Thermodynamic dissection of the intrinsically disordered N-terminal domain of human glucocorticoid receptor

Journal of Biological Chemistry

Volumn 287, Issue 32, 2012, Pages 26777-26787

  Li, Jing ^a,b   Motlagh, Hesam N ^b   Chakuroff, Carolyn ^a   Thompson, E Brad ^c,d   Hilser, Vincent J ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c University of Houston   (United States)

^d University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SIGNALING; DEGREE OF COUPLING; FOLDED STATE; FOLDING TRANSITION; FUNCTIONAL SITES; GLOBULAR PROTEINS; GLUCOCORTICOID RECEPTOR; ISOFORMS; N-TERMINAL DOMAINS; NATURALLY OCCURRING; OSMOLYTES; REGULATORY REGIONS; STEROID HORMONE RECEPTORS; TRANSCRIPTIONAL ACTIVITY; TRIMETHYLAMINE N OXIDES;

TRANSCRIPTION FACTORS;

HORMONES;

GLUCOCORTICOID RECEPTOR; TRIMETHYLAMINE OXIDE;

AMINO TERMINAL SEQUENCE; ARTICLE; MOLECULAR SIZE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STABILITY; THERMODYNAMICS;

CIRCULAR DICHROISM; HUMANS; PROTEIN CONFORMATION; RECEPTORS, GLUCOCORTICOID; SPECTROMETRY, FLUORESCENCE; SPECTROPHOTOMETRY, ULTRAVIOLET; THERMODYNAMICS; TRYPTOPHAN;

EID: 84864545860     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.355651     Document Type: Article

References (55)

1. Tantos, A., Han, K. H., and Tompa, P. (2012) Intrinsic disorder in cell signaling and gene transcription. Mol. Cell. Endocrinol. 348, 457-465
2. Liu, J., Perumal, N. B., Oldfield, C. J., Su, E. W., Uversky, V. N., and Dunker, A. K. (2006) Intrinsic disorder in transcription factors. Biochemistry 45, 6873-6888 (Pubitemid 43856673)
3. Tompa, P. (2002) Intrinsically unstructured proteins. Trends Biochem. Sci. 27, 527-533
4. Uversky, V. N. (2011) Intrinsically disordered proteins from A to Z. Int. J. Biochem. Cell Biol. 43, 1090-1103
5. Dyson, H. J., and Wright, P. E. (2005) Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6, 197-208 (Pubitemid 40314921)
6. Fink, A. L. (2005) Natively unfolded proteins. Curr. Opin. Struct. Biol. 15, 35-41
7. Dyson, H. J., and Wright, P. E. (2002) Coupling of folding and binding for unstructured proteins. Curr. Opin. Struct. Biol. 12, 54-60 (Pubitemid 34142721)
8. Babu, M. M., van der Lee, R., de Groot, N. S., and Gsponer, J. (2011) Intrinsically disordered proteins: regulation and disease. Curr. Opin. Struct. Biol. 21, 432-440
9. Midic, U., Oldfield, C. J., Dunker, A. K., Obradovic, Z., and Uversky, V. N. (2009) Unfoldomics of human genetic diseases: illustrative examples of ordered and intrinsically disordered members of the human diseasome. Protein Pept. Lett. 16, 1533-1547
10. Kumar, R., Lee, J. C., Bolen, D. W., and Thompson, E. B. (2001) The conformation of the glucocorticoid receptor af1/tau1 domain induced by osmolyte binds co-regulatory proteins. J. Biol. Chem. 276, 18146-18152
11. Baskakov, I., and Bolen, D. W. (1998) Forcing thermodynamically unfolded proteins to fold. J. Biol. Chem. 273, 4831-4834 (Pubitemid 28108630)
12. Auton, M., and Bolen, D. W. (2005) Predicting the energetics of osmolyte-induced protein folding/unfolding. Proc. Natl. Acad. Sci. U.S.A. 102, 15065-15068 (Pubitemid 41513335)
13. Griekspoor, A., Zwart, W., Neefjes, J., and Michalides, R. (2007) Visualizing the action of steroid hormone receptors in living cells. Nucl. Recept. Signal. 5, e003
14. McEwan, I. J., Lavery, D., Fischer, K., and Watt, K. (2007) Natural disordered sequences in the amino terminal domain of nuclear receptors: lessons from the androgen and glucocorticoid receptors. Nucl. Recept. Signal. 5, e001
15. Lavery, D. N., and McEwan, I. J. (2005) Structure and function of steroid receptor AF1 transactivation domains: induction of active conformations. Biochem. J. 391, 449-464 (Pubitemid 41634771)
16. Hollenberg, S. M., and Evans, R. M. (1988) Multiple and cooperative transactivation domains of the human glucocorticoid receptor. Cell 55, 899-906
17. Dahlman-Wright, K., Almlöf, T., McEwan, I. J., Gustafsson, J. A., and Wright, A. P. (1994) Delineation of a small region within the major transactivation domain of the human glucocorticoid receptor that mediates transactivation of gene expression. Proc. Natl. Acad. Sci. U.S.A. 91, 1619-1623 (Pubitemid 24080256)
18. Bray, P. J., and Cotton, R. G. (2003) Variations of the human glucocorticoid receptor gene (NR3C1): pathological and in vitro mutations and polymorphisms. Hum. Mutat. 21, 557-568 (Pubitemid 36667344)
19. Lu, N. Z., and Cidlowski, J. A. (2005) Translational regulatory mechanisms generate N-terminal glucocorticoid receptor isoforms with unique transcriptional target genes. Mol. Cell 18, 331-342 (Pubitemid 41350538)
20. Bolen, D. W., and Baskakov, I. V. (2001) The osmophobic effect: natural selection of a thermodynamic force in protein folding. J. Mol. Biol. 310, 955-963 (Pubitemid 32738368)
21. Bolen, D. W. (2001) Protein stabilization by naturally occurring osmolytes. Methods Mol. Biol. 168, 17-36
22. Baskakov, I. V., Kumar, R., Srinivasan, G., Ji, Y. S., Bolen, D. W., and Thompson, E. B. (1999) Trimethylamine N-oxide-induced cooperative folding of an intrinsically unfolded transcription-activating fragment of human glucocorticoid receptor. J. Biol. Chem. 274, 10693-10696
23. Kumar, R., Baskakov, I. V., Srinivasan, G., Bolen, D. W., Lee, J. C., and Thompson, E. B. (1999) Interdomain signaling in a two-domain fragment of the human glucocorticoid receptor. J. Biol. Chem. 274, 24737-24741
24. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4, 2411-2423
25. Tsumoto, K., Umetsu, M., Kumagai, I., Ejima, D., Philo, J. S., and Arakawa, T. (2004) Role of arginine in protein refolding, solubilization, and purification. Biotechnol. Prog. 20, 1301-1308 (Pubitemid 39351313)
26. Uversky, V. N. (2002) Natively unfolded proteins: a point where biology waits for physics. Protein Sci. 11, 739-756
27. Whitmore, L., Woollett, B., Miles, A. J., Klose, D. P., Janes, R. W., and Wallace, B. A. (2011) PCDDB: the Protein Circular Dichroism Data Bank, a repository for circular dichroism spectral and metadata. Nucleic Acids Res. 39, D480-D486
28. Santoro, M. M., and Bolen, D. W. (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl α-chymotrypsin using different denaturants. Biochemistry 27, 8063-8068
29. Wu, P., and Bolen, D. W. (2006) Osmolyte-induced protein folding free energy changes. Proteins 63, 290-296
30. Tanford, C. (1964) Isothermal unfolding of globular proteins in Aqueous Urea Solutions. J. Am. Chem. Soc. 86, 2050-2059
31. Auton, M., and Bolen, D. W. (2007) Application of the transfer model to understand how naturally occurring osmolytes affect protein stability. Methods Enzymol. 428, 397-418
32. Henikoff, S., and Henikoff, J. G. (1992) Amino acid substitution matrices from protein blocks. Proc. Natl. Acad. Sci. U.S.A. 89, 10915-10919
33. Midic, U., Dunker, A. K., and Obradovic, Z. (2009) Protein sequence alignment and structural disorder: a substitution matrix for an extended alphabet. StReBio 9, 27-31
34. Wright, P. E., and Dyson, H. J. (1999) Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J. Mol. Biol. 293, 321-331 (Pubitemid 29516173)
35. Ghosh, K., and Dill, K. A. (2009) Computing protein stabilities from their chain lengths. Proc. Natl. Acad. Sci. U.S.A. 106, 10649-10654
36. Pradeep, L., and Udgaonkar, J. B. (2004) Osmolytes induce structure in an early intermediate on the folding pathway of barstar. J. Biol. Chem. 279, 40303-40313 (Pubitemid 39287615)
37. Henkels, C. H., Kurz, J. C., Fierke, C. A., and Oas, T. G. (2001) Linked folding and anion binding of the Bacillus subtilis ribonuclease P protein. Biochemistry 40, 2777-2789 (Pubitemid 32198279)
38. Mello, C. C., and Barrick, D. (2003) Measuring the stability of partly folded proteins using TMAO. Protein Sci. 12, 1522-1529 (Pubitemid 36759355)
39. Kumar, R., Serrette, J. M., Khan, S. H., Miller, A. L., and Thompson, E. B. (2007) Effects of different osmolytes on the induced folding of the N-terminal activation domain (AF1) of the glucocorticoid receptor. Arch. Biochem. Biophys. 465, 452-460 (Pubitemid 47362005)
40. Shortle, D. (1995) Staphylococcal nuclease: a showcase of m-value effects. Adv. Protein Chem. 46, 217-247
41. Whitten, S. T., Wooll, J. O., Razeghifard, R., García-Moreno, E. B., and Hilser, V. J. (2001) The origin of pH-dependent changes in m-values for the denaturant-induced unfolding of proteins. J. Mol. Biol. 309, 1165-1175 (Pubitemid 32623315)
42. Hilser, V. J., and Thompson, E. B. (2007) Intrinsic disorder as a mechanism to optimize allosteric coupling in proteins. Proc. Natl. Acad. Sci. U.S.A. 104, 8311-8315 (Pubitemid 47175484)
43. Luque, I., Leavitt, S. A., and Freire, E. (2002) The linkage between protein folding and functional cooperativity: two sides of the same coin? Annu. Rev. Biophys. Biomol. Struct. 31, 235-256 (Pubitemid 34666832)
44. Monod, J., Wyman, J., and Changeux, J. P. (1965) On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12, 88-118
45. Koshland, D. E., Jr., Némethy, G., and Filmer, D. (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5, 365-385
46. Hilser, V. J. (2010) Biochemistry. An ensemble view of allostery. Science 327, 653-654
47. Cooper, A., and Dryden, D. T. (1984) Allostery without conformational change. A plausible model. Eur. Biophys. J. 11, 103-109
48. Bai, F., Branch, R. W., Nicolau, D. V., Jr., Pilizota, T., Steel, B. C., Maini, P. K., and Berry, R. M. (2010) Conformational spread as a mechanism for cooperativity in the bacterial flagellar switch. Science 327, 685-689
49. Pan, H., Lee, J. C., and Hilser, V. J. (2000) Binding sites in Escherichia coli dihydrofolate reductase communicate by modulating the conformational ensemble. Proc. Natl. Acad. Sci. U.S.A. 97, 12020-12025
50. Popovych, N., Sun, S., Ebright, R. H., and Kalodimos, C. G. (2006) Dynamically driven protein allostery. Nat. Struct. Mol. Biol. 13, 831-838 (Pubitemid 44338778)
51. Reichheld, S. E., Yu, Z., and Davidson, A. R. (2009) The induction of folding cooperativity by ligand binding drives the allosteric response of tetracycline repressor. Proc. Natl. Acad. Sci. U.S.A. 106, 22263-22268
52. Kobayashi, Y., Mercado, N., Barnes, P. J., and Ito, K. (2011) Defects of protein phosphatase 2A causes corticosteroid insensitivity in severe asthma. PLoS One 6, e27627
53. Freiburger, L. A., Baettig, O. M., Sprules, T., Berghuis, A. M., Auclair, K., Mittermaier, A. K. (2011) Competing allosteric mechanisms modulate substrate binding in a dimeric enzyme. Nat. Struct. Mol. Biol. 18, 288-294
54. Garcia-Pino, A., Balasubramanian, S., Wyns, L., Gazit, E., De Greve, H., Magnuson, R. D., Charlier, D., van Nuland, N. A., and Loris, R. (2010) Allostery and intrinsic disorder mediate transcription regulation by conditional cooperativity. Cell 142, 101-111
55. Motlagh, H. N., and Hilser, V. J. (2012) Agonism/antagonism switching in allosteric ensembles. Proc. Natl. Acad. Sci. U.S.A. 109, 4134-4139