Cumulus cell transcripts transit to the bovine oocyte in preparation for maturation

Angus D. Macaulay; Isabelle Gilbert; Sara Scantland; Eric Fournier; Fazl Ashkar; Alexandre Bastien; Habib A. Shojaei Saadi; Dominic Gagné; Marc-André Sirard; Édouard W. Khandjian; François J. Richard; Poul Hyttel; Claude Robert

doi:10.1095/biolreprod.114.127571

Cumulus cell transcripts transit to the bovine oocyte in preparation for maturation

Angus D. Macaulay, Isabelle Gilbert, Sara Scantland, Eric Fournier, Fazl Ashkar, Alexandre Bastien, Habib A. Shojaei Saadi, Dominic Gagné, Marc-André Sirard, Édouard W. Khandjian, François J. Richard, Poul Hyttel, Claude Robert

69 Citations (Scopus)

Abstract

So far, the characteristics of a good quality egg have been elusive, similar to the nature of the physiological, cellular, and molecular cues leading to its production both in vivo and in vitro. Current understanding highlights a strong and complex interdependence between the follicular cells and the gamete. Secreted factors induce cellular responses in the follicular cells, and direct exchange of small molecules from the cumulus cells to the oocyte through gap junctions controls meiotic arrest. Studying the interconnection between the cumulus cells and the oocyte, we previously demonstrated that the somatic cells also contribute transcripts to the gamete. Here, we show that these transcripts can be visualized moving down the transzonal projections (TZPs) to the oocyte, and that a time course analysis revealed progressive RNA accumulation in the TZPs, indicating that RNA transfer occurs before the initiation of meiosis resumption under a timetable fitting with the acquisition of developmental competence. A comparison of the identity of the nascent transcripts trafficking in the TZPs, with those in the oocyte increasing in abundance during maturation, and that are present on the oocyte's polyribosomes, revealed transcripts common to all three fractions, suggesting the use of transferred transcripts for translation. Furthermore, the removal of potential RNA trafficking by stripping the cumulus cells caused a significant reduction in maturation rates, indicating the need for the cumulus cell RNA transfer to the oocyte. These results offer a new perspective to the determinants of oocyte quality and female fertility, as well as provide insight that may eventually be used to improve in vitro maturation conditions.

Original language	English
Article number	16
Journal	Biology of Reproduction
Volume	94
Issue number	1
Number of pages	11
ISSN	0006-3363
DOIs	https://doi.org/10.1095/biolreprod.114.127571
Publication status	Published - 1 Jan 2016

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title = "Cumulus cell transcripts transit to the bovine oocyte in preparation for maturation",

abstract = "So far, the characteristics of a good quality egg have been elusive, similar to the nature of the physiological, cellular, and molecular cues leading to its production both in vivo and in vitro. Current understanding highlights a strong and complex interdependence between the follicular cells and the gamete. Secreted factors induce cellular responses in the follicular cells, and direct exchange of small molecules from the cumulus cells to the oocyte through gap junctions controls meiotic arrest. Studying the interconnection between the cumulus cells and the oocyte, we previously demonstrated that the somatic cells also contribute transcripts to the gamete. Here, we show that these transcripts can be visualized moving down the transzonal projections (TZPs) to the oocyte, and that a time course analysis revealed progressive RNA accumulation in the TZPs, indicating that RNA transfer occurs before the initiation of meiosis resumption under a timetable fitting with the acquisition of developmental competence. A comparison of the identity of the nascent transcripts trafficking in the TZPs, with those in the oocyte increasing in abundance during maturation, and that are present on the oocyte's polyribosomes, revealed transcripts common to all three fractions, suggesting the use of transferred transcripts for translation. Furthermore, the removal of potential RNA trafficking by stripping the cumulus cells caused a significant reduction in maturation rates, indicating the need for the cumulus cell RNA transfer to the oocyte. These results offer a new perspective to the determinants of oocyte quality and female fertility, as well as provide insight that may eventually be used to improve in vitro maturation conditions.",

author = "Macaulay, {Angus D.} and Isabelle Gilbert and Sara Scantland and Eric Fournier and Fazl Ashkar and Alexandre Bastien and Saadi, {Habib A. Shojaei} and Dominic Gagn{\'e} and Marc-Andr{\'e} Sirard and Khandjian, {{\'E}douard W.} and Richard, {Fran{\c c}ois J.} and Poul Hyttel and Claude Robert",

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T1 - Cumulus cell transcripts transit to the bovine oocyte in preparation for maturation

AU - Macaulay, Angus D.

AU - Gilbert, Isabelle

AU - Scantland, Sara

AU - Fournier, Eric

AU - Ashkar, Fazl

AU - Bastien, Alexandre

AU - Saadi, Habib A. Shojaei

AU - Gagné, Dominic

AU - Sirard, Marc-André

AU - Khandjian, Édouard W.

AU - Richard, François J.

AU - Hyttel, Poul

AU - Robert, Claude

PY - 2016/1/1

Y1 - 2016/1/1

N2 - So far, the characteristics of a good quality egg have been elusive, similar to the nature of the physiological, cellular, and molecular cues leading to its production both in vivo and in vitro. Current understanding highlights a strong and complex interdependence between the follicular cells and the gamete. Secreted factors induce cellular responses in the follicular cells, and direct exchange of small molecules from the cumulus cells to the oocyte through gap junctions controls meiotic arrest. Studying the interconnection between the cumulus cells and the oocyte, we previously demonstrated that the somatic cells also contribute transcripts to the gamete. Here, we show that these transcripts can be visualized moving down the transzonal projections (TZPs) to the oocyte, and that a time course analysis revealed progressive RNA accumulation in the TZPs, indicating that RNA transfer occurs before the initiation of meiosis resumption under a timetable fitting with the acquisition of developmental competence. A comparison of the identity of the nascent transcripts trafficking in the TZPs, with those in the oocyte increasing in abundance during maturation, and that are present on the oocyte's polyribosomes, revealed transcripts common to all three fractions, suggesting the use of transferred transcripts for translation. Furthermore, the removal of potential RNA trafficking by stripping the cumulus cells caused a significant reduction in maturation rates, indicating the need for the cumulus cell RNA transfer to the oocyte. These results offer a new perspective to the determinants of oocyte quality and female fertility, as well as provide insight that may eventually be used to improve in vitro maturation conditions.

AB - So far, the characteristics of a good quality egg have been elusive, similar to the nature of the physiological, cellular, and molecular cues leading to its production both in vivo and in vitro. Current understanding highlights a strong and complex interdependence between the follicular cells and the gamete. Secreted factors induce cellular responses in the follicular cells, and direct exchange of small molecules from the cumulus cells to the oocyte through gap junctions controls meiotic arrest. Studying the interconnection between the cumulus cells and the oocyte, we previously demonstrated that the somatic cells also contribute transcripts to the gamete. Here, we show that these transcripts can be visualized moving down the transzonal projections (TZPs) to the oocyte, and that a time course analysis revealed progressive RNA accumulation in the TZPs, indicating that RNA transfer occurs before the initiation of meiosis resumption under a timetable fitting with the acquisition of developmental competence. A comparison of the identity of the nascent transcripts trafficking in the TZPs, with those in the oocyte increasing in abundance during maturation, and that are present on the oocyte's polyribosomes, revealed transcripts common to all three fractions, suggesting the use of transferred transcripts for translation. Furthermore, the removal of potential RNA trafficking by stripping the cumulus cells caused a significant reduction in maturation rates, indicating the need for the cumulus cell RNA transfer to the oocyte. These results offer a new perspective to the determinants of oocyte quality and female fertility, as well as provide insight that may eventually be used to improve in vitro maturation conditions.

U2 - 10.1095/biolreprod.114.127571

DO - 10.1095/biolreprod.114.127571

M3 - Journal article

C2 - 26586844

SN - 0006-3363

VL - 94

JO - Biology of Reproduction

JF - Biology of Reproduction

IS - 1

M1 - 16

ER -

Cumulus cell transcripts transit to the bovine oocyte in preparation for maturation

Abstract

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