Steroid-induced conformational changes of rat glucocorticoid receptor cause altered trypsin cleavage of the putative helix 6 in the ligand binding domain

Molecular and Cellular Endocrinology

Volumn 155, Issue 1-2, 1999, Pages 85-100

  Xu, Min ^a   Modarress, Kevin J ^a   Meeker, James E W ^a   Simons Jr , S Stoney ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Apo glucocorticoid receptor; Helix 6; Meroreceptor; Trypsin digestion

Indexed keywords

AMINO ACID; ARGININE; ESTROGEN RECEPTOR; GLUCOCORTICOID RECEPTOR; PROGESTERONE RECEPTOR; STEROID; TRYPSIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CONFORMATIONAL TRANSITION; LIGAND BINDING; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN TERTIARY STRUCTURE; RAT;

AMINO ACID SUBSTITUTION; ANIMALS; BINDING SITES; COS CELLS; DEXAMETHASONE; HUMANS; KINETICS; LIGANDS; MICE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PEPTIDE FRAGMENTS; PROTEIN BIOSYNTHESIS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; RATS; RECEPTORS, GLUCOCORTICOID; RECOMBINANT FUSION PROTEINS; TRANSCRIPTION, GENETIC; TRANSFECTION; TRYPSIN;

EID: 0032860359     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0303-7207(99)00110-0     Document Type: Article

References (82)

1. Allan G.F., Leng X., Tsai S.Y., Weigel N.L., Edwards D.P., Tsai M.-J., O'Malley B.W. Hormone and antihormone induce distinct conformational changes which are central to steroid receptor activation. J. Biol. Chem. 267:1992;19513-19520.
2. Allan G.F., Lombardi E., Haynes-Johnson D., Palmer S., Kiddoe M., Kraft P., Campen C., Rybczynski P., Combs D.W., Phillips A. Induction of a novel conformation in the progesterone receptor by ZK299 involves a defined region of the carboxyl-terminal tail. Mol. Endocrinol. 10:1996;1206-1213.
3. Berry M., Metzger D., Chambon P. Role of the two activating domains of the oestrogen receptor in the cell-type and promoter-context dependent agonistic activity of the anti-oestrogen 4-hydroxytamoxifen. EMBO J. 9:1990;2811-2818.
4. Bourguet W., Ruff M., Chambon P., Gronemeyer H., Moras D. Crystal structure of the ligand-binding domain of the human nuclear receptor RXR-alpha. Nature. 375:1995;377-382.
5. Bresnick E.H., Dalman F.C., Sanchez E.R., Pratt W.B. Evidence that the 90-kDa heat shock protein is necessary for the steroid binding conformation of the L cell glucocorticoid receptor. J. Biol. Chem. 264:1989;4992-4997.
6. Brzozowski A.M., Pike A.C.W., Dauter Z., Hubbard R.E., Bonn T., Engstrom O., Ohman L., Greene G.L., Gustafsson J.-A., Carlquist M. Molecular basis of agonism and antagonism in the oestrogen receptor. Nature. 389:1997;753-758.
7. Carlstedt-Duke J., Stromstedt P.-E., Wrange O., Bergman T., Gustafsson J.-A., Jornvall H. Domain structure of the glucocorticoid receptor protein. Proc. Natl. Acad. Sci. USA. 84:1987;4437-4440.
8. Chakraborti P.K., Simons S.S. Jr. Association of heat shock protein 90 with the 16 kDa steroid binding core fragment of rat glucocorticoid receptors. Biochem. Biophys. Res. Commun. 176:1991;1338-1344.
9. Chakraborti P.K., Garabedian M.J., Yamamoto K.R., Simons S.S. Jr. Creation of 'super' glucocorticoid receptors by point mutations in the steroid binding domain. J. Biol. Chem. 266:1991;22075-22078.
10. Chakraborti P.K., Garabedian M.J., Yamamoto K.R., Simons S.S. Jr. Role of cysteines 640, 656, and 661 in steroid binding to rat glucocorticoid receptors. J. Biol. Chem. 267:1992;11366-11373.
11. Couette B., Fagart J., Jalaguier S., Lombes M., Souque A., Rafestin-Oblin M.-E. Ligand-induced conformational change in the human mineralocorticoid receptor occurs within its hetero-oligomeric structure. Biochem. J. 315:1996;421-427.
12. de Castro M., Elliot S., Kino T., Bamberger C., Karl M., Webster E., Chrousos G.P. The non-ligand binding beta-isoform of the human glucocorticoid receptor (hGR beta): tissue levels, mechanism of action, and potential physiologic role. Mol. Med. 2:1996;597-607.
13. r=90,000 heat shock protein with the steroid-binding domain of the glucocorticoid receptor. J. Biol. Chem. 263:1988;18520-18523.
14. Eisen L.P., Reichman M.E., Thompson E.B., Gametchu B., Harrison R.W., Eisen H.J. Monoclonal antibody to the rat glucocorticoid receptor. Relationship between the immunoreactive and DNA-binding domain. J. Biol. Chem. 260:1985;11805-11810.
15. Flach H., Kaiser U., Westphal H.M. Monoclonal antipeptide antibodies to the glucocorticoid receptor. J. Steroid Biochem. Mol. Biol. 42:1992;467-474.
16. Fontana A., Fassina G., Vita C., Dalzoppo D., Zamai M., Zambonin M. Correlation between sites of limited proteolysis and segmental mobility in thermolysin. Biochemistry. 25:1986;1847-1851.
17. Fritsch M., Leary C.M., Furlow J.D., Ahrens H., Schuh T.J., Mueller G.C., Gorski J.A. Ligand-induced conformational change in the estrogen receptor is localized in the steroid binding domain. Biochemistry. 31:1992;5303-5311.
18. Fritsch M., Anderson I., Leary C.M., Gorski J. Two populations of the estrogen receptor separated and characterized using aqueous two-phase partitioning. Biochemistry. 36:1997;6230-6242.
19. Guido E.C., Delorme E.O., Clemm D.L., Stein R.B., Rosen J., Miner J.N. Determinants of promoter-specific activity by glucocorticoid receptor. Mol. Endocrinol. 10:1996;1178-1190.
20. Ho S.N., Hunt H.D., Horton R.M., Pullen J.K., Pease L.R. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene. 77:1989;51-59.
21. Hoeck W., Rusconi S., Groner B. Down-regulation and phosphorylation of glucocorticoid receptors in cultured cells. J. Biol. Chem. 264:1989;14396-14402.
22. r discrepancy in gel migration of the mouse glucocorticoid receptor to the major phosphorylated cyanogen bromide fragment in the transactivating domain. J. Steroid Biochem. Mol. Biol. 46:1993;681-686.
23. Ikonen T., Palvimo J.J., Janne O.A. Interaction between the amino- and carboxyl-terminal regions of the rat androgen receptor modulates transcriptional activity and is influenced by nuclear receptor coactivators. J. Biol. Chem. 272:1997;29821-29828.
24. Kahmann S., Vassen L., Klein-Hitpass L. Synergistic enhancement of PRb-mediated RU486 and R5020 agonist activities through cyclic adenosine 3′,5′-monophosphate represents a delayed primary response. Mol. Endocrinol. 12:1998;278-289.
25. Kasper C.B. Fragmentation of proteins for sequence studies and separation of peptide mixtures. Mol. Biol. Biochem. Biophys. 8:1975;114-161.
26. Katzenellenbogen J.A., O'Malley B.W., Katzenellenbogen B.S. Tripartite steroid hormone receptor pharmacology: interaction with multiple effector sites as a basis for the cell- and promoter-specific action of these hormones. Mol. Endocrinol. 10:1996;119-131.
27. Keidel S., Lamour F.P.Y., Apfel C.M. Mutational analysis reveals that all-trans-retinoic acid, 9-cis-retinoic acid, and antagonist interact with distinct binding determinants of RARalpha. J. Biol. Chem. 272:1997;18267-18272.
28. Kuil C.W., Berrevoets C.A., Mulder E. Ligand-induced conformational alterations of the androgen receptor analyzed by limited trypsinization. J. Biol. Chem. 270:1995;27569-27576.
29. Kumar V., Chambon P. The estrogen receptor binds tightly to its responsive element as a ligand-induced homodimer. Cell. 55:1988;145-156.
30. 2-/carboxyl-terminal interactions in androgen receptor dimerization revealed by mutations that cause androgen insensitivity. J. Biol. Chem. 273:1998;92-101.
31. Lanz R.B., Rusconi S. A conserved carboxy-terminal subdomain is important for ligand interpretation and transactivation by nuclear receptors. Endocrinology. 135:1994;2183-2194.
32. Lopez S., Miyashita Y., Simons S.S. Jr. Structurally based, selective interaction of arsenite with steroid receptors. J. Biol. Chem. 265:1990;16039-16042.
33. McDonnell D.P., Clemm D.L., Hermann T., Goldman M.E., Pike J.W. Analysis of estrogen receptor function in vitro reveals three distinct classes of antiestrogens. Mol. Endocrinol. 9:1995;659-669.
34. McInerney E.M., Tsai M.-J., O'Malley B.W., Katzenellenbogen B.S. Analysis of estrogen receptor transcriptional enhancement by a nuclear hormone receptor coactivator. Proc. Natl. Acad. Sci. USA. 93:1996;10069-10073.
35. Mercier L., Thompson E.B., Simons S.S. Jr. Dissociation of steroid binding to receptors and steroid induction of biological activity in a glucocorticoid responsive cell. Endocrinology. 112:1983;601-609.
36. Mercier L., Miller P.A., Simons S.S. Jr. Antiglucocorticoid steroids have increased agonist activity in those hepatoma cell lines that are more sensitive to glucocorticoids. J. Steroid Biochem. 25:1986;11-20.
37. Meyer M.-E., Pornon A., Ji J., Bocquel M.-T., Chambon P., Gronemeyer H. Agonistic and antagonistic activities of RU486 on the functions of the human progesterone receptor. EMBO J. 9:1990;3923-3932.
38. Miller N.R., Simons S.S. Jr. Steroid binding to hepatoma tissue culture cell glucocorticoid receptors involves at least two sulfhydryl groups. J. Biol. Chem. 263:1988;15217-15225.
39. Minucci S., Leid M., Toyama R., Saint-Jeannet J.-P., Peterson V.J., Horn V., Ishmael J.E., Bhattacharyya N., Dey A., Dawid I.B., Ozato K. Retinoid X receptor (RXR) within the RXR-retinoic acid receptor heterodimer binds its ligand and enhances retinoid-dependent gene expression. Mol. Cell. Biol. 17:1997;644-655.
40. Modarress K.J., Cavanaugh A.H., Chakraborti P.K., Simons S.S. Jr. Metal oxyanion stabilization of the rat glucocorticoid receptor is independent of thiols. J. Biol. Chem. 269:1994;25621-25628.
41. Modarress K.J., Opoku J., Xu M., Sarlis N.J., Simons S.S. Jr. Steroid-induced conformational changes at ends of the hormone binding domain in the rat glucocorticoid receptor are independent of agonist vs. antagonist activity. J. Biol. Chem. 272:1997;23986-23994.
42. Nayeri S., Kahlen J.-P., Carlberg C. The high affinity ligand binding conformation of the nuclear 1,25-dihydroxyvitamin D3 receptor is functionally linked to the transactivation domain 2 (AF-2). Nucleic Acids Res. 24:1996;4513-4518.
43. Nolte R.T., Wisely G.B., Westin S., Cobb J.E., Lambert M.H., Kurokawa R., Rosenfeld M.G., Willson T.M., Glass C.K., Milburn M.V. Ligand binding and co-activator assembly of the peroxisome proliferator-activated receptor-gamma. Nature. 395:1998;137-143.
44. Ohara-Nemoto Y., Stromstedt P.-E., Dahlman-Wright K., Nemoto T., Gustafsson J.-A., Carlstedt-Duke J. The steroid-binding properties of recombinant glucocorticoid receptor: a putative role for heat shock protein hsp90. J. Steroid Biochem. Mol. Biol. 37:1990;481-490.
45. Oshima H., Simons S.S. Jr. Modulation of transcription factor activity by a distant steroid modulatory element. Mol. Endocrinol. 6:1992;416-428.
46. Picard D., Khursheed B., Garabedian M.J., Fortin M.G., Lindquist S., Yamamoto K.R. Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature. 348:1990;166-168.
47. Pratt W.B. The role of heat shock proteins in regulating the function, folding, and trafficking of the glucocorticoid receptor. J. Biol. Chem. 268:1993;21455-21458.
48. Pratt W.B., Toft D.O. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev. 18:1997;306-360.
49. Reichman M.E., Foster C.M., Eisen L.P., Eisen H.J., Torain B.F., Simons S.S. Jr. Limited proteolysis of covalently labeled glucocorticoid receptors as a probe of receptor structure. Biochemistry. 23:1984;5376-5384.
50. Renaud J.-P., Rochel N., Ruff M., Vivat V., Chambon P., Gronemeyer H., Moras D. Crystal structure of the RAR-gramma ligand-binding domain bound to all-trans retinoic acid. Nature. 378:1995;681-689.
51. Rexin M., Busch W., Segnitz B., Gehring U. Structure of the glucocorticoid receptor in intact cells in the absence of hormone. J. Biol. Chem. 267:1992;9619-9621.
52. Santos M.A.S., Tuite M.F. The CUG codon is decoded in vivo as serine and not leucine in Candida albicans. Nucleic Acids Res. 23:1995;1481-1486.
53. Schulman I.G., Shao G., Heyman R.A. Transactivation by retinoid X receptor-peroxisome proliferator-activated receptor gamma (PPARgamma) heterodimers: intermolecular synergy requires only the PPARgamma hormone-dependent activation function. Mol. Cell. Biol. 18:1998;3483-3494.
54. Seielstad D.A., Carlson K.E., Kushner P.J., Greene G.L., Katzenellenbogen J.A. Analysis of the structural core of the human estrogen receptor ligand binding domain by selective proteolysis/mass spectrometric analysis. Biochemistry. 34:1995;12605-12615.
55. Sherman M.R., Pickering L.A., Rollwagen F.M., Miller L.K. Mero-receptors: proteolytic fragments of receptors containing the steroid-binding site. Fed. Proc. 37:1978;167-173.
56. Sherman M.R., Moran M.C., Tuazon F.B., Stevens Y.-W. Structure, dissociation, and proteolysis of mammalian steroid receptors. Multiplicity of glucocorticoid receptor forms and proteolytic enzymes in rat liver and kidney cytosols. J. Biol. Chem. 258:1983;10366-10377.
57. Shiau A.K., Barstad D., Loria P.M., Cheng L., Kushner P.J., Agard D.A., Greene G.L. The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell. 95:1998;927-937.
58. Simons S.S. Jr. Function/activity of specific amino acids in glucocorticoid receptors. Vitamins Horm. 48:1994;49-130.
59. Simons, S.S., Jr., 1998. Structure and function of the steroid and nuclear receptor ligand-binding domain. In: Freedman, L.P. (Ed.), The Molecular Biology of Steroid and Nuclear Hormone Receptors, Birkhäuser, Boston, MA, pp. 35-104.
60. Simons S.S. Jr., Miller P.A. Comparison of DNA binding properties of activated, covalent and noncovalent glucocorticoid receptor-steroid complexes from HTC cells. Biochemistry. 23:1984;6876-6882.
61. Simons S.S. Jr., Thompson E.B. Dexamethasone 21-mesylate: an affinity label of glucocorticoid receptors from rat hepatoma tissue culture cells. Proc. Natl. Acad. Sci. USA. 78:1981;3541-3545.
62. Simons S.S. Jr., Pons M., Johnson D.F. α-Keto mesylate: a reactive thiol-specific functional group. J. Org. Chem. 45:1980;3084-3088.
63. Simons S.S. Jr., Pumphrey J.G., Rudikoff S., Eisen H.J. Identification of cysteine-656 as the amino acid of HTC cell glucocorticoid receptors that is covalently labeled by dexamethasone 21-mesylate. J. Biol. Chem. 262:1987;9676-9680.
64. Simons S.S. Jr., Sistare F.D., Chakraborti P.K. Steroid binding activity is retained in a 16-kDa fragment of the steroid binding domain of rat glucocorticoid receptors. J. Biol. Chem. 264:1989;14493-14497.
65. Simons S.S. Jr., Chakraborti P.K., Cavanaugh A.H. Arsenite and cadmium(II) as probes of glucocorticoid receptor structure and function. J. Biol. Chem. 265:1990;1938-1945.
66. Simons S.S. Jr., Oshima H., Szapary D. Higher levels of control: modulation of steroid hormone-regulated gene transcription. Mol. Endocrinol. 6:1992;995-1002.
67. Szapary D., Xu M., Simons S.S. Jr. Induction properties of a transiently transfected glucocorticoid-responsive gene vary with glucocorticoid receptor concentration. J. Biol. Chem. 271:1996;30576-30582.
68. Tanenbaum D.M., Wang Y., Williams S.P., Sigler P.B. Crystallographic comparison of the estrogen and progesterone receptor's ligand binding domains. Proc. Natl. Acad. Sci. USA. 95:1998;5998-6003.
69. Tetel M.J., Jung S., Carbajo P., Ladtkow T., Skafar D.F., Edwards D.P. Hinge and amino-terminal sequences contribute to solution dimerization of human progesterone receptor. Mol. Endocrinol. 11:1997;1114-1128.
70. Thole H.H. Assignment of the ligand binding site of the porcine estradiol receptor to the N-terminal 17 KDa part of domain E. FEBS Lett. 320:1993;92-96.
71. Thole H.H., Jungblut P.W. The ligand-binding site of the estradiol receptor resides in a non-covalent complex of two consecutive peptides of 17 and 7 kDa. Biochem. Biophys. Res. Commun. 199:1994;826-833.
72. Towers T.L., Freedman L.P. Granulocyte-macrophage colony-stimulating factor gene transcription is directly repressed by the vitamin D3 receptor. Implications for allosteric influences on nuclear receptor structure and function by a DNA element. J. Biol. Chem. 273:1998;10338-10348.
73. Trapp T., Holsboer F. Ligand-induced conformational changes in the mineralocorticoid receptor analyzed by protease mapping. Biochem. Biophys. Res. Commun. 215:1995;286-291.
74. Tzukerman M.T., Esty A., Santiso-Mere D., Danielian P., Parker M.G., Stein R.B., Pike J.W., McDonnell D.P. Human estrogen receptor transactivational capacity is determined by both cellular and promoter context and mediated by two functionally distinct intramolecular regions. Mol. Endocrinol. 8:1994;21-30.
75. Vedeckis W.V. Limited proteolysis of the mouse liver glucocorticoid receptor. Biochemistry. 22:1983;1975-1983.
76. Wagner R.L., Apriletti J.W., McGrath M.E., West B.L., Baxter J.D., Fletterick R.J. A structural role for hormone in the thyroid hormone receptor. Nature. 378:1995;690-697.
77. Wasner G., Oshima H., Thompson E.B., Simons S.S. Jr. Unlinked regulation of the sensitivity of primary glucocorticoid-inducible responses in mouse mammary tumor virus infected Fu5-5 rat hepatoma cells. Mol. Endocrinol. 2:1988;1009-1017.
78. Williams S.P., Sigler P.B. Atomic structure of progesterone complexed with its receptor. Nature. 393:1998;392-396.
79. Wurtz J.-M., Bourguet W., Renaud J.-P., Vivat V., Chambon P., Moras D., Gronemeyer H. A canonical structure for the ligand-binding domain of nuclear receptors. Nat. Struct. Biol. 3:1996;87-94.
80. Xu M., Chakraborti P.K., Garabedian M.J., Yamamoto K.R., Simons S.S. Jr. Modular structure of glucocorticoid receptor domains is not equivalent to functional independence. Stability and activity of the steroid binding domain are controlled by sequences in separate domains. J. Biol. Chem. 271:1996;21430-21438.
81. Xu M., Dittmar K.D., Giannoukos G., Pratt W.B., Simons S.S.J. Jr. Binding of hsp90 to the glucocorticoid receptor requires a specific 7-amino acid sequence at the amino terminus of the hormone-binding domain. J. Biol. Chem. 273:1998;13918-13924.
82. Zhang S., Liang X., Danielsen M. Role of the C terminus of the glucocorticoid receptor in hormone binding and agonist/antagonist discrimination. Mol. Endocrinol. 10:1996;24-34.