (NCBD) underlies plasticity in ligand recognition Biochemistry 52, 1686-1693 10.1021/bi4001062
21. 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 10.1074/jbc.M112.399436
22. 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 10.1038/srep02076
23. 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. 53, 1548-1551 10.1002/anie.201307712
24. Jemth, P., Mu, X., Engström, Å., and Dogan, J. (2014) A frustrated binding interface for intrinsically disordered proteins J. Biol. Chem. 289, 5528-5533 10.1074/jbc.M113.537068
25. Malatesta, F. (2005) The study of bimolecular reactions under non-pseudo-first order conditions Biophys. Chem. 116, 251-256 10.1016/j.bpc.2005.04.006
26. Fersht, A. (1999) Structure and mechanism in protein science: A guide to enzyme catalysis and protein folding, Macmillan, New York.
27. Schreiber, G., Haran, G., and Zhou, H.-X. (2009) Fundamental aspects of protein-protein association kinetics Chem. Rev. 109, 839-860 10.1021/cr800373w
28. 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 10.1021/bi701767j
29. Kjaergaard, M., Nørholm, A.-B., Hendus-Altenburger, R., Pedersen, S. F., Poulsen, F. M., and Kragelund, B. B. (2010) Temperature-dependent structural changes in intrinsically disordered proteins: formation of alpha-helices or loss of polyproline II? Protein Sci. 19, 1555-1564 10.1002/pro.435
30. Lee, H., Mok, K. H., Muhandiram, R., Park, K. H., Suk, J. E., Kim, D. H., Chang, J., Sung, Y. C., Choi, K. Y., and Han, K. H. (2000) Local structural elements in the mostly unstructured transcriptional activation domain of human p53 J. Biol. Chem. 275, 29426-29432 10.1074/jbc.M003107200
31. Wells, M., Tidow, H., Rutherford, T. J., Markwick, P., Jensen, M. R., Mylonas, E., Svergun, D. I., Blackledge, M., and Fersht, A. R. (2008) Structure of tumor suppressor p53 and its intrinsically disordered N-terminal transactivation domain Proc. Natl. Acad. Sci. U. S. A. 105, 5762-5767 10.1073/pnas.0801353105
32. 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 10.1074/jbc.M600237200
33. Uversky, V. N. (2013) A decade and a half of protein intrinsic disorder: biology still waits for physics Protein Sci. 22, 693-724 10.1002/pro.2261
34. Schreiber, G. (2002) Kinetic studies of protein-protein interactions Curr. Opin. Struct. Biol. 12, 41-47 10.1016/S0959-440X(02)00287-7
35. Bachmann, A., Wildemann, D., Praetorius, F., Fischer, G., and Kiefhaber, T. (2011) Mapping backbone and side-chain interactions in the transition state of a coupled protein folding and binding reaction Proc. Natl. Acad. Sci. U. S. A. 108, 3952-3957 10.1073/pnas.1012668108
36. Haq, S. R., Chi, C. N., Bach, A., Dogan, J., Engström, Å., Hultqvist, G., Karlsson, O. A., Lundström, P., Montemiglio, L. C., Strømgaard, K., Gianni, S., and Jemth, P. (2012) Side-chain interactions form late and cooperatively in the binding reaction between disordered peptides and PDZ domains J. Am. Chem. Soc. 134, 599-605 10.1021/ja209341w
37. Karlsson, O. A., Chi, C. N., Engström, A., and Jemth, P. (2012) The transition state of coupled folding and binding for a flexible β-finger J. Mol. Biol. 417, 253-261 10.1016/j.jmb.2012.01.042
38. 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 10.1016/j.bbrc.2012.09.112
39. Toto, A., Giri, R., Brunori, M., and Gianni, S. (2014) The mechanism of binding of the KIX domain to the mixed lineage leukemia protein and its allosteric role in the recognition of c-Myb Protein Sci. 23, 962-969 10.1002/pro.2480
40. Dosnon, M., Bonetti, D., Morrone, A., Erales, J., di Silvio, E., Longhi, S., and Gianni, S. (2015) Demonstration of a Folding after Binding Mechanism in the Recognition between the Measles Virus NTAIL and X Domains ACS Chem. Biol. 10, 795-802 10.1021/cb5008579
41. Rogers, J. M., Wong, C. T., and Clarke, J. (2014) Coupled Folding and Binding of the Disordered Protein PUMA Does Not Require Particular Residual Structure J. Am. Chem. Soc. 136, 5197-5200 10.1021/ja4125065
42. Gibbs, E. B. and Showalter, S. A. (2015) Quantitative biophysical characterization of intrinsically disordered proteins Biochemistry 54, 1314-1326 10.1021/bi501460a
43. Zhou, H.-X., Pang, X., and Lu, C. (2012) Rate constants and mechanisms of intrinsically disordered proteins binding to structured targets Phys. Chem. Chem. Phys. 14, 10466-10476 10.1039/c2cp41196b
44. Ganguly, D., Otieno, S., Waddell, B., Iconaru, L., Kriwacki, R. W., and Chen, J. (2012) Electrostatically accelerated coupled binding and folding of intrinsically disordered proteins J. Mol. Biol. 422, 674-684 10.1016/j.jmb.2012.06.019
45. Ganguly, D., Zhang, W., and Chen, J. (2013) Electrostatically accelerated encounter and folding for facile recognition of intrinsically disordered proteins PLoS Comput. Biol. 9, e1003363 10.1371/journal.pcbi.1003363
46. Knott, M. and Best, R. B. (2014) Discriminating binding mechanisms of an intrinsically disordered protein via a multi-state coarse-grained model J. Chem. Phys. 140, 175102 10.1063/1.4873710
47. Teufel, D. P., Freund, S. M., Bycroft, M., and Fersht, A. R. (2007) Four domains of p300 each bind tightly to a sequence spanning both transactivation subdomains of p53 Proc. Natl. Acad. Sci. U. S. A. 104, 7009-7014 10.1073/pnas.0702010104
48. Blöchliger, N., Xu, M., and Caflisch, A. (2015) Peptide Binding to a PDZ Domain by Electrostatic Steering via Nonnative Salt Bridges Biophys. J. 108, 2362-2370 10.1016/j.bpj.2015.03.038