Skip to main content
Log in

Heterologous gap junctions between oocytes and follicle cells of an insect, Dysdercus intermedius, and their potential role as ion current pathways

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

In telotrophic insect ovaries, the oocytes develop in association with two kinds of supporting cells. Each ovary contains five to seven ovarioles. An ovariole consists of a single strand of several oocytes. At the apex of each ovariole is a syncytium of nurse cells (the tropharium), which connects by strands of cytoplasm (the trophic cords) to four or more previtellogenic oocytes. In addition, each oocyte is surrounded by an epithelium of follicle cells, with which it may form gap junctions. To study the temporal and spatial patterns of these associations, Lucifer yellow was microinjected into ovaries of the red cotton bug, Dysdercus intermedius. Freeze-fracture replicas were examined to analyze the distribution of gap junctions between the oocyte and the follicle cells. Dye-coupling between oocytes and follicle cells was detectable early in previtellogenesis and was maintained through late vitellogenesis. It was restricted to the lateral follicle cells. The anterior and posterior follicle cells were not dye-coupled. Freeze-fracture analysis showed microvilli formed by the oocyte during mid-previtellogenesis, and the gap junctions became located at the tips of these. As the microvilli continued to elongate until late vitellogenesis, gap junction particles between them and follicle cell membranes became arranged in long arrays. The morphological findings raise questions about pathways for the intrafollicular phase of the ion currents known to surround the previtellogenic and vitellogenic growth zones of the ovariole.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abu-Hakima R, Davey KG (1975) Two actions of juvenile hormone on the follicle cells of Rhodnius prolixus. Can J Zool 53:1187–1188

    Google Scholar 

  • Amsterdam A, Josephs R, Liebermann ME, Lindner HR (1976) Organization of intramembrane particles in freeze-cleaved gap junctions of rat Graafian follicles: optical-diffraction analysis. J Cell Sci 21:93–105

    Google Scholar 

  • Anderson E, Albertini DF (1976) Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J Cell Biol 71:680–686

    Google Scholar 

  • Bardele CF (1983) Mapping of highly ordered membrane domains in the plasma membrane of Cyclidium glaucoma. J Cell Sci 61:1–30

    Google Scholar 

  • Bilinski SM, Hage JW, Bluemink JG (1985) Gap junctions between the follicle cells and the oocyte during oogenesis in an insect, Tribolium destructor/Coleoptera. Roux's Arch Dev Biol 194:296–300

    Google Scholar 

  • Bohrmann J, Dorn A, Sander K, Gutzeit H (1986) The extracellular electrical current pattern and its variability in vitellogenic Drosophila follicles. J Cell Sci 81:189–206

    Google Scholar 

  • Brink PR (1985) The effects of deuterium oxide on junctional membrane permeability and conductance. In: Bennett MVL, Spray DC (eds) Gap junctions. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp 123–138

    Google Scholar 

  • Brower PT, Schultz RM (1982) Intercellular communication between granulosa cells and mouse oocytes: existence and possible nutritional role during oocyte growth. Dev Biol 90:144–153

    Google Scholar 

  • Dittmann F, Ehni R, Engels W (1981) Bioelectric aspects of the hemipteran telotrophic ovariole (Dysdercus intermedius). Roux's Arch Dev Biol 190:221–225

    Google Scholar 

  • Gilula NB, Epstein ML, Beers WH (1978) Cell-to-cell communication and ovulation: a study of the cumulus cell-oocyte complex. J Cell Biol 78:58–75

    Google Scholar 

  • Huebner E (1984) Developmental cell interactions in female insect reproductive organs. In: Engels W, Clark WH jr, Fischer A, Oliver PJW, Went DF (eds) Advances in invertebrate reproduction, vol 3. Elsevier Science, Amsterdam, pp 97–105

    Google Scholar 

  • Huebner E, Injeyan HC (1980) Patency of the follicular epithelium in Rhodnius prolixus. A re-examination of the hormone response and technique refinement. Can J Zool 58:1617–1625

    Google Scholar 

  • Huebner E, Injeyan HC (1981) Follicular modulation during oocyte development in an insect: formation and modification of septate and gap junctions. Dev Biol 83:101–113

    Google Scholar 

  • Jaffe LF, Woodruff RI (1979) Large electrical currents traverse developing Cecropia follicles. Proc Natl Acad Sci USA 76:1328–1332

    Google Scholar 

  • Münz A, Dittmann F (1987) Voltage gradients and microtubules both involved in intercellular protein and mitochondria transport in the telotrophic ovariole of Dysdercus intermedius. Roux's Arch Dev Biol 196:391–396

    Google Scholar 

  • Overall R, Jaffe LF (1984) Patterns of ionic currents through Drosophila follicles and eggs. Dev Biol 108:102–119

    Google Scholar 

  • Sheridan JD, Hammer-Wilson M, Pruns D, Johnson RG (1978) Quantitative analysis of low-resistance junctions between cultured cells and correlation with gap-junctional areas. J Cell Biol 76:532–544

    Google Scholar 

  • Spray DC, White RL, Verselis V, Bennett MVL (1985) General and comparative physiology of gap junction channels. In: Bennett MVL, Spray DC (eds) Gap junctions. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp 139–153

    Google Scholar 

  • Stewart WW (1978) Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 14:741–759

    Google Scholar 

  • Verachtert B, De Loof A (1986) Electrical fields around the polytrophic ovarian follicles of Sarcophaga bullata and the panoistic follicles of Locusta migratoria. In: Nucitelli R (ed) Ionic currents in development. Liss, New York, pp 173–179

    Google Scholar 

  • Wollberg Z, Cohen E, Kalina N (1976) Electrical properties of developing oocytes of the migratory locust, Locusta migratoria. J Cell Physiol 88:145–158

    Google Scholar 

  • Woodruff RI (1979) Electrotonic junctions in Cecropia moth ovaries. Dev Biol 69:281–295

    Google Scholar 

  • Woodruff RI, Anderson KL (1984) Nutritive cord connection and dye-coupling of the follicular epithelium to the growing oocytes in the telotrophic ovarioles in Oncopeltus fasciatus, the milk-weed bug. Roux's Arch Dev Biol 193:158–163

    Google Scholar 

  • Woodruff RI, Huebner E, Telfer WH (1986) Ion currents in Hyalophora ovaries: the role of the epithelium and the intercellular spaces of the trophic cap. Dev Biol 117:405–416

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Supported by the Deutsche Forschungsgemeinschaft (Schwerpunkt Differenzierung)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Münz, A. Heterologous gap junctions between oocytes and follicle cells of an insect, Dysdercus intermedius, and their potential role as ion current pathways. Cell Tissue Res. 252, 147–155 (1988). https://doi.org/10.1007/BF00213836

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00213836

Key words

Navigation