Oocyte–follicle cell interactions during ovarian follicle development, as seen by high resolution scanning and transmission electron microscopy in humans

Abstract

The aim of this article is to summarize and update, through an integrated analysis by transmission electron microscopy (TEM) and high resolution scanning electron microscopy (SEM) after osmium-dimethyl sulfoxide-osmium (ODO) maceration, the studies of our research group on the morphodynamics of oocyte-follicle cell associations during follicle development in humans. In resting oocytes, follicular cells project few and short cytoplasmic processes in the perioocytic space. They often form bulbous terminals very close to the oolemma where zonulae adherentes, maculae adherentes, and gap junctions are present. The oolemma mostly appears smooth with short and scanty microvilli. In early growing follicles, follicular cell projections appear as (a) long and tortuous microvilli or (b) large and short extensions. The oolemma shows numerous short microvilli. By TEM, long and thin follicular "intraooplasmic processes" have been seen to penetrate deeply into some oolemma invaginations. In macerated samples, they are observed by SEM to come very close to the nucleus and contact different oocyte organelles. These processes are more likely involved in early oocyte growth. In late growing follicles, oocyte-somatic cell interactions-now established through the interposition of the zona pellucida (ZP)-preserve the general features of early growth stage, with the exceptions of "intraooplasmic processes," which are no more present. In mature follicles subjected to a long ODO maceration, corona cells appear to contact the oocyte through an apical plume of numerous very long "curly hair-like microvilli." Corona cell microvilli, quite likely provide a sort of cytoplasmic skeleton for the ZP and they are possibly involved in (a) release of nutrients or removal catabolites to/from oocyte and vice versa and (b) transfer of substances to build up ZP. In conclusion, among oocyte and somatic cells a structural and functional association is revealed. This association, certainly highly dynamic in vivo, plays a key role in regulating the healthy folliculogenesis to assure a correct and timed oocyte maturation and ovulation.

Impact of the LH surge on granulosa cell transcript levels as markers of oocyte developmental competence in cattle

“…Evidence accumulated over the past few decades suggests that a bidirectional communication between the oocyte and the surrounding somatic cells takes place during folliculogenesis (Buccione et al 1990a, 1990b, Eppig et al 2002, Gilchrist et al 2004, Makabe et al 2006, Sirard et al 2006, Buratini & Price 2011, Conti et al 2012, confirming a link between oocyte competence and the follicular environment. This communication can be achieved through paracrine signaling and direct cell-to-cell communication via gap junction channels (reviewed in Kidder & Vanderhyden (2010)).…”

Apical and lateral cell protrusions interconnect epithelial cells in live Drosophila wing imaginal discs

“…Microvilli of follicle cells projecting toward the oocyte have also been described in amphibians and mammals (Dantzer, 1985;Villecco et al, 2002;Makabe et al, 2006), suggesting that follicle cell microvilli might establish connections with oocytes in many animal species. Considering that, over the past decades, microvilli have been identified in a plethora of epithelia and organisms, we speculate that microvilli might connect apposed epithelia during different developmental stages in several organisms.…”

History, origin, and function of transzonal projections: the bridges of communication between the oocyte and its environment

“…First, as reported by several groups based on observation and recently quantified by us, the number of TZPs increases by at least an order of magnitude during oocyte growth (Makabe et al, 2006;Li and Albertini, 2013;El-Hayek et al, 2018). Second, because the zona pellucida is laid down early during oocyte growth, many granulosa cells adjacent to the oocyte must be born after this event.…”

“…Both gap junctions, discussed in more detail below, and tight junctions are present at the sites of plasma membrane apposition (Anderson and Albertini, 1976;Gilula et al, 1978). Multiple TZPs project from a single granulosa cell -as many as 70 have been reported (Makabe et al, 2006) -apparently originating from one or a small number of central hubs or foci. TZPs have been described in a wide range of mammals (De Smedt and Szollosi, 1991;De Lesegno et al, 2008).…”

“…TZPs have been described in a wide range of mammals (De Smedt and Szollosi, 1991;De Lesegno et al, 2008). In primates, TZPs have been identified that project deep into the oocyte, reaching even as far as the nucleus (Hope, 1965;Motta et al, 1994;Makabe et al, 2006). Studies such as these unequivocally established the nature of the germ line-soma interaction.…”