Cumulus cell contact during oocyte maturation in mice regulates meiotic spindle positioning and enhances developmental competence

Abstract

Purpose To investigate the role of cumulus cell contact during oocyte maturation on meiotic spindle assembly and the acquisition of developmental competence. Methods Cumulus oocyte complexes isolated from mouse ovaries subjected to in vitro or in vivo maturation were analyzed by confocal microscopy with respect to oocyte somatic cell contacts and for their ability to develop after parthenogenic activation during embryo culture. Results Cell contact is maintained during maturation in vivo, predisposing oocytes to cortical meiotic spindle assembly and developmental competence acquisition. In contrast, oocytes matured in vitro lose cell contact coincident with central meiotic spindle assembly that results in cleavage delays upon egg activation and failure to form blastocysts. Experimental disruption of cell contact by the actin-depolymerizing agent latrunculin B results in the formation of enlarged meiotic spindles with dispersed chromosomes unlike the compact ordering of chromosomes observed on spindles formed after in vivo maturation, suggesting a link between cell contact and the acquisition of developmental competence. Conclusions Somatic cell contact optimizes oocyte quality during meiotic maturation by regulating the spatial organization and function of the meiotic spindle through actindependent mechanisms that enhance development.

Biomarkers of human oocyte developmental competence expressed in cumulus cells before ICSI: a preliminary study

“…Consistent with our results which showed a significant decrease of its expression, the GJA1 underexpression was suggested as a good marker of oocyte quality and successful pregnancy [57]. Interestingly, the CCs transzonal projections (TZP) structures based on actin filaments were recently shown to be intact in mouse CCs in vivo [73]. Based on these findings, selective regulation of cumulus-oocyte exchanges looks to occur through membrane cytoplasmic extensions mainly the transzonal projections (TZP) until ovulation.…”

“…Its expression was also reported in granulosa cells of rat and bovine species [69,70]. Keeping in mind the fact that synaptic vesicles transport was also achieved via microfilament and microtubule networks [71] and that similar cytoskeleton structures were reported in the transzonal cytoplasmic projections between CCs and the oocyte [72][73][74][75], one can assume the involvement of neuronal genes and molecules/vesicles exchange in CCs-oocyte dialogue.…”

“…The protein kinases' interactions (PI3K, AKT, PKA, MAPK, ERK, PKC, PKN2, PLCB2) are very common pathways and involve several cross-talks which emphasizes the complexity of the molecular events in CCs prior to ovulation. Unfortunately, the whole molecular network of these candidates is still poorly understood despite recognized studies conducted in rodents and mammalians including mice, porcine, bovine and human species,( [36,56,73,90] and reviewed by [91]). Further studies are required to improve our understanding of these pathways (disruption in animal models) and to facilitate oocyte developmental potential prediction.…”

The impact of vitrification on immature oocyte cell cycle and cytoskeletal integrity in a rat model

“…Specifically, drugs that disassemble the actin cytoskeleton may protect subunits and filaments from the adverse effects of temperature and CPAs allowing for the dynamic components to be reassembled following thawing and re-equilibration. Finally, we would propose that the sensitivity of the actin cytoskeleton demonstrated in this work infers that the actin targets are manifold and may have the overall effect of disengaging filament interactions at the oocyte cortex and chromatin as has been shown recently [28].…”

Developmental competence in oocytes and cumulus cells: candidate genes and networks

“…The GO ontology analysis shows that regulation of this process is important for oocyte developmental competence. It has been shown that cumulus cell contact with the oocyte during maturation regulates the spatial organization and function of the meiotic spindle through actin-dependent mechanisms to enhance oocyte quality and developmental competence [Barrett and Albertini 2010]. This illustrates the importance of cell adhesion molecules as well as actin filaments involved in cytoskeleton regulation.…”