title: The gametic synapse: RNA transfer to the bovine oocyte.
abstract: Even after several decades of quiescent storage in the ovary, the female germ cell is capable of reinitiating transcription to build the reserves that are essential to support early embryonic development. In the current model of mammalian oogenesis, there exists bilateral communication between the gamete and the surrounding cells that is limited to paracrine signaling and direct transfer of small molecules via gap junctions existing at the end of the somatic cells' projections that are in contact with the oolemma. The purpose of this work was to explore the role of cumulus cell projections as a means of conductance of large molecules, including RNA, to the mammalian oocyte. By studying nascent RNA with confocal and transmission electron microscopy in combination with transcript detection, we show that the somatic cells surrounding the fully grown bovine oocyte contribute to the maternal reserves by actively transferring large cargo, including mRNA and long noncoding RNA. This occurrence was further demonstrated by the reconstruction of cumulus-oocyte complexes with transfected cumulus cells transferring a synthetic transcript. We propose selective transfer of transcripts occurs, the delivery of which is supported by a remarkable synapselike vesicular trafficking connection between the cumulus cells and the gamete. This unexpected exogenous contribution to the maternal stores offers a new perspective on the determinants of female fertility.
authors.affiliation: Département des sciences animales, Centre de recherche en biologie de la reproduction, Institut sur la nutrition et les aliments fonctionnels, Université Laval, Québec City, Québec, Canada.
authors.forename: Angus D
authors.initials: AD
authors.lastname: Macaulay
authors.affiliation: Département des sciences animales, Centre de recherche en biologie de la reproduction, Institut sur la nutrition et les aliments fonctionnels, Université Laval, Québec City, Québec, Canada.
authors.forename: Isabelle
authors.initials: I
authors.lastname: Gilbert
authors.affiliation: Département des sciences animales, Centre de recherche en biologie de la reproduction, Institut sur la nutrition et les aliments fonctionnels, Université Laval, Québec City, Québec, Canada.
authors.forename: Julieta
authors.initials: J
authors.lastname: Caballero
authors.affiliation: Veterinarian Medicine Department, São Paulo University, São Paulo, Brazil.
authors.forename: Rodrigo
authors.initials: R
authors.lastname: Barreto
authors.affiliation: Département des sciences animales, Centre de recherche en biologie de la reproduction, Institut sur la nutrition et les aliments fonctionnels, Université Laval, Québec City, Québec, Canada.
authors.forename: Eric
authors.initials: E
authors.lastname: Fournier
authors.affiliation: Département des sciences animales, Centre de recherche en biologie de la reproduction, Institut sur la nutrition et les aliments fonctionnels, Université Laval, Québec City, Québec, Canada.
authors.forename: Prudencio
authors.initials: P
authors.lastname: Tossou
authors.affiliation: Département des sciences animales, Centre de recherche en biologie de la reproduction, Institut sur la nutrition et les aliments fonctionnels, Université Laval, Québec City, Québec, Canada.
authors.forename: Marc-André
authors.initials: MA
authors.lastname: Sirard
authors.affiliation: Department of Obstetrics and Gynecology, McGill University Health Centre, Montréal, Québec, Canada.
authors.forename: Hugh J
authors.initials: HJ
authors.lastname: Clarke
authors.affiliation: Département de Psychiatrie et Neurosciences, Institut universitaire en santé mentale de Québec, Université Laval, Québec City, Québec, Canada.
authors.forename: Édouard W
authors.initials: ÉW
authors.lastname: Khandjian
authors.affiliation: Département des sciences animales, Centre de recherche en biologie de la reproduction, Institut sur la nutrition et les aliments fonctionnels, Université Laval, Québec City, Québec, Canada.
authors.forename: Francois J
authors.initials: FJ
authors.lastname: Richard
authors.affiliation: Department of Veterinary Clinical and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
authors.forename: Poul
authors.initials: P
authors.lastname: Hyttel
authors.affiliation: Département des sciences animales, Centre de recherche en biologie de la reproduction, Institut sur la nutrition et les aliments fonctionnels, Université Laval, Québec City, Québec, Canada claude.robert@fsaa.ulaval.ca.
authors.forename: Claude
authors.initials: C
authors.lastname: Robert
mesh_terms: D000818:Animals; D030801:Animals, Genetically Modified; D002417:Cattle / Q000235:genetics* / Q000502:physiology*; D019295:Computational Biology; D054885:Cumulus Cells / Q000502:physiology / Q000648:ultrastructure; D005260:Female; D005786:Gene Expression Regulation; D009865:Oocytes / Q000502:physiology*; D009866:Oogenesis / Q000502:physiology; D012313:RNA / Q000378:metabolism*; D059467:Transcriptome
chemical_list: D012313:RNA
keywords: in vitro maturation (IVM); intercellular communication; oocyte development; oocyte maturation