Parallel changes between the percentage of fetal pituitary cells immunoreactive to oestrogen receptor α and the concentration of 17β-oestradiol in fetal and maternal plasma during gestation in sheep
Sheng Cui A B , Jia li Liu A , Yu jing Shao A and Jian Chao Zhang AA Department of Animal Physiology, College of Biological Sciences, China Agricultural University, Beijing 100094, PR China.
B To whom correspondence should be addressed. email: cuisheng@cau.edu.cn
Reproduction, Fertility and Development 16(6) 611-616 https://doi.org/10.1071/RD02104
Submitted: 24 December 2002 Accepted: 23 April 2004 Published: 9 August 2004
Abstract
The present study was designed to investigate the relationship between fetal sheep pituitary oestrogen receptor (ER) α expression and changes in fetal and maternal plasma 17β-oestradiol (E2) concentrations during gestation. The results revealed that immunoreactivity for ERα was located in the nuclei and distributed throughout the fetal pituitary gland during gestation. The percentage of ERα-positive cells was approximately 2% of the total cell population in female fetuses at Day 60 of gestation, increased to approximately 7% and 13% of the total cell population at Days 90 and 120 of gestation, respectively, and then declined to approximately 10% at birth. The fetal plasma E2 concentrations were approximately 19 and 71 pg mL−1 at Days 90 and 120 of gestation, respectively, and decreased to 22 pg mL−1 after birth. In male fetuses, plasma E2 concentrations and the percentage of ERα-positive cells were similar to values in female fetuses throughout gestation, except on Day 120 when the plasma E2 level in female fetuses was significantly higher than in male fetuses. These data demonstrate that changes in the percentage of fetal pituitary ERα-positive cells parallel fetal plasma E2 concentrations throughout gestation.
Acknowledgments
This work was supported by grants from the Natural Science Foundation of China (30325034, 30170693) and the Science and Technology Key Program (01018) of the China Educational Ministry.
Alexander, D. P. , Britton, H. G. , Corker, C. S. , Naftolin, F. , and Nixon, D. A. (1973). Plasma luteinizing hormone and oestrogen in the foetal and maternal sheep. J. Endocrinol. 56, 331–332.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Brooks, A. N. , Hagan, D. M. , Sheng, C. , McNeilly, A. S. , and Sweeney, T. (1996). Prenatal gonadotrophins in the sheep. Anim. Reprod. Sci. 42, 471–481.
| Crossref | GoogleScholarGoogle Scholar |
![](../../media/share/OpenURL_Image.gif)
Cardenas, H. , Burke, K. A. , Bigsby, R. M. , Pope, W. F. , and Nephew, K. P. (2001). Estrogen receptor beta in the sheep ovary during the estrous cycle and early pregnancy. Biol. Reprod. 65, 128–134.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Couse, J. F. , and Korach, K. S. (1999). Estrogen receptor null mice: what have we learned and where will they lead us? Endocr. Rev. 20, 358–417.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Demay, F. , Tiffoche, C. , and Thieulant, M. L. (1996). Effect of gonadotropin-releasing hormone on estrogen receptor messenger ribonucleic acid level in perifused pituitary cells. Cell. Mol. Neurobiol. 16, 397–402.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Demay, F. , De Monti, M. , Tiffoche, C. , Vaillant, C. , and Thieulant, M. L. (2001). Steroid-independent activation of ER by GnRH in gonadotrope pituitary cells. Endocrinology 142, 3340–3347.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Findlay, J. K. , and Cox, R. I. (1970). Oestrogens in the plasma of the sheep fetus. J. Endocrinol. 46, 281–282.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Gluckman, P. D. , Marti-Henneberg, C. , Kaplan, S. L. , and Grumbach, M. M. (1983). Hormone ontogeny in the ovine fetus. XIV: the effect of 17 beta-estradiol infusion on fetal plasma gonadotrophins and prolactin and the maturation of sex steroid-dependent negative feedback. Endocrinology 112, 1618–1623.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Hileman, S. M. , Handa, R. J. , and Jackson, G. L. (1999). Distribution of estrogen receptor beta messenger ribonucleic acid in the male sheep hypothalamus. Biol. Reprod. 60, 1279–1284.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Hiroi, H. , Inoue, S. , Watanabe, T. , Goto, W. , Orimo, A. , Momoeda, M. , Tsutsumi, O. , Taketani, Y. , and Muramatsu, M. (1999). Differential immunolocalization of estrogen receptor alpha and beta in rat ovary and uterus. J. Mol. Endocrinol. 22, 37–44.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Jansen, H. T. , West, C. , Lehman, M. N. , and Padmanabhan, V. (2001). Ovarian estrogen receptor-beta (ER beta) regulation: I. Changes in ER beta messenger RNA expression prior to ovulation in the ewe. Biol. Reprod. 65, 866–872.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Kuiper, G. G. J. M. , Enmark, E. , Pelto-Huikko, M. , Nilsson, S. , and Gustafsson, J. A. (1996). Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc. Natl Acad. Sci. USA 93, 5925–5930.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Kuiper, G. G. J. M. , Carlsson, B. , Grandien, K. , Enmark, E. , Haggblad, J. , Nilsson, S. , and Gustafsson, J. A. (1997). Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138, 863–870.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
MacLusky, N. J. , Lieberburg, I. , and McEwen, B. S. (1979). The development of estrogen receptor systems in the rat brain: perinatal development. Brain Res. 178, 129–142.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Madigou, T. , Tiffoche, C. , Lazennec, G. , Pelletier, J. , and Thieulant, M. L. (1996). The sheep estrogen receptor: cloning and regulation of expression in the hypothalamo–pituitary axis. Mol. Cell. Endocrinol. 121, 153–163.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
McNatty, K. P. , Smith, P. , Hudson, N. L. , Heath, D. A. , Tisdall, D. J. , and Braw-Tal, R. (1995). Development of the sheep ovary during fetal and early neonatal life and the effect of fecundity genes. J. Reprod. Fertil. Suppl. 49, 123–135.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Messaoud-Toumi, L. H. , Taragnat, C. , and Durand, P. (1993). Castration effects on the gonadotrope cell populations of the fetal sheep pituitary in late gestation. Neuroendocrinology 58, 548–554.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Molter-Gerard, C. , Caraty, A. , Guerin, S. , Fontaine, J. , and Taragnat, C. (2000). Dynamic changes in the gonadotrope cell populations during an estradiol-induced surge in the ewe. Biol. Reprod. 63, 1084–1091.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Mosselman, S. , Polman, J. , and Dijkema, R. (1996). ER-beta: identification and characterization of a novel human estrogen receptor. FEBS Lett. 392, 49–53.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Murdoch, F. E. , and Gorski, J. (1991). The role of ligand in estrogen receptor regulation of gene expression. Mol. Cell. Endocrinol. 78, 103–108.
| Crossref | GoogleScholarGoogle Scholar |
![](../../media/share/OpenURL_Image.gif)
Nathanielsz, P. W. , Elsner, C. , Magyar, D. , Fridshal, D. , Freeman, A. , and Buster, J. E. (1982). Time trend analysis of plasma unconjugated and sulfoconjugated estrone and 3 beta-delta 5-steroids in fetal and maternal sheep plasma in relation to spontaneous parturition at term. Endocrinology 110, 1402–1407.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Nishihara, E. , Nagayama, Y. , Inoue, S. , Hiroi, H. , Muramatsu, M. , Yamashita, S. , and Koji, T. (2000). Ontogenetic changes in the expression of estrogen receptor alpha and beta in rat pituitary gland detected by immunohistochemistry. Endocrinology 141, 615–620.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Pasqualini, C. , Guivarch, D. , Boxberg, Y. V. , Nothias, F. , Vincent, J. D. , and Vernier, P. (1999). Stage- and region-specific expression of estrogen receptor alpha isoforms during ontogeny of the pituitary gland. Endocrinology 140, 2781–2789.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Pasterkamp, R. J. , Yuri, K. , Visser, D. T. , Hayashi, S. , and Kawata, M. (1996). The perinatal ontogeny of estrogen receptor-immunoreactivity in the developing male and female rat hypothalamus. Dev. Brain Res. 91, 300–303.
| Crossref | GoogleScholarGoogle Scholar |
![](../../media/share/OpenURL_Image.gif)
Saunders, P. T. K. (1998). Oestrogen receptor beta (ER-beta). Rev. Reprod. 3, 164–171.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Schomberg, D. W. , Couse, J. F. , Mukherjee, A. , Lubahn, D. B. , Sar, M. , Mayo, K. E. , and Korach, K. S. (1999). Targeted disruption of the estrogen receptor-alpha gene in female mice: characterization of ovarian responses and phenotype in the adult. Endocrinology 140, 2733–2744.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Schreihofer, D. A. , Stoler, M. H. , and Shupnik, M. A. (2000). Differential expression and regulation of estrogen receptors (ERs) in rat pituitary and cell lines: estrogen decreases ER alpha protein and estrogen responsiveness. Endocrinology 141, 2174–2184.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Scott, C. J. , Tilbrook, A. J. , Simmons, D. M. , Rawson, J. A. , Chu, S. , Fuller, P. J. , Ing, N. H. , and Clarke, I. J. (2000). The distribution of cells containing estrogen receptor-alpha (ER alpha) and ER beta messenger ribonucleic acid in the preoptic area and hypothalamus of the sheep: comparison of males and females. Endocrinology 141, 2951–2962.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Scully, K. M. , Gleiberman, A. S. , Lindzey, J. , Lubahn, D. B. , Korach, K. S. , and Rosenfeld, M. G. (1997). Role of estrogen receptor-alpha in the anterior pituitary gland. Mol. Endocrinol. 11, 674–681.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Sheng, C. , Millar, M. , Brooks, J. , and McNeilly, A. S. (1995). Change in pituitary oestrogen receptor during the oestrous cycle in the ewe. J. Endocrinol. Suppl. 144, 342.
![](../../media/share/OpenURL_Image.gif)
Sheng, C. , McNeilly, A. S. , and Brooks, A. N. (1998). Immunohistochemical distribution of oestrogen receptor and luteinizing hormone B subunit in the bovine pituitary gland during foetal development. J. Neuroendocrinol. 10, 713–718.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Sheng, H. Z. , Moriyama, K. , Yamashita, T. , Li, H. , Potter, S. S. , Mahon, K. A. , and Westphal, H. (1997). Multistep control of pituitary organogenesis. Science 278, 1809–1812.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Singh, P. , and Muldoon, T. G. (1982). A direct effect on LHRH on anterior pituitary estrogen receptors in the female rat. J. Steroid Biochem. 16, 31–37.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Singh, P. , and Muldoon, T. G. (1986). Baseline and luteinizing hormone-releasing hormone-perturbed patterns of estrogen receptor distribution in anterior pituitary cell nuclei. Endocrinology 118, 2355–2361.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Sklar, C. A. , Mueller, P. L. , Gluckman, P. D. , Kaplan, S. L. , Rudolph, A. M. , and Grumbach, M. M. (1981). Hormone ontogeny in the ovine fetus. VII. Circulating luteinizing hormone and follicle-stimulating hormone in mid- and late gestation. Endocrinology 108, 874–880.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Sprangers, S. A. , Fahrenbach, W. H. , and Bethea, C. L. (1991). Steroid action on estrogen and progestin receptors in monkey pituitary cell cultures. Endocrinology 128, 1907–1917.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Thomas, G. B. , McNeilly, A. S. , and Brooks, A. N. (1993). Development of gonadotrophs and thyrotrophs in the female foetal sheep pituitary: immunocytochemical localization studies. J. Neuroendocrinol. 5, 157–161.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Tobin, V. A. , Pompolo, S. , and Clarke, I. J. (2001). The percentage of pituitary gonadotropes with immunoreactive oestradiol receptors increases in the follicular phase of the ovine oestrous cycle. J. Neuroendocrinol. 13, 846–854.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Vaillant, C. , Chesnel, F. , Schausi, D. , Tiffoche, C. , and Thieulant, M. L. (2002). Expression of estrogen receptor subtypes in rat pituitary gland during pregnancy and lactation. Endocrinology 143, 4249–4258.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Vito, C. C. , and Fox, T. O. (1981). Androgen and estrogen receptors in embryonic and neonatal rat brain. Brain Res. 254, 97–110.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Wilson, M. E. , Price, R. H. , and Handa, R. J. (1998). Estrogen receptor-beta messenger ribonucleic acid expression in the pituitary gland. Endocrinology 139, 5151–5156.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Wood, C. E. , and Saoud, C. J. (1997). Influence of estradiol and androstenedione on ACTH and cortisol secretion in the ovine fetus. J. Soc. Gynecol. Invest. 4, 279–283.
| Crossref | GoogleScholarGoogle Scholar |
![](../../media/share/OpenURL_Image.gif)
Woods, J. E. , Otten, L. M. , and Thommes, R. C. (1995). Ontogeny of 17β-estradiol (E2)- and estrogen receptor (ER)-immunostained cells in the hypothalamus and adenohyophyseal pars distalis of the chicken embryo. Growth Dev. Aging 59, 93–105.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Wu, W. X. , Owiny, J. , Zhang, Q. , Ma, X. H. , and Nathanielz, P. W. (1996). Regulation of the estrogen receptor and its messenger ribonucleic acid in the ovariectomized sheep myometrium and endometrium: the role of estradiol and progesterone. Biol. Reprod. 55, 762–768.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Wynick, D. , Hammond, P. J. , Akinsanya, K. O. , and Bloom, S. R. (1993). Galanin regulates basal and oestrogen-stimulated lactotroph function. Nature 364, 529–532.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Yu, H. K. , Cabalum, T. , Jansen, C. A. , Buster, J. E. , and Nathanielsz, P. W. (1983). Androstenedione, testosterone, and estradiol concentrations in fetal and maternal plasma in late pregnancy in the sheep. Endocrinology 113, 2216–2220.
| PubMed |
![](../../media/share/OpenURL_Image.gif)