Skip to main content
Log in

Electrically mediated protein movement inDrosophila follicles

  • Published:
Roux's archives of developmental biology Aims and scope Submit manuscript

Summary

Distribution of rhodamine-conjugated lysozyme injected into the sixteen-cell syncytium comprising the germ-line portion of theDrosophila follicle is shown to be affected by charge. Positive molecules are able to migrate through intercellular bridges from the oocyte to the nurse cells, but are unable to migrate detectably from nurse cells to the oocyte. Their negatively charged counterparts can move from the nurse cells to the oocyte, but are unable to traverse the intercellular bridges in the counter direction. This charge-dependent movement of molecules is accompanied by an electrical potential difference, focused across the nurse cell-oocyte bridges, which makes the nurse cells negatively charged to the oocyte. The addition of insect hemolymph to the physiological salt solution in which the experiments were performed resulted in only a small increase in the transmembrane resistance, but enhanced the potential difference between oocyte and nurse cells from 0.2±0.3 (SE) mV (nurse cells negative) to 2.3±0.45 (SE) mV (nurse cells negative).

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

  • Bohrmann J, Heinrich UR, Dorn A, Sander K, Gutzeit HO (1984) Electrical phenomena and their possible significance in vitellogenic follicles ofDrosophila melanogastor. J Embryol Exp Morph 8 [Suppl]: 151

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Bohrmann J, Gutzeit HO (1987) Evidence against electrophoresis as the principal mode of protein transport in vitellogenic follicles ofDrosophila. Development 101: 279–288

    PubMed  CAS  Google Scholar 

  • Bohrmann J, Huebner E, Sander K, Gutzeit HO (1986b) Intercellular electrical potential measurements inDrosophila follicles. J Cell Sci 81: 207–221

    PubMed  CAS  Google Scholar 

  • Chino H (1985) Lipid transport: biochemistry of hemolymph lipophorin. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry ans pharmacology, vol 10. Pergamon Press, Oxford, pp 115–135

    Google Scholar 

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

    Article  Google Scholar 

  • Gutzeit HO (1986) Transport of molecules and organelles in meroistic ovarioles in insects. Differentiation 31: 155–165

    CAS  Google Scholar 

  • Hoffman R, Gross L (1975) Modulation contrast microscope. Appl Optics 14: 1169–1176

    Article  Google Scholar 

  • Huebner E, Sigurdson W (1986) Extracellular currents during insect oogenesis: special emphasis on telotrophic ovarioles. In: Nuccitelli R (ed) Ionic currents in development. AR Liss, New York, pp 155–163

    Google Scholar 

  • Huebner E, Woodruff RI, Telfer WH 1980 Electrophysiological and structural aspects of nurse cell-oocyte interaction in the telotrophic ovarioles ofRhodinus prolixus. Am. Zool 20: 867

    Google Scholar 

  • Inoue S (1986) Video microscopy. Plenum Press, New York, p 584

    Google Scholar 

  • Jaffe LF (1969) On the centripetal course of development, theFucus egg, and self-electrophoresis. Dev Biol [Suppl 3]: 83–111

    Google Scholar 

  • Jaffe LF, Nuccitelli R (1974) An ultrasensitive vibrating probe for measuring steady extracellular current. J Cell Biol 63: 614–628

    Article  PubMed  CAS  Google Scholar 

  • Jaffe LF, Overall R (1985) Patterns of ionic current throughDrosophila follicles and eggs. Dev Biol 108: 102–119

    Article  PubMed  Google Scholar 

  • Jaffe LF, Woodruff RI (1977) Electrical current patterns through developingCecropia follicles. J Cell Biol 75: 23a

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Kiehart DP (1981) Microinjections ofEchinoderm eggs. Apparatus and procedure. In: Wilson L (ed) Methods and perspectives in cell biology. The cytoskeleton, vol, 25 part B, biological systems and functional methods. Academic Press, Orlando, pp 13–31

    Google Scholar 

  • King RC, Buning J (1983) The origin and functioning of insect oocytes and nurse cells. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology biochemistry and pharmacology. Pergamon Press, New York

    Google Scholar 

  • Kunkel JG (1986) Dorsoventral currents are associated with vitellogenesis inCockroach ovarioles. In: Nuccitelli R (ed) Ionic currents in Development. AR Liss, New York, pp 165–172

    Google Scholar 

  • Munz A, Dittmann F (1988) Voltage gradient and microtubules both involved in intracellular protein and mitochondira transport in the telotrophic ovarioles ofDysdercus intermedius. Roux's Arch Dev Biol (in press)

  • Robb JA (1969) Maintenance of imiginal dises ofDrosophila melanogaster in chemically defined media. J Cell Biol 44: 876–884

    Article  Google Scholar 

  • Sun YA, Wyman RJ (1987) Lack of an oocyte to nurse cell voltage difference inDrosophila. Neurosci 13: 1139

    Google Scholar 

  • Telfer WH (1975) Development and physiology of the oocyte-nurse cell syncytium. Insect Physiol 11: 223–319

    Article  Google Scholar 

  • Telfer WH, Woodruff RI, Hucbner E (1981) Electrical polarity and cellular differentiation in meroistic ovaries. Am Zool 21: 675–686

    Google Scholar 

  • Verachtert B, De Loof A (1986) Electrical fields around the polytrophic ovarian follicles ofSarcophga bullata and the panoistic folliclesLocusta migratoria. In: Nuccitelli R (ed) Tonic currents in development. AR Liss, New York, pp 173–179

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Woodruff RI, Telfer WH (1973) Polarized intercellular bridges in ovarian follicles of theCecropia moth. J Cell Biol 58: 172–188

    Article  PubMed  CAS  Google Scholar 

  • Woodruff RI, Telfer WH (1974) Electrical properties of ovarian cells linked by intercellular bridges. NY Aca Sci 238: 408–419

    CAS  Google Scholar 

  • Woodruff RI, Telfer WH (1980) Electrophoresis of proteins in intercellular bridges. Nature 286: 84–86

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Woodruff RI, Huebner E, Telfer WH (1986a) Electrical properties of insect ovarian follicles: some challenges of a multicellular system. In: Nuccitelli R (ed) Tonic currents in development. AR Liss, New York, pp 147–154

    Google Scholar 

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

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Supported by NSF Grant # DB-18617

Rights and permissions

Reprints and permissions

About this article

Cite this article

Woodruff, R.I., Kulp, J.H. & LaGaccia, E.D. Electrically mediated protein movement inDrosophila follicles. Roux’s Arch Dev Biol 197, 231–238 (1988). https://doi.org/10.1007/BF02439430

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02439430

Key words

Navigation