Glucocorticoid fast feedback inhibition of stress-induced ACTH secretion in the male rat: Rate independence and stress-state resistance

Endocrinology

Volumn 157, Issue 7, 2016, Pages 2785-2798

  Osterlund, Chad D ^a   Rodriguez Santiago, Mariana ^a   Woodruff, Elizabeth R ^a   Newsom, Ryan J ^a   Chadayammuri, Anjali P ^a   Spencer, Robert L ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOTROPIN; GLUCOCORTICOID; POMC PROTEIN; PROLACTIN; PROTEIN; RNA; UNCLASSIFIED DRUG; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR;

ADENOHYPOPHYSIS; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; CORTICOTROPIN BLOOD LEVEL; CORTICOTROPIN RELEASE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IN VIVO STUDY; MALE; NEGATIVE FEEDBACK; NONHUMAN; PARAVENTRICULAR THALAMIC NUCLEUS; PRIORITY JOURNAL; PROLACTIN RELEASE; RAT; STRESS; ADRENALECTOMY; ANIMAL; DRUG EFFECTS; EXERCISE; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MENTAL STRESS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGICAL FEEDBACK; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SECRETION (PROCESS); SPRAGUE DAWLEY RAT;

ADRENALECTOMY; ADRENOCORTICOTROPIC HORMONE; ANIMALS; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; FEEDBACK, PHYSIOLOGICAL; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PITUITARY-ADRENAL SYSTEM; RATS; RATS, SPRAGUE-DAWLEY; RESTRAINT, PHYSICAL; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 84977107248     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2016-1123     Document Type: Article

References (74)

1. McEwenBS. Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol. 2008;583(2-3):174-185
2. Reagan LP, Grillo CA, Piroli GG. The As and Ds of stress: metabolic, morphological and behavioral consequences. Eur J Pharmacol. 2008;585(1):64-75
3. Dallman MF, Akana SF, Cascio CS, Darlington DN, Jacobson L, Levin N. Regulation of ACTH secretion: variations on a theme of B. Recent Prog Horm Res. 1987;43:113-173
4. Fink G, Rosie R, Sheward WJ, Thomson E, Wilson H. Steroid control of central neuronal interactions and function. J Steroid Biochem Mol Biol. 1991;40(1-3):123-132
5. Myers B, McKlveen JM, Herman JP. Neural regulation of the stress response: the many faces of feedback. Cell Mol Neurobiol. 2012; 32(5):683-694
6. Di S, Malcher-Lopes R, Halmos KC, Tasker JG. Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J Neurosci. 2003;23(12):4850-4857
7. Wamsteeker Cusulin JI, Füzesi T, Inoue W, Bains JS. Glucocorticoid feedback uncovers retrograde opioid signaling at hypothalamic synapses. Nat Neurosci. 2013;16(5):596-604
8. Wamsteeker JI, Bains JS. A synaptocentric view of the neuroendocrine response to stress. Eur J Neurosci. 2010;32(12):2011-2021
9. Deng Q, Riquelme D, Trinh L, et al. Rapid glucocorticoid feedback inhibition of ACTH secretion involves ligand-dependent membrane association of glucocorticoid receptors. Endocrinology. 2015; 156(9):3215-3227
10. Verkuyl JM, Karst H, Joëls M. GABAergic transmission in the rat paraventricular nucleus of the hypothalamus is suppressed by corticosterone and stress. Eur J Neurosci. 2005;21(1):113-121
11. Dallman MF, Yates FE. Dynamic asymmetries in the corticosteroid feedback path and distribution-metabolism-binding elements of the adrenocortical system. Ann NY Acad Sci. 1969;156(2):696-721
12. Keller-Wood ME, Dallman MF. Corticosteroid inhibition ofACTH secretion. Endocr Rev. 1984;5(1):1-24
13. Hodges JR, Jones MT. The effect of injected corticosterone on the release of adrenocorticotrophic hormone in rats exposed to acute stress. J Physiol (Lond). 1963;167:30-37
14. Dallman MF, JONES MT. Corticosteroid feedback control of ACTHsecretion: effect of stress-induced corticosterone secretion on subsequent stress responses in the rat. Endocrinology. 1973;92(5): 1367-1375
15. Keller-Wood ME, Shinsako J, Dallman MF. Feedback inhibition of adrenocorticotropic hormone by physiological increases in plasma corticosteroids in conscious dogs. J Clin Invest. 1983;71(4):859-866
16. Dallman MF, Akana SF, Scribner KA, et al. Stress, feedback and facilitation in the hypothalamo-pituitary-adrenal axis. J Neuroendocrinol. 1992;4(5):517-526
17. Jones MT, Hillhouse EW, Burden JL. Dynamics and mechanics of corticosteroid feedback at the hypothalamus and anterior pituitary gland. J Endocrinol. 1977;73(3):405-417
18. Jones MT, Tiptaft EM, Brush FR, Fergusson DA, Neame RL. Evidence for dual corticosteroid-receptor mechanisms in the feedback control of adrenocorticotrophin secretion. J Endocrinol. 1974; 60(2):223-233
19. Dallman MF. Fast glucocorticoid actions on brain: back to the future. Front Neuroendocrinol. 2005;26(3-4):103-108
20. Wamsteeker JI, Kuzmiski JB, Bains JS. Repeated stress impairs endocannabinoid signaling in the paraventricular nucleus of the hypothalamus. J Neurosci. 2010;30(33):11188-11196
21. Jones MT, Brush FR, Neame RL. Characteristics of fast feedback control of corticotrophin release by corticosteroids. J Endocrinol. 1972;55(3):489-497
22. Kaneko M, Hiroshige T. Fast, rate-sensitive corticosteroid negative feedback during stress. Am J Physiol. 1978;234(1):R39-R45
23. Hinz B, Hirschelmann R. Rapid non-genomic feedback effects of glucocorticoids on CRF-induced ACTH secretion in rats. Pharm Res. 2000;17(10):1273-1277
24. Joëls M, Sarabdjitsingh RA, Karst H. Unraveling the time domains of corticosteroid hormone influences on brain activity: rapid, slow, and chronic modes. Pharmacol Rev. 2012;64(4):901-938
25. Herman JP, Schafer MK, Thompson RC, Watson SJ. Rapid regulation of corticotropin-releasing hormone gene transcription in vivo. Mol Endocrinol. 1992;6(7):1061-1069
26. Autelitano DJ, Lundblad JR, Blum M, Roberts JL. Hormonal regulation of POMC gene expression. Annu Rev Physiol. 1989;51: 715-726
27. Armario A, Lopez-Calderon A, Jolin T, Castellanos JM. Sensitivity of anterior pituitary hormones to graded levels of psychological stress. Life Sci. 1986;39(5):471-475
28. Krulich L. The role of central monoamines in the stress-related changes of the secretion of prolactin and TSH. Psychopharmacol Bull. 1976;12(4):22-24
29. Gala RR. The physiology and mechanisms of the stress-induced changes in prolactin secretion in the rat. Life Sci. 1990;46(20):1407-1420
30. Watts AG. Glucocorticoid regulation of peptide genes in neuroendocrine CRH neurons: a complexity beyond negative feedback. Front Neuroendocrinol. 2005;26(3-4):109-130
31. Osterlund C, Spencer RL. Corticosterone pretreatment suppresses stress-induced hypothalamic-pituitary-adrenal axis activity via multiple actions that vary with time, site of action, and de novo protein synthesis. J Endocrinol. 2011;208(3):311-322
32. Orth DN. Methods of hormone radioimmunoassay. In: Jaffe B, ed. Adrenocorticotropic Hormone (ACTH). 2nd ed. San Diego: Academic Press; 1978:245-284
33. Osterlund CD, Jarvis E, Chadayammuri A, Unnithan R, Weiser MJ, Spencer RL. Tonic, but not phasic corticosterone, constrains stress activated extracellular-regulated-kinase 1/2 immunoreactivity within the hypothalamic paraventricular nucleus. J Neuroendocrinol. 2011;23(12):1241-1251
34. Dayas CV, Buller KM, Crane JW, Xu Y, Day TA. Stressor categorization: acute physical and psychological stressors elicit distinctive recruitment patterns in the amygdala and in medullary noradrenergic cell groups. Eur J Neurosci. 2001;14(7):1143-1152
35. Vahl TP, Ulrich-Lai YM, Ostrander MM, et al. Comparative analysis of ACTH and corticosterone sampling methods in rats. Am J Physiol Endocrinol Metab 2005;289(5):E823-E828
36. Jacobson L, Akana SF, Cascio CS, Shinsako J, Dallman MF. Circadian variations in plasma corticosterone permit normal termination of adrenocorticotropin responses to stress. Endocrinology. 1988;122(4):1343-1348
37. Nicholson WE, Davis DR, Sherrell BJ, Orth DN. Rapid radioimmunoassay for corticotropin in unextracted human plasma. Clin Chem. 1984;30(2):259-265
38. Pace TWW, Gaylord RI, Jarvis E, Girotti M, Spencer RL. Differential glucocorticoid effects on stress-induced gene expression in the paraventricular nucleus of the hypothalamus and ACTH secretion in the rat. Stress (Amsterdam, Netherlands). 2009;12(5):400-411
39. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego: Academic Press; 2007
40. Girotti M, Pace TWW, Gaylord RI, Rubin BA, Herman JP, Spencer RL. Habituation to repeated restraint stress is associated with lack of stress-induced c-fos expression in primary sensory processing areas of the rat brain. Neuroscience. 2006;138(4):1067-1081
41. Osterlund CD, Thompson V, Hinds L, Spencer RL. Absence of glucocorticoids augments stress-induced Mkp1 mRNA expression within the hypothalamic-pituitary-adrenal axis. J Endocrinol. 2014; 220(1):1-11
42. PaceTWW,Gaylord R, Topczewski F, Girotti M, Rubin B, Spencer RL. Immediate-early gene induction in hippocampus and cortex as a result of novel experience is not directly related to the stressfulness of that experience. Eur J Neurosci. 2005;22(7):1679-1690
43. Glenister DW, Yates FE. Sex difference in the rate of disappearance of corticosterone-4-C14 from plasma of intact rats: further evidence for the influence of hepatic -4-steroid hydrogenase activity on adrenal cortical function. Endocrinology. 1961;68(5):747-758
44. Schapiro S, Percin CJ, Kotichas FJ. Half-life of plasma corticosterone during development. Endocrinology. 1971;89(1):284-286
45. Andrews MH, Wood SA, Windle RJ, Lightman SL, Ingram CD. Acute glucocorticoid administration rapidly suppresses Basal and stress-induced hypothalamo-pituitary-adrenal axis activity. Endocrinology. 2012;153(1):200-211
46. Evanson NK, Tasker JG, Hill MN, Hillard CJ, Herman JP. Fast feedback inhibition of the HPA axis by glucocorticoids is mediated by endocannabinoid signaling. Endocrinology. 2010;151(10): 4811-4819
47. Jacobson L, Sapolsky R. Augmented ACTH responses to stress in adrenalectomized rats replaced with constant, physiological levels of corticosterone are partially normalized by acute increases in corticosterone. Neuroendocrinology. 1993;58(4):420-429
48. Thrivikraman KV, Nemeroff CB, Plotsky PM. Sensitivity to glucocorticoid-mediated fast-feedback regulation of the hypothalamicpituitary-adrenal axis is dependent upon stressor specific neurocircuitry. Brain Res. 2000;870(1-2):87-101
49. Nahar J, Haam J, Chen C, et al. Rapid Nongenomic glucocorticoid actions in male mouse hypothalamic neuroendocrine cells are dependent on the nuclear glucocorticoid receptor. Endocrinology. 2015;156(8):2831-2842
50. Kaneko M, Hiroshige T. Site of fast, rate-sensitive feedback inhibition of adrenocorticotropin secretion during stress. Am J Physiol. 1978;234(1):R46-R51
51. Bali B, Kovács KJ. GABAergic control of neuropeptide gene expression in parvocellular neurons of the hypothalamic paraventricular nucleus. Eur J Neurosci. 2003;18(6):1518-1526
52. Verkuyl JM, Hemby SE, Joëls M. Chronic stress attenuates GABAergic inhibition and alters gene expression of parvocellular neurons in rat hypothalamus. Eur J Neurosci. 2004;20(6):1665-1673
53. Cullinan WE, Ziegler DR, Herman JP. Functional role of local GABAergic influences on the HPA axis. Brain Struct Funct. 2008; 213(1-2):63-72
54. Sarkar J, Wakefield S, MacKenzie G, Moss SJ, Maguire J. Neurosteroidogenesis is required for the physiological response to stress: role of neurosteroid-sensitive GABAA receptors. J Neurosci. 2011; 31(50):18198-18210
55. 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(1):308-313
56. Shipston MJ. Mechanism(s) of early glucocorticoid inhibition of adrenocorticotropin secretion from anterior pituitary corticotropes. Trends Endocrinol Metab. 1995;6(8):261-266
57. Jeanneteau FD, Lambert WM, Ismaili N, et al. BDNF and glucocorticoids regulate corticotrophin-releasing hormone (CRH) homeostasis in the hypothalamus. Proc Natl Acad Sci USA. 2012; 109(4):1305-1310
58. Vázquez DM, Morano MI, Taylor L, Akil H. Kinetics of radiolabeled adrenocorticotropin hormone in infant and weanling rats. J Neuroendocrinol. 1997;9(7):529-536
59. Young EA. Normal glucocorticoid fast feedback following chronic 50% corticosterone pellet treatment. Psychoneuroendocrinology. 1995;20(7):771-784
60. Inoue W, Baimoukhametova DV, Füzesi T, et al. Noradrenaline is a stress-associated metaplastic signal at GABA synapses. Nat Neurosci. 2013;16(5):605-612
61. Kuzmiski JB, Marty V, Baimoukhametova DV, Bains JS. Stressinduced priming of glutamate synapses unmasks associative shortterm plasticity. Nat Neurosci. 2010;13(10):1257-1264
62. Ginsberg AB, Campeau S, Day HE, Spencer RL. Acute glucocorticoid pretreatment suppresses stress-induced hypothalamic-pituitary-adrenal axis hormone secretion and expression of corticotropin-releasing hormone hnRNA but does not affect c-fos mRNA or fos protein expression in the paraventricular nucleus of the hypothalamus. J Neuroendocrinol. 2003;15(11):1075-1083
63. Fevurly RD, Spencer RL. Fos expression is selectively and differentially regulated by endogenous glucocorticoids in the paraventricular nucleus of the hypothalamus and the dentate gyrus. J Neuroendocrinol. 2004;16(12):970-979
64. Kononen J, Honkaniemi J, Alho H, Koistinaho J, Iadarola M, Pelto-Huikko M. Fos-like immunoreactivity in the rat hypothalamic-pidoi tuitary axis after immobilization stress. Endocrinology. 1992; 130(5):3041-3047
65. Weiser MJ, Osterlund C, Spencer RL. Inhibitory effects of corticosterone in the hypothalamic paraventricular nucleus (PVN) on stress-induced adrenocorticotrophic hormone secretion and gene expression in the PVN and anterior pituitary. J Neuroendocrinol. 2011;23(12):1231-1240
66. Tasker JG, Herman JP. Mechanisms of rapid glucocorticoid feedback inhibition of the hypothalamic-pituitary-adrenal axis. Stress (Amsterdam, Netherlands). 2011;14(4):398-406
67. Bali B, Ferenczi S, Kovács KJ. Direct inhibitory effect of glucocorticoids on corticotrophin-releasing hormone gene expression in neurones of the paraventricular nucleus in rat hypothalamic organotypic cultures. J Neuroendocrinol. 2008;20(9):1045-1051
68. Evans AN, Liu Y, Macgregor R, Huang V, Aguilera G. Regulation of hypothalamic corticotropin-releasing hormone transcription by elevated glucocorticoids. Mol Endocrinol. 2013;27(11):1796-1807
69. Pariante CM, Papadopoulos AS, Poon L, et al.Anovel prednisolone suppression test for the hypothalamic-pituitary-adrenal axis. Biol Psychiatry. 2002;51(11):922-930
70. Yehuda R, Golier JA, Halligan SL, Meaney M, Bierer LM. The ACTHresponse to dexamethasone in PTSD.AmJ Psychiatry. 2004; 161(8):1397-1403
71. Bruehl H, Rueger M, Dziobek I, et al. Hypothalamic-pituitary-adrenal axis dysregulation and memory impairments in type 2 diabetes. J Clin Endocrinol Metab. 2007;92(7):2439-2445
72. Jerjes WK, Taylor NF, Wood PJ, Cleare AJ. Enhanced feedback sensitivity to prednisolone in chronic fatigue syndrome. Psychoneuroendocrinology. 2007;32(2):192-198
73. Galli U, Gaab J, Ettlin DA, Ruggia F, Ehlert U, Palla S. Enhanced negative feedback sensitivity of the hypothalamus-pituitary-adrenal axis in chronic myogenous facial pain. Eur J Pain. 2009;13(6):600-605
74. Mittal VA, Dhruv S, Tessner KD, Walder DJ, Walker EF. The relations among putative biorisk markers in schizotypal adolescents: minor physical anomalies, movement abnormalities, and salivary cortisol. Biol Psychiatry. 2007;61(10):1179-1186