Paracrine Regulation of Granulosa Cell Development in the Antral Follicles in Mammals

Overview

Journal Reprod Med Biol

Specialty Biology

Date 2023 Aug 28

PMID 37638351

Authors

Koji Sugiura

Natsumi Maruyama

Yuki Akimoto

Kodai Matsushita

Tsutomu Endo

Affiliations

Soon will be listed here.

Abstract

Background: Development of ovarian follicles is regulated by a complex interaction of intra- and extra-follicular signals. Oocyte-derived paracrine factors (ODPFs) play a central role in this process in cooperation with other signals.

Methods: This review provides an overview of the recent advances in our understanding of the paracrine regulation of antral follicle development in mammals. It specifically focuses on the regulation of granulosa cell development by ODPFs, along with other intrafollicular signals.

Main Findings: Bi-directional communication between oocytes and surrounding cumulus cells is a fundamental mechanism that determines cumulus cell differentiation. Along with estrogen, ODPFs promote the expression of forkhead box L2, a critical transcription factor required for mural granulosa cells. Follicle-stimulating hormone (FSH) facilitates these processes by stimulating estrogen production in mural granulosa cells.

Conclusion: Cooperative interactions among ODPFs, FSH, and estrogen are critical in determining the fate of cumulus and mural granulosa cells, as well as the development of oocytes.

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References

Salustri A, Ulisse S, Yanagishita M, Hascall V . Hyaluronic acid synthesis by mural granulosa cells and cumulus cells in vitro is selectively stimulated by a factor produced by oocytes and by transforming growth factor-beta. J Biol Chem. 1990; 265(32):19517-23. View

Nekola M, NALBANDOV A . Morphological changes of rat follicular cells as influenced by oocytes. Biol Reprod. 1971; 4(2):154-60. DOI: 10.1093/biolreprod/4.2.154. View

Wilson T, Wu X, Juengel J, Ross I, Lumsden J, Lord E . Highly prolific Booroola sheep have a mutation in the intracellular kinase domain of bone morphogenetic protein IB receptor (ALK-6) that is expressed in both oocytes and granulosa cells. Biol Reprod. 2001; 64(4):1225-35. DOI: 10.1095/biolreprod64.4.1225. View

Machado M, Caixeta E, Sudiman J, Gilchrist R, Thompson J, Lima P . Fibroblast growth factor 17 and bone morphogenetic protein 15 enhance cumulus expansion and improve quality of in vitro-produced embryos in cattle. Theriogenology. 2015; 84(3):390-8. DOI: 10.1016/j.theriogenology.2015.03.031. View

Vitt U, Hayashi M, Klein C, Hsueh A . Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles. Biol Reprod. 2000; 62(2):370-7. DOI: 10.1095/biolreprod62.2.370. View

Souza C, MacDougall C, Campbell B, McNeilly A, Baird D . The Booroola (FecB) phenotype is associated with a mutation in the bone morphogenetic receptor type 1 B (BMPR1B) gene. J Endocrinol. 2001; 169(2):R1-6. DOI: 10.1677/joe.0.169r001. View

Vanderhyden B, Telfer E, Eppig J . Mouse oocytes promote proliferation of granulosa cells from preantral and antral follicles in vitro. Biol Reprod. 1992; 46(6):1196-204. DOI: 10.1095/biolreprod46.6.1196. View

Yi S, Lapolt P, Yoon B, Chen J, Lu J, Lyons K . The type I BMP receptor BmprIB is essential for female reproductive function. Proc Natl Acad Sci U S A. 2001; 98(14):7994-9. PMC: 35456. DOI: 10.1073/pnas.141002798. View

Ito H, Emori C, Kobayashi M, Maruyama N, Fujii W, Naito K . Cooperative effects of oocytes and estrogen on the forkhead box L2 expression in mural granulosa cells in mice. Sci Rep. 2022; 12(1):20158. PMC: 9691737. DOI: 10.1038/s41598-022-24680-x. View

10.

Alam M, Lee J, Miyano T . GDF9 and BMP15 induce development of antrum-like structures by bovine granulosa cells without oocytes. J Reprod Dev. 2018; 64(5):423-431. PMC: 6189575. DOI: 10.1262/jrd.2018-078. View

11.

Cheng G, Weihua Z, Makinen S, Makela S, Saji S, Warner M . A role for the androgen receptor in follicular atresia of estrogen receptor beta knockout mouse ovary. Biol Reprod. 2001; 66(1):77-84. DOI: 10.1095/biolreprod66.1.77. View

12.

Zhang M, Su Y, Sugiura K, Xia G, Eppig J . Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science. 2010; 330(6002):366-9. PMC: 3056542. DOI: 10.1126/science.1193573. View

13.

Sugiura K, Su Y, Diaz F, Pangas S, Sharma S, Wigglesworth K . Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development. 2007; 134(14):2593-603. DOI: 10.1242/dev.006882. View

14.

Carabatsos M, Elvin J, Matzuk M, Albertini D . Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev Biol. 1999; 204(2):373-84. DOI: 10.1006/dbio.1998.9087. View

15.

Miyoshi T, Otsuka F, Yamashita M, Inagaki K, Nakamura E, Tsukamoto N . Functional relationship between fibroblast growth factor-8 and bone morphogenetic proteins in regulating steroidogenesis by rat granulosa cells. Mol Cell Endocrinol. 2010; 325(1-2):84-92. DOI: 10.1016/j.mce.2010.04.012. View

16.

Schmidt D, Ovitt C, Anlag K, Fehsenfeld S, Gredsted L, Treier A . The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development. 2004; 131(4):933-42. DOI: 10.1242/dev.00969. View

17.

Su Y, Sugiura K, Eppig J . Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Semin Reprod Med. 2009; 27(1):32-42. PMC: 2742468. DOI: 10.1055/s-0028-1108008. View

18.

Wigglesworth K, Lee K, Emori C, Sugiura K, Eppig J . Transcriptomic diversification of developing cumulus and mural granulosa cells in mouse ovarian follicles. Biol Reprod. 2014; 92(1):23. PMC: 4434932. DOI: 10.1095/biolreprod.114.121756. View

19.

Buratini Jr J, Teixeira A, Costa I, Glapinski V, Pinto M, Giometti I . Expression of fibroblast growth factor-8 and regulation of cognate receptors, fibroblast growth factor receptor-3c and -4, in bovine antral follicles. Reproduction. 2005; 130(3):343-50. DOI: 10.1530/rep.1.00642. View

20.

Middlebrook B, Eldin K, Li X, Shivasankaran S, Pangas S . Smad1-Smad5 ovarian conditional knockout mice develop a disease profile similar to the juvenile form of human granulosa cell tumors. Endocrinology. 2009; 150(12):5208-17. PMC: 2819741. DOI: 10.1210/en.2009-0644. View