Distribution and hormone regulation of estrogen receptor immunoreactive cells in the hippocampus of male and female rats

Journal of Comparative Neurology

Volumn 388, Issue 4, 1997, Pages 603-612

  Weiland, N G ^a   Orikasa, C ^b   Hayashi, S ^c   McEwen, B S ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b NIPPON MEDICAL SCHOOL   (Japan)

^c TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

CA1; Cortex; Dentate gyrus; Progesterone receptor; Synaptic plasticity

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR; PROGESTERONE RECEPTOR;

ANIMAL TISSUE; ARTICLE; DENTATE GYRUS; FEMALE; HIPPOCAMPUS; HORMONAL REGULATION; INTERNEURON; LEARNING; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; RECEPTOR DENSITY; SEX DIFFERENCE;

ANIMALS; DOWN-REGULATION; ESTROGENS; FEMALE; HIPPOCAMPUS; INTERNEURONS; MALE; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE; SEX CHARACTERISTICS;

EID: 0030810111     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19971201)388:4<603::AID-CNE8>3.0.CO;2-6     Document Type: Article

References (68)

1. Amaral, D.G. (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat. J. Comp. Neurol. 182:851-914.
2. Backstrom, T. (1976) Epileptic seizures in women related to plasma estrogen and progesterone during the menstrual cycle. Acta Neurol. Scand. 54:321-347.
3. Barley, J., M. Ginsburg, N. MacLusky, I.D. Morris, and P.J. Thomas (1977) Sex differences in the distribution of cytoplasmic oestrogen receptors in rat brain and pituitary: Effects of gonadectomy and neonatal androgen treatment. Brain Res. 129:309-318.
4. Berghorn, K.A., J.H. Bonnett, and G.E. Hoffman (1994) cFos immunoreactivity is enhanced with biotin amplification. J. Histochem. Cytochem. 42:1635-1642.
5. Bettini, E., G. Pollio, S. Santagati, and A. Maggi (1992) Estrogen receptor in the rat brain: Presence in the hippocampal formation. Neuroendocrinology 56:502-508.
6. Blaustein, J.D. (1992) Cytoplasmic estrogen receptors in rat brain: Immunocytochemical evidence using three antibodies with distinct epitopes. Endocrinology 131:1336-1342.
7. Brown, T.J., R.B. Hochberg, J.E. Zielinski, and N.J. MacLusky (1988) Regional sex differences in cell nuclear estrogen-binding capacity in the rat hypothalamus and preoptic area. Endocrinology 123:1761-1770.
8. Buckmaster, P.S., and P.A. Schwartzkroin (1995) Interneurons and inhibition in the dentate gyrus of the rat in vivo. J. Neurosci. 15:774-789.
9. Clancy, A.N., and R.P. Michael (1994) Effects of testosterone and aromatase inhibition on estrogen receptor-like immunoreactivity in male rat brain. Neuroendocrinology 59:552-560.
10. Daniel, J.M., A.J. Fader, A. Spencer, and B.E.F. Wee (1996) Effects of estrogen and environment on radial maze acquisition. Soc. Neurosci. Abstr. 22:1386.
11. DonCarlos, L.L., E. Monroy, and J.I. Morrell (1991) Distribution of estrogen receptor-immunoreactive cells in the forebrain of the female guinea pig. J. Comp. Neurol. 305:591-612.
12. Feder, A.J., A.W. Hendricson, and G.P. Dohanich (1996) Effects of estrogen treatment on T-maze alteration in female and male rats. Soc. Neurosci. Abstr. 22:1386.
13. Fillit, H., H. Weinreb, I. Cholst, V. Luine, B. McEwen, R. Amador, and J. Zabriskie (1986) Observations in a preliminary open trial of estradiol therapy for senile dementia-Alzheimer's type. Psychoneuroendocrinology 11:337-345.
14. Freund, T.F., and G. Buzsáki (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
15. Gazzaley, A.H., N.G. Weiland, B.S. McEwen, and J.H. Morrison (1996) Differential regulation of NMDAR1 mRNA and protein by estradiol in the rat hippocampus. J. Neurosci. 16:6830-6838.
16. Gould, E., C.S. Woolley, M. Frankfurt, and B.S. McEwen (1990) Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci. 10:1286-1291.
17. Greene, G.L., N.B. Sobel, W.J. King, and E.V. Jensen (1984) Immunocytochemical studies of estrogen receptors. J. Steroid Biochem. 20:51-56.
18. Halasy, K., R. Miettinen, E. Szabat, and T.F. Freund (1992) GABAergic interneurons are the major postsynaptic targets of median raphe afferents in the rat dentate gyrus. Eur. J. Neurosci. 4:144-153.
19. Henderson, V.W., A. Paganini-Hill, C.K. Emanuel, M.E. Dunn, and J.G. Buckwalter (1994) Estrogen replacement therapy in older women: Comparisons between Alzheimer's disease cases and nondemented control subjects. Arch. Neurol. 51:896-900.
20. Henderson, V.W., L. Watt, and J.G. Buckwalter (1996) Cognitive skills associated with estrogen replacement in women with Alzheimer's disease. Psychoneuroendocrinology 12:421-430.
21. Juraska, J.M., and S.G. Warren (1996) Spatial memory decline in aged, noncycling female rats varies with the phase of estropause. Soc. Neurosci. Abstr. 22:1387.
22. Koehorst, S.G.A., J.J. Cox, G.H. Donker, S. Lopes da Silva, J.P.H. Burbach, J.H.H. Thijssen, and M.A. Blankenstein (1994) Functional analysis of an alternatively spliced estrogen receptor lacking exon 4 isolated from MCF-7 breast cancer cells and meningioma tissue. Mol. Cell. Endocrinol. 101:237-245.
23. Korol, D.L., J.M. Couper, C.K. McIntyre, and P.E. Gold (1996) Strategies for learning across the estrous cycle in female rats. Soc. Neurosci. Abstr. 22:1386.
24. 2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res. 419:119-130.
25. Kuiper, G.G.J.M., E. Enmark, M. Pelto-Huikko, S. Nilsson, and J.A. Gustafsson (1996) Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. USA 93:5925-5930.
26. Kuiper, G.G.J.M., B. Carlsson, K. Graddien, E. Enmark, J. Häggblad, S. Nilsson, and J.-Å. Gustafsson (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors a and β. Endocrinology 138:863-870.
27. Lacaille, J.-C., A.L. Mueller, D.D. Kunkel, and P.A. Schwartzkroin (1987) Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: Electrophysiology and morphology. J. Neurosci. 7:1979-1993.
28. Lewis, C., B.S. McEwen, and M. Frankfurt (1995) Estrogen-induction of dendritic spines in ventromedial hypothalamus and hippocampus: Effects of neonatal aromatase blockade and adult GDX. Dev. Brain Res. 87:91-95.
29. Loy, R., J.L. Gerlach, and B.S. McEwen (1988) Autoradiographic localization of estradiol-binding neurons in the rat hippocampal formation and entorhinal cortex. Dev. Brain Res. 39:245-251.
30. Luine, V.N., J. Renatas, L. Sterbank, and K. Beck (1996) Estradiol effects on rat spatial memory. Soc. Neurosci. Abstr. 22:1387.
31. Maggi, A., L. Susanna, E. Bettini, G. Mantero, and I. Zucchi (1989) Hippocampus: A target for estrogen action in mammalian brain. Mol. Endocrinol. 3:1165-1170.
32. 3H]muscimol binding in hippocampus, hypothalamus and midbrain in rats. J. Neuroendocrinol. 4:393-399.
33. O'Keefe, J.A., E.B. Pedersen, A.J. Castro, and R.J. Handa (1993) The ontogeny of estrogen receptors in heterochronic hippocampal and neocortical transplants demonstrates an intrinsic development program. Dev. Brain Res. 75:105-112.
34. O'Keefe, J.A., Y. Li, L.H. Burgess, and R.J. Handa (1995) Estrogen receptor mRNA alterations in the developing rat hippocampus. Mol. Brain Res. 30:115-124.
35. O'Neil, M.F., L.W. Means, M.C. Poole, and R.J. Hamm (1996) Estrogen affects performance of ovariectomized rats in a two-choice water-escape working memory task. Psychoneuroendocrinology 21:51-65.
36. Okamura, H., K. Yamamoto, S. Hayashi, A. Kuroiwa, and M. Muramatsu (1992) Apolyclonal antibody to the rat oestrogen receptor expressed in Escherichia coli: Characterization and application to immunohistochemistry. J. Endocrinol. 135:333-341.
37. Orikasa, C., H. Okamura, and S. Hayashi (1994) Estrogen receptor found in the facial nucleus of the newborn rat is suppressed by exogenous estrogen: Immuno- and in situ hybridization histochemical studies. Dev. Brain Res. 82:9-17.
38. Paganini-Hill, A., and V.W. Henderson (1994) Estrogen deficiency and risk of Alzheimer's disease in women. Am. J. Epidemiol. 3:3-16.
39. Pelletier, G., N. Liao, N. Follea, and M.V. Govindan (1988) Mapping of estrogen receptor-producing cells in the rat brain by in situ hybridization. Neurosci. Lett. 94:23-28.
40. Pfaff, D., and M. Keiner (1973) Atlas of estradiol-concentrating cells in the central nervous system of the female rat. J. Comp. Neurol. 151:121-157.
41. Pfeffer, U., E. Fecarotta, L. Castagnetta, and G. Vidali (1993) Estrogen receptor variant messenger RNA lacking exon 4 in estrogen-responsive human breast cancer cell lines. Cancer Res. 53:741-743.
42. Phillips, S.M., and B.B. Sherwin (1992a) Effects of estrogen on memory function in surgically menopausal women. Psychoneuroendocrinology 17:485-495.
43. Phillips, S.M., and B.B. Sherwin (1992b) Variations in memory function and sex steroid hormones across the menstrual cycle. Psychoneuroendocrinology 17:497-506.
44. Rainbow, T.C., B. Parsons, and B.S. McEwen (1982) Sex differences in rat brain oestrogen and progestin receptors. Nature 300:648-649.
45. Samulack, D.D., S. Williams, and J. Lacaille (1993) Hvperpolarizing synaptic potentials evoked in CA1 pyramidal cells by glutamate stimulation of interneurons from the oriens/alveus border of rat hippocampal slices: I. Electrophysiological response properties. Hippocampus 3:331-344.
46. Segarra, A.C., and B.S. McEwen (1991) Estrogen increases spine density in ventromedial hypothalamic neurons of peripubertal rats. Neuroendocrinology 54:365-372.
47. Sherwin, B.B. (1988) Estrogen and/or androgen replacement therapy and cognitive functioning in surgically menopausal women. Psychoneuroendocrinology 13:345-357.
48. Sherwin, B.B., and T. Tulandi (1996) "Add-back" estrogen reverses cognitive deficits induced by a gonadotropin-releasing agonist in women with leiomyomata uteri. J. Clin. Endocrinol. Metab. 81:2545-2549.
49. Sik, A., A. Ylinin, M. Penttonen, and G. Buzsaki (1994) Inhibitory CA1-CA3-hilar region feedback in the hippocampus. Science 265:1722-1724.
50. Sik, A., M. Penttonen, A. Ylinen, and G. Buzsaki (1995) Hippocampal CA1 interneurons: An in vivo intracellular labeling study. J. Neurosci. 15:6651-6665.
51. Simerly, R.B., C. Chang, M. Muramatsu, and L.W. Swanson (1990) Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: An in situ hybridization study. J. Comp. Neurol. 294:76-95.
52. Skipper, J.K., L.J. Young, J.M. Bergeron, M.T. Tetzlaff, C.T. Osborn, and D. Crews (1993) Identification of an isoform of the estrogen receptor messenger RNA lacking exon four and present in the brain. Proc. Natl. Acad. Sci. USA 90:7172-7175.
53. Sloviter, R.S. (1989) Chemically defined hippocampal interneurons and their possible relationship to seizure mechanisms. In V. Chan-Palay and C. Kohler (eds): Neurology and Neurobiology, Vol. 52. New York: Alan R. Liss, Inc. pp. 443-461.
54. Sloviter, R.S., and G. Nilaver (1987) Immunocytochemical localization of GABA-, cholecystokinin-, vasoactive intestinal polypeptide-, and somatostatin-like immunoreactivity in the area dentata and hippocampus of the rat. J. Comp. Neurol. 256:42-60.
55. Swanson, L.W. (1992) Brain Maps: Structure of the Rat Brain. New York: Elsevier.
56. Tang, M.X., D. Jacobs, Y. Stern, K. Marder, P. Schofield, B. Gurland, H. Andrews, and R. Mayeux (1996) Effect of oestrogen during menopause on risk and age of onset of Alzheimer's disease. Endocrinology 115:1412-1417.
57. Terasawa, E., and P.S. Timiras (1968) Electrical activity during the estrous cycle of the rat: Cyclic changes in limbic structures. Endocrinology 83:207-216.
58. Traish, A.B., and H.H. Wotiz (1990) Monoclonal and polyclonal antibodies to human progesterone receptor peptide-(533-547) recognize a specific site in unactivated (8s) and activated (4S) progesterone receptor and distinguish between intact and proteolyzed receptors. Endocrinology 127:1167-1175.
59. Walaas, I. (1983) The hippocampus. In P.C. Emson (ed): Clinical Neuroanatomy. New York: Raven Press, pp. 337-358.
60. Warren, S.G., A.G. Humphreys, J.M. Juraska, and W.T. Greenough (1995) LTP varies across the estrous cycle: Enhanced synaptic plasticity in proestrus rats. Brain Res. 703:26-30.
61. Weiland, N.G. (1992a) Glutamic acid decarboxylase messenger ribonucleic acid is regulated by estradiol and progesterone in the hippocampus. Endocrinology 131:2697-2702.
62. Weiland, N.G. (1992b) Estradiol selectively regulates agonist binding sites on the N-methyl-D-aspartate receptor complex in the CA1 region of the hippocampus. Endocrinology 131:662-668.
63. A receptor are regulated by progesterone in subfields of the hippocampus. Mol. Brain Res. 32:271-278.
64. Woolley, C.S., N.G. Weiland, B.S. McEwen, and P.A. Schwartzkroin (1997) Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to N-methyl-D-aspartate receptor-mediated synaptic input: Correlation with dendritic spine density. J. Neurosci. 17:1848-1859.
65. Woolley, C.S., and B.S. McEwen (1992) Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J. Neurosci. 12:2549-2554.
66. Woolley, C.S., and B.S. McEwen (1994) Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J. Neurosci. 14:7680-7687.
67. Yuan, H., D.A. Bowlby, T.J. Brown, R.B. Hochberg, and N.J. MacLusky (1995) Distribution of occupied and unoccupied estrogen receptors in the rat brain: Effects of physiological gonadal steroid exposure. Endocrinology 136:96-105.
68. Zhou, Y., P.J. Shughrue, and D.M. Dorsa (1995) Estrogen receptor protein is differentially regulated in the preoptic area of the brain and in the uterus during the rat estrous cycle. Neuroendocrinology 61:276-283.