A folded excited state of ligand-free nuclear coactivator binding domain (NCBD) underlies plasticity in ligand recognition

Biochemistry

Volumn 52, Issue 10, 2013, Pages 1686-1693

  Kjaergaard, Magnus ^a   Andersen, Lisbeth ^a   Nielsen, Lau Dalby ^a   Teilum, Kaare ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONAL ENSEMBLE; CONFORMATIONAL EXCHANGE; CONFORMATIONAL SELECTION; INTRINSICALLY DISORDERED PROTEINS; LIGAND RECOGNITION; MILLISECOND DYNAMICS; NUCLEAR COACTIVATOR; RELAXATION DISPERSION;

BINDING ENERGY; CONFORMATIONS; DISPERSIONS; GROUND STATE; LIGANDS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PLASTICITY; PROTEINS; REACTION KINETICS;

EXCITED STATES;

BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; LIGAND; NUCLEAR COACTIVATOR BINDING DOMAIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PLASTICITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING;

ANIMALS; CREB-BINDING PROTEIN; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; INTERFERON REGULATORY FACTOR-3; INTRINSICALLY DISORDERED PROTEINS; LIGANDS; MICE; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEAR PROTEINS; NUCLEAR RECEPTOR COACTIVATOR 3; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; STATIC ELECTRICITY; THERMODYNAMICS;

EID: 84874963976     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4001062     Document Type: Article

References (51)

1. 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
2. Wright, P. E. and Dyson, H. J. (2009) Linking folding and binding Curr. Opin. Struct. Biol. 19, 31-38
3. Dyson, H. J. and Wright, P. E. (2005) Intrinsically unstructured proteins and their functions Nat. Rev. Mol. Cell Biol. 6, 197-208
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
5. 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
6. 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
7. Zhang, W., Ganguly, D., and Chen, J. (2012) Residual structures, conformational fluctuations, and electrostatic interactions in the synergistic folding of two intrinsically disordered proteins PLoS Comput. Biol. 8, e1002353
8. Burger, V. M., Ramanathan, A., Savol, A. J., Stanley, C. B., Agarwal, P. K., and Chennubhotla, C. S. (2012) Quasi-anharmonic analysis reveals intermediate States in the nuclear co-activator receptor binding domain ensemble Pac. Symp. Biocomput. 70-81
9. Naganathan, A. N. and Orozco, M. (2011) The native ensemble and folding of a protein molten-globule: functional consequence of downhill folding J. Am. Chem. Soc. 133, 12154-12161
10. Ganguly, D., Zhang, W., and Chen, J. (2012) Synergistic folding of two intrinsically disordered proteins: searching for conformational selection Mol. BioSyst. 8, 198-209
11. 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
12. 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
13. Keppel, T. R., Howard, B. A., and Weis, D. D. (2011) Mapping unstructured regions and synergistic folding in intrinsically disordered proteins with amide H/D exchange mass spectrometry Biochemistry 50, 8722-8732
14. Kjaergaard, M., Poulsen, F. M., and Teilum, K. (2012) Is a malleable protein necessarily highly dynamic? The hydrophobic core of the nuclear coactivator binding domain is well ordered Biophys. J. 102, 1627-1635
15. Dolgikh, D. A., Kolomiets, A. P., Bolotina, I. A., and Ptitsyn, O. B. (1984) 'Molten-globule' state accumulates in carbonic anhydrase folding FEBS Lett. 165, 88-92
16. Japrung, D., Dogan, J., Freedman, K. J., Nadzeyka, A., Bauerdick, S., Albrecht, T., Kim, M. J., Jemth, P., and Edel, J. B. (2013) Single molecule studies of intrinsically disordered proteins using solid-state nanopores Anal. Chem. 10.1021/ac3035025
17. Knott, M. and Best, R. B. (2012) A preformed binding interface in the unbound ensemble of an intrinsically disordered protein: evidence from molecular simulations PLoS Comput. Biol. 8, e1002605
18. Baldwin, A. J. and Kay, L. E. (2009) NMR spectroscopy brings invisible protein states into focus Nat. Chem. Biol. 5, 808-814
19. Lundström, P., Teilum, K., Carstensen, T., Bezsonova, I., Wiesner, S., Hansen, D. F., Religa, T. L., Akke, M., and Kay, L. E. (2007) Fractional 13C enrichment of isolated carbons using [1-13C]- or [2-13C]-glucose facilitates the accurate measurement of dynamics at backbone Calpha and side-chain methyl positions in proteins J. Biomol. NMR 38, 199-212
20. Teilum, K., Brath, U., Lundström, P., and Akke, M. (2006) Biosynthetic 13C labeling of aromatic side chains in proteins for NMR relaxation measurements J. Am. Chem. Soc. 128, 2506-2507
21. Otten, R., Villali, J., Kern, D., and Mulder, F. A. (2010) Probing microsecond time scale dynamics in proteins by methyl (1)H Carr-Purcell-Meiboom- Gill relaxation dispersion NMR measurements. Application to activation of the signaling protein NtrC(r) J. Am. Chem. Soc. 132, 17004-17014
22. Tollinger, M., Skrynnikov, N. R., Mulder, F. A., Forman-Kay, J. D., and Kay, L. E. (2001) Slow dynamics in folded and unfolded states of an SH3 domain J. Am. Chem. Soc. 123, 11341-11352
23. Lundström, P., Hansen, D. F., and Kay, L. E. (2008) Measurement of carbonyl chemical shifts of excited protein states by relaxation dispersion NMR spectroscopy: comparison between uniformly and selectively (13)C labeled samples J. Biomol. NMR 42, 35-47
24. Mulder, F. A., Hon, B., Mittermaier, A., Dahlquist, F. W., and Kay, L. E. (2002) Slow internal dynamics in proteins: application of NMR relaxation dispersion spectroscopy to methyl groups in a cavity mutant of T4 lysozyme J. Am. Chem. Soc. 124, 1443-1451
25. Mulder, F. A., Skrynnikov, N. R., Hon, B., Dahlquist, F. W., and Kay, L. E. (2001) Measurement of slow (micros-ms) time scale dynamics in protein side chains by (15)N relaxation dispersion NMR spectroscopy: application to Asn and Gln residues in a cavity mutant of T4 lysozyme J. Am. Chem. Soc. 123, 967-975
26. Mulder, F. A., De Graaf, R. A., Kaptein, R., and Boelens, R. (1998) An off-resonance rotating frame relaxation experiment for the investigation of macromolecular dynamics using adiabatic rotations J. Magn. Reson. 131, 351-357
27. Igumenova, T. I. and Palmer, A. G. (2006) Off-resonance TROSY-selected R1rho experiment with improved sensitivity for medium- and high-molecular-weight proteins J. Am. Chem. Soc. 128, 8110-8111
28. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6, 277-293
29. Carver, J. and Richards, R. (1972) A general two-site solution for the chemical exchange produced dependence of T2 upon the carr-Purcell pulse separation J. Magn. Reson. 6, 89-105
30. Kjaergaard, M., Brander, S., and Poulsen, F. M. (2011) Random coil chemical shift for intrinsically disordered proteins: effects of temperature and pH J. Biomol. NMR 139-149
31. Kjaergaard, M. and Poulsen, F. M. (2011) Sequence correction of random coil chemical shifts: correlation between neighbor correction factors and changes in the Ramachandran distribution J. Biomol. NMR 50, 157-165
32. Kjaergaard, M., Iešmantavičius, V., and Poulsen, F. M. (2011) The interplay between transient α-helix formation and side chain rotamer distributions in disordered proteins probed by methyl chemical shifts Protein Sci. 20, 2023-2034
33. Kovrigin, E. L., Kempf, J. G., Grey, M. J., and Loria, J. P. (2006) Faithful estimation of dynamics parameters from CPMG relaxation dispersion measurements J. Magn. Reson. 180, 93-104
34. Teilum, K., Smith, M. H., Schulz, E., Christensen, L. C., Solomentsev, G., Oliveberg, M., and Akke, M. (2009) Transient structural distortion of metal-free Cu/Zn superoxide dismutase triggers aberrant oligomerization Proc. Natl. Acad. Sci. U. S. A. 106, 18273-18278
35. Korzhnev, D. M., Religa, T. L., Banachewicz, W., Fersht, A. R., and Kay, L. E. (2010) A transient and low-populated protein-folding intermediate at atomic resolution Science 329, 1312-1316
36. Bouvignies, G., Vallurupalli, P., Hansen, D. F., Correia, B. E., Lange, O., Bah, A., Vernon, R. M., Dahlquist, F. W., Baker, D., and Kay, L. E. (2011) Solution structure of a minor and transiently formed state of a T4 lysozyme mutant Nature 477, 111-114
37. Neudecker, P., Robustelli, P., Cavalli, A., Walsh, P., Lundström, P., Zarrine-Afsar, A., Sharpe, S., Vendruscolo, M., and Kay, L. E. (2012) Structure of an intermediate state in protein folding and aggregation Science 336, 362-366
38. Vallurupalli, P., Hansen, D. F., Stollar, E., Meirovitch, E., and Kay, L. E. (2007) Measurement of bond vector orientations in invisible excited states of proteins Proc. Natl. Acad. Sci. U. S. A. 104, 18473-18477
39. Baldwin, A. J. and Kay, L. E. (2012) Measurement of the signs of methyl 13C chemical shift differences between interconverting ground and excited protein states by R(1ρ): an application to αB-Crystallin J. Biomol. NMR 53, 1-12
40. Auer, R., Hansen, D. F., Neudecker, P., Korzhnev, D. M., Muhandiram, D. R., Konrat, R., and Kay, L. E. (2010) Measurement of signs of chemical shift differences between ground and excited protein states: a comparison between H(S/M)QC and R1rho methods J. Biomol. NMR 46, 205-216
41. Mulder, F. A. (2009) Leucine side-chain conformation and dynamics in proteins from 13C NMR chemical shifts ChemBioChem 10, 1477-1479
42. Hansen, D. F., Neudecker, P., and Kay, L. E. (2010) Determination of isoleucine side-chain conformations in ground and excited states of proteins from chemical shifts J. Am. Chem. Soc. 132, 7589-7591
43. Hansen, D. F., Neudecker, P., Vallurupalli, P., Mulder, F. A., and Kay, L. E. (2010) Determination of Leu side-chain conformations in excited protein states by NMR relaxation dispersion J. Am. Chem. Soc. 132, 42-43
44. London, R. E., Wingad, B. D., and Mueller, G. A. (2008) Dependence of amino acid side chain 13C shifts on dihedral angle: application to conformational analysis J. Am. Chem. Soc. 130, 11097-11105
45. Sahakyan, A. B., Vranken, W. F., Cavalli, A., and Vendruscolo, M. (2011) Structure-based prediction of methyl chemical shifts in proteins J. Biomol. NMR 50, 331-346
46. 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
47. 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
48. Bryan, P. N. and Orban, J. (2010) Proteins that switch folds Curr. Opin. Struct. Biol. 20, 482-488
49. Hammes, G. G., Chang, Y.-C., and Oas, T. G. (2009) Conformational selection or induced fit: a flux description of reaction mechanism Proc. Natl. Acad. Sci. U. S. A. 106, 13737-13741
50. Dogan, J., Schmidt, T., Mu, X., Engström, A., and Jemth, P. (2012) Fast association and slow transitions in the interaction between two intrinsically disordered protein domains J. Biol. Chem. 287, 34316-34324
51. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems: application to microtubules and the ribosome Proc. Natl. Acad. Sci. U. S. A. 98, 10037-10041