TY - JOUR
T1 - The gametic synapse
T2 - RNA transfer to the bovine oocyte
AU - Macaulay, Angus D.
AU - Gilbert, Isabelle
AU - Caballero, Julieta
AU - Barreto, Rodrigo
AU - Fournier, Eric
AU - Tossou, Prudencio
AU - Sirard, Marc-André
AU - Clarke, Hugh J.
AU - Khandjian, Édouard W.
AU - Richard, Francois J.
AU - Hyttel, Poul
AU - Robert, Claude
N1 - © 2014 by the Society for the Study of Reproduction, Inc.
PY - 2014/10/1
Y1 - 2014/10/1
N2 - 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.
AB - 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.
U2 - 10.1095/biolreprod.114.119867
DO - 10.1095/biolreprod.114.119867
M3 - Journal article
C2 - 25143353
SN - 0006-3363
VL - 91
JO - Biology of Reproduction
JF - Biology of Reproduction
IS - 4
M1 - 90
ER -