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Functional signaling and gene regulatory networks between the oocyte and the surrounding cumulus cells

ABSTRACT: The maturation of an oocyte, the female gamete, during folliculogenesis is highly dependent on the molecular interaction with the somatic cells. Here we generated transcriptome data of single oocytes and the surrounding cumulus cells from antral follicles, and developed an analytical framework to unveil their inter-cellular communication. We identified hundreds of ligand-receptors pairs that can transduce paracrine signaling between oocyte and cumulus. Several of the ligand-coding genes expressed in oocytes and cumulus cells are also functionally associated with regulation of transcription. Ligand-coding genes expressed in oocytes or cumulus showed distinct enrichment for biological functions that are likely associated with a coordinated formation of the transzonal projections from the cumulus that reach the oocyte’s membrane. Finally, there were thousands of gene pairs with non-trivial linear co-expression pattern between oocytes and cumulus cells. Our analyses revealed a complex and functional regulatory circuit between the oocyte and surrounding cumulus cells.

ORGANISM(S): Bos taurus

PROVIDER: GSE99678 | GEO | 2017/06/21

SECONDARY ACCESSION(S): PRJNA389288

REPOSITORIES: GEO

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Project description:The present study was undertaken to discover molecular markers in bovine cumulus cells predictive of oocyte competence and elucidate their functional significance. Differences in RNA transcript abundance in cumulus cells harvested from oocytes of adult versus prepubertal animals (model of poor oocyte quality) were identified by microarray analysis. Four genes of interest encoding for the lysosomal cysteine proteinases cathepsin B, S, K and Z and displaying greater transcript abundance in cumulus cells surrounding oocytes harvested from prepubertal animals were chosen for further investigation. Greater mRNA abundance for such genes in cumulus cells of prepubertal oocytes was confirmed by real time RT-PCR. Elevated transcript abundance for cathepsins B, S and Z was also observed in cumulus cells surrounding adult metaphase II oocytes that developed to the blastocyst stage at a low percentage following parthenogenetic activation, versus those that developed at a high percentage. Functional significance of cumulus cell cathepsin expression to oocyte competence was confirmed by treatment of cumulus oocyte complexes during in vitro oocyte maturation with a cell permeable cysteine proteinase (cathepsin) inhibitor. Inhibitor treatment decreased apoptotic nuclei in the cumulus layer and enhanced development of parthenogenetically activated and in vitro fertilized adult oocytes to the blastocyst stage. Stimulatory effects of inhibitor treatment during meiotic maturation on subsequent embryonic development were not observed when oocytes were matured in the absence of cumulus cells. Results support a functional role for cumulus cell cathepsins in compromised oocyte competence and suggest that cumulus cell cathepsin mRNA abundance may be predictive of oocyte quality. Keywords: Bovine, microarray, cDNA, cumulus cells Differences in RNA transcript abundance in cumulus cells harvested from oocytes of adult versus prepubertal animals (model of poor oocyte quality) were identified by microarray analysis. Total RNA from pools of cumulus cells (n = 4) collected from adult and prepubertal animals for microarray experiments was amplified. Two color microarray experiments were conducted using a bovine cDNA array containing expressed sequence tags (ESTs) representing approximately 15200 unique genes. Hybridizations were performed on duplicate slides (prepubertal versus adult) and incorporated a dye swap. The total number of slides used is eight.

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Functional signaling and gene regulatory networks between the oocyte and the surrounding cumulus cells

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