Skip to main content
Log in

Immunohistochemical localization of estrogen receptors ERα and ERβ in the spiny mouse (Acomys cahirinus) ovary during postnatal development

  • Original paper
  • Published:
Journal of Molecular Histology Aims and scope Submit manuscript

Abstract

This study was designed to determine the expression pattern of estrogen receptor (ER) subtypes in the Acomys cahirinus ovarian cells during its postnatal development.

Immunohistochemical studies revealed the presence of ERα and ERβ in germinal epithelium cells and interstitial tissue. Both these ER subtypes were also seen in granulosa cells and oocytes of growing follicles, however, the level of ERβ expression was higher in comparison with ERα. In contrast to ERβ, ERα protein was also present in theca cells.

The expression of ERs increased with animals’ age, but it decreased during follicular maturation. Moreover, the immunolocalization of ER subtypes in luteal cells showed that not ERβ, but ERα expression is up-regulated throughout corpus luteum development.

These immunohistochemical studies demonstrate, for the first time, that ERα is also expressed in the mouse granulosa cells and it may be a mediator of estrogen action in granulosa cells proliferation and differentiation.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ainsworth L, Tsang BK, Downey BR, Marcus GJ (1990) The synthesis and actions of steroids and prostaglandins during follicular maturation in the pig. J Reprod Fert Suppl 40:137–150

    CAS  Google Scholar 

  • Bai W, Oliveros-Saunders B, Wang Q, Acevedo-Duncan ME, Nicosia SV (2000) Estrogen stimulation of ovarian surface epithelial cell proliferation. In Vitro Cell Dev Biol Anim 36:657–666

    Article  PubMed  CAS  Google Scholar 

  • Bill CH, Keyes PL (1983) 17 beta-estradiol maintains normal function of corpora lutea throughout pseudopregnancy in hypophysectomized rabbits. Biol Reprod 28:608–617

    Article  PubMed  CAS  Google Scholar 

  • Boa B, Kumar N, Karp RM, Garwerick HA, Sundaram K (2000) Estrogen receptor-ß expression in relation to the expression of luteinizing hormone receptor and cytochrome P450 enzymes in rat ovarian follicles. Biol Reprod 63:1747–1755

    Article  Google Scholar 

  • Britt KL, Saunders PK, McPherson SJ, Misso ML, Simpson ER, Findlay JK (2004) Estrogen actions on follicle formation and early follicle development. Biol Reprod 71:1712–1723

    Article  PubMed  CAS  Google Scholar 

  • Byers M, Kuiper GGJM, Gustafsson JA, Park-Sarge OK (1997) Estrogen receptor-ß mRNA expression in rat ovary: down-regulation by gonadotropins. Mol Endocrinol 11:172–182

    Article  PubMed  CAS  Google Scholar 

  • Channing CP, Tsafriri A (1977) Mechanism of action of luteinizing hormone and follicle-stimulating hormone on the ovary in vitro. Metabolism 26:413–468

    Article  PubMed  CAS  Google Scholar 

  • Chiang C, Cheng KW, Igarashi S, Nathwani PS, Leong PCK (2000) Hormonal regulation of estrogen receptor α and ß gene expression in human granulosa-luteal cells in vitro. J Clin Endocrinol Metab 85:3828–3839

    Article  PubMed  CAS  Google Scholar 

  • Conneely OM, Mulac-Jericevic B, DeMayo F, Lydon JP, O’Malley BW (2002) Reproductive functions of progesterone receptors. Recent Prog Horm Res 57:339–355

    Article  PubMed  CAS  Google Scholar 

  • Cowley SM, Hoare S, Mosselman S, Parker MG (1997) Estrogen receptors α and ß form heterodimers on DNA. J Biol Chem 271:19858–19862

    Article  Google Scholar 

  • Dierschke DJ, Braw RH, Tsafriri A (1983) Estradiol 17-β reduces number of ovulations in adult rats: Direct actions on the ovary? Biol Reprod 29:1147–1154

    Article  PubMed  CAS  Google Scholar 

  • Drummond AE, Baillie AJ, Findlay JK (1999a) Ovarian estrogen receptor α and ß mRNA expression: impact of development and estrogen. Mol Cell Endocrinol 149:153–161

    Article  CAS  Google Scholar 

  • Drummond AE, Findlay JK (1999b) The role of estrogen in folliculogenesis. Mol Cell Endocrinol 151:57–64

    Article  CAS  Google Scholar 

  • Economou E, Papamitsou T, Papaioannidou PG, Manthos A, Alvanou A, Miliaras D (2002) Estrogen receptors alpha are present in human ovarian cells. Reprod Biol 78:163–164

    Google Scholar 

  • Findlay JK, Drummond AE, Britt KL, Dyson M, Wreford NG, Robertson DM, Groome NP, Jones MEE, Simpson ER (2000) The roles of activins, inhibins and estrogen in early committed follicles. Mol Cell Endocrinol 163:81–87

    Article  PubMed  CAS  Google Scholar 

  • Fitzpatric SL, Funkhouser JM, Sindoni DM, Stevis PE, Deecher DC, Bapat AR, Merchenthaler I, Frail DE (1999) Expression of estrogen receptor-ß protein in rodent ovary. Endocrinol 140:2581–2591

    Article  Google Scholar 

  • Glass JD, Fitz TA, Niswender GD (1984) Cytosolic receptor for estradiol in the corpus luteum of the ewe: variation throughout the estrous cycle and distribution between large and small steroidogenic cell types. Biol Reprod 31:967–974

    Article  PubMed  CAS  Google Scholar 

  • Greenwald GS (1986) Hormonal changes associated with estrogen induced luteolysis in the pregnant hamster: a reevaluation of the luteotropic complex. Proc Soc Exp Biol Med 181:284–288

    PubMed  CAS  Google Scholar 

  • Guo C, Savage L, Sarze KD, Park-Sarge OK (2001) Gonadotropins decrease estrogen receptor-ß messenger ribonucleic acid stability in rat granulosa cells. Endocrinol 142:2230–2237

    Article  CAS  Google Scholar 

  • Hall JM, McDonnell DP (1999) The estrogen receptor beta-isoform (ERbeta) of the human estrogen receptor modulates ERalpha transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinol 140:5566–5578

    Article  CAS  Google Scholar 

  • Haney AF, Schomberg DW (1978) Steroidal modulation of progesterone secretion by granulosa cells from large porcine follicles: a role for androgens and estrogens in controlling steroidogenesis. Biol Reprod 19:242–248

    Article  PubMed  CAS  Google Scholar 

  • Hiroi H, Inoue S, Watanable T, Goto W, Orimo A, Momoeda M, Tsutsumi O, Taketani Y, Muramatsu M (1999) Differential immunolocalization of estrogen receptor α and ß in rat ovary and uterus. J Mol Endocrinol 22:37–44

    Article  PubMed  CAS  Google Scholar 

  • Hirshfield AN, DeSanti AM (1995) Patterns of ovarian cell proliferation in rats during the embryonic period and the first 3 weeks postpartum. Biol Reprod 53:1208–1221

    Article  PubMed  CAS  Google Scholar 

  • Hishikawa Y, Damavandi E, Izumi S, Kojo T (2003) Molecular histochemical analysis of estrogen receptor α and ß expressions in the mouse ovary: in situ hybridization and Southwestern histochemistry. Med Electron Microsc 36:67–73

    PubMed  CAS  Google Scholar 

  • Hułas M, Gawron A, Orfin G (2003) A comparative study of ovary development in the precocial spiny mouse (Acomys cahirinus) and the altricial Norway rat (Rattus Norvegicus). Isr J Zool 49:307–313

    Article  Google Scholar 

  • Hutz RJ, Dierschke DJ, Wolf RC (1990) Role of estradiol in regulating ovarian follicular atresia in rhesus monkeys: a review. J Med Primatol 19:553–571

    PubMed  CAS  Google Scholar 

  • Iwai M, Yasuda K, Fukuoka K, Iwai T, Takakura K, Taii S, Nakanishi S, Mori T (1991) Luteinizing hormone induces progesterone receptor gene expression in cultured porcine granulosa cells. Endocrinol 129:1621–1627

    Article  CAS  Google Scholar 

  • Jefferson WN, Couse JF, Banks EP, Korach KS, Newblod RR (2000) Expression of estrogen receptor ß is developmentally regulated in reproductive tissues of male and female mice. Biol Reprod 62:310–317

    Article  PubMed  CAS  Google Scholar 

  • Kraeling RR, Barb CR, Davis BJ (1975) Prostaglandin-induced regression of porcine corpora lutea maintained by estrogen. Prostaglandins 9:459–462

    Article  PubMed  CAS  Google Scholar 

  • Lindberg MK, Moverare S, Skrtic S, Gao H, Dahlman-Wright K, Gustaffson JA, Ohlsson C (2003) Estrogen receptor (ER-ß) reduces ER-α regulated gene transcription, supporting “Ying Yang” relationship between ER α and ER ß in mice. Mol Endocrinol 17:203–208

    Article  PubMed  CAS  Google Scholar 

  • Lischinsky A, Armstrong DT (1983) Granulosa cell stimulation of thecal androgen synthesis. Pharmacol 61:472–477

    CAS  Google Scholar 

  • Merk FB, Botticelli CHR, Albright JT (1972) An intercellular response to estrogen by granulosa cells in the rat ovary; an electron microscope study. Endocrinol 90:992–1007

    CAS  Google Scholar 

  • Merkel C, Nelson WO (1940) The relation of the estrogenic hormone to the information and maintenance of corpora lutea in mature and immature rats. Anat Rec 76:391–407

    Article  Google Scholar 

  • Miller JB, Toft DO (1983) Characterization and physiological variation of estrogen receptors in rabbit corpora lutea throughout pregnancy and pseudopregnancy: the effect of hysterectomy and sustained estradiol treatment. Biol Reprod 29:620–629

    Article  PubMed  CAS  Google Scholar 

  • Misao R, Nakanishi Y, Sun WS, Fujimoto J, Iwagaki S, Hirose R, Tamara T (1999) Expression of oestrogen receptor alpha and beta mRNA in corpus luteum of human subjects. Mol Hum Reprod 5:17–21

    Article  PubMed  CAS  Google Scholar 

  • Palter SF, Tavares AB, Hourvitz A, Veldhuis JD, Adashi EY (2001) Are estrogens of important to primate/human ovarian folliculogenesis. Endocrin Rev 22:389–424

    Article  CAS  Google Scholar 

  • Park-Sarge OK, Mayo KE (1994) Regulation of the progesterone receptor gene by gonadotropins and cyclic adenosine 3, 5-monophosphate in rat granulosa cells. Endocrinol 134:709–718

    Article  CAS  Google Scholar 

  • Peters H (1969) The development of the mouse ovary from birth to maturity. Acta Endocrinol 62:98–116

    PubMed  CAS  Google Scholar 

  • Pettersson K, Grandien K, Kuiper GGJ, Gustafsson JA (1997) Mouse estrogen receptor ß forms estrogen response element-binding heterodimers with estrogen receptor α. Mol Endocrinol 11:1486–1496

    Article  PubMed  CAS  Google Scholar 

  • Roberts AJ, Skinner MK (1990) Mesenchymal-epithelial cell interactions in the ovary: estrogen-induced theca cell steroidogenesis. Mol Cell Endocrinol 72:R1–R5

    Article  PubMed  CAS  Google Scholar 

  • Roy SK, Albee L (2000) Requirement for follicle-stimulating hormone action in the formation of primordial follicles during perinatal ovarian development in the hamster. Endocrinol 141:4449–4456

    Article  CAS  Google Scholar 

  • Sar M, Welsch F (1999) Differential expression of estrogen receptor-ß and estrogen receptor-α in the rat ovary. Endocrinol 140:963–971

    Article  CAS  Google Scholar 

  • Saunders PTK, Millar MR, Williams K, Macpherson S, Harkiss D, Anderson RA, Orr B, Groome NP, Scobie G, Fraser HM (2000) Differential expression of estrogen receptor α and β and androgen receptor in the ovaries of marmosets and humans. Biol Reprod 63:1098–1105

    Article  PubMed  CAS  Google Scholar 

  • Słomczyńska M, Duda M, Galas J (2001) Estrogen receptor alpha and beta expression in the porcine ovary. Histochem Cytobiol 39:137–138

    Google Scholar 

  • Tetsuka M, Milne M, Hillier SG (1998) Expression of estrogen receptor isoforms in relation to enzymes of estrogen synthesis in rat ovary. Mol Cell Endocrinol 141:29–35

    Article  PubMed  CAS  Google Scholar 

  • Tomanek M, Pisselet C, Monet P, Madigou T, Thieulant ML, Monniaux D (1997) Estrogen receptor protein and mRNA expression in the ovary of sheep. Mol Reprod Dev 48:53–62

    Article  PubMed  CAS  Google Scholar 

  • Vegeto E, Shahbaz MM, Wen DX, Goldman ME, O’Malley BW, McDonell DP (1993) Human progesterone receptor A forms is a cell- and promoter-specific repressor of human progesterone receptor B function. Endocrinol 7:1241–1243

    Google Scholar 

  • Wang H, Eriksson H, Sahlin L (2000) Estrogen receptors α and β in the female reproductive tract of the rat during the estrous cycle. Biol Reprod 63:1331–1340

    Article  PubMed  CAS  Google Scholar 

  • Wu TC, Wang L, Wan YJ (1992) Expression of estrogen receptor gene in mouse oocyte and during embryogenesis. Mol Reprod Dev 33:407–412

    Article  PubMed  CAS  Google Scholar 

  • Wu TC, Wang L, Wan YJ (1993) Detection of estrogen receptor messenger ribonucleic acid in human oocytes and cumulus-oocyte complexes using reverse transcriptase-polymerase chain reaction. Fertil Steril 59:54–59

    PubMed  CAS  Google Scholar 

  • Yang P, Kriatchko A, Roy SK (2002) Expression of ER-α and ER-ß in the hamster ovary:differential regulation by gonadotropins and ovarian steroid hormones. Endocrinol 143:2385–2398

    Article  CAS  Google Scholar 

  • Yang P, Wang J, Shen Y, Roy SK (2004) Developmental expression of estrogen receptor (ER) α and ERβ in the hamster ovary: regulation by follicle-stimulating hormone. Endocrinol 145:5757–5766

    Article  CAS  Google Scholar 

  • Zachos NC, Billiar RB, Albrecht ED, Pepe GJ (2004) Regulation of oocyte microvilli development in the baboon fetal ovary by estrogen. Endocrinol 145:959–966

    Article  CAS  Google Scholar 

  • Zięba D, Bilińska B, Schmalz-Frączek B, Murawski M (2000) Immunohistochemical localization of estrogen receptors in the ovine corpus luteum throughout the estrus cycle. Folia Histochem Cytobiol 38:111–117

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Monika Hułas-Stasiak.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hułas-Stasiak, M., Gawron, A. Immunohistochemical localization of estrogen receptors ERα and ERβ in the spiny mouse (Acomys cahirinus) ovary during postnatal development. J Mol Hist 38, 25–32 (2007). https://doi.org/10.1007/s10735-006-9072-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10735-006-9072-3

Keywords

Navigation