Estradiol initially enhances but subsequently suppresses (via adrenal steroids) granule cell proliferation in the dentate gyrus of adult female rats

Journal of Neurobiology

Volumn 55, Issue 2, 2003, Pages 247-260

  Ormerod, B K ^a   Lee, T T Y ^a   Galea, L A M ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Adult neurogenesis; Bromodeoxyuridine; Corticosterone; Dentate gyrus; Estradiol

Indexed keywords

BROXURIDINE; ESTRADIOL; ESTRADIOL BENZOATE;

ADRENALECTOMY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; DOSE TIME EFFECT RELATION; ESTROGEN ACTIVITY; FEMALE; GRANULE CELL; HIPPOCAMPUS; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OBSERVATION; OVARIECTOMY; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; REPRODUCTION; STATISTICAL SIGNIFICANCE; STEM CELL; TIME; VOLE;

ADRENAL CORTEX HORMONES; ADRENALECTOMY; AGING; ANIMALS; BROMODEOXYURIDINE; CELL DIVISION; DENTATE GYRUS; ESTRADIOL; FEMALE; GROWTH INHIBITORS; HYDROCORTISONE; OVARIECTOMY; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 0037402860     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10181     Document Type: Article

References (83)

1. Akana SF, Shinsako J, Dallman MF. 1983. Relationships among adrenal weight, corticosterone, and stimulated adrenocorticotropin levels in rats. Endocrinol 113:2232-2237.
2. Amaral DG, Witter MP. 1995. Hippocampal formation. In: Paxinos G, editor. The rat nervous system. New York: Academic Press, p 443-493.
3. Arnold SF, Obourn JD, Jaffe H, Notides AC. 1995. Phosphorylation of the human estrogen receptor on tyrosine 537 in vivo and by Src family tyrosine kinases in vitro. Mol Endocrinol 9:24-33.
4. Banasr M, Hery M, Brezun J, Daszuta A. 2001. Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus. Eur J Neurosci 14:1417-1424.
5. Buckingham JC, Dohler K-D, Wilson CA. 1978. Activity of the pituitary-adrenocortical system and thyroid gland during the oestrous cycle of the rat. J Endocrinol 78:359-366.
6. Burgess LH, Handa RJ. 1992. Chronic estrogen-induced alterations in adrenocorticotropin and corticosterone secretion and glucocorticoid receptor-mediated function in female rats. Endocrinol 131:1261-1269.
7. Cameron HA, Gould E. 1994. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61:203-209.
8. Cameron HA, Gould E. 1996. Distinct populations of cells in the adult dentate gyrus undergo mitosis or apoptosis in response to adrenalectomy. J Comp Neurol 369:56-63.
9. Cameron HA, McEwen BS, Gould E. 1995. Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J Neurosci 15:4687-4692.
10. Cameron HA, McKay RDG. 1999. Restoring production of hippocampal neurons in old age. Nat Neurosci 2:894-897.
11. Cameron HA, McKay RDG. 2001. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406-417.
12. Cameron HA, Tanapat P, Gould E. 1998. Adrenal steroids and N-methyl-D-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway. Neuroscience 82:349-354.
13. Cameron HA, Woolley CS, McEwen BS, Gould E. 1993. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56:337-344.
14. Christian JJ. 1975. Hormonal control of population growth. In: Eleftheriou BE, Sprott RL, editors. Hormonal Correlates of Behaviour, New York: Plenum Publishing Corporation, p 205-274.
15. Cordoba Montoya DA, Carrer HF. 1997. Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats. Brain Res 778:430-438.
16. Coyne MD, Kitay JI. 1969. Effect of ovariectomy on pituitary secretion of ACTH. Endocrinol 85:1097-1102.
17. Desmond NL, Zhang DX, Levy WB. 2000. Estradiol enhances the induction of homosynaptic long-term depression in the CA1 region of the adult, ovariectomized rat. Neurobiol Learn Mem 73:180-187.
18. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. 1998. Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317.
19. Ferrini M, De Nicola AF, 1991. Estrogens up-regulate Type I and Type II glucocorticoid receptors in brain regions from ovariectomized rats. Life Sci 48:2593-2601.
20. Fowler CD, Liu Y, Ouimet C, Wang Z. 2001. The effects of social environment on adult neurogenesis in the female prairie vole. J Neurobiol 51:115-128.
21. Francis F, Koulakoff A, Boucher D, Chafey P, Schaar B, Vinet MC, Friocourt G, McDonnell N, Reiner O, Kahn A, McConnell SK, Berwald-Netter Y, Denoulet P, Chelly J. 1999. Doublecortin is a developmentally regulated, microtubule associated protein expressed widely by migrating neurons. Neuron 23:247-256.
22. Fuchs E, Gould E. 2000. Mini-review: in vivo neurogenesis in the adult brain: regulation and functional implications. Eur J Neurosci 12:2211-2214.
23. Galea LAM, McEwen BS. 1999. Sex and seasonal differences in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles. Neurosci 89:955-964.
24. Galea LAM, Wide JK, Paine TA, Holmes MM, Ormerod BK, Floresco SB. 2001. High levels of estradiol disrupt conditioned place preference learning, stimulus response learning and reference memory but have limited effects on working memory. Behav Brain Res 126:115-126.
25. Garcia-Segura LM, Naftolin F, Hutchison JB, Azcoitia I, Chowen JA. 1999. Role of astroglia in estrogen regulation of synaptic plasticity and brain repair. J Neurobiol 40:574-584.
26. Gazzaley AH, Weiland NG, McEwen BS, Morrison JH. 1996. Differential regulation of NMDAR1 and mRNA and protein by estradiol in the rat hippocampus. J Neurosci 16:6830-6838.
27. Gleeson JG, Lin PT, Flanagan LA, Walsh CA. 1999. Doublecortin is a microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23:257-271.
28. Good M, Day M, Muir JL. 1999. Cyclical changes in endogenous levels of oestrogen modulate the induction of LTD and LTP in the hippocampal CA1 region. Eur J Neurosci 11:4476-4480.
29. Gould E, Beylin A, Tanapat P, Reeves A, Shots T. 1999a. Learning enhances adult neurogenesis in the hippocampal formation. Nature Neurosci 2:260-265.
30. Gould E, Cameron HA, Daniels DC, Woolley CS, McEwen BS. 1992. Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 12:3642-3650.
31. Gould E, McEwen BS, Tanapat P, Galea LAM, Fuchs E. 1997. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 17:2492-2498.
32. Gould E, Reeves AJ, Fallah M, Tanapat P, Gross CG, Fuchs E. 1999b. Hippocampal neurogenesis in Old World primates. Proc Natl Acad Sci USA 96:5263-5267.
33. Gould E, Tanapat P. 1997. Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat. Neurosci 80:427-436.
34. Gould E, Tanapat P, McEwen BS, Flügge G, Fuchs E. 1998. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 95:3168-3171.
35. Gould E, Woolley CS, McEwen BS. 1990. Short-term glucocorticoids manipulations affect neuronal morphology and survival in the adult dentate gyrus. Neurosci 37:367-375.
36. Gould E, Woolley CS, McEwen BS. 1991. Adrenal steroids regulate postnatal development of the rat dentate gyrus: I. Effects of glucocorticoids on cell death. J Comp Neurol 313:479-485.
37. Gu Q, Moss RL. 1996. 17β-estradiol potentiates kainite-induced currents via activation of the cAMP cascade. J Neurosci 16:3620-3629.
38. Gunderson HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B. 1988. The new stereological tools: dissector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96:857-881.
39. Gupta RR, Sen S, Diepenhorst LL, Rudick CN, Maren S. 2001. Estrogen modulates sexually dimorphic contextual fear conditioning and hippocampal long-term potentiation (LTP) in rats(1). Brain Res 888:356-365.
40. Handa RJ, Burgess LH, Kerr JE, O'Keefe JA. 1994. Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Horm Behav 28:464-476.
41. Hastings NB, Gould E. 1999. Rapid extension of axons into the CA3 region by adult-generated granule neurons. J Comp Neurol 413:146-154.
42. Hogervorst E, Williams J, Budge M, Riedel W, Jolles J. 2000. The nature of the effect of female gonadal hormone replacement therapy on cognitive function in post-menopausal women: a meta-analysis. Neurosci 101:485-512.
43. Holmes MM, Wide JK, Galea LAM. 2002. Low levels of estradiol facilitate while high levels of estradiol impair working memory performance in the working/reference memory version of the radial arm maze. Behav Neurosci, to appear.
44. Improta-Brears T, Whorton AR, Codazzi F, York JD, Meyer T, McDonnel DP. 1999. Estrogen-induced activation of mitogen-activated protein kinase requires mobilization of intracellular calcium. Proc Natl Acad Sci USA 96:4686-4691.
45. Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP. Greenberg DA. 2001. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci USA 98:4710-4715.
46. Kempermann G, Gage FH. 1999. New nerve cells for the adult brain. Sci Am 280:48-53.
47. Kempermann G, Kuhn HG, Gage FH. 1997. Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc Natl Acad Sci USA 94:10409-10414.
48. Kolb B, Pederson B, Ballerman M, Gibb R, Whishaw IQ. 1999. Embryonic and postnatal injections of bromodeoxyuridine produce age-dependent morphological and behavioral abnormalities. J Neurosci 19:2337-2346.
49. Kornack DR, Rakic P. 1999. Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc Natl Acad Sci USA 96:5768-5773.
50. Lemaire V, Koehl M, Le Moal M, Abrous DN. 2000. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 97:11032-11037.
51. Lemaire V, Taylor GT, Mormede P. 1997. Adrenal axis activation by chronic social stress fails to inhibit gonadal function in male rats. Psychoneuroendocr 22:563-573.
52. Lupien SJ, de Leon M, de Santi S, Convit A, Tarshish C, Nair NP, Thakur M, McEwen BS, Hauger RL, Meaney MJ. 1998. Cortisol levels during human ageing predict hippocampal atrophy and memory deficits. Nat Neurosci 1:69-73.
53. Lupien SJ, Nair NP, Briere S, Maheu F, Tu MT, Lemay M, McEwen BS, Meaney MJ. 1999. Increased cortisol levels and impaired cognition in human aging: implication for depression and dementia in later. Rev Neurosci 10:117-139.
54. Lupien SJ, Wilkinson CW, Briere S, Ng Ying Kin NM, Meaney MJ, Nair NP. 2002. Acute modulation of aged human memory by pharmacological manipulation of glucocorticoids. J Clin Endocrinol Metab 87:3798-3807
55. McDonnell DP, Morris JD. 2002. Connections and regulation of the human estrogen receptor. Science 296:1642-1644.
56. Milner TA, McEwen BS, Hayashi S, Li CJ, Reagan LP, Alves SE. 2001. Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J Comp Neurol 429:355-371.
57. Nowak KW, Neri G, Nussdorfer GG, Malendowicz LK. 1995. Effects of sex hormones on the steroidogenic activity of dispersed adrenocortical cells of the rat adrenal cortex. Life Sci 57:833-837.
58. Nowakowski RS, Hayes NL. 2000. New neurons: extraordinary evidence or extraordinary conclusion? Science 288:771a.
59. Ormerod BK, Galea LAM. 2000. Mechanism and function of adult neurogenesis. In: Shaw CS, McEachern J, editors. Toward a theory of plasticity. Philadelphia: Psychology Press. p 85-100.
60. Ormerod BK, Galea LAM. 2001. Reproductive status regulates cell proliferation within the dentate gyrus of the adult female meadow vole: A possible regulatory role for estradiol. Neurosci 2:169-179.
61. Palmer TD, Willhoite AR, Gage FH. 2000. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479-494.
62. th ed. London: Academic Press. 83 p.
63. Quinn CC, Gray GE, Hockfield S. 1999. A family of proteins implicated in axon guidance and outgrowth. Neurobiol 41:158-164.
64. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A. 2001. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153-7160.
65. Shors TJ, Meisegaes G, Beylin A, Zhao M, Rydel T, Gould E. 2001. Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372-376.
66. Shughrue PJ, Bushnell CD, Dorsa DM. 1992. Estrogen receptor messenger ribonucleic acid in female rat brain during the estrous cycle: a comparison with ovariectomized females and intact males. Endocrinol 131:381-388.
67. Shughrue PJ, Lane MV, Merchenthaler I. 1997. Comparative distribution of estrogen receptor-α and -β mRNA in the rat central nervous system. J Comp Neurol 388:507-525.
68. Shyamala G, Guiot MC. 1992. Activation of κ-b specific proteins by estradiol. Proc Natl Acad Sci USA 89:10628-10632.
69. Sing M, Setalo Jr G, Guan X, Warren M, Toran-Allerand CD. 1999. Estrogen-induced activation of mitogen-activated protein kinase in cerebral cortical explants: convergence of estrogen and neurotrophin signaling pathways. J Neurosci 19:1179-1188.
70. Smith MT, Pencea V, Want Z, Luskin MB, Insel TR. 2001. Increased number of BrdU-labeled neurons in the rostral migratory stream of the estrous prairie vole. Horm Behav 39:11-21.
71. Tanapat P, Hastings NB, Reeves AJ, Gould E. 1999. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19:5792-5801.
72. Tanapat P, Hastings NB, Rydel TA, Galea LAM, Gould E. 2001. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J Comp Neurol 437:496-504.
73. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. 2002. Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
74. Wang S, Scott B, Wojtowicz JM. 2000. Heterogenous properties of dentate granule neurons in the adult rat. J Neurobiol 42:248-257.
75. Warren SG, Humphreys AG, Juraska JM, Greenough WT. 1995. LTP varies across the estrous cycle: enhanced synaptic plasticity in proestrus rats. Brain Res 703:26-30.
76. Webb P, Nguyen P, Valentine C, Lopez GN, Kwok GR, McInerney E, Katzenellenbogen BS, Enmark E, Gustafsson J-Å, Nilsson S, Kushner PJ. 1999. The estrogen receptor enhances AP-1 activity by two distinct mechanisms with different requirement for receptor transactivation functions. Mol Endocrinol 13:1672-1685.
77. Weiland NG. 1992. Estradiol selectively regulates agonist binding sites on N-methyl-D-aspartate receptor complex in the CA1 region of the hippocampus. Endocrinol 131:662-669.
78. Weiland NG, Orikasa C, Hayashi S, McEwen BS. 1997. Distribution and hormone regulation of estrogen immunoreactive cells in the hippocampus of adult male and female rats. J Comp Neurol 388:603-612.
79. Weinberg J, Nezio S. 1987. Alcohol-induced changes in pituitary-adrenal activity during pregnancy. Alcohol Clin Exp Res 11:274-280.
80. West MJ, Slomianka L, Gundersen HJ. 1991. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
81. Woolley CS, Gould E, Frankfurt M, McEwen BS. 1990. Naturally-occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10:4035-4039.
82. Woolley CS, McEwen BS. 1993. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 336:293-306.
83. Ziylan YZ, Lefauconnier JM, Bernard G, Bourre JM. 1990. Blood-brain permeability: regional alterations after acute and chronic administration of ethinyl estradiol. Neurosci Lett 118:181-184.