Skip to main content

Advertisement

Log in

Distribution of estrogen receptor β mRNA-containing cells in ovariectomized and estrogen-treated female rat brain

  • Original Article
  • Published:
Anatomical Science International Aims and scope Submit manuscript

Abstract

Estrogen receptor (ER)-β is a member of the nuclear receptor superfamily and mediates various estrogenic actions. Changes in ER-α mRNA expression induced by estrogen have been well documented, whereas those with regard to ER-β have only been reported for a part of the hypothalamus. In the present study, we examined the effect of estrogen on ER-β mRNA expression in the female rat brain. Detection of ER-β mRNA using the in situ hybridization method with a digoxigenin-labeled RNA probe was performed in two groups of female rats: ovariectomized (OVX) and estrogen (E2)-treated. A wide distribution of ER-β mRNA-containing cells was demonstrated in both groups. In the E2-treated group compared with the OVX group, the number of ER-β mRNA-containing cells was significantly reduced in the external plexiform layer of the olfactory bulb, entorhinal cortex, intermediate part of the lateral septal nucleus, nucleus of the horizontal limb of the diagonal band, amygdala (lateral, medial and basolateral part), thalamus (anteroventral, laterodorsal and lateral posterior part), medial geniculate nucleus, suprachiasmatic nucleus and Purkinje cells in the cerebellum. These results reveal that ER-β mRNA-containing cells were decreased by estrogen in several brain regions in the female rat brain, suggesting that ER-β mRNA is downregulated by the physiological level of estrogen in a region-specific manner.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Brown TJ, Scherz B, Hochberg RB, MacLusky NJ (1996) Regulation of estrogen receptor concentrations in the rat brain: Effects of sustained androgen and estrogen exposure. Neuroendocrinology 63, 53–60.

    Article  PubMed  CAS  Google Scholar 

  • Butcher RL, Collins WE, Fugo NW (1974) Plasma concentration of LH, FSH, prolactin, progesterone and estradiol-17β throughout the 4-day estrous cycle of the rat. Endocrinology 94, 1704–8.

    PubMed  CAS  Google Scholar 

  • Cowley SM, Hoare S, Mosselman S, Parker MG (1997) Estrogen receptors α and β form heterodimers on DNA. J Biol Chem 272, 19 858–62.

    Google Scholar 

  • Hrabovszky E, Kalló I, Hajszán T, Shughrue PJ, Merchenthaler I, Liposits Z (1998) Expression of estrogen receptor-b messenger ribonucleic acid in oxytocin and vasopressin neurons of the rat supraoptic and paraventricular nuclei. Endocrinology 139, 2600–4.

    Article  PubMed  CAS  Google Scholar 

  • Hrabovszky E, Steinhauser A, Barab SK et al. (2000) Estrogen receptor-β immunoreactivity in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 142, 3261–4.

    Article  Google Scholar 

  • Jakab RL, Wong JK, Belcher SM (2001) Estrogen receptor beta immunoreactivity in differentiating cells of the developing rat cerebellum. J Comp Neurol 430, 396–409.

    Article  PubMed  CAS  Google Scholar 

  • Koch M (1990) Effects of Treatment with estradiol and parental experience on the number and distribution of estrogen-binding neurons in the ovariectomized mouse brain. Neuroendocrinology 51, 505–14.

    Article  PubMed  CAS  Google Scholar 

  • Koch M, Ehret G (1989) Immunocytochemical localization and quantitation of estrogen-binding cells in the male and female (virgin, pregnant, lactating) mouse brain. Brain Res 489, 101–12.

    Article  PubMed  CAS  Google Scholar 

  • Krege JH, Hodgin JB, Couse JF et al. (1998) Generation and reproductive phenotypes of mice lacking estrogen receptor β. Proc Natl Acad Sci USA 95, 15 677–82.

    Google Scholar 

  • Kuiper GGJM, Carlsson B, Grandien K et al. (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptor α and β. Endocrinology 138, 863–70.

    Article  PubMed  CAS  Google Scholar 

  • Kuiper GGJM, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson J-Å (1996) Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA 93, 5925–30.

    Article  PubMed  CAS  Google Scholar 

  • Lauber AH, Mobbs CV, Muramatsu M, Pfaff DW (1991) Estrogen receptor messenger RNA expression in rat hypothalamus as a function of genetic sex and estrogen dose. Endocrinology 129, 3180–6.

    PubMed  CAS  Google Scholar 

  • Legan SJ, Coon GA, Karsch FJ (1975) Role of estrogen as initiator of daily LH surges in the ovariectomized rat. Endocrinology 96, 50–6.

    Article  PubMed  CAS  Google Scholar 

  • Lubahn DB, Moyer JS, Goldin TS, Couse JF, Korach KS, Smithies O (1993) Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA 90, 11 162–6.

    Google Scholar 

  • Mufson EJ, Cai WJ, Jaffar S et al. (1999) Estrogen receptor immunoreactivity within subregions of the rat forebrain: Neuronal distribution and association with perikarya containing choline acetyltransferase. Brain Res 849, 253–74.

    Article  PubMed  CAS  Google Scholar 

  • Ogawa S, Chan J, Chester AE, Gustafsson J-Å, Korach KS, Pfaff DW (1999) Survival of reproductive behaviors in estrogen receptor β gene-deficient (βERKO) male and female mice. Proc Natl Acad Sci USA 96, 12 887–92.

    Google Scholar 

  • Ogawa S, Inoue S, Watanabe T et al. (1998) The complete primary structure of human estrogen receptor β (hERβ) and its heterodimerization with ERα in vivo and in vitro. Biochem Biophysics Res Commun 243, 122–6.

    Article  CAS  Google Scholar 

  • Ogawa S, Taylor JA, Lubahn DB, Korach KS, Pfaff DW (1996) Reversal of sex roles in genetic female mice by disruption of estrogen receptor gene. Neuroendocrinology 64, 467–70.

    Article  PubMed  CAS  Google Scholar 

  • Orikasa C, Kondo Y, Hayashi S, McEwen BS, Sakuma Y (2002) Sexually dimorphic expression of estrogen receptor β in the anteroventral periventricular nucleus of the rat preoptic area: Implication in luteinizing hormone surge. Proc Natl Acad Sci USA 99, 3306–11.

    Article  PubMed  CAS  Google Scholar 

  • Orikasa C, McEwen BS, Hayashi H, Sakuma Y, Hayashi S (2000) Estrogen receptor alpha, but not beta, is expressed in the interneurons of the hippocampus in prepubertal rats: An in situ hybridization study. Dev Brain Res 120, 245–54.

    Article  CAS  Google Scholar 

  • Österlund M, Kuiper GGJM, Gustafsson J-Å, Hurd YL (1998) Differential distribution and regulation of estrogen receptor-α and -β mRNA within the female rat brain. Mol Brain Res 54, 175–80.

    Article  PubMed  Google Scholar 

  • Pace P, Taylor J, Suntharalingam S, Coombes RC, Ali S (1997) Human estrogen receptor β binds DNA in a manner similar to and dimerizes with estrogen receptor α. J Biol Chem 272, 25 832–8.

    Google Scholar 

  • Pasterkamp RJ, Yuri K, Morita N, Kawata M (1997) Differential expression of estrogen receptor mRNA and protein in the female rat preoptic area. Neurosci Lett 239, 81–4.

    Article  PubMed  CAS  Google Scholar 

  • Patisaul HB, Whitten PL, Young LJ (1999) Regulation of estrogen receptor beta mRNA in the brain: Opposite effects of 17β-estradiol and the phytoestrogen, coumestrol. Mol Brain Res 67, 165–71.

    Article  PubMed  CAS  Google Scholar 

  • Paxinos G, Watson C (1998) The Rat Brain in Stereotaxic Coordinates. Academic Press, New York.

    Google Scholar 

  • Pettersson K, Grandien K, Kuiper GGJM, Gustafsson J-Å (1997) Mouse estrogen receptor β forms estrogen response elementbinding heterodimers with estrogen receptor α. Mol Endocrinol 11, 1486–96.

    Article  PubMed  CAS  Google Scholar 

  • Pettersson K, Gustafsson J-Å (2001) Role of estrogen receptor beta in estrogen action. Annu Rev Physiol 63, 165–92.

    Article  PubMed  CAS  Google Scholar 

  • Price Jr RH, Handa RJ (2000) Expression of estrogen receptorbeta protein and mRNA in the cerebellum of the rat. Neurosci Lett 288, 115–8.

    Article  PubMed  CAS  Google Scholar 

  • Rissman EF, Wersinger SR, Fugger HN, Foster TC (1999) Sex with knockout models: Behavioral studies of estrogen receptor α. Brain Res 835, 80–90.

    Article  PubMed  CAS  Google Scholar 

  • Shughrue PJ, Komm B, Merchenthaler I (1996) The distribution of estrogen receptor-β mRNA in the rat hypothalamus. Steroids 61, 678–81.

    Article  PubMed  CAS  Google Scholar 

  • 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, 507–25.

    Article  PubMed  CAS  Google Scholar 

  • Shughrue PJ, Merchenthaler I (2001) Distribution of estrogen receptor β immunoreactivity in the rat central nervous system. J Comp Neurol 436, 64–81.

    Article  PubMed  CAS  Google Scholar 

  • Shughrue PJ, Scrimo PJ, Merchenthaler I (1998) Evidence for the colocalization of estrogen receptor-β mRNA and estrogen receptor-α immunoreactivity in neurons of the rat forebrain. Endocrinology 139, 5267–70.

    Article  PubMed  CAS  Google Scholar 

  • Shupnik MA, Gordon MS, Chin WW (1989) Tissue-specific regulation of rat estrogen receptor mRNAs. Mol Endocrinol 3, 660–5.

    PubMed  CAS  Google Scholar 

  • Simerly RB, Chang C, Muramatsu M, Swanson LW (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.

    Article  PubMed  CAS  Google Scholar 

  • Simerly RB, Young BJ (1991) Regulation of estrogen receptor messenger ribonucleic acid in rat hypothalamus by sex steroid hormones. Mol Endocrinol 5, 424–32.

    PubMed  CAS  Google Scholar 

  • Simpson ER (1998) Genetic mutations resulting in estrogen insufficiency in the male. Mol Cell Endocrinol 145, 55–9.

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Andersson S, Warner M, Gustafsson J-Å (2001) Morphological abnormalities in the brains of estrogen receptor β knockout mice. Proc Natl Acad Sci USA 98, 2792–6.

    Article  PubMed  CAS  Google Scholar 

  • Yuri K, Kawata M (1991) The effect of estrogen on the estrogen receptor-immunoreactive cells in the rat medial preoptic nucleus. Brain Res 548, 50–4.

    Article  PubMed  CAS  Google Scholar 

  • Zhang J-Q, Cai W-Q, Zhou D-S, Su B-Y (2002) Distribution and differences of estrogen receptor beta immunoreactivity in the brain of adult male and female rats. Brain Res 935, 73–80.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kazunari Yuri.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shima, N., Yamaguchi, Y. & Yuri, K. Distribution of estrogen receptor β mRNA-containing cells in ovariectomized and estrogen-treated female rat brain. Anato Sci Int 78, 85–97 (2003). https://doi.org/10.1046/j.0022-7722.2003.00042.x

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1046/j.0022-7722.2003.00042.x

Key words

Navigation