Live Cell Imaging Unveils Multiple Domain Requirements for In Vivo Dimerization of the Glucocorticoid Receptor

PLoS Biology

Volumn 12, Issue 3, 2014, Pages

  Presman, Diego M ^a,b,c   Ogara, M Florencia ^b,c   Stortz, Martín ^b   Alvarez, Lautaro D ^b   Pooley, John R ^a,d   Schiltz, R Louis ^a   Grøntved, Lars ^a   Johnson, Thomas A ^a   Mittelstadt, Paul R ^a   Ashwell, Jonathan D ^a   Ganesan, Sundar ^e   Burton, Gerardo ^b   Levi, Valeria ^b   Hager, Gordon L ^a   Pecci, Adali ^b,c  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c INSTITUTO DE FISIOLOGÍA   (Argentina)

^d UNIVERSITY OF BRISTOL   (United Kingdom)

^e NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CELLS, CULTURED; DNA; MICE; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, GLUCOCORTICOID;

EID: 84899032002     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001813     Document Type: Article

References (56)

1. Necela BM, Cidlowski JA, (2004) Mechanisms of glucocorticoid receptor action in noninflammatory and inflammatory cells. Proc Am Thorac Soc 1: 239-246.
2. Clark AR, Belvisi MG, (2011) Maps and legends: the quest for dissociated ligands of the glucocorticoid receptor. Pharmacol Ther 134: 54-67.
3. Chalepakis G, Schauer M, Cao XA, Beato M, (1990) Efficient binding of glucocorticoid receptor to its responsive element requires a dimer and DNA flanking sequences. DNA Cell Biol 9: 355-368.
4. Cairns W, Cairns C, Pongratz I, Poellinger L, Okret S, (1991) Assembly of a glucocorticoid receptor complex prior to DNA binding enhances its specific interaction with a glucocorticoid response element. J Biol Chem 266: 11221-11226.
5. Wrange O, Eriksson P, Perlmann T, (1989) The purified activated glucocorticoid receptor is a homodimer. J Biol Chem 264: 5253-5259.
6. Drouin J, Sun YL, Tremblay S, Lavender P, Schmidt TJ, et al. (1992) Homodimer formation is rate-limiting for high affinity DNA binding by glucocorticoid receptor. Mol Endocrinol 6: 1299-1309.
7. Tsai SY, Carlstedt-Duke J, Weigel NL, Dahlman K, Gustafsson JA, et al. (1988) Molecular interactions of steroid hormone receptor with its enhancer element: evidence for receptor dimer formation. Cell 55: 361-369.
8. Dahlman-Wright K, Wright A, Gustafsson JA, Carlstedt-Duke J, (1991) Interaction of the glucocorticoid receptor DNA-binding domain with DNA as a dimer is mediated by a short segment of five amino acids. J Biol Chem 266: 3107-3112.
9. Hudson WH, Youn C, Ortlund EA, (2013) The structural basis of direct glucocorticoid-mediated transrepression. Nat Struct Mol Biol 20: 53-58.
10. Bledsoe RK, Stewart EL, Pearce KH, (2004) Structure and function of the glucocorticoid receptor ligand binding domain. Vitam Horm 68: 49-91.
11. De Bosscher K, Haegeman G, (2009) Minireview: latest perspectives on antiinflammatory actions of glucocorticoids. Mol Endocrinol 23: 281-291.
12. Kleiman A, Tuckermann JP, (2007) Glucocorticoid receptor action in beneficial and side effects of steroid therapy: lessons from conditional knockout mice. Mol Cell Endocrinol 275: 98-108.
13. Kumar R, Thompson EB, (2005) Gene regulation by the glucocorticoid receptor: structure:function relationship. J Steroid Biochem Mol Biol 94: 383-394.
14. Luisi BF, Xu WX, Otwinowski Z, Freedman LP, Yamamoto KR, et al. (1991) Crystallographic analysis of the interaction of the glucocorticoid receptor with DNA. Nature 352: 497-505.
15. Bledsoe RK, Montana VG, Stanley TB, Delves CJ, Apolito CJ, et al. (2002) Crystal structure of the glucocorticoid receptor ligand binding domain reveals a novel mode of receptor dimerization and coactivator recognition. Cell 110: 93-105.
16. Heck S, Kullmann M, Gast A, Ponta H, Rahmsdorf HJ, et al. (1994) A distinct modulating domain in glucocorticoid receptor monomers in the repression of activity of the transcription factor AP-1. EMBO J 13: 4087-4095.
17. Beck IM, De Bosscher K, Haegeman G, (2011) Glucocorticoid receptor mutants: man-made tools for functional research. Trends Endocrinol Metab 22: 295-310.
18. Reichardt HM, Kaestner KH, Tuckermann J, Kretz O, Wessely O, et al. (1998) DNA binding of the glucocorticoid receptor is not essential for survival. Cell 93: 531-541.
19. Meijsing SH, Pufall MA, So AY, Bates DL, Chen L, et al. (2009) DNA binding site sequence directs glucocorticoid receptor structure and activity. Science 324: 407-410.
20. Watson LC, Kuchenbecker KM, Schiller BJ, Gross JD, Pufall MA, et al. (2013) The glucocorticoid receptor dimer interface allosterically transmits sequence-specific DNA signals. Nat Struct Mol Biol 20: 876-883.
21. Rogatsky I, Wang JC, Derynck MK, Nonaka DF, Khodabakhsh DB, et al. (2003) Target-specific utilization of transcriptional regulatory surfaces by the glucocorticoid receptor. Proc Natl Acad Sci U S A 100: 13845-13850.
22. Jewell CM, Scoltock AB, Hamel BL, Yudt MR, Cidlowski JA, (2012) Complex Human Glucocorticoid Receptor dim Mutations Define Glucocorticoid Induced Apoptotic Resistance in Bone Cells. Mol Endocrinol 26: 244-256.
23. Digman MA, Dalal R, Horwitz AF, Gratton E, (2008) Mapping the number of molecules and brightness in the laser scanning microscope. Biophys J 94: 2320-2332.
24. Presman DM, Alvarez LD, Levi V, Eduardo S, Digman MA, et al. (2010) Insights on glucocorticoid receptor activity modulation through the binding of rigid steroids. PLoS ONE 5: e13279.
25. Robertson S, Allie-Reid F, Vanden Berghe W, Visser K, Binder A, et al. (2010) Abrogation of glucocorticoid receptor dimerization correlates with dissociated glucocorticoid behavior of compound a. J Biol Chem 285: 8061-8075.
26. Robblee JP, Miura MT, Bain DL, (2012) Glucocorticoid receptor-promoter interactions: energetic dissection suggests a framework for the specificity of steroid receptor-mediated gene regulation. Biochemistry 51: 4463-4472.
27. Stavreva DA, Wiench M, John S, Conway-Campbell BL, McKenna MA, et al. (2009) Ultradian hormone stimulation induces glucocorticoid receptor-mediated pulses of gene transcription. Nat Cell Biol 11: 1093-1102.
28. Voss TC, Schiltz RL, Sung MH, Yen PM, Stamatoyannopoulos JA, et al. (2011) Dynamic exchange at regulatory elements during chromatin remodeling underlies assisted loading mechanism. Cell 146: 544-554.
29. Gebhardt JC, Suter DM, Roy R, Zhao ZW, Chapman AR, et al. (2013) Single-molecule imaging of transcription factor binding to DNA in live mammalian cells. Nat Methods 10: 421-426.
30. Robertson S, Rohwer JM, Hapgood JP, Louw A, (2013) Impact of glucocorticoid receptor density on ligand-independent dimerization, cooperative ligand-binding and basal priming of transactivation: a cell culture model. PLoS ONE 8: e64831.
31. Adams M, Meijer OC, Wang J, Bhargava A, Pearce D, (2003) Homodimerization of the glucocorticoid receptor is not essential for response element binding: activation of the phenylethanolamine N-methyltransferase gene by dimerization-defective mutants. Mol Endocrinol 17: 2583-2592.
32. McNally JG, Muller WG, Walker D, Wolford R, Hager GL, (2000) The glucocorticoid receptor: rapid exchange with regulatory sites in living cells. Science 287: 1262-1265.
33. Ghosh G, Wang VY, Huang DB, Fusco A, (2012) NF-kappaB regulation: lessons from structures. Immunol Rev 246: 36-58.
34. De Bosscher K, Vanden Berghe W, Beck IM, Van Molle W, Hennuyer N, et al. (2005) A fully dissociated compound of plant origin for inflammatory gene repression. Proc Natl Acad Sci U S A 102: 15827-15832.
35. Digman MA, Wiseman PW, Choi C, Horwitz AR, Gratton E, (2009) Stoichiometry of molecular complexes at adhesions in living cells. Proc Natl Acad Sci U S A 106: 2170-2175.
36. Nixon M, Andrew R, Chapman KE, (2013) It takes two to tango: dimerisation of glucocorticoid receptor and its anti-inflammatory functions. Steroids 78: 59-68.
37. Veleiro AS, Alvarez LD, Eduardo SL, Burton G, (2010) Structure of the glucocorticoid receptor, a flexible protein that can adapt to different ligands. ChemMedChem 5: 649-659.
38. Alvarez LD, Marti MA, Veleiro AS, Presman DM, Estrin DA, et al. (2008) Exploring the molecular basis of action of the passive antiglucocorticoid 21-hydroxy-6,19-epoxyprogesterone. J Med Chem 51: 1352-1360.
39. Arvey A, Agius P, Noble WS, Leslie C, (2012) Sequence and chromatin determinants of cell-type-specific transcription factor binding. Genome Res 22: 1723-1734.
40. John S, Sabo PJ, Thurman RE, Sung MH, Biddie SC, et al. (2011) Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat Genet 43: 264-268.
41. Surjit M, Ganti KP, Mukherji A, Ye T, Hua G, et al. (2011) Widespread negative response elements mediate direct repression by agonist-liganded glucocorticoid receptor. Cell 145: 224-241.
42. John S, Johnson TA, Sung MH, Biddie SC, Trump S, et al. (2009) Kinetic complexity of the global response to glucocorticoid receptor action. Endocrinology 150: 1766-1774.
43. Clark AR, (2007) Anti-inflammatory functions of glucocorticoid-induced genes. Mol Cell Endocrinol 275: 79-97.
44. Hager GL, McNally JG, Misteli T, (2009) Transcription dynamics. Mol Cell 35: 741-753.
45. Stavreva DA, Muller WG, Hager GL, Smith CL, McNally JG, (2004) Rapid glucocorticoid receptor exchange at a promoter is coupled to transcription and regulated by chaperones and proteasomes. Mol Cell Biol 24: 2682-2697.
46. Frijters R, Fleuren W, Toonen EJ, Tuckermann JP, Reichardt HM, et al. (2010) Prednisolone-induced differential gene expression in mouse liver carrying wild type or a dimerization-defective glucocorticoid receptor. BMC Genomics 11: 359.
47. Vandevyver S, Dejager L, Tuckermann J, Libert C, (2013) New insights into the anti-inflammatory mechanisms of glucocorticoids: an emerging role for glucocorticoid-receptor-mediated transactivation. Endocrinology 154: 993-1007.
48. Burton G, Lantos C, Veleiro A (2006) Method for the preparation of 21-hydroxy-6,19-oxidoprogesterone (21OH-6,19OP). U.S. Patent ed. pp. 7,071,328.
49. Qiu Y, Zhao Y, Becker M, John S, Parekh BS, et al. (2006) HDAC1 acetylation is linked to progressive modulation of steroid receptor-induced gene transcription. Mol Cell 22: 669-679.
50. Murakoshi H, Lee SJ, Yasuda R, (2008) Highly sensitive and quantitative FRET-FLIM imaging in single dendritic spines using improved non-radiative YFP. Brain Cell Biol 36: 31-42.
51. Sung MH, Salvatore L, De Lorenzi R, Indrawan A, Pasparakis M, et al. (2009) Sustained oscillations of NF-kappaB produce distinct genome scanning and gene expression profiles. PLoS ONE 4: e7163.
52. Wang L, Jin Q, Lee JE, Su IH, Ge K, (2010) Histone H3K27 methyltransferase Ezh2 represses Wnt genes to facilitate adipogenesis. Proc Natl Acad Sci U S A 107: 7317-7322.
53. Walker D, Htun H, Hager GL, (1999) Using inducible vectors to study intracellular trafficking of GFP-tagged steroid/nuclear receptors in living cells. Methods 19: 386-393.
54. Mittelstadt PR, Monteiro JP, Ashwell JD, (2012) Thymocyte responsiveness to endogenous glucocorticoids is required for immunological fitness. J Clin Invest 122: 2384-2394.
55. Hellriegel C, Caiolfa VR, Corti V, Sidenius N, Zamai M, (2011) Number and brightness image analysis reveals ATF-induced dimerization kinetics of uPAR in the cell membrane. FASEB J 25: 2883-2897.
56. Liu J, DeFranco DB, (1999) Chromatin recycling of glucocorticoid receptors: implications for multiple roles of heat shock protein 90. Mol Endocrinol 13: 355-365.