Mammalian cumulus-oocyte complex communication: a dialog through long and short distance messaging

Abstract

Communications are crucial to ovarian follicle development and to ovulation, and while both folliculogenesis and oogenesis are distinct processes, they share highly interdependent signaling pathways. Signals from distant organs such as the brain must be processed and compartments within the follicle have to be synchronized. The hypothalamic–pituitary–gonadal (HPG) axis relies on long-distance signalling analogous to wireless communication by which data is disseminated in the environment and cells equipped with the appropriate receptors receive and interpret the messages. In contrast, direct cell-to-cell transfer of molecules is a very targeted, short distance messaging system. Numerous signalling pathways have been identified and proven to be essential for the production of a developmentally competent egg. The development of the cumulus-oocyte complex relies largely on short distance communications or direct transfer type via extensions of corona radiata cells through the zona pellucida. The type of information transmitted through these transzonal projections is still largely uncharacterized. This review provides an overview of current understanding of the mechanisms by which the gamete receives and transmits information within the follicle. Moreover, it highlights the fact that in addition to the well-known systemic long-distance based communications from the HPG axis, these mechanisms acting more locally should also be considered as important targets for controlling/optimizing oocyte quality.

Intercellular communication in the cumulus–oocyte complex during folliculogenesis: A review

“…Meanwhile, EVs were observed around the tips of TZPs, suggesting that some EVs might also be released by TZPs ( Macaulay et al, 2014 ; Macaulay et al, 2016 ). The number of EVs gradually increased as the follicles developed, and their contents also changed ( Marchais et al, 2022 ).…”

Oogenesis in Caenorhabditis elegans

“…Loss of INX-14 and INX-22 results in ectopic MAPK activation in the absence of MSP [Govindan et al, 2006]. The somatic-germ cell gap junctions in C. elegans appear to share a similar role as the cumulus granulosa cells in mammals, which also are involved in inhibiting meiotic maturation (reviewed in [Marchais et al, 2022]), highlighting the evolutionary conservation of somagerm cell communication between vertebrates and invertebrates.…”

Maternal metabolic health and fertility: we should not only care about but also for the oocyte!

“…Next to the FF composition, many cumulus cell gene and proteome markers have been identified as good predictors for oocyte quality (Bunel et al 2015;Alves et al 2019;Si et al 2021). Cumulus cell physiology is intimately linked with oocyte quality as has been elegantly overviewed in detail by Marchais et al (2022).…”