Cumulus Cell Transcripts Transit to the Bovine Oocyte in Preparation for Maturation1

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.

Quadrupling efficiency in production of genetically modified pigs through improved oocyte maturation

“…Possibly linked to these biochemical changes were more marked declines in the sizes of the COCs and a greater number of TZP connections. The better preservation of the TZPs during early-phase maturation would likely allow more trafficking of the metabolites and informational molecules essential to promote oocyte cytoplasmic maturation (49,50).…”

“…Analysis of TZP was performed as previously described with minor modifications (49). COCs were fixed in 4% (vol/vol) paraformaldehyde in PBS for 30 min at room temperature.…”

Regulation and roles of the hyaluronan system in mammalian reproduction

“…The cumulus oophorus supports oocyte maturation, ovulation and fertilisation (Magier et al 1990, Tanghe et al 2002. Before ovulation, the cumulus oophorus contributes to the control of cytoplasmic maturation and meiotic arrest (El-Hayek & Clarke 2016, Macaulay et al 2016. During ovulation, it facilitates oocyte movement into the oviduct (Akison et al 2012, mouse) and shortly after ovulation, it participates in the complex mechanisms controlling the access of spermatozoa to the oocyte (Russell et al 2016).…”

Follicular environment and oocyte maturation: roles of local peptides and steroids

“…BMP15 and FGF8 were shown to cooperate to increase the expression and activity of glycolytic enzymes phosphofructokinase (PFKP) and lactate dehydrogenase (LDHA) in cumulus cells from COCs arrested at the germinal vesicle (GV) stage in mice (Sugiura et al, 2007). On the other hand, in bovine COCs undergoing IVM, the combination of BMP15 with FGF17, a member of the FGF8 superfamily also expressed by the bovine oocyte and capable of activating the same receptors that FGF8, did not alter PFKP mRNA levels in cumulus cells (Zhang et al, 2006;Machado et al, 2009Machado et al, , 2015. Therefore, additional studies dissecting the influence of species, COC developmental stage and culture conditions are needed for a clearer understanding of the roles of OSF in the regulation of glucose metabolism in the COC.…”