Rapid glucocorticoid feedback inhibition of ACTH secretion involves ligand-dependent membrane association of glucocorticoid receptors

Endocrinology (United States)

Volumn 156, Issue 9, 2015, Pages 3215-3227

  Deng, Qiong ^a,b   Riquelme, Denise ^a   Trinh, Loc ^a   Low, Malcolm J ^c   Tomic, Melanija ^a   Stojilkovic, Stanko ^a   Aguilera, Greti ^a  

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

^b JILIN UNIVERSITY   (China)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; CORTICOSTERONE; CORTICOTROPIN; DACTINOMYCIN; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HISTONE DEACETYLASE 1; MIFEPRISTONE; PROTEIN TYROSINE KINASE; CORTICOTROPIN RELEASING FACTOR; LIGAND;

ACTH SECRETING CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CLEARANCE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORTICOTROPIN RELEASE; ENZYME PHOSPHORYLATION; FEMALE; IMMUNOREACTIVITY; MALE; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; RAT; WESTERN BLOTTING; ANIMAL; CELL CULTURE; FEEDBACK SYSTEM; METABOLISM; PHOSPHORYLATION; SECRETION (PROCESS); SPRAGUE DAWLEY RAT;

ADRENOCORTICOTROPIC HORMONE; ANIMALS; CALCIUM SIGNALING; CELLS, CULTURED; CORTICOSTERONE; CORTICOTROPHS; CORTICOTROPIN-RELEASING HORMONE; FEEDBACK, PHYSIOLOGICAL; FEMALE; GLUCOCORTICOIDS; LIGANDS; MALE; PHOSPHORYLATION; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUCOCORTICOID; SRC-FAMILY KINASES;

EID: 84942769778     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/EN.2015-1265     Document Type: Article

References (61)

1. Munck A, Guyre PM, Holbrook NJ Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr Rev. 1984; 5:25-44.
2. Lightman SL, Conway-Campbell BL. The crucial role of pulsatile activity of the HPA axis for continuous dynamic equilibration. Nat Rev Neurosci. 2010; 11:710-718.
3. Ochedalski T, Rabadan-Diehl C, Aguilera G. Interaction between glucocorticoids and corticotropin releasing hormone (CRH) in the regulation of the pituitary CRH receptor in vivo in the rat. J Neuroendocrinol. 1998; 10:363-369.
4. Falkenstein E, Tillmann HC, Christ M, Feuring M., Wehling M. Multiple actions of steroid hormones-a focus on rapid, nongenomic effects. Pharmacol Rev. 2000; 52:513-556.
5. Uchoa ET, Aguilera G, Herman J.P., Fiedler JL, Deak T, de Sousa MBC. Novel aspects of glucocorticoid actions. J Neuroendocrinol. 2014; 26:557-572.
6. Lowenberg M, Verhaar A, van den Brink GR, Hommes D. Glucocorticoid signaling: a nongenomic mechanism for T-cell immunosuppression. Trends Mol Med. 2007; 13:158-163.
7. Sarabdjitsingh RA, Joels M, de Kloet ER. Glucocorticoid pulsatility and rapid corticosteroid actions in the central stress response. Physiol Behav. 2012; 106:73-80.
8. Pedram A, Razandi M, Sainson R.C., Kim JK, Hughes CC, Levin ER. A conserved mechanism for steroid receptor translocation to the plasma membrane. J Biol Chem. 2007; 282:22278-22288.
9. Roozendaal B, Hernandez A, Cabrera S.M., et al. Membrane-associated glucocorticoid activity is necessary for modulation of longterm memory via chromatin modification. J Neurosci. 2010; 30: 5037-5046.
10. Song IH, Buttgereit F. Non-genomic glucocorticoid effects to provide the basis for new drug developments. Mol Cell Endocrinol. 2006; 246:142-146.
11. Stojadinovic O, Sawaya A, Pastar I., Tomic-Canic M. Glucocorticoid receptor localizes to adherens junctions at the plasma membrane of keratinocytes. PloS One. 2013; 8:e63453.
12. Gametchu B, Chen F, Sackey F, Powell C, Watson CS. Plasma membrane-resident glucocorticoid receptors in rodent lymphoma and human leukemia models. Steroids. 1999; 64:107-119.
13. Orchinik M, Murray TF, Moore FL A corticosteroid receptor in neuronal membranes. Science. 1991; 252:1848-1851.
14. Samarasinghe RA, Di Maio R, Volonte D, et al Nongenomic glucocorticoid receptor action regulates gap junction intercellular communication and neural progenitor cell proliferation. Proc Natl Acad Sci USA. 2011; 108:16657-16662.
15. Johnson LR, Farb C, Morrison J.H., McEwen BS, LeDoux JE. Localization of glucocorticoid receptors at postsynaptic membranes in the lateral amygdala. Neuroscience. 2005; 136:289-299.
16. Komatsuzaki Y, Murakami G, Tsurugizawa T., et al. Rapid spinogenesis of pyramidal neurons induced by activation of glucocorticoid receptors in adult male rat hippocampus. Biochem Biophys Res Commun. 2005; 335:1002-1007.
17. Liposits Z, Bohn MC Association of glucocorticoid receptor immunoreactivity with cell membrane and transport vesicles in hippocampal and hypothalamic neurons of the rat. J Neurosci Res. 1993; 35:14-19.
18. Engler D, Pham T, Liu J.P., Fullerton MJ, Clarke IJ, Funder JW. Studies of the regulation of the hypothalamic-pituitary-adrenal axis in sheep with hypothalamic-pituitary disconnection. II. Evidence for in vivo ultradian hypersecretion of proopiomelanocortin peptides by the isolated anterior and intermediate pituitary. Endocrinology. 1990; 127:1956-1966.
19. Muglia LJ, Jacobson L, Weninger S.C., et al. Impaired diurnal adrenal rhythmicity restored by constant infusion of corticotropin-releasing hormone in corticotropin-releasing hormone-deficient mice. J Clin Invest. 1997; 99:2923-2929.
20. Walker JJ, Spiga F, Waite E., et al. The origin of glucocorticoid hormone oscillations. PLoS Biol. 2012; 10:e1001341.
21. Hentges ST, Otero-Corchon V, Pennock R.L., King CM, Low MJ. Proopiomelanocortin expression in both GABA and glutamate neurons. J Neurosci. 2009; 29:13684-13690.
22. Mercer AJ, Stuart RC, Attard C.A., Otero-Corchon V, Nillni EA, Low MJ. Temporal changes in nutritional state affect hypothalamic POMC peptide levels independently of leptin in adult male mice. Am J Physiol Endocrinol Metab. 2014; 306:E904-E915.
23. Kasckow J, Mulchahey JJ, Aguilera G, et al Corticotropin-releasing hormone (CRH) expression and protein kinase A mediated CRH receptor signalling in an immortalized hypothalamic cell line. J Neuroendocrinol. 2003; 15:521-529.
24. Deng Q, Waxse B, Riquelme D., Zhang J, Aguilera G. Helix 8 of the ligand binding domain of the glucocorticoid receptor (GR) is essential for ligand binding. Mol Cell Endocrinol. 2015; 408:23-32.
25. Rotsztejn W, Lalonde J, Normand M, Fortier C. Feedback inhibition of adrenocorticotropin release by corticosterone infusions in the adrenalectomized rat. Can J Physiol Pharmacol. 1975; 53:475-478.
26. Mahmoud SN, Scaccianoce S, Scraggs P.R., Nicholson SA, Gillham B, Jones MT. Characteristics of corticosteroid inhibition of adrenocorticotrophin release from the anterior pituitary gland of the rat. J Endocrinol. 1984; 102:33-42.
27. Widmaier EP, Dallman MF The effects of corticotropin-releasing factoron adrenocorticotropin secretion from perifused pituitaries in vitro: rapid inhibition by glucocorticoids. Endocrinology. 1984; 115:2368-2374.
28. Hinz B, Hirschelmann R. Rapid non-genomic feedback effects of glucocorticoids on CRF-induced ACTH secretion in rats. Pharmaceut Res. 2000; 17:1273-1277.
29. Russell GM, Henley DE, Leendertz J, et al Rapid glucocorticoid receptor-mediated inhibition of hypothalamic-pituitary-adrenal ultradian activity in healthy males. J Neurosci. 2010; 30:6106-6115.
30. Dayanithi G, Antoni FA Rapid as well as delayed inhibitory effects of glucocorticoid hormones on pituitary adrenocorticotropic hormone release are mediated by type II glucocorticoid receptors and require newly synthesized messenger ribonucleic acid as well as protein. Endocrinology. 1989; 125:308-313.
31. Iwasaki Y, Aoki Y, Katahira M., Oiso Y, Saito H. Non-genomic mechanisms of glucocorticoid inhibition of adrenocorticotropin secretion: possible involvement of GTP-binding protein. Biochem Biophys Res Commun. 1997; 235:295-299.
32. Fink G, Robinson IC, Tannahill LA Effects of adrenalectomy and glucocorticoids on the peptides CRF-41, AVP and oxytocin in rat hypophysial portal blood. J Physiol. 1988; 401:329-345.
33. Plotsky PM, Vale W. Hemorrhage-induced secretion of corticotropin-releasing factor-like immunoreactivity into the rat hypophysial portal circulation and its inhibition by glucocorticoids. Endocrinology. 1984; 114:164-169.
34. Henley DE, Lightman SL New insights into corticosteroid-binding globulin and glucocorticoid delivery. Neuroscience. 2011; 180:1-8.
35. Qian X, Droste SK, Lightman SL, Reul JM, Linthorst AC. Circadian and ultradian rhythms of free glucocorticoid hormone are highly synchronized between the blood, the subcutaneous tissue, and the brain. Endocrinology. 2012; 153:4346-4353.
36. Ramamoorthy S, Cidlowski JA Ligand-induced repression of the glucocorticoid receptor gene is mediated by an NCoR1 repression complex formed by long-range chromatin interactions with intragenic glucocorticoid response elements. Mol Cell Biol. 2013; 33: 1711-1722.
37. Findling JW, Raff H. Cushing's Syndrome: important issues in diagnosisand management. JCI in Endocrinol Metab.2006;91:3746-3753.
38. Watson CS, Gametchu B. Proteins of multiple classes may participatein nongenomic steroid actions. Exp Biol Med. 2003; 228:1272-1281.
39. Losel R, Wehling M. Nongenomic actions of steroid hormones. Nat Rev Mol Cell Biol. 2003; 4:46-56.
40. Di S, Malcher-Lopes R, Halmos K.C., Tasker JG. Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: afast feedback mechanism. J Neurosci. 2003; 23:4850-4857.
41. Yang S, Roselli F, Patchev A.V., Yu S., Almeida OF. Non-receptor-tyrosine kinases integrate fast glucocorticoid signaling in hippocampal neurons. J Biol Chem. 2013; 288:23725-23739.
42. Ginsberg AB, Pecoraro NC, Warne J.P., Horneman HF, Dallman MF. Rapid alteration of stress-induced hypothalamic-pituitary-adrenal hormone secretion in the rat: a comparison of glucocorticoids and cannabinoids. Stress. 2010; 13:248-257.
43. Chivers JE, Cambridge LM, Catley M.C., et al. Differential effects of RU486 reveal distinct mechanisms for glucocorticoid repression of prostaglandin E release. Eur J Biochem. 2004; 271:4042-4052.
44. Pariante CM, Pearce BD, Pisell T.L., Su C., Miller AH. The steroid receptor antagonists RU40555 and RU486 activate glucocorticoid receptor translocation and are not excreted by the steroid hormones transporter in L929 cells. J Endocrinol. 2001; 169:309-320.
45. Dibas A, Jiang M, Fudala R., et al. Fluorescent protein-labeled glucocorticoid receptor α isoform trafficking in cultured human trabecular meshwork cells. Invest Ophthalmol Vis Sci. 2012; 53:2938-2950.
46. Migliaccio A, Castoria G, Di Domenico M, et al. Steroid-induced androgen receptor-oestradiol receptor β-Src complex triggers prostate cancer cell proliferation. EMBO J. 2000; 19:5406-5417.
47. Boonyaratanakornkit V, Scott MP, Ribon V, et al Progesterone receptor contains a proline-rich motif that directly interacts with SH3 domains and activates c-Src family tyrosine kinases. Mol Cell. 2001; 8:269-280.
48. Kousteni S, Bellido T, Plotkin L.I., et al. Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell. 2001; 104:719-730.
49. Clark TP, Kemppainen RJ Glucocorticoids do not affect intracellular calcium transients in corticotrophs: evidence supporting an effect distal to calcium influx. NeuroEndocrinology. 1994; 60:273-282.
50. Chen S, Wang XH, Zhang X.Z., et al. High-dose glucocorticoids induce decreases calcium in hypothalamus neurons via plasma membrane Ca(2 +) pumps. Neuroreport. 2011; 22:660-663.
51. Antoni FA, Hoyland J, Woods M.D., Mason WT. Glucocorticoid inhibition of stimulus-evoked adrenocorticotrophin release caused by suppression of intracellular calcium signals. J Endocrinol. 1992; 133:R13-R16.
52. Park YS, Ha Choi Y, Park CH, Kim KT. Nongenomic glucocorticoid effects on activity-dependent potentiation of catecholamine release in chromaffin cells. Endocrinology. 2008; 149:4921-4927.
53. Link H, Dayanithi G, Gratzl M. Glucocorticoids rapidly inhibit oxytocin-stimulated adrenocorticotropin release from rat anterior pituitary cells, without modifying intracellular calcium transients. Endocrinology. 1993; 132:873-878.
54. Castellino F, Heuser J, Marchetti S., Bruno B, Luini A. Glucocorticoid stabilization of actin filaments: a possible mechanism for inhibition of corticotropin release. Proc Natl Acad Sci USA. 1992; 89: 3775-3779.
55. Aunis D, Bader MF The cytoskeleton as a barrier to exocytosis in secretory cells. J Exp Biol. 1988; 139:253-266.
56. Burgess TL, Kelly RB Constitutive and regulated secretion of proteins. Annu Rev Cell Biol. 1987; 3:243-293.
57. Croxtall JD, Choudhury Q, Flower RJ Glucocorticoids act within minutes to inhibit recruitment of signalling factors to activated EGF receptors through a receptor-dependent, transcription-independent mechanism. Br J Pharmacol. 2000; 130:289-298.
58. Taylor AD, Cowell AM, Flower J, Buckingham JC Lipocortin 1 mediates an early inhibitory action of glucocorticoids on the secretion of ACTH by the rat anterior pituitary gland in vitro. Neuroendocrinology. 1993; 58:430-439.
59. Taylor AD, Cowell AM, Flower R.J., Buckingham JC. Dexamethasone suppresses the release of prolactin from the rat anterior pituitary gland by lipocortin 1 dependent and independent mechanisms. Neuroendocrinology. 1995; 62:530-542.
60. Taylor AD, Christian HC, Morris J.F., Flower RJ, Buckingham JC. An antisense oligodeoxynucleotide to lipocortin 1 reverses the inhibitory actions of dexamethasone on the release of adrenocorticotropin from rat pituitary tissue in vitro. Endocrinology. 1997; 138: 2909-2918.
61. Solito E, Mulla A, Morris JF, Christian HC, Flower RJ, Buckingham JC. Dexamethasone induces rapid serine-phosphorylation and membrane translocation of annexin 1 in a human folliculostellate cell line via a novel nongenomic mechanism involving the glucocorticoid receptor, protein kinaseC, phosphatidylinositol 3-kinase, and mitogen-activated protein kinase. Endocrinology. 2003; 144:1164-1174.