Disrupted corticosterone pulsatile patterns attenuate responsiveness to glucocorticoid signaling in rat brain

Endocrinology

Volumn 151, Issue 3, 2010, Pages 1177-1186

  Sarabdjitsingh, R Angela ^a   Isenia, Sheena ^a   Polman, Annelies ^a   Mijalkovic, Jona ^a   Lachize, Servane ^a   Datson, Nicole ^a   De Kloet, E Ron ^a   Meijer, Onno C ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTEROID; CORTICOSTERONE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; MINERALOCORTICOID RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; BRAIN; CIRCADIAN RHYTHM; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE TRANSLOCATION; HIPPOCAMPUS; MALE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PULSATILE HORMONE RELEASE; RAT; STRESS; ULTRADIAN RHYTHM;

ACTIVITY CYCLES; ANIMALS; BRAIN; CORTICOSTERONE; DOWN-REGULATION; GENE EXPRESSION PROFILING; GLUCOCORTICOIDS; HIPPOCAMPUS; IMMEDIATE-EARLY PROTEINS; MALE; PROMOTER REGIONS, GENETIC; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUCOCORTICOID; RECEPTORS, MINERALOCORTICOID; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 77149163007     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2009-1119     Document Type: Article

References (56)

1. de Kloet ER, Joëls M, Holsboer F 2005 Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6:463-475
2. Herbert J, Goodyer IM, Grossman AB, Hastings MH, de Kloet ER, Lightman SL, Lupien SJ, Roozendaal B, Seckl JR 2006 Do corticosteroids damage the brain? J Neuroendocrinol 18:393-411
3. Tapp WN, Holaday JW, Natelson BH 1984 Ultradian glucocorticoid rhythms in monkeys and rats continue during stress. Am J Physiol 247:R866-R871
4. Jasper MS, Engeland WC 1991 Synchronous ultradian rhythms in adrenocortical secretion detected by microdialysis in awake rats. Am J Physiol 261:R1257-R1268
5. Windle RJ, Wood SA, Lightman SL, Ingram CD 1998 The pulsatile characteristics of hypothalamo-pituitary-adrenal activity in female Lewis and Fischer 344 rats and its relationship to differential stress responses. Endocrinology 139:4044-4052
6. Cook CJ 2002 Glucocorticoid feedback increases the sensitivity of the limbic system to stress. Physiol Behav 75:455-464
7. Droste SK, de Groote L, Atkinson HC, Lightman SL, Reul JM, Linthorst AC 2008 Corticosterone levels in the brain show a distinct ultradian rhythm but a delayed response to forced swim stress. Endocrinology 149:3244-3253
8. Lightman SL, Windle RJ, Julian MD, Harbuz MS, Shanks N, Wood SA, Kershaw YM, Ingram CD 2000 Significance of pulsatility in the HPAaxis. Novartis Found Symp 227:244-257; discussion 257-260
9. Deuschle M, Schweiger U, Weber B, Gotthardt U, Körner A, Schmider J, Standhardt H, Lammers CH, Heuser I 1997 Diurnal activity and pulsatility of the hypothalamus-pituitary-adrenal system in male depressed patients and healthy controls. J Clin Endocrinol Metab 82:234-238
10. Hartmann A, Veldhuis JD, Deuschle M, Standhardt H, Heuser I 1997 Twenty-four hour cortisol release profiles in patients with Alzheimer's and Parkinson's disease compared to normal controls: ultradian secretory pulsatility and diurnal variation. Neurobiol Aging 18:285-289
11. Young EA, Abelson J, Lightman SL 2004 Cortisol pulsatility and its role in stress regulation and health. Front Neuroendocrinol 25:69-76
12. de Kloet ER, Sarabdjitsingh RA 2008 Everything has rhythm: focus on glucocorticoid pulsatility. Endocrinology 149:3241-3243
13. Lightman SL, Wiles CC, Atkinson HC, Henley DE, Russell GM, Leendertz JA, McKenna MA, Spiga F, Wood SA, Conway-Campbell BL 2008 The significance of glucocorticoid pulsatility. Eur J Pharmacol 583:255-262
14. Reul JM, de Kloet ER 1985 Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117:2505-2511
15. Herman JP 1993 Regulation of adrenocorticosteroid receptor mRNA expression in the central nervous system. Cell Mol Neurobiol 13:349-372
16. De Kloet ER, Vreugdenhil E, Oitzl MS, Joëls M 1998 Brain corticosteroid receptor balance in health and disease. Endocr Rev 19: 269-301
17. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schütz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P, Evans RM 1995 The nuclear receptor superfamily: the second decade. Cell 83: 835-839
18. Datson NA, Morsink MC, Meijer OC, de Kloet ER 2008 Central corticosteroid actions: search for gene targets. Eur J Pharmacol 583: 272-289
19. Kitchener P, Di Blasi F, Borrelli E, Piazza PV 2004 Differences between brain structures in nuclear translocation and DNA binding of the glucocorticoid receptor during stress and the circadian cycle. Eur J Neurosci 19:1837-1846
20. Stavreva DA, Wiench M, John S, Conway-Campbell BL, McKenna MA, Pooley JR, Johnson TA, Voss TC, Lightman SL, Hager GL 2009 Ultradian hormone stimulation induces glucocorticoid receptor-mediated pulses of gene transcription. Nat Cell Biol 11: 1093-1102
21. Conway-Campbell BL, McKenna MA, Wiles CC, Atkinson HC, de Kloet ER, Lightman SL 2007 Proteasome-dependent down-regulation of activated nuclear hippocampal glucocorticoid receptors determines dynamic responses to corticosterone. Endocrinology 148: 5470-5477
22. Métivier R, Penot G, Hübner MR, Reid G, Brand H, Kos M, Gannon F 2003 Estrogen receptor-α directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 115:751-763
23. George AA, Schiltz RL, Hager GL 2009 Dynamic access of the glucocorticoid receptor to response elements in chromatin. Int J Biochem Cell Biol 41:214-224
24. Kino T 2007 Tissue glucocorticoid sensitivity: beyond stochastic regulation on the diverse actions of glucocorticoids. Horm Metab Res 39:420-424
25. Hauffa BP 2001 Clinical implications of pulsatile hormone signals. Growth Horm IGF Res 11(Suppl A):S1-S8
26. Akana SF, Cascio CS, Shinsako J, Dallman MF 1985 Corticosterone: narrow range required for normal body and thymus weight and ACTH. Am J Physiol 249:R527-R532
27. Akana SF, Scribner KA, Bradbury MJ, Strack AM, Walker CD, Dallman MF 1992 Feedback sensitivity of the rat hypothalamopituitary-adrenal axis and its capacity to adjust to exogenous corticosterone. Endocrinology 131:585-594
28. Meijer OC, Van Oosten RV, De Kloet ER 1997 Elevated basal trough levels of corticosterone suppress hippocampal 5-hydroxytryptamine(1A) receptor expression in adrenally intact rats: implication for the pathogenesis of depression. Neuroscience 80:419-426
29. Fluttert M, Dalm S, Oitzl MS 2000 A refined method for sequential blood sampling by tail incision in rats. Lab Anim 34:372-378
30. Sarabdjitsingh RA, Spiga F, Meijer OC, Lightman SL, de Kloet ER, Chronic glucocorticoid administration affects endogenous diurnal and ultradian rhythms in rats and stress responsiveness. Proc 8th Annual Meeting Dutch Endo-Neuro-Psycho (ENP), Doorwerth, The Netherlands 2009 (Abstract, 1.12, 90)
31. Haché RJ, Tse R, Reich T, Savory JG, Lefebvre YA 1999 Nucleocytoplasmic trafficking of steroid-free glucocorticoid receptor. J Biol Chem 274:1432-1439
32. Gomez-Sanchez CE, de Rodriguez AF, Romero DG, Estess J, Warden MP, Gomez-Sanchez MT, Gomez-Sanchez EP 2006 Development of a panel of monoclonal antibodies against the mineralocorticoid receptor. Endocrinology 147:1343-1348
33. Sarabdjitsingh RA, Meijer OC, Schaaf MJ, de Kloet ER 2009 Subregion-specific differences in translocation patterns of mineralocorticoid and glucocorticoid receptors in rat hippocampus. Brain Res 1249:43-53
34. van der Laan S, Lachize SB, Schouten TG, Vreugdenhil E, de Kloet ER, Meijer OC 2005 Neuroanatomical distribution and colocalisation of nuclear receptor corepressor (N-CoR) and silencing mediator of retinoid and thyroid receptors (SMRT) in rat brain. Brain Res 1059:113-121
35. Meijer OC, Steenbergen PJ, De Kloet ER 2000 Differential expression and regional distribution of steroid receptor coactivators SRC-1 and SRC-2 in brain and pituitary. Endocrinology 141:2192-2199
36. van der Laan S, Sarabdjitsingh RA, Van Batenburg MF, Lachize SB, Li H, Dijkmans TF, Vreugdenhil E, de Kloet ER, Meijer OC 2008 Chromatin immunoprecipitation scanning identifies glucocorticoid receptor binding regions in the proximal promoter of a ubiquitously expressed glucocorticoid target gene in brain. J Neurochem 106: 2515-2523
37. van Gemert NG, Meijer OC, Morsink MC, Joëls M 2006 Effect of brief corticosterone administration on SGK1 and RGS4 mRNA expression in rat hippocampus. Stress 9:165-170
38. Wang JC, Derynck MK, Nonaka DF, Khodabakhsh DB, Haqq C, Yamamoto KR 2004 Chromatin immunoprecipitation (ChIP) scanning identifies primary glucocorticoid receptor target genes. Proc Natl Acad Sci USA 101:15603-15608
39. Yachi K, Inoue K, Tanaka H, Yoshikawa H, Tohyama M 2007 Localization of glucocorticoid-induced leucine zipper (GILZ) expressing neurons in the central nervous system and its relationship to the stress response. Brain Res 1159:141-147
40. Spencer RL, Miller AH, Stein M, McEwen BS 1991 Corticosterone regulation of type I and type II adrenal steroid receptors in brain, pituitary, and immune tissue. Brain Res 549:236-246
41. Arriza JL, Simerly RB, Swanson LW, Evans RM 1988 The neuronal mineralocorticoid receptor as a mediator of glucocorticoid response. Neuron 1:887-900
42. Ahima RS, Harlan RE 1990 Charting of type II glucocorticoid receptor-like immunoreactivity in the rat central nervous system. Neuroscience 39:579-604
43. Sapolsky RM, Krey LC, McEwen BS 1984 Stress down-regulates corticosterone receptors in a site-specific manner in the brain. Endocrinology 114:287-292
44. Reul JM, Pearce PT, Funder JW, Krozowski ZS 1989 Type I and type II corticosteroid receptor gene expression in the rat: effect of adrenalectomy and dexamethasone administration. Mol Endocrinol 3:1674-1680
45. Bradbury MJ, Akana SF, Dallman MF 1994 Roles of type I and II corticosteroid receptors in regulation of basal activity in the hypothalamo-pituitary-adrenal axis during the diurnal trough and the peak: evidence for a nonadditive effect of combined receptor occupation. Endocrinology 134:1286-1296
46. Joëls M, Karst H, Krugers HJ, Lucassen PJ 2007 Chronic stress: implications for neuronal morphology, function and neurogenesis. Front Neuroendocrinol 28:72-96
47. Karst H, Joëls M 2007 Brief RU 38486 treatment normalizes the effects of chronic stress on calcium currents in rat hippocampal CA1 neurons. Neuropsychopharmacology 32:1830-1839
48. Karten YJ, Nair SM, van Essen L, Sibug R, Joëls M 1999 Long-term exposure to high corticosterone levels attenuates serotonin responses in rat hippocampal CA1 neurons. Proc Natl Acad Sci USA 96:13456-13461
49. John S, Johnson TA, Sung MH, Biddie SC, Trump S, Koch-Paiz CA, Davis SR, Walker R, Meltzer PS, Hager GL 2009 Kinetic complexity of the global response to glucocorticoid receptor action. Endocrinology 150:1766-1774
50. Meijer OC 2006 Understanding stress through the genome. Stress 9:61-67
51. Biddie SC, Hager GL 2009 Glucocorticoid receptor dynamics and gene regulation. Stress 12:193-205
52. Waxman DJ, Ram PA, Park SH, Choi HK 1995 Intermittent plasma growth hormone triggers tyrosine phosphorylation and nuclear translocation of a liver-expressed, Stat 5-related DNA binding protein. Proposed role as an intracellular regulator of male-specific liver gene transcription. J Biol Chem 270:13262-13270
53. Belchetz PE, Plant TM, Nakai Y, Keogh EJ, Knobil E 1978 Hypophysial responses tocontinuousandintermittent delivery ofhypopthalamic gonadotropin-releasing hormone. Science 202:631-633
54. Wildt L, Häusler A, Marshall G, Hutchison JS, Plant TM, Belchetz PE, Knobil E 1981 Frequency and amplitude of gonadotropin-releasing hormone stimulation and gonadotropin secretion in the rhesus monkey. Endocrinology 109:376-385
55. Amato G, Mazziotti G, Di Somma C, Lalli E, De Felice G, Conte M, Rotondi M, Pietrosante M, Lombardi G, Bellastella A, Carella C, Colao A 2000 Recombinant growth hormone (GH) therapy in GH-deficient adults: a long-term controlled study on daily versus thrice weekly injections. J Clin Endocrinol Metab 85:3720-3725
56. Shoupe D 2001 HRT dosing regimens: continuous versus cyclicpros and cons. Int J Fertil Womens Med 46:7-15