Roles of the cumulus–oocyte transzonal network and the Fragile X protein family in oocyte competence

in Reproduction
Authors:
Elolo Karen Nenonene Département des sciences animales, Faculté des sciences de l’agriculture et de l’alimentation
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI)
Réseau Québécois en Reproduction (RQR), Université Laval, Québec, Québec, Canada

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Mallorie Trottier-Lavoie Département des sciences animales, Faculté des sciences de l’agriculture et de l’alimentation
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI)
Réseau Québécois en Reproduction (RQR), Université Laval, Québec, Québec, Canada

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Mathilde Marchais Département des sciences animales, Faculté des sciences de l’agriculture et de l’alimentation
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI)
Réseau Québécois en Reproduction (RQR), Université Laval, Québec, Québec, Canada

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Alexandre Bastien Département des sciences animales, Faculté des sciences de l’agriculture et de l’alimentation
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI)
Réseau Québécois en Reproduction (RQR), Université Laval, Québec, Québec, Canada

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Isabelle Gilbert Département des sciences animales, Faculté des sciences de l’agriculture et de l’alimentation
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI)
Réseau Québécois en Reproduction (RQR), Université Laval, Québec, Québec, Canada

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Angus D Macaulay Département des sciences animales, Faculté des sciences de l’agriculture et de l’alimentation
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI)

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Edouard W Khandjian Centre de recherche CERVO, Département de psychiatrie et de neurosciences, Faculté de médecine, Université Laval, Québec, Québec, Canada

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Alberto Maria Luciano Reproductive and Developmental Biology Laboratory, Department of Veterinary Medicine and Animal Science, University of Milan, Milan, Italy

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https://orcid.org/0000-0002-8016-9919
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Valentina Lodde Reproductive and Developmental Biology Laboratory, Department of Veterinary Medicine and Animal Science, University of Milan, Milan, Italy

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Robert S Viger Département d’obstétrique, gynécologie et reproduction, Faculté de médecine, Université Laval, Québec, Québec, Canada
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI)
Réseau Québécois en Reproduction (RQR), Université Laval, Québec, Québec, Canada

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Claude Robert Département des sciences animales, Faculté des sciences de l’agriculture et de l’alimentation
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI)
Réseau Québécois en Reproduction (RQR), Université Laval, Québec, Québec, Canada

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https://orcid.org/0000-0001-9690-8088

Correspondence should be addressed to C Robert; Email: claude.robert@fsaa.ulaval.ca
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In brief

RNA granules travel through the cumulus cell network of transzonal projections which is associated with oocyte developmental competence, and RNA packaging involves RNA-binding proteins of the Fragile X protein family.

Abstract

The determinants of oocyte developmental competence have puzzled scientists for decades. It is known that follicular conditions can nurture the production of a high-quality oocyte, but the underlying mechanisms remain unknown. Somatic cumulus cells most proximal to the oocyte are known to have cellular extensions that reach across the zona pellucida and contact with the oocyte plasma membrane. Herein, it was found that transzonal projections (TZPs) network quality is associated with developmental competence. Knowing that ribonucleoparticles are abundant within TZPs, the distribution of RNA-binding proteins was studied. The Fragile X-related proteins (FXR1P and FXR2P) and two partnering protein families, namely cytoplasmic FMRP-interacting protein and nuclear FMRP-interacting protein, exhibited distinctive patterns consistent with roles in regulating mRNA packaging, transport, and translation. The expression of green fluorescent protein (GFP)–FMRP fusion protein in cumulus cells showed active granule formation and their transport and transfer through filipodia connecting with neighboring cells. Near the projections’ ends was found the cytoskeletal anchoring protein Filamin A and active protein synthesis sites. This study highlights key proteins involved in delivering mRNA to the oocyte. Thus, cumulus cells appear to indeed support the development of high-quality oocytes via the transzonal network.

 

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