An isolated helix persists in a sparsely populated form of KIX under native conditions

Biochemistry

Volumn 45, Issue 29, 2006, Pages 8885-8893

  Tollinger, Martin ^a   Kloiber, Karin ^a   Ágoston, Bianka ^a   Dorigoni, Cornelia ^a   Lichtenecker, Roman ^a   Schmid, Walther ^a   Konrat, Robert ^a  

^a UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CONFORMATIONS; ELECTRON ENERGY LEVELS; HYDROPHOBICITY; NUCLEAR MAGNETIC RESONANCE; PERTURBATION TECHNIQUES; PLASMA PROBES;

FOLDING INTERMEDIATE; KIX; THREE-HELIX BUNDLE; TIME SCALE MOTIONS;

PROTEINS;

CELL PROTEIN; PROTEIN KIX; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CARBON NUCLEAR MAGNETIC RESONANCE; EQUILIBRIUM CONSTANT; FLOW KINETICS; HYDROPHOBICITY; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; STOPPED FLOW KINETICS;

CREB-BINDING PROTEIN; HYDROPHOBICITY; KINETICS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING;

EID: 33746239699     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0607305     Document Type: Article

References (63)

1. Shortle, D. (1996) The denatured state (the other half of the folding equation) and its role in protein stability, FASEB J. 10, 27-34.
2. Crowhurst, K. A., and Forman-Kay, J. D. (2003) Aromatic and methyl NOEs highlight hydrophobic clustering in the unfolded state of an SH3 domain, Biochemistry 42, 8687-8695.
3. Religa, T. L., Markson, J. S., Mayor, U., Freund, S. M., and Fersht, A. R. (2005) Solution structure of a protein denatured state and folding intermediate, Nature 437, 1053-1056.
4. Englander, S. W. (2000) Protein folding intermediates and pathways studied by hydrogen exchange, Annu. Rev. Biophys. Biomol. Struct. 29, 213-238.
5. Krishna, M. M., Hoang, L., Lin, Y., and Englander, S. W. (2004) Hydrogen exchange methods to study protein folding, Methods 34, 51-64.
6. Bai, Y., Chung, J., Dyson, H. J., and Wright, P. E. (2001) Structural and dynamic characterization of an unfolded state of poplar apoplastocyanin formed under nondenaturing conditions, Protein Sci. 10, 1056-1066.
7. Mayor, U., Grossmann, J. G., Foster, N. W., Freund, S. M., and Fersht, A. R. (2003) The denatured state of engrailed homeodomain under denaturing and native conditions, J. Mol. Biol. 333, 977-991.
8. Chugha, P., Sage, H. J., and Oas, T. G. (2006) Methionine oxidation of monomeric λ repressor: The denatured state ensemble under nondenaturing conditions, Protein Sci. 15, 533-542.
9. Myers, J. K., and Oas, T. G. (2002) Mechanism of fast protein folding, Annu. Rev. Biochem. 71, 783-815.
10. Palmer, A. G., III, Kroenke, C. D., and Loria, J. P. (2001) Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules, Methods Enzymol. 339, 204-238.
11. Korzhnev, D. M., Salvatella, X., Vendruscolo, M., Di Nardo, A. A., Davidson, A. R., Dobson, C. M., and Kay, L. E. (2004) Low-populated folding intermediates of Fyn SH3 characterized by relaxation dispersion NMR, Nature 430, 586-590.
12. Korzhnev, D. M., Neudecker, P., Mittermaier, A., Orekhov, V. Y., and Kay, L. E. (2005) Multiple-site exchange in proteins studied with a suite of six NMR relaxation dispersion experiments: An application to the folding of a Fyn SH3 domain mutant, J. Am. Chem. Soc. 127, 15602-15611.
13. 562, J. Am. Chem. Soc. 127, 5066-5072.
14. Grey, M. J., Tang, Y., Alexov, E., McKnight, C. J., Raleigh, D. P., and Palmer, A. G., III (2006) Characterizing a partially folded intermediate of the villin headpiece domain under non-denaturing conditions: Contribution of His41 to the pH-dependent stability of the N-terminal subdomain, J. Mol. Biol. 355, 1078-1094.
15. Mittermaier, A., Korzhnev, D. M., and Kay, L. E. (2005) Side-chain interactions in the folding pathway of a Fyn SH3 domain mutant studied by relaxation dispersion NMR spectroscopy, Biochemistry 44, 15430-15436.
16. Goodman, R. H., and Smolik, S. (2000) CBP/p300 in cell growth, transformation, and development, Genes Dev. 14, 1553-1577.
17. Giordano, A., and Avantaggiati, M. L. (1999) p300 and CBP: Partners for life and death, J. Cell. Physiol. 181, 218-230.
18. Dyson, H. J., and Wright, P. E. (2005) Intrinsically unstructured proteins and their functions, Nat. Rev. Mol. Cell Biol. 6, 197-208.
19. Radhakrishnan, I., Perez-Alvarado, G. C., Parker, D., Dyson, H. J., Montminy, M. R., and Wright, P. E. (1997) Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: A model for activator:coactivator interactions, Cell 91, 741-752.
20. Zor, T., De Guzman, R. N., Dyson, H. J., and Wright, P. E. (2004) Solution structure of the KIX domain of CBP bound to the transactivation domain of c-Myb, J. Mol. Biol. 337, 521-534.
21. Campbell, K. M., and Lumb, K. J. (2002) Structurally distinct modes of recognition of the KIX domain of CBP by Jun and CREB, Biochemistry 41, 13956-13964.
22. De Guzman, R. N., Goto, N. K., Dyson, H. J., and Wright, P. E. (2006) Structural basis for cooperative transcription factor binding to the CBP coactivator, J. Mol. Biol. 355, 1005-1013.
23. Goto, N. K., Zor, T., Martinez-Yamout, M., Dyson, H. J., and Wright, P. E. (2002) Cooperativity in transcription factor binding to the coactivator CREB-binding protein (CBP). The mixed lineage leukemia protein (MLL) activation domain binds to an allosteric site on the KIX domain, J. Biol. Chem. 277, 43168-43174.
24. Ernst, P., Wang, J., Huang, M., Goodman, R. H., and Korsmeyer, S. J. (2001) MLL and CREB bind cooperatively to the nuclear coactivator CREB-binding protein, Mol. Cell. Biol. 21, 2249-2258.
25. Rutledge, S. E., Volkman, H. M., and Schepartz, A. (2003) Molecular recognition of protein surfaces: High affinity ligands for the CBP KIX domain, J. Am. Chem. Soc. 125, 14336-14347.
26. 2H-labeled proteins, J. Biomol. NMR 13, 369-374.
27. Lichtenecker, R., Ludwiczek, M. L., Schmid, W., and Konrat, R. (2004) Simplification of protein NOESY spectra using bioorganic precursor synthesis and NMR spectral editing, J. Am. Chem. Soc. 126, 5348-5349.
28. Loria, J. P., Rance, M., and Palmer, A. G., III (1999) A relaxation-compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy, J. Am. Chem. Soc. 121, 2331-2332.
29. Tollinger, M., Skrynnikov, N. R., Mulder, F. A. 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.
30. Skrynnikov, N. R., Mulder, F. A., Hon, B., Dahlquist, F. W., and Kay, L. E. (2001) Probing slow time scale dynamics at methyl-containing side chains in proteins by relaxation dispersion NMR measurements: Application to methionine residues in a cavity mutant of T4 lysozyme, J. Am. Chem. Soc. 123, 4556-4566.
31. McConnell, H. M. (1958) Reaction rates by nuclear magnetic resonance, J. Chem. Phys. 28, 430-431.
32. Motulsky, H., and Christopoulos, A. (2004) Fitting Models to Biological Data using Linear and Nonlinear Regression, Oxford University Press, Oxford, U.K.
33. Schwarzinger, S., Kroon, G. J., Foss, T. R., Chung, J., Wright, P. E., and Dyson, H. J. (2001) Sequence-dependent correction of random coil NMR chemical shifts, J. Am. Chem. Soc. 123, 2970-2978.
34. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects, J. Biomol. NMR J, 67-81.
35. Bai, Y., Milne, J. S., Mayne, L., and Englander, S. W. (1993) Primary structure effects on peptide group hydrogen exchange, Proteins 17, 75-86.
36. Pace, C. N., and Shaw, K. L. (2000) Linear extrapolation method of analyzing solvent denaturation curves, Proteins Suppl. 4, 1-7.
37. Maxwell, K. L., Wildes, D., Zarrine-Afsar, A., De Los Rios, M. A., Brown, A. G., Friel, C. T., Hedberg, L., Horng, J. C., Bona, D., Miller, E. J., Vallee-Belisle, A., Main, E. R., Bemporad, F., Qiu, L., Teilum, K., Vu, N. D., Edwards, A. M., Ruczinski, I., Poulsen, F. M., Kragelund, B. B., Michnick, S. W., Chili, F., Bai, Y., Hagen, S. J., Serrano, L., Oliveberg, M., Raleigh, D. P., Wittung-Stafshede, P., Radford, S. E., Jackson, S. E., Sosnick, T. R., Marqusee, S., Davidson, A. R., and Plaxco, K. W. (2005) Protein folding: Defining a "standard" set of experimental conditions and a preliminary kinetic data set of two-state proteins, Protein Sci. 14, 602-616.
38. 15N NMR relaxation, Biochemistry 33, 5984-6003.
39. Korzhnev, D. M., Skrynnikov, N. R., Millet, O., Torchia, D. A., and Kay, L. E. (2002) An NMR experiment for the accurate measurement of heteronuclear spin-lock relaxation rates, J. Am. Chem. Soc. 124, 10743-10753.
40. Kloiber, K., Tollinger, M., and Konrat, R. Manuscript in preparation.
41. 15N 'Random Coil' Chemical Shifts, J. Am. Chem. Soc. 116, 8466-8469.
42. Brockwell, D., Yu, L., Cooper, S., McCleland, S., Cooper, A., Attwood, D., Gaskell, S. J., and Barber, J. (2001) Physicochemical consequences of the perdeuteriation of glutathione S-transferase from S. japonicum, Protein Sci. 10, 572-580.
43. Clarke, J., and Fersht, A. R. (1996) An evaluation of the use of hydrogen exchange at equilibrium to probe intermediates on the protein folding pathway, Folding Des. 1, 243-254.
44. Clarke, J., Itzhaki, L. S., and Fersht, A. R. (1997) Hydrogen exchange at equilibrium: A short cut for analysing protein-folding pathways? Trends Biochem. Sci. 22, 284-287.
45. Mittermaier, A., and Kay, L. E. (2006) New tools provide new insights in NMR studies of protein dynamics, Science 312, 224-228.
46. Eaton, W, A., Munoz, V., Thompson, P. A., Henry, E. R., and Hofrichter, J. (1998) Kinetics and Dynamics of Loops, α-Helices, β-Hairpins and Fast Folding Proteins, Acc. Chem. Res. 31, 745-753.
47. Tompa, P. (2005) The interplay between structure and function in intrinsically unstructured proteins, FEBS Lett. 579, 3346-3354.
48. Iakoucheva, L. M., Brown, C. J., Lawson, J. D., Obradovic, Z., and Dunker, A. K. (2002) Intrinsic disorder in cell-sgnalling and cancer-associated proteins, J. Mol. Biol. 323, 573-584.
49. Horng, J. C., Tracz, S. M., Lumb, K. J., and Raleigh, D. P. (2005) Slow folding of a three-helix protein via a compact intermediate, Biochemistry 44, 627-634.
50. Mayor, U., Guydosh, N. R., Johnson, C. M., Grossmann, J. G., Sato, S., Jas, G. S., Freund, S. M., Alonso, D. O., Daggett, V., and Fersht, A. R. (2003) The complete folding pathway of a protein from nanoseconds to microseconds, Nature 421, 863-867.
51. Raschke, T. M., and Marqusee, S. (1997) The kinetic folding intermediate of ribonuclease H resembles the acid molten globule and partially unfolded molecules detected under native conditions, Nat. Struct. Biol. 4, 298-304.
52. Bai, Y., Sosnick, T. R., Mayne, L., and Englander, S. W. (1995) Protein folding intermediates: Native-state hydrogen exchange, Science 269, 192-197.
53. Gsponer, J., Hopearuoho, H., Whittaker, S. B., Spence, G. R., Moore, G. R., Paci, E., Radford, S. E., and Vendruscolo, M. (2006) Determination of an ensemble of structures representing the intermediate state of the bacterial immunity protein Im7, Proc. Natl. Acad. Sci. U.S.A. 103, 99-104.
54. Krishna, M. M., Lin, Y., Mayne, L., and Englander, S. W. (2003) Intimate view of a kinetic protein folding intermediate: residue-resolved structure, interactions, stability, folding and unfolding rates, homogeneity, J. Mol. Biol. 334, 501-513.
55. Jennings, P. A., and Wright, P. E. (1993) Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin, Science 262, 892-896.
56. Maity, H., Maity, M., Krishna, M. M., Mayne, L., and Englander, S. W. (2005) Protein folding: The stepwise assembly of foldon units, Proc. Natl. Acad. Sci. U.S.A. 102, 4741-4746.
57. Kim, P. S., and Baldwin, R. L. (1982) Specific intermediates in the folding reactions of small proteins and the mechanism of protein folding, Annu. Rev. Biochem. 51, 459-489.
58. Baldwin, R. L., and Rose, G. D. (1999) Is protein folding hierarchic? I. Local structure and peptide folding, Trends Biochem. Sci. 24, 26-33.
59. Daggett, V., and Fersht, A. R. (2003) Is there a unifying mechanism for protein folding? Trends Biochem. Sci. 28, 18-25.
60. Gianni, S., Guydosh, N. R., Khan, F., Caldas, T. D., Mayor, U., White, G. W., DeMarco, M. L., Daggett, V., and Fersht, A. R. (2003) Unifying features in protein-folding mechanisms, Proc. Natl. Acad. Sci. U.S.A. 100, 13286-13291.
61. White, G. W., Gianni, S., Grossmann, J. G., Jemth, P., Fersht, A. R., and Daggett, V. (2005) Simulation and experiment conspire to reveal cryptic intermediates and a slide from the nucleation-condensation to framework mechanism of folding, J. Mol. Biol. 350, 757-775.
62. Cranz-Mileva, S., Friel, C. T., and Radford, S. E. (2005) Helix stability and hydrophobicity in the folding mechanism of the bacterial immunity protein Im9, Protein Eng., Des. Sel. 18, 41-50.
63. Lacroix, E., Viguera, A. R., and Serrano, L. (1998) Elucidating the folding problem of α-helices: Local motifs, long-range electrostatics, ionic-strength dependence and prediction of NMR parameters, J. Mol. Biol. 284, 173-191.