Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-17T14:23:58.795Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of oestrogen on mouse follicle growth and meiotic resumption

Published online by Cambridge University Press:  27 October 2021

Heng Chi  and
Zuowu Cao Open the ORCID record for Zuowu Cao [Opens in a new window]
Heng Chi
Affiliation:
Department of Developmental and Regenerative Biology, Jinan University College of Life Science and Technology, Guangzhou, China
Zuowu Cao*
Affiliation:
Department of Developmental and Regenerative Biology, Jinan University College of Life Science and Technology, Guangzhou, China
*
Author for correspondence: Zuowu Cao. Department of Developmental and Regenerative Biology, Jinan University College of Life Science and Technology, Guangzhou, 510632, China. E-mail: zuowu.cao@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

Many studies have shown that oestrogen affects late follicular development, but whether oestrogen is involved in other aspects of folliculogenesis remains unclear. In this study, two antagonists of oestrogen, tamoxifen and G15, were used to determine the effects of oestrogen on folliculogenesis. Mouse preantral follicles and cumulus–oocyte complexes (COCs) were cultured in vitro. The results showed that follicle growth stimulated using pregnant mare serum gonadotrophin (PMSG) was inhibited using tamoxifen, whether in vivo or in vitro. The average diameters, the maximum diameters of follicles and the numbers of follicles with a diameter of more than 300 μm decreased significantly following a 4-day culture with tamoxifen. G15, the antagonist of oestrogen via the membrane receptor, did not change follicular growth stimulated by PMSG in vitro. Results of in vitro maturation of COCs showed that germinal vesicle breakdown (GVBD) occurred spontaneously (95.1%) after 2 h in culture, and the GVBD ratio changed little with the addition of either oestrogen or 10 μM G15. However, first polar body (PBI) extrusion was driven by oestrogen markedly and supplementation with 10 μM G15 inhibited PBI extrusion (82.4% vs 55.0%) significantly. These results demonstrated that oestrogen promotes follicle growth through the nuclear receptor during follicle growth and then triggers the transition of metaphase to anaphase through the membrane receptor during meiotic resumption. So oestrogen plays a progressive role in the two phases of follicle growth and oocyte meiotic resumption.

Keywords

FolliculogenesisMeiotic resumptionOestrogenOocytePolar body
Type
Research Article
Information
Zygote , Volume 30 , Issue 3 , June 2022 , pp. 330 - 337
Copyright
© The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Antal, MC, Krust, A, Chambon, P and Mark, M (2008). Sterility and absence of histopathological defects in nonreproductive organs of a mouse ER beta-null mutant. Proc Natl Acad Sci USA 105, 2433–8.CrossRefGoogle Scholar
Bayne, S, Li, H, Jones, ME, Pinto, AR, van Sinderen, M, Drummond, A, Simpson, ER and Liu, JP (2011). Estrogen deficiency reversibly induces telomere shortening in mouse granulosa cells and ovarian aging in vivo . Protein Cell 2, 333–46.CrossRefGoogle ScholarPubMed
Billig, H, Furuta, I and Hsueh, AJ (1993). Estrogens inhibit and androgens enhance ovarian granulosa cell apoptosis. Endocrinology 133, 2204–12.CrossRefGoogle ScholarPubMed
Britt, KL and Findlay, JK (2003). Regulation of the phenotype of ovarian somatic cells by estrogen. Mol Cell Endocrinol 202(1–2), 11–7.CrossRefGoogle ScholarPubMed
Britt, KL, Drummond, AE, Cox, VA, Dyson, M, Wreford, NG, Jones, MEE, Simpson, ER and Findlay, JK (2000). An age-related ovarian phenotype in mice with targeted disruption of the Cyp 19 (aromatase) gene. Endocrinology 141, 2614–23.CrossRefGoogle ScholarPubMed
Britt, KL, Saunders, PK, McPherson, SJ, Misso, ML, Simpson, ER and Findlay, JK (2004). Estrogen actions on follicle formation and early follicle development. Biol Reprod 71, 1712–23.CrossRefGoogle ScholarPubMed
Dennis, MK, Burai, R, Ramesh, C, Petrie, WK, Alcon, SN, Nayak, TK, Bologa, CG, Leitao, A, Brailoiu, E, Deliu, E, Dun, NJ, Sklar, LA, Hathaway, HJ, Arterburn, JB, Oprea, TI and Prossnitz, ER (2009). In vivo effects of a GPR30 antagonist. Nat Chem Biol 5, 421–7.CrossRefGoogle ScholarPubMed
Dupont, S, Krust, A, Gansmuller, A, Dierich, A, Chambon, P and Mark, M (2000). Effect of single and compound knockouts of estrogen receptors alpha (ER alpha) and beta (ER beta) on mouse reproductive phenotypes. Development 127, 4277–91.CrossRefGoogle Scholar
Gore-Langton, RE and Dorrington, JH (1981). FSH induction of aromatase in cultured rat granulosa cells measured by a radiometric assay. Mol Cell Endocrinol 22, 135–51.CrossRefGoogle ScholarPubMed
Greene, GL, Gilna, P, Waterfield, M, Baker, A, Hort, Y and Shine, J (1986). Sequence and expression of human estrogen receptor complementary DNA. Science 231(4742), 1150–4.CrossRefGoogle ScholarPubMed
Khalid, M, Haresign, W and Luck, MR (2000). Secretion of IGF-1 by ovine granulosa cells: effects of growth hormone and follicle stimulating hormone. Anim Reprod Sci 58(3–4), 261–72.CrossRefGoogle ScholarPubMed
Krege, JH, Hodgin, JB, Couse, JF, Enmark, E, Warner, M, Mahler, JF, Sar, M, Korach, KS, Gustafsson, JA and Smithies, O (1998). Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci USA 95, 15677–82.CrossRefGoogle ScholarPubMed
Kuiper, GG, Enmark, E, Pelto-Huikko, M, Nilsson, S and Gustafsson, JA (1996). Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA 93, 5925–30.CrossRefGoogle ScholarPubMed
Lee, KB, Zhang, M, Sugiura, K, Wigglesworth, K, Uliasz, T, Jaffe, LA and Eppig, JJ (2013). Hormonal coordination of natriuretic peptide type C and natriuretic peptide receptor 3 expression in mouse granulosa cells. Biol Reprod 88, 42.CrossRefGoogle Scholar
Li, YR, Ren, CE, Zhang, Q, Li, JC and Chian, RC (2013). Expression of G protein estrogen receptor (GPER) on membrane of mouse oocytes during maturation. J Assist Reprod Genet 30, 227–32.CrossRefGoogle ScholarPubMed
Liu, J, Yao, R, Lu, SH, Xu, R, Zhang, H, Wei, J, Zhao, C, Tang, Y, Li, C, Liu, H, Zhao, X, Wei, Q and Ma, BH (2020). Synergistic effect between LH and estrogen in the acceleration of cumulus expansion via GPR30 and EGFR pathways. Aging 12, 20801–16.CrossRefGoogle ScholarPubMed
Liu, W, Xin, Q, Wang, X, Wang, S, Wang, H, Zhang, W, Yang, Y, Zhang, Y, Zhang, Z, Wang, C, Xu, Y, Duan, E and Xia, G (2017). Estrogen receptors in granulosa cells govern meiotic resumption of pre-ovulatory oocytes in mammals. Cell Death Dis 8, e2662.CrossRefGoogle ScholarPubMed
Lubahn, DB, Moyer, JS, Golding, TS, Couse, JF, Korach, KS and 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, 11162–6.CrossRefGoogle Scholar
Maneix, L, Antonson, P, Humire, P, Rochel-Maia, S, Castañeda, J, Omoto, Y, Kim, HJ, Warner, M and Gustafsson, JÅ (2015). Estrogen receptor β exon 3-deleted mouse: the importance of non-ERE pathways in ERβ signaling. Proc Natl Acad Sci USA 112, 5135–40.CrossRefGoogle ScholarPubMed
McGee, E, Spears, N, Minami, S, Hsu, SY, Chun, SY, Billig, H and Hsueh, AJW (1997). Preantral ovarian follicles in serum-free culture: suppression of apoptosis after activation of the cyclic guanosine 3¢,5¢-monophosphate pathway and stimulation of growth and differentiation by follicle-stimulating hormone. Endocrinology 138, 2417–24.CrossRefGoogle Scholar
Press, MF, Nousek-Goebl, NA, Bur, M and Greene, GL (1986). Estrogen receptor localization in the female genital tract. Am J Pathol 123, 280–92.Google ScholarPubMed
Quirk, SM, Cowan, RG and Harman, RM (2006). The susceptibility of granulosa cells to apoptosis is influenced by oestradiol and the cell cycle. J Endocrinol 189, 441–53.CrossRefGoogle ScholarPubMed
Roy, SK and Greenwald, GS (1989). Hormonal requirements for the growth and differentiation of hamster preantral follicles in long-term culture. J Reprod Fertil 87, 103–14.CrossRefGoogle ScholarPubMed
Schomberg, DW, Couse, JF, Mukherjee, A, Lubahn, DB, Sar, M, Mayo, KE and Korach, KS (1999). Targeted disruption of the estrogen receptor-alpha gene in female mice: characterization of ovarian responses and phenotype in the adult. Endocrinology 140, 2733–44.CrossRefGoogle ScholarPubMed
Wang, C, Prossnitz, ER and Roy, SK (2007). Expression of G protein-coupled receptor 30 in the hamster ovary: differential regulation by gonadotropins and steroid hormones. Endocrinology 148, 4853–64.CrossRefGoogle ScholarPubMed
Wang, XN, Roy, SK and Greenwald, GS (1991). In vitro DNA synthesis by isolated preantral to preovulatory follicles from the cyclic mouse. Biol Reprod 44, 857–63.CrossRefGoogle ScholarPubMed
Zhang, H, Wei, Q, Gao, Z, Ma, C, Yang, Z, Zhao, H, Liu, C, Liu, J, Zhao, X and Ma, B (2019). G protein-coupled receptor 30 mediates meiosis resumption and gap junction communications downregulation in goat cumulus–oocyte complexes by 17beta-estradiol. J Steroid Biochem Mol Biol 187, 58–67.CrossRefGoogle ScholarPubMed
Zhang, M, Su, YQ, Sugiura, K, Wigglesworth, K, Xia, G and Eppig, JJ (2011). Estradiol promotes and maintains cumulus cell expression of natriuretic peptide receptor 2 (NPR2) and meiotic arrest in mouse oocytes in vitro . Endocrinology 152, 4377–85.CrossRefGoogle ScholarPubMed