Acetylation-mediated epigenetic regulation of glucocorticoid receptor activity: Circadian rhythm-associated alterations of glucocorticoid actions in target tissues

Molecular and Cellular Endocrinology

Volumn 336, Issue 1-2, 2011, Pages 23-30

  Kino, Tomoshige ^a   Chrousos, George P ^b  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

Author keywords

Acetylation; Circadian rhythm; Clock; Histone acetyltransferase (HAT); Histone deacetylase (HDAC); Hypothalamic pituitary adrenal (HPA) axis; Sirt1

Indexed keywords

GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HISTONE ACETYLTRANSFERASE; LYSINE; TRANSCRIPTION FACTOR CLOCK;

ACETYLATION; CARDIOVASCULAR DISEASE; CHRONIC STRESS; CIRCADIAN RHYTHM; ENZYME ACTIVITY; GENETIC REGULATION; HORMONE ACTION; HUMAN; HYPERCORTISOLISM; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LONGEVITY; METABOLIC SYNDROME X; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW; WELLBEING;

ACETYLATION; CIRCADIAN RHYTHM; CLOCK PROTEINS; EPIGENESIS, GENETIC; GLUCOCORTICOIDS; HUMANS; MODELS, BIOLOGICAL; ORGAN SPECIFICITY; RECEPTORS, GLUCOCORTICOID;

EID: 79952072398     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2010.12.001     Document Type: Review

References (93)

1. Abel G.A., Wochnik G.M., Ruegg J., Rouyer A., Holsboer F., Rein T. Activity of the GR in G2 and mitosis. Mol. Endocrinol. 2002, 16:1352-1366.
2. Aguilera G. HPA axis responsiveness to stress: implications for healthy aging. Exp. Gerontol. 2010, 10.1016/j.exger.2010.08.023.
3. Amat R., Solanes G., Giralt M., Villarroya F. SIRT1 is involved in glucocorticoid-mediated control of uncoupling protein-3 gene transcription. J. Biol. Chem. 2007, 282:34066-34076.
4. An W. Histone acetylation and methylation: combinatorial players for transcriptional regulation. Subcell. Biochem. 2007, 41:351-369.
5. Arafah B.M. Hypothalamic pituitary adrenal function during critical illness: limitations of current assessment methods. J. Clin. Endocrinol. Metab. 2006, 91:3725-3745.
6. Bao A.M., Meynen G., Swaab D.F. The stress system in depression and neurodegeneration: focus on the human hypothalamus. Brain Res. Rev. 2008, 57:531-553.
7. Barnes P.J. Anti-inflammatory actions of glucocorticoids: molecular mechanisms. Clin. Sci. (Lond.) 1998, 94:557-572.
8. Beato M., Chalepakis G., Schauer M., Slater E.P. DNA regulatory elements for steroid hormones. J. Steroid Biochem. 1989, 32:737-747.
9. Blander G., Guarente L. The Sir2 family of protein deacetylases. Annu. Rev. Biochem. 2004, 73:417-435.
10. Cheung P., Tanner K.G., Cheung W.L., Sassone-Corsi P., Denu J.M., Allis C.D. Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol. Cell 2000, 5:905-915.
11. Chrousos G.P. The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation. N. Engl. J. Med. 1995, 332:1351-1362.
12. Chrousos G.P. Glucocorticoid therapy. Endocrinology & Metabolism 2001, 609-632. McGraw-Hill, New York. P. Felig, L.A. Frohman (Eds.).
13. Chrousos G.P. Stress and disorders of the stress system. Nat. Rev. 2009, 5:374-381.
14. Chrousos G.P. Stress and sex versus immunity and inflammation. Sci. Signal. 2010, 3:pe36.
15. Chrousos G.P., Kino T. Intracellular glucocorticoid signaling: a formerly simple system turns stochastic. Sci. STKE 2005, 2005:pe48.
16. Chrousos G.P., Kino T. Glucocorticoid action networks and complex psychiatric and/or somatic disorders. Stress 2007, 10:213-219.
17. Cidlowski J.A., Michaels G.A. Alteration in glucocorticoid binding site number during the cell cycle in HeLa cells. Nature 1977, 266:643-645.
18. Clayton A.L., Mahadevan L.C. MAP kinase-mediated phosphoacetylation of histone H3 and inducible gene regulation. FEBS Lett. 2003, 546:51-58.
19. Cole T.J., Blendy J.A., Monaghan A.P., Krieglstein K., Schmid W., Aguzzi A., Fantuzzi G., Hummler E., Unsicker K., Schutz G. Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation. Genes Dev. 1995, 9:1608-1621.
20. Davidson A.J., Sellix M.T., Daniel J., Yamazaki S., Menaker M., Block G.D. Chronic jet-lag increases mortality in aged mice. Curr. Biol. 2006, 16:R914-916.
21. Ehrhart-Bornstein M., Bornstein S.R. Cross-talk between adrenal medulla and adrenal cortex in stress. Ann. N.Y. Acad. Sci. 2008, 1148:112-117.
22. Ekstrand K., Bostrom P.A., Arborelius M., Nilsson J.A., Lindell S.E. Cardiovascular risk factors in commercial flight aircrew officers compared with those in the general population. Angiology 1996, 47:1089-1094.
23. Elenkov I.J., Wilder R.L., Chrousos G.P., Vizi E.S. The sympathetic nerve-an integrative interface between two supersystems: the brain and the immune system. Pharmacol. Rev. 2000, 52:595-638.
24. Eskandari F., Sternberg E.M. Neural-immune interactions in health and disease. Ann. N.Y. Acad. Sci. 2002, 966:20-27.
25. Faus H., Haendler B. Post-translational modifications of steroid receptors. Biomed. Pharmacother. 2006, 60:520-528.
26. Fu M., Liu M., Sauve A.A., Jiao X., Zhang X., Wu X., Powell M.J., Yang T., Gu W., Avantaggiati M.L., Pattabiraman N., Pestell T.G., Wang F., Quong A.A., Wang C., Pestell R.G. Hormonal control of androgen receptor function through SIRT1. Mol. Cell. Biol. 2006, 26:8122-8135.
27. Fu M., Wang C., Reutens A.T., Wang J., Angeletti R.H., Siconolfi-Baez L., Ogryzko V., Avantaggiati M.L., Pestell R.G. p300 and p300/cAMP-response element-binding protein-associated factor acetylate the androgen receptor at sites governing hormone-dependent transactivation. J. Biol. Chem. 2000, 275:20853-20860.
28. Gaughan L., Logan I.R., Cook S., Neal D.E., Robson C.N. Tip60 and histone deacetylase 1 regulate androgen receptor activity through changes to the acetylation status of the receptor. J. Biol. Chem. 2002, 277:25904-25913.
29. Gaviglio A.L., Daniel A.R., Czaplicki L.M., Hillard C.J., Lange C.A. Progesterone receptor hinge region regulates the kinetics of transcriptional response through phosphorylation, acetylation, and nuclear retention. City 2010, 114.
30. Haelens A., Tanner T., Denayer S., Callewaert L., Claessens F. The hinge region regulates DNA binding, nuclear translocation, and transactivation of the androgen receptor. Cancer Res. 2007, 67:4514-4523.
31. Hager G.L. The dynamics of intranuclear movement and chromatin remodeling by the glucocorticoid receptor. Ernst Schering Res. Found Workshop 2002, 40:111-129.
32. Harrington M. Location, location, location: important for jet-lagged circadian loops. J. Clin. Invest. 2010, 120:2265-2267.
33. He B., Lee L.W., Minges J.T., Wilson E.M. Dependence of selective gene activation on the androgen receptor NH2- and COOH-terminal interaction. J. Biol. Chem. 2002, 277:25631-25639.
34. Hollenberg S.M., Weinberger C., Ong E.S., Cerelli G., Oro A., Lebo R., Thompson E.B., Rosenfeld M.G., Evans R.M. Primary structure and expression of a functional human glucocorticoid receptor cDNA. Nature 1985, 318:635-641.
35. Ichijo T., Chrousos G.P., Kino T. Activated glucocorticoid receptor interacts with the INHAT component Set/TAF-Iβ and releases it from a glucocorticoid-responsive gene promoter, relieving repression: implications for the pathogenesis of glucocorticoid resistance in acute undifferentiated leukemia with Set-Can translocation. Mol. Cell. Endocrinol. 2008, 283:19-31.
36. Ichijo T., Voutetakis A., Cotrim A.P., Bhattachryya N., Fujii M., Chrousos G.P., Kino T. The Smad6-histone deacetylase 3 complex silences the transcriptional activity of the glucocorticoid receptor: potential clinical implications. J. Biol. Chem. 2005, 280:42067-42077.
37. Ishida A., Mutoh T., Ueyama T., Bando H., Masubuchi S., Nakahara D., Tsujimoto G., Okamura H. Light activates the adrenal gland: timing of gene expression and glucocorticoid release. Cell Metab. 2005, 2:297-307.
38. Ismaili N., Garabedian M.J. Modulation of glucocorticoid receptor function via phosphorylation. Ann. N.Y. Acad. Sci. 2004, 1024:86-101.
39. Ito K., Yamamura S., Essilfie-Quaye S., Cosio B., Ito M., Barnes P.J., Adcock I.M. Histone deacetylase 2-mediated deacetylation of the glucocorticoid receptor enables NF-κB suppression. J. Exp. Med. 2006, 203:7-13.
40. Itoh M., Adachi M., Yasui H., Takekawa M., Tanaka H., Imai K. Nuclear export of glucocorticoid receptor is enhanced by c-Jun N-terminal kinase-mediated phosphorylation. Mol. Endocrinol. 2002, 16:2382-2392.
41. Kalsbeek A., Palm I.F., La Fleur S.E., Scheer F.A., Perreau-Lenz S., Ruiter M., Kreier F., Cailotto C., Buijs R.M. SCN outputs and the hypothalamic balance of life. J. Biol. Rhythms 2006, 21:458-469.
42. Kiessling S., Eichele G., Oster H. Adrenal glucocorticoids have a key role in circadian resynchronization in a mouse model of jet lag. J. Clin. Invest. 2010, 120:2600-2609.
43. Kim M.Y., Woo E.M., Chong Y.T., Homenko D.R., Kraus W.L. Acetylation of estrogen receptor α by p300 at lysines 266 and 268 enhances the deoxyribonucleic acid binding and transactivation activities of the receptor. Mol. Endocrinol. 2006, 20:1479-1493.
44. Kino T. Tissue glucocorticoid sensitivity: beyond stochastic regulation on the diverse actions of glucocorticoids. Horm. Metab. Res. 2007, 39:420-424.
45. Kino T., Chrousos G.P. Glucocorticoid and mineralocorticoid receptors and associated diseases. Essays Biochem. 2004, 40:137-155.
46. Kino T., Chrousos G.P. Glucocorticoid effect on gene expression. Handbook on Stress and the Brain 2005, 295-312. Elsevier BV, Amsterdam. T. Steckler, N.H. Kalin, J.M.H.M. Reul (Eds.).
47. Kino T., De Martino M.U., Charmandari E., Mirani M., Chrousos G.P. Tissue glucocorticoid resistance/hypersensitivity syndromes. J. Steroid Biochem. Mol. Biol. 2003, 85:457-467.
48. Kino T., Ichijo T., Amin N.D., Kesavapany S., Wang Y., Kim N., Rao S., Player A., Zheng Y.L., Garabedian M.J., Kawasaki E., Pant H.C., Chrousos G.P. Cyclin-dependent kinase 5 differentially regulates the transcriptional activity of the glucocorticoid receptor through phosphorylation: clinical implications for the nervous system response to glucocorticoids and stress. Mol. Endocrinol. 2007, 21:1552-1568.
49. Kino T., Jaffe H., Amin N.D., Chakrabarti M., Zheng Y.L., Chrousos G.P., Pant H.C. Cyclin-dependent kinase 5 modulates the transcriptional activity of the mineralocorticoid receptor and regulates expression of brain-derived neurotrophic factor. Mol. Endocrinol. 2010, 24:941-952.
50. Kino T., Su Y.A., Chrousos G.P. Human glucocorticoid receptor isoform β: recent understanding of its potential implications in physiology and pathophysiology. Cell. Mol. Life Sci. 2009, 66:3435-3448.
51. Kiyohara Y.B., Tagao S., Tamanini F., Morita A., Sugisawa Y., Yasuda M., Yamanaka I., Ueda H.R., van der Horst G.T., Kondo T., Yagita K. The BMAL1C terminus regulates the circadian transcription feedback loop. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:10074-10079.
52. Ko C.H., Takahashi J.S. Molecular components of the mammalian circadian clock. Hum. Mol. Genet. 2006, 15:R271-277.
53. Kondratov R.V., Kondratova A.A., Lee C., Gorbacheva V.Y., Chernov M.V., Antoch M.P. Post-translational regulation of circadian transcriptional CLOCK(NPAS2)/BMAL1 complex by CRYPTOCHROMES. Cell Cycle 2006, 5:890-895.
54. Kovacs J.J., Murphy P.J., Gaillard S., Zhao X., Wu J.T., Nicchitta C.V., Yoshida M., Toft D.O., Pratt W.B., Yao T.P. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol. Cell 2005, 18:601-607.
55. Kudielka B.M., Wust S. Human models in acute and chronic stress: assessing determinants of individual hypothalamus-pituitary-adrenal axis activity and reactivity. Stress 2010, 13:1-14.
56. Kyrou I., Tsigos C. Stress hormones: physiological stress and regulation of metabolism. Curr. Opin. Pharmacol. 2009, 9:787-793.
57. Li X., Zhang S., Blander G., Tse J.G., Krieger M., Guarente L. SIRT1 deacetylates and positively regulates the nuclear receptor LXR. Mol. Cell 2007, 28:91-106.
58. Loven M.A., Davis R.E., Curtis C.D., Muster N., Yates J.R., Nardulli A.M. A novel estrogen receptor α-associated protein alters receptor-deoxyribonucleic acid interactions and represses receptor-mediated transcription. Mol. Endocrinol. 2004, 18:2649-2659.
59. Lu N.Z., Cidlowski J.A. Translational regulatory mechanisms generate N-terminal glucocorticoid receptor isoforms with unique transcriptional target genes. Mol. Cell 2005, 18:331-342.
60. McKenna N.J., O'Malley B.W. Combinatorial control of gene expression by nuclear receptors and coregulators. Cell 2002, 108:465-474.
61. Melvin V.S., Harrell C., Adelman J.S., Kraus W.L., Churchill M., Edwards D.P. The role of the C-terminal extension (CTE) of the estrogen receptor alpha and β DNA binding domain in DNA binding and interaction with HMGB. J. Biol. Chem. 2004, 279:14763-14771.
62. Miller A.L., Webb M.S., Copik A.J., Wang Y., Johnson B.H., Kumar R., Thompson E.B. p38 Mitogen-activated protein kinase (MAPK) is a key mediator in glucocorticoid-induced apoptosis of lymphoid cells: correlation between p38 MAPK activation and site-specific phosphorylation of the human glucocorticoid receptor at serine 211. Mol. Endocrinol. 2005, 19:1569-1583.
63. Miller D.B., O'Callaghan J.P. Neuroendocrine aspects of the response to stress. Metabolism 2002, 51:5-10.
64. Minucci S., Pelicci P.G. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat. Rev. Cancer 2006, 6:38-51.
65. Murphy P.J., Morishima Y., Kovacs J.J., Yao T.P., Pratt W.B. Regulation of the dynamics of hsp90 action on the glucocorticoid receptor by acetylation/deacetylation of the chaperone. J. Biol. Chem. 2005, 280:33792-33799.
66. Nader N., Chrousos G.P., Kino T. Circadian rhythm transcription factor CLOCK regulates the transcriptional activity of the glucocorticoid receptor by acetylating its hinge region lysine cluster: potential physiological implications. FASEB J. 2009, 23:1572-1583.
67. Nader N., Chrousos G.P., Kino T. Interactions of the circadian CLOCK system and the HPA axis. Trends Endocrinol. Metab. 2010, 21:277-286.
68. Nader N., Ng S.S., Lambrou G.I., Pervanidou P., Wang Y., Chrousos G.P., Kino T. AMPK regulates metabolic actions of glucocorticoids by phosphorylating the glucocorticoid receptor through p38 MAPK. Mol. Endocrinol. 2010, 24:1748-1764.
69. Nicolaides N.C., Galata Z., Kino T., Chrousos G.P., Charmandari E. The human glucocorticoid receptor: molecular basis of biologic function. Steroids 2010, 75:1-12.
70. O'Malley B. The steroid receptor superfamily: more excitement predicted for the future. Mol. Endocrinol. 1990, 4:363-369.
71. Oster H., Damerow S., Kiessling S., Jakubcakova V., Abraham D., Tian J., Hoffmann M.W., Eichele G. The circadian rhythm of glucocorticoids is regulated by a gating mechanism residing in the adrenal cortical clock. Cell Metab. 2006, 4:163-173.
72. Pippal J.B., Yao Y., Rogerson F.M., Fuller P.J. Structural and functional characterization of the interdomain interaction in the mineralocorticoid receptor. Mol. Endocrinol. 2009, 23:1360-1370.
73. Pratt W.B. The role of heat shock proteins in regulating the function, folding, and trafficking of the glucocorticoid receptor. J. Biol. Chem. 1993, 268:21455-21458.
74. Reichardt H.M., Kaestner K.H., Tuckermann J., Kretz O., Wessely O., Bock R., Gass P., Schmid W., Herrlich P., Angel P., Schutz G. DNA binding of the glucocorticoid receptor is not essential for survival. Cell 1998, 93:531-541.
75. Revollo J.R., Cidlowski J.A. Mechanisms generating diversity in glucocorticoid receptor signaling. Ann. N.Y. Acad. Sci. 2009, 1179:167-178.
76. Ripperger J.A., Schibler U. Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions. Nat. Genet. 2006, 38:369-374.
77. Rogatsky I., Waase C.L., Garabedian M.J. Phosphorylation and inhibition of rat glucocorticoid receptor transcriptional activation by glycogen synthase kinase-3 (GSK-3). Species-specific differences between human and rat glucocorticoid receptor signaling as revealed through GSK-3 phosphorylation. J. Biol. Chem. 1998, 273:14315-14321.
78. Rogerson F.M., Fuller P.J. Interdomain interactions in the mineralocorticoid receptor. Mol. Cell. Endocrinol. 2003, 200:45-55.
79. Rosenfeld M.G., Lunyak V.V., Glass C.K. Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev. 2006, 20:1405-1428.
80. Savory J.G., Hsu B., Laquian I.R., Giffin W., Reich T., Hache R.J., Lefebvre Y.A. Discrimination between NL1- and NL2-mediated nuclear localization of the glucocorticoid receptor. Mol. Cell Biol. 1999, 19:1025-1037.
81. Scheer F.A., Hilton M.F., Mantzoros C.S., Shea S.A. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:4453-4458.
82. Seo S.B., McNamara P., Heo S., Turner A., Lane W.S., Chakravarti D. Regulation of histone acetylation and transcription by INHAT, a human cellular complex containing the set oncoprotein. Cell 2001, 104:119-130.
83. Sheridan J. The HPA axis SNS, and immunity: a commentary. Brain Behav. Immun. 2003, 17(1):S17.
84. So A.Y., Chaivorapol C., Bolton E.C., Li H., Yamamoto K.R. Determinants of cell- and gene-specific transcriptional regulation by the glucocorticoid receptor. PLoS Genet. 2007, 3:e94.
85. Szatmary Z., Garabedian M.J., Vilcek J. Inhibition of glucocorticoid receptor-mediated transcriptional activation by p38 mitogen-activated protein (MAP) kinase. J. Biol. Chem. 2004, 279:43708-43715.
86. Takahashi J.S., Hong H.K., Ko C.H., McDearmon E.L. The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat. Rev. Genet. 2008, 9:764-775.
87. Thompson J., Saatcioglu F., Janne O.A., Palvimo J.J. Disrupted amino- and carboxyl-terminal interactions of the androgen receptor are linked to androgen insensitivity. Mol. Endocrinol. 2001, 15:923-935.
88. Thomson S., Clayton A.L., Mahadevan L.C. Independent dynamic regulation of histone phosphorylation and acetylation during immediate-early gene induction. Mol. Cell 2001, 8:1231-1241.
89. Ulrich-Lai Y.M., Arnhold M.M., Engeland W.C. Adrenal splanchnic innervation contributes to the diurnal rhythm of plasma corticosterone in rats by modulating adrenal sensitivity to ACTH. Am. J. Physiol. 2006, 290:R1128-1135.
90. van der Vaart M., Schaaf M.J. Naturally occurring C-terminal splice variants of nuclear receptors. Nucl. Recept. Signal. 2009, 7:e007.
91. Wang Z., Garabedian M.J. Modulation of glucocorticoid receptor transcriptional activation, phosphorylation, and growth inhibition by p27Kip1. J. Biol. Chem. 2003, 278:50897-50901.
92. Webster J.I., Moayeri M., Sternberg E.M. Novel repression of the glucocorticoid receptor by anthrax lethal toxin. Ann. N.Y. Acad. Sci. 2004, 1024:9-23.
93. Wurtman R.J. Stress and the adrenocortical control of epinephrine synthesis. Metabolism 2002, 51:11-14.