Recent Advances in Insect Embryology in Japan and Poland
Edited by H. Ando and Cz. JuraArthropod. EmbryoL. Soc. Jpn.
(lSEBU Co. Ltd., Tsukuba) 1987

19

Heterocellular Gap Junctions
in Vitellogenic Follicles of Campodea spp. (Diplura),Szczepan BILINSKI
Synopsis
Oocyte-follicle cell interface has been examined ultrastructurally in the ovaries of Campodea
spp. Gap junctions between the oocyte and enveloping follicle cells (termed: heterocellular gap
junctions) occur only during vitellogenesis. These junctions are located between the tips of folliclecell processes and the oocyte surface.

Introduction
The occurrence of heterocellular gap junctions (i. e. gap junctions between theoocyte and enveloping follicle cells) in the ovaries of insects was first suggested by electrophysiological studies performed by Wollberg et al. (1976). Recently, such junctions
have been described in the ovaries of several insect species (Woodruff, 1979; Huebner,1981; Bilinski and Klag, 1982; Bilinski et al., 1985; Mazzini and Giorgi, 1985; Giorgi
and Postlethwait, 1985). Experiments with the injection of fluorescent dyes have demonstrated that these junctions are in functional state at least during the period of yolk
accumulation (Woodruff, 1979; Woodruff and Anderson, 1984; Bilinski et al., 1985).
Heterocellular gap junctions are assumed to play a part in the coordination of the joint
differentiation of the oocyte and the follicular epithelium and in the transfer of low
molecular weight molecules from the follicle cells to the oocyte (Huebner, 1981; Telferet al., 1982; Bilinski et al., 1985). Moreover, the fact that oocyte-follicle cell contacts arelost during atresia (Huebner, 1981) shows that heterocellular gap junctions play a keyrole in the regulation and/or maintenance of normal oocyte growth (Huebner, 1981).
In this paper the occurrence of oocyte-follicle cell gap junctions in the ovary ofCampodea spp. is reported.

20Fig. 1.

S. Bilinski

The oocyte-follicle cell interface during vitellogenesis . fc, follicle cell; 00, oocyte; v,microvilli; arrows, gap junction; asterisk, follicle cell process. X 42,800.

Gap junctions in vitellogenic follicles of Campodea

21

Material and Methods
The methods employed are described by Bilinski and Tylek (1987).

Results and Discussion
During vitellogenesis the oocyte surface is supplied with short, irregular microvilli(Fig. 1), at the bases of which numerous pinocytotic vesicles are observed (Fig. 1). Elements of rough endoplasmic reticulum, ribosomes and mitochondria occur also in thecortical ooplasm (Fig. 1). It should be stressed out that the oocyte microvilli make nocontact with the follicle cell membrane.
Detailed examination of the oocyte-follicle cell interface has shown that apicalplasma membrane of the follicle cell is equipped with fine processes (Fig. 1, asterisk).
These processes are infrequent and occur predominantly in the central part of the follicle cell. The follicle cell processes traverse the perioocytic space to make contact withthe oocyte surface (Fig. 1). At the contact sites of the processes with the oocyte plasma
membrane, the gap junctions are observed (Fig. 1, arrows). The two plasma membranes, within the junction, are parallel and spaced about 3-4 nm apart.
The follicle cell processes as well as the oocyte microvilli are immersed in dense
flocculent substance that fills the whole perioocytic space (Fig. 1).
The organization of the oocyte-follicle cell contacts in Campodea shows much similarity to that in another apterygotan insect - Acerentomon (Bilinski and Klag, 1982). In
this species heterocellular gap junctions occur also between specialized follicle cell processes and the oocyte surface. In contrast, in pterygotan insects such junctions occur atthe contact sites of the tips of the oocyte microvilli with the comparatively flat membrane of the follicle cell (Bilinski et al., 1985) or between interdigitating microvilli of theoocyte and the follicle cells (Huebner, 1981; Giorgi and Postlethwait, 1985).
In the species studied heterocellular gap junctions are observed only during vitellogenesis; they are not found in pre- and postvitellogenesis. Similarly, in Tribolium(Bilinski et at., 1985) and Oncopeltus (Woodruff and Anderson, 1984) such junctions before the phase of yolk accumulation are infrequent and/or nonfunctional. At the onsetof vitellogenesis in these species the number of gap junctions increases and thus thefollicle cells become dye-coupled to the oocyte (Woodruff and Anderson, 1984; Bilinski
et al., 1985). These observations lead to the suggestion that the formation of heterocellular gap junctions (or the increase of their number) is due to the action of a juvenile hormone, which is known to act at the beginning of the vitellogenesis in insects.

References
Bilinski, S., W. J. Rage and J. G. Bluemink, 1985. Gap junctions between the follicle cells andthe oocyte during oogenesis in an insect, Tribolium destructor (Coleoptera). Roux's Arch. Devl.
Bioi. 194: 296-300.
- - - - - , and J. Klag, 1982. Gap junctions between oocyte and follicle cells in Acerentomonsp. (Insecta, Protura). Int. J. Invert. Reproduct. 5: 331-335.

22S. Bilinski- - - - - - , and W. Tylek, 1987. Intermediate nurse cells in Campodea spp. (Diplura). Differentiation and possible role during oogenesis. In H. Ando and Cz. Jura (eds. ), Recent
Advances in Insect Embryology in Japan and Poland, 23-29. Arthropod. Embryo!. Soc. Jpn.
(ISEBU Co. Ltd., Tsukuba).
Giorgi, F. and J. H. Postlethwait, 1985. Development of gap junctions in normal and mutantovaries of Drosophila meianogaster. J. Morphol. 185: 115-129.
Huebner, E., 1981. Oocyte-follicle cell interaction during normal oogenesis and atresia in an insect. J. Ultrastruct. Res. 74: 95-104.
Mazzini, M. and F. Giorgi, 1985. The follicle cell-oocyte interaction in ovarian follicles of thestick insect Bacillus rossius (Rossi) (Insecta: Phasmatodea). J. Morphol. 185: 37-49.
Telfer, W. H., E. Huebner and D. S. Smith, 1982. The cell biology of vitellogenic follicles inHyalophora and Rhodnius. In R. C. King and H. Akai (eds. ), Insect Ultrastructure, Vo!. I,
118-149. Plenum, New York.
Wollberg, Z., E. Cohen and M. Kalina, 1976. Electrical properties of developing oocytes of themigratory locust, Locusta migratoria. J. Cell Physioi. 88: 145-157.
Woodruff, R. I., 1979. Electrotonic junctions in Cecropia moth ovaries. Devl. Bioi. 69: 281-295.
- - - - - - , and K. L. Anderson, 1984. Nutritive cord connection and dye-coupling of the follicular epithelium to the growing oocytes in the telotrophic ovarioles in Oncopeltus jasciatus,
the milkweed bug. Roux's Arch. Devi. BioI. 193: 158-163.

Author's address: Dr. S. Bilinski
Department of Systematic Zoology, Institute of Zoology, Jagiellonian University, ul. Karasia 6, 30-060 Krak6w,Poland