Estrogens normalize the hypothalamic-pituitary-adrenal axis response to stress and increase glucocorticoid receptor immunoreactivity in hippocampus of aging male rats

Neuroendocrinology

Volumn 69, Issue 2, 1999, Pages 129-137

  Ferrini, Monica ^a,b   Piroli, Gerardo ^a,b   Frontera, Miriam ^b   Falbo, Andrea ^b   Lima, Analia ^a   De Nicola, Alejandro F ^a,b,c,d  

^a UBA CONICET ^*  (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c Argentina   (Argentina)

^d INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

Author keywords

Adrenal steroid receptors; Adrenal steroids; Aging; Corticotropin; Gonadal steroids; Hippocampus; Stress

Indexed keywords

CORTICOSTERONE; ESTROGEN; GLUCOCORTICOID RECEPTOR;

AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; ESTROGEN THERAPY; FEEDBACK SYSTEM; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOREACTIVITY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; STRESS; SUBICULUM;

ADRENAL GLANDS; AGING; ANIMALS; CORTICOSTERONE; ESTRADIOL; ETHER, ETHYL; HIPPOCAMPUS; HYPOTHALAMUS; KINETICS; MALE; ORGAN SIZE; PITUITARY GLAND; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUCOCORTICOID; STRESS;

EID: 0033039242     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000054411     Document Type: Article

References (55)

1. Lanfield PW, Waymire JC, Lynch G: Hippocampal aging and adrenocorticoids: quantitative correlations. Science 1978;202:1098-1101.
2. Sapolsky R, Krey LC, McEwen BS: The neuroendocrinology of stress and aging: The glucocorticoid cascade hypothesis. Endocr Rev 1986;7:284-304.
3. Sonntag WE, Goliszek AG, Brodish A, Eldridge JE: Diminished diurnal secretion of adrenocorticotropin (ACTH) but not corticosterone, in old male rats: Possible relation to increased adrenal sensitivity to ACTH in vivo. Endocrinology 1987;120:2308-2315.
4. Issa A, Rowe W, Gauthier S, Meaney M: Hypothalamic-pituitary-adrenal activity in aged, cognitively unimpaired rats. J Neurosci 1990; 10:3247-3254.
5. Lorens SA, Hata N, Handa RJ, Van der Kar LD, Guschwan M, Goral J, Lee JM, Hamilton ME, Bethea CL, Clancy J: Neurochemical, endocrine and immunological responses to stress in young and old Fischer 344 male rats. Neurobiol Aging 1990;11:139-150.
6. Pfeiffer A, Barden N, Meaney MJ: Age-related changes in glucocorticoid receptor binding and mRNA levels in the rat brain and pituitary. Neurobiol Aging 1991;12:475-479.
7. Sapolsky R: Do glucocorticoid concentrations rise with age in the rat? Neurobiol Aging 1991; 13:171-174.
8. Van Eekelen JAM, Rots NY, Sutanto W, de Kloet ER: The effect of aging on stress responsiveness and central corticosteroid receptors in the Brown Norway rat. Neurobiol Aging 1991; 13:159-170.
9. Cizza G, Calogero AE, Brady LS, Bagdy G, Bergamini E, Blackmail MR, Chrousos GP, Gold PW: Male Fischer 344/N rats show a progressive central impairment of the hypothalamic-pituitary-adrenal axis with advancing age. Endocrinology 1994;134:1611-1620.
10. Morano MI, Vazquez DM, Akil H: The role of the hippocampal mineralocorticoid and glucocorticoid receptors in the hypothalamo-pituitary-adrenal axis of the aged Fischer rat. Mol Cell Neurosci 1994;5:400-412.
11. Cai A, Wise PM: Age-related changes in the diurnal rhythm of CRH gene expression in the paraventricular nuclei. Am J Physiol 1996; 33:E238-E243.
12. Reul JMHM, de Kloet ER: Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation. Endocrinology 1985;117:2505-2511.
13. McEwen BS, Cameron H, Chao HM, Gould E. Magariños AM, Watanabe Y, Wooley CS: Adrenal steroid and plasticity of hippocampal neurons: Toward an understanding of underlying cellular and molecular mechanisms. Cell Mol Neurobiol 1993;13:457-482.
14. Tornello S, Orti E, De Nicola AF, Rainbow TC, McEwen BS: Regulation of glucocorticoid receptors in brain by corticosterone treatment of adrenalectomized rats. Neuroendocrinology 1982;35:411-417.
15. Watanabe Y, Gould E, McEwen BS: Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 1992;588:341-345.
16. Woolley CS, Gould E, McEwen BS: Exposure to excess gluocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 1990;531:225-231.
17. Lanfield P, Eldridge C: Increased affinity of type II corticosteroid binding in aged rat hippocampus. Exp Neurol 1989;106:110-113.
18. Rachmanin G, Lutge W, Hunter B, Walker D: Neither chronic exposure to ethanol nor aging affects type I or type II corticosteroid receptors in rat hippocampus. Exp Neurol 1989;106: 164-171.
19. McEwen BS: Re-examination of the glucocorticoid hypothesis of stress and aging. Progr Brain Res 1992;93:365-383.
20. Seckl JR, Olsson T: Glucocorticoid hypersecretion and the age-impaired hippocampus. J Endocrinol 1995;145:201-211.
21. Weiland NG, Orisaka C, Hayashi S, McEwen BS: Distribution and hormone regulation of estrogen receptor immunoreactive cells in the hippocampus of male and female rats. J Comp Neurol 1997;388:603-612.
22. Kuiper GGJ, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustaffson J-A: Comparison of the ligand bindings specificity and transcript tissue distribution of estrogen receptors α and β. Endocrinology 1997;138:863-870.
23. Shugrue PJ, Lane MV, Merchenthaler I: Comparative distribution of estrogen receptor-α and -β mRNA in the rat central nervous system. J Comp Neurol 1997;388:507-525.
24. Gould E, Wooley CS, Frankfurt M, McEwen BS: Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 1990;10:1286-1291.
25. Woolley CS, McEwen BS: Estradiol regulated hippocampal dendritic spine density via an N-metyl-D-aspartate receptor-dependent mechanism. J Neurosci 1994;14:7680-7687.
26. Henderson V: The epidemiology of estrogen replacement therapy and Alzheimer's disease. Neurology 1997;48(suppl 7):S27-S35.
27. Goodman Y, Bruce AJ, Cheng B, Mattson MP: Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid β-peptide toxicity in hippocampal neurons. J Neurochem 1996;66:1836-1844.
28. Behl C. Widmann M, Trapp T, Holsboer F: 17β-Estradiol protects neurons from oxidative stress-induced cell death in vitro. Biochem Biophys Res Commun 1995;216:473-482.
29. Regan RF, Guo Y: Estrogens attenuate neuronal injury due to hemoglobin, chemical hypoxia, and excitatory amino acids in murine cortical cultures. Brain Res 1997;764:133-140.
30. Viau V, Meaney MJ: Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 1991;129:2503-2511.
31. Pfeiffer A, Lapointe B, Barden N: Hormonal regulation of type II gluocorticoid receptor messenger ribonucleic acid in rat brain. Endocrinology 1991;129:2166-2174.
32. Redei E, Li L, Halasz I, McGivern RF, Aird F: Fast glucocorticoid feedback inhibition of ACTH secretion in the ovariectomized rat: Effect of chronic estrogen and progesterone. Neuroendocrinology 1994;60:113-126.
33. Ferrini M, De Nicola AF: Estrogens up-regulate type I and type II glucocorticoid receptors in brain regions from ovariectomized rats. Life Sci 1991;48:2593-2601.
34. Ferrini M, Lima A, De Nicola AF: Estradiol abolishes down-regulation of glucocorticoid receptors in brain. Life Sci 1995;57:2403-2412.
35. Ferrini M, Grillo C, Piroli G, de Kloet ER, De Nicola AF: Sex differences in glucocorticoid regulation of vasopressin mRNA in the paraventricular hypothalamic nucleus. Cell Mol Neurobiol 1997;17:671-686.
36. Lindheim SR, Legro RS, Bernstein L: Behavioral stress responses in premenopausal and postmenopausal women and the effects of estrogen. Am J Obstet Gynecol 1992;167:1831-1836.
37. Meites J, Nicoll CS: Adenohypophysis prolactin. Ann Rev Physiol 1966;28:57-88.
38. Weisenberg L, Fridman O, Libertun C, De Nicola AF: Changes in nuclear translocation of estradiol-receptor complex in anterior pituitary and uterus of rats with streptozotocin diabetes. J Steroid Biochem Mol Biol 1983;19:1737-1741.
39. Magarinos AM, Somoza G, De Nicola AF: Glucocorticoid negative feedback and glucocorticoid receptors after hippocampectomy in rats. Horm Metab Res 1987;19:105-109.
40. Piroli G, Grillo C, Lux de Lantos V, Libertun C, De Nicola AF: Glucocorticoid receptors and inhibition of serum prolactin by dexamethasone are reduced in rats with estrogen-induced pituitary tumors. Neuroendocrinol Lett 1991; 13:75-81.
41. Fuxe K, Wikstrom AC, Okret S, Agnati LF, Harfstrand A, Yu Z-Y, Granholm L, Zoli M, Vale W, Gustafsson J-A: Mapping of glucocorticoid receptor immunoreactive neurons in the rat tel- and diencephalon using a monoclonal antibody against rat liver glucocorticoid receptor. Endocrinology 1985;117:1803-1812.
42. Van Eckelen JAM, Kiss JZ, Westphal HM, de Kloet ER: Immunocytochemical study on the intracellular localization of the type 2 glucocorticoid receptor in the rat brain. Brain Res 1987; 436:120-128.
43. Herman JP, Schafer MKH, Young A, Thompson R, Douglas J, Akil H, Watson SJ: Evidence for hippocampal regulation of neuroendocrine neurons of the hypothalamo-pituitary-adrenocortical axis. J Neurosci 1989;9:3072-3082.
44. Hatzinger M, Reul JMHM, Landgraf R, Holsboer F, Neumann I: Combined dexamethasone/CRH test in rats: Hypothalamo-pituitary-adrenocortical system alterations in aging. Neuroendocrinology 1996;64:349-356.
45. O'Brien JT, Schweitzer I, Ames D, Tuckwell V, Mastwyck M: Cortisol suppression by dexamethasone in the healthy elderly: Effects of age, dexamethasone levels, and cognitive function. Biol Psychiatry 1994;36:389-394.
46. Wilkstrom A-N, Bakke O, Okret S, Bronnegard M, Gustafsson J-A: Intracellular localization of the glucocorticoid receptor: Evidence for cytoplasmic and nuclear localization. Endocrinology 1987;120:1232-1242.
47. Patchev V, Hayashi S, Onkasa C, Almeida OFX: Implications of estrogen-dependenl brain organization for gender differences in hypothalamo-pituitary-adrenal regulation. FASEB J 1995;9:419-423.
48. Turner BB: Sex differences in the binding of Type I and Type II corticosteroid receptors in rat hippocampus. Brain Res 1992;581:229-236.
49. Turner BB: Influence of gonadal steroid on brain corticosteroid receptors: A minireview. Neurochem Res 1997;22:1375-1385.
50. Luine VN: Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats. Exp Neurol 1985;89:484-490.
51. Gibbs R: Effects of estrogens on basal forebrain cholinergic neurons vary as a function of dose and duration of treatment. Brain Res 1997; 757:10-16.
52. Yau JLW, Dow RC, Fink G, Seckl JR: Medial septal lesions increase hippocampal mineralocorticoid and glucocorticoid receptor messenger RNA expression. Brain Res 1992;577:155-160.
53. De Kloet ER: Brain corticosteroid receptor balance and homeostatic control. Front Neuroendocrinol 1991;12:95-164.
54. Oxenkrug GF, Pomara N, McIntyre IM, Branconier RJ, Staley M, Gershon S: Aging and cortisol resistance to suppression by dexamethasone: A positive correlation. Psychiatry Res 1983;10:125-130.
55. De Leon MJ, Mcrae T, Tsai JR, George AE, Marcus DL, Freedman M, Wolf AP, McEwen BS: Abnormal cortisol response in Alzheimer's disease linked to hippocampal atrophy. Lancet 1988;ii:391-392.