Stages in follicle cell/oocyte interface during vitellogenesis in caecilians Ichthyophis tricolor and Gegeneophis ramaswamii: a transmission electron-microscopic study

Abstract

We describe the ultrastructural organization of the vitellogenic follicle stages in two caecilian species. Monthly samples of slices of ovary of Ichthyophis tricolor and Gegeneophis ramaswamii from the Western Ghats of India were subjected to transmission electron-microscopic analysis, with special attention to the follicle cell/oocyte interface. In order to maintain uniformity of the stages among the amphibians, all the stages in the caecilian follicles were assigned to stages I-VI, the vitellogenic and post-vitellogenic follicles being assigned to stages III-VI. Stage III commences with the appearance of precursors of vitelline envelope material in the perivitelline space. Stages IV and V have been assigned appropriate substages. During the transition of stage III to stage VI oocytes, a sequential change occurs in the manifestations of follicle cells, perivitelline space, vitelline envelope and oocyte cortex. The vitelline envelope becomes a tough coat through the tunnels of which the macrovilli pass to interdigitate between the microvilli. The oocyte surface forms pinocytic vesicles that develop into coated pits and, later, coated vesicles. Contributions of the oocyte cortex to the vitelline envelope and of the follicle cells to yolk material via synthesis within them are indicated. The follicle cell/oocyte interface of vitellogenic follicles of these two caecilians resembles that in anurans and urodeles, with certain features being unique to caecilians. Thus, this paper throws light on the possible relationships of caecilians to anurans and urodeles with special reference to ovarian follicles.

Microscopic structures of the ovary and female genital ducts of Supachai's caecilian, Ichthyophis supachaii Taylor, 1960 (Amphibia: Gymnophiona)

“…; Beyo et al . , ). The vitelline envelope of amphibian oocytes, including I. supachaii , is composed of neutral glycoproteins that are reactive to PAS and are likely homologous to the mammalian zona pellucida glycoproteins (Barisone et al .…”

“…The vitelline envelope of I. supachaii and perhaps other caecilians is an extracellular matrix layer, which appears striated under a light microscope. Accumulated evidence indicates that this striation is due to projection and interdigitation between macrovilli from follicular cells and microvilli from oocytes, both projecting into the fenestrated vitelline envelope, thus allowing crosstalk at the follicular cell-oocyte interface (Villecco et al 2002;Beyo et al 2007Beyo et al , 2008. The vitelline envelope of amphibian oocytes, including I. supachaii, is composed of neutral glycoproteins that are reactive to PAS and are likely homologous to the mammalian zona pellucida glycoproteins (Barisone et al 2002(Barisone et al , 2007Jovine et al 2002).…”

Accumulation of yolk in a caecilian (Gegeneophis ramaswamii) oocyte: A light and transmission electron microscopic study

“…Each month three female animals were sacrificed using 25% MS-222 (tricaine methane sulfonate) anesthesia and dissected to expose the female reproductive system. In accordance with Beyo et al (2008), the ovarian follicles were assigned to stages. The ovaries were removed, washed thoroughly in an amphibian saline solution, and then fixed in 2.5% glutaraldehyde solution.…”

“…The follicle cell-oocyte interface, with special reference to macrovilli of follicle cells, microvilli of oocytes and different kinds of membrane associations between the two, provides for transfer of the heterosynthetic yolk precursor material from the follicle cells to the oocyte (Beyo et al, 2008). Gap and tight junctions that appear in the perivitelline space between macro and microvilli facilitate pinocytic uptake of heterosynthetic yolk precursor material 2 from the follicle cells to the oocyte (see Fig.…”

“…Therefore, to provide an in-depth knowledge about the aspects of ovarian changes in caecilians, taking advantage of the fairly abundant distribution of caecilians in the Western Ghats of India (Oommen et al, 2000), an extensive study was conducted on Ichthyophis tricolor and Gegeneophis ramaswamii, using transmission electron microscopy (TEM). We have recently described in these caecilians about the stages in the female reproductive cycle and the follicle cell-oocyte interface (Beyo et al, 2008), folliculogenesis (Beyo et al, 2007a), and the ultrastructural organization of previtellogenic follicles (Beyo et al, 2007b). Because these two species do not differ much in ovarian cycles (Beyo et al, 2007a(Beyo et al, ,b, 2008, further studies were limited to G. ramaswamii because it is more abundant than I. tricolor in the collection area.…”