FOLLICLE CELL BRIDGES IN THE MOSQUITO OVARY: SYNCYTIA FORMATION AND BRIDGE MORPHOLOGY
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1 jf. Cell Set. 31, (1978) 137 Printed in Great Britain Company of Biologists Limited I<)TS FOLLICLE CELL BRIDGES IN THE MOSQUITO OVARY: SYNCYTIA FORMATION AND BRIDGE MORPHOLOGY ANNELISE FIIL Institute of Medical Genetics, University of Copenhagen, Tagensvej 14, DK-2200 Copenhagen N, Denmark SUMMARY In the mosquito, Culex pipiens quinqefasciatus, the follicle cells enveloping the oocyte and the nurse cells are connected by intercellular bridges. The bridges are formed by incomplete cytokinesis, and they persist for more than 30 h after their formation. Reconstructions from serial sections showed that one syncytiaj group contained at least 32 cells; several cells continued outside the series. The cells in a syncytium divide asynchronously; this results in an irregular, branched organization. The bridges may be either embedded in the cytoplasm of the cells, or they may form an extracellular connexion. INTRODUCTION Syncytial arrangement of oogonia and oocytes or spermatogonia and spermatocytes have been described in both vertebrates and invertebrates (e.g. Koch & King, 1966; Ruby, Dyer, Gasser & Skalko, 1970; Dym & Fawcett, 1971; King & Akai, 1971). In insects with meroistic ovaries (ovaries with nurse cells) the oocyte is connected to one or more nurse cells. The nurse cells feed RNA and possibly organelles into the oocyte and thereby facilitate the rapid development of the oocyte (Telfer, 1975). Insects with meroistic, polytrophic oogenesis have each oocyte with its attendant nurse cell(s) enveloped by a layer of follicle cells, which are thought to be of somatic origin (mesodermal). The oocyte and the nurse cells are interconnected by cytoplasmic bridges, which arise by incomplete cytokinesis (Telfer, 1975). In the polytrophic ovaries of mosquitoes the follicle cells of the ovariole divide from the time of emergence of the adult female until vitellogenesis is well under way (Laurence & Simpson, 1974). The enlarging nurse chamber is thus covered by an increasing number of follicle cells. Intercellular bridges have been found between the follicle cells in the mosquito Aedes aegypti and the stableflystomoxys caldtrans (Meola, MoUenhauer & Thompson, 1977), in the honeybee Apis mellifica (Ramamurty & Engels, 1977), and possibly in Drosophila immigrans (Mahowald, 1972). The present paper traces the formation of follicle cell syncytia in the mosquito, Culex pipiens quinquefasciatus, and shows some morphological aspects of bridge formation.
2 A. Fill MATERIALS AND METHODS The mosquitoes were reared at C. Larvae were fed dog pellets, and the adults maintained on a 5 % glucose/sucrose solution. After emergence the oocytes develop to a resting stage, and completion of oogenesis occurs only after a blood meal has been taken. The ovaries were dissected out in thefixative,2 % glutaraldehyde in 0-05 or 0-08 M phosphate buffer. They werefixedfor 2 h, washed, and postfixed in 1 % osmium tetroxide. After dehydration they were embedded in Epon. Fixation and embedding were done at room temperature. The reconstructions of follicle cell bridges were based on series of about 150 sections (30 h after emergence), and 300 sections (12 and 24 h after the blood meal). 20 h after emergence 12 h after blood 24 h after blood Fig. 1. Diagram of follicle cell syncytia. At 24 h after the blood meal there are no more cell divisions., extracellular bridge (as in Fig. 8); -*, bridge rims lie in the cytoplasm of one cell (arrows have the same polarity as in Fig. 2);, cell continues outside the series. RESULTS Follicle cell clusters At emergence of the adult female the oocytes are at pachytene. The flattened follicle cells barely cover the egg chambers, which each contain one oocyte and 7 nurse cells. Mitotic divisions occur among the follicle cells until about 20 h after the blood meal; at this time the oocytes are at diplotene and vitellogenesis is progressing rapidly. The frequency of mitotic divisions among the follicle cells was very low from emergence till the resting stage 3-4 days later (oocytes at late pachytene-early diplotene). Intercellular bridges in 3 follicle cell groups were traced at 30 h after emergence. Two groups consisted of 2 cells each, and one of 3 cells (Fig. 1). Many
3 . Mm Follicle cell bridges y c Fig h after the blood meal. Intercellular bridges (arrows) connect 5 follicle cells. d, dividing cell, x Fig h after the blood meal. Cell which has recently divided; the midbody (arrow) has started to form, c, chromatin; n, nucleolus. x
4 14<3 A. Fiil
5 Follicle cell bridges 141 cells at 10 h and 30 h after emergence had 2 bridges, indicating the presence of at least 3 interconnected cells. After the blood meal there is an increase in follicle cell divisions. Among the about 50 cells observed 12 h after the blood meal 2 were dividing, and several others had recently divided. These cells can be identified by their dense cytoplasm (Figs. 2, 7). Two complete cell clusters were traced. The clusters contained 6 and 8 cells respectively, which were arranged in linear order (Figs. 1, 2). In ovaries fixed 22 and 24 h after the blood meal the mitotic divisions among the follicle cells had ceased; several bridges still contained midbodies, which indicates that the bridges had recently formed (Fig. 5). One cell cluster traced at 24 h after the blood meal consisted of 32 cells; 7 of these continued outside the series, and it is likely that at least some of them were connected to new cells, making the cluster larger than the 32 cells observed. Among the 32 cells (7 of which may have additional bridges) there was one cell with 5 bridges, one with 4 bridges, 3 cells with 3 bridges, and the remaining had 1 or 2 bridges (Fig. 1). The 7 cells which continue outside the series comprise 3 groups containing 1, 2 and 4 cells (the cells marked with squares in Fig. 1). The groups are widely separated on the surface of the egg-chamber. The clusters observed at 30 h after emergence and at 12 h after the blood meal were located partly above the oocyte and partly above the nurse cells. The cells of the cluster observed 24 h after the blood meal were all located above the oocyte, which at this stage is larger than the 7 nurse cells combined. Bridge morphology A dividing follicle cell at telophase is shown in Fig. 3. The midbody (arrow) has just started to form; microtubules are embedded in the 2 chromosome masses through openings in the nuclear membranes. After the bridge is formed the midbody persists for some time (Figs. 4, 5), and then it disappears. For comparison a newly formed cystocyte bridge with remnants of the midbody is shown in Fig. 6. The diameter of the follicle cell bridges is /tm, whereas the cystocyte bridges are 2-4/tm (compare Figs. 5 and 6, which are at the same magnification). As indicated on Fig. 1 and shown in Figs. 2 and 4, many of the bridges have their rims entirely in the cytoplasm of one of the 2 interconnected cells. This type of bridge is seen most frequently (Fig. 1); when the bridge is not perpendicular to the plasma Fig h after the blood meal. Remnants (arrow) of the midbody are still present in the bridge, nu, nucleus, x Fig h after the blood meal. Extracellular bridge with midbody. nu, nucleus. x Fig h after emergence. Cystocyte bridge with remnants of the midbody (arrows), x Fig h after the blood meal. The bridge lies in the cytoplasm of 2 cells. The lower (darker) has recently divided, x Fig h after the blood meal. Microtubules are present in the bridge; one (arrowhead) is continuous with the bridge rim. nu, nucleus, x c E L 31
6 142 A. Fiil membranes the rim lies in the cytoplasm of both cells (Fig. 7). Finally the bridge may form an extracellular cytoplasmic connexion (Fig. 8). The mitotic divisions stop around 20 h after the blood meal and presumably no new bridges are formed after this time. The existing bridges contain ribosomes, a few microtubules, and sometimes rough or smooth endoplasmic reticulum. They remain unaltered for at least 30 h. During this time tritiated thymidine is incorporated by all the follicle cells and they are thus becoming polyploid. DISCUSSION Woodruff & Telfer (1973) showed that in the Cecropia moth an electrical gradient is present between the nurse cells and the oocyte, and that this gradient may contribute to the polarized transfer of material from the nurse cells into the oocyte. Functional differentiation also exists among the follicle cells: pinocytosis occurs at the oocyte surface towards the follicle cells (Roth & Porter, 1964; Anderson & Spielman, 1971), but not at the nurse cell surfaces, and the vitelline membrane and chorion are formed only above the oocyte, not above the nurse cells. Most of the material taken up pinocytotically by the oocyte is synthesized in the fat body (Hagedorn, 1974), but the follicle cells may contribute some proteins, as has been found in Cecropia (Anderson & Telfer, 1969). During early vitellogenesis all the follicle cells incorporate radioactive histidine and leucine (unpublished results), and the synthesized proteins may be transported through the bridges to the cells covering the oocyte, and subsequently transferred to the oocyte. Later, when the synthesis of the vitelline membrane begins, most of the 500 or more follicle cells (Laurence & Simpson, 1974) are associated with the oocyte, and it is unlikely that the few cells which are not could play an effective 'nurse' role. Thus the bridges may during some stages of oogenesis have the same function as the cystocyte bridges, and allow polarized transfer of material. The ovarioles are not rigid structures; they increase continuously in volume, and sections of them show that they are squeezed and deformed by neighbouring ovarioles. During the movements the follicle cells are variously stretched and squeezed, and when 2 interconnected cells pull apart the bridge may change from a cytoplasmic position (Fig. 7) to an extracellular one (Fig. 8). Similar variations in bridge morphology has been observed in the ovary of the mouse (Ruby, Dyer & Skalko, 1969). The bridges do not synchronize the mitotic divisions, as is obvious from the asymmetry of the cell cluster observed 24 h after the blood meal. Whether a cell goes through one or several divisions seems to be determined at the level of the particular cell. A similar asynchrony in cell divisions among interconnected cells was reported in the spermatogonia and spermatocytes of the rat (Moens & Hugenholtz, 1975). The bridges may facilitate the synchronization of other events, such as the switch from mitotic divisions to polyploidization and the almost simultaneous start of vitelline membrane synthesis. It seems, though, that these functions might be regulated through communicating junctions (Mahowald, 1972).
7 Follicle cell bridges 143 REFERENCES ANDERSON, L. M. & TELFER, W. H. (1969). A follicle cell contribution to the yolk spheres of moth oocytes. Tissue & Cell 1, ANDERSON, W. A. & SPIHLMAN, A. (1971). Permeability of the ovarian follicle of Aedes aegypti mosquitoes. J. Cell Biol. 50, DYM, M. & FAWCETT, D. W. (1971). Further observations on the numbers of spermatogonia, spermatocytes, and spermatids connected by intercellular bridges in the mammalian testis. Biol. Reprod. 4, HAGEDORN, H. H. (1974). The control of vitellogenesis in the mosquito, Aedes aegypti. Am. Zool. 14, KING, R. C. & AKAI, H. (1971). Spermatogenesis in Bombyx mori. I. The canal system joining sister spermatocytes. J. Morph. 134, KOCH, E. A. & KING, R. C. (1966). The origin and early differentiation of the egg chamber of Drosophila melanogaster. J. Morph. 119, LAURENCE, B. R. & SIMPSON, M. G. (1974). Cell replication in the follicular epithelium of the adult mosquito. J. Insect Physiol. 20, MAHOWALD, A. P. (1972). Ultra8tructural observations on oogenesis in Drosophila. J. Morph MEOLA, S. M., MOLLENHAUER, H. H. & THOMPSON, J. M. (1977). Cytoplasmic bridges within the follicular epithelium of the ovarioles of two Diptera, Aedes aegypti and Stomoxys calcitrans. J. Morph. 153, MOENS, P. B. & HUGENHOLTZ, A. D. (1975). The arrangement of germ cells in the rat seminiferous tubule: An electron-microscope study. J. Cell Sci. 19, RAMAMURTY, P. S. & ENGELS, W. (1977). Occurrence of intercellular bridges between follicle epithelial cells in the ovary of Apis mellifica queens. J. Cell Sci. 24, ROTH, T. F. & PORTER, K. R. (1964). Yolk protein uptake in the oocyte of the mosquito Aedes aegypti L. J. Cell Biol. ao, RUBY, J. R., DYER, R. F., GASSER, R. F. & SKALKO, R. G. (1970). Intercellular connections between germ cells in the developing human ovary. Z. Zellforsch. mikrosk. Anat. 105, RUBY, J. R., DYER, R. F. & SKALKO, R. G. (1969). The occurrence of intercellular bridges during oogenesis in the mouse. J. Morph. 127, TELFER, W. H. (1975). Development and physiology of the oocyte-nurse cell syncytium. In Advances in Insect Physiology, vol. 11 (ed. J. E. Trehene, M. J. Berridge & V. B. Wigglesworth), pp London, New York and San Francisco: Academic Press. WOODRUFF, R. I. & TELFER, W. H. (1973). Polarized intercellular bridges in ovarian follicles of the Cecropia moth. J. Cell Biol. 58, (Received 10 October 1977)
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