Artigo Acesso aberto Revisado por pares

Mammalian Oocytes Locally Remodel Follicular Architecture to Provide the Foundation for Germline-Soma Communication

2018; Elsevier BV; Volume: 28; Issue: 7 Linguagem: Inglês

10.1016/j.cub.2018.02.039

ISSN

1879-0445

Autores

Stephany El‐Hayek, Qin Yang, Laleh Abbassi, Greg FitzHarris, Hugh J. Clarke,

Tópico(s)

Renal and related cancers

Resumo

Germ cells develop in a microenvironment created by the somatic cells of the gonad [1Matunis E.L. Stine R.R. de Cuevas M. Recent advances in Drosophila male germline stem cell biology.Spermatogenesis. 2012; 2: 137-144Crossref PubMed Google Scholar, 2Kidder G.M. Vanderhyden B.C. Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence.Can. J. Physiol. Pharmacol. 2010; 88: 399-413Crossref PubMed Scopus (202) Google Scholar, 3El-Hayek S. Clarke H.J. Control of oocyte growth and development by intercellular communication within the follicular niche.Results Probl. Cell Differ. 2016; 58: 191-224Crossref PubMed Scopus (35) Google Scholar]. Although in males, the germ and somatic support cells lie in direct contact, in females, a thick extracellular coat surrounds the oocyte, physically separating it from the somatic follicle cells [4Wassarman P.M. Litscher E.S. Biogenesis of the mouse egg’s extracellular coat, the zona pellucida.Curr. Top. Dev. 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Albertini D.F. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte.Nat. Rev. Mol. Cell Biol. 2013; 14: 141-152Crossref PubMed Scopus (314) Google Scholar, 9Macaulay A.D. Gilbert I. Caballero J. Barreto R. Fournier E. Tossou P. Sirard M.A. Clarke H.J. Khandjian E.W. Richard F.J. et al.The gametic synapse: RNA transfer to the bovine oocyte.Biol. Reprod. 2014; 91: 90Crossref PubMed Scopus (126) Google Scholar]. These delicate structures provide the sole platform for the contact-mediated communication between the oocyte and its follicular environment that is indispensable for production of a fertilizable egg [8Li R. Albertini D.F. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte.Nat. Rev. Mol. Cell Biol. 2013; 14: 141-152Crossref PubMed Scopus (314) Google Scholar, 10Jaffe L.A. Egbert J.R. Regulation of mammalian oocyte meiosis by intercellular communication within the ovarian follicle.Annu. Rev. 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Burns K.H. Viveiros M.M. Eppig J.J. Intercellular communication in the mammalian ovary: oocytes carry the conversation.Science. 2002; 296: 2178-2180Crossref PubMed Scopus (739) Google Scholar]. Identifying the mechanisms underlying their formation should uncover conserved regulators of fertility. We show here in mice that these structures, termed transzonal projections (TZPs), are specialized filopodia whose number amplifies enormously as oocytes grow, enabling increased germ-soma communication. By creating chimeric complexes of genetically tagged oocytes and follicle cells, we demonstrate that follicle cells elaborate new TZPs that push through the extracellular coat to reach the oocyte surface. We further show that growth-differentiation factor 9, produced by the oocyte, drives the formation of new TZPs, uncovering a key yet unanticipated role for the germ cell in building these essential bridges of communication. Moreover, TZP number and germline-soma communication are strikingly reduced in reproductively aged females. Thus, the growing oocyte locally remodels follicular architecture to ensure that its developmental needs are met, and an inability of somatic follicle cells to respond appropriately to oocyte-derived cues may contribute to human infertility.

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