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Localisation of potassium pumps in Drosophila ovarian follicles

Published online by Cambridge University Press:  26 September 2008

Johannes Bohrmann  and
Ulf-Rüdiger Heinrich
Johannes Bohrmann*
Affiliation:
Institut für Biologie I, University of Freiburg, and HNO-Klinik, University of Mainz, Germany.
Ulf-Rüdiger Heinrich
Affiliation:
Institut für Biologie I, University of Freiburg, and HNO-Klinik, University of Mainz, Germany.
*
J. Bohrmann, Institut für Biologie I (Zoologie), Universität Freiburg, Albertstrasse 21a, D-79104 Freiburg, Germany. Tel: 0761/2032583. Fax: 0761/2032596.
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Summary

It has been shown previously that, in Drosophila oogenesis, potassium ions are important for bioelectric phenomena as well as for other physiological and development processes. In the present study we determined the spatial distribution and activity of the (Na+, K+)-pump and of ouabain-insensitive K+ pumps in plasma membranes of vitellogenic ovarian follicles (stage 10). We used that light micorscopic anthroylouabain method as well as the cytochemical lead and cerium precipitation methods in combination with electron spectroscopic imaging (ESI) and elelctronm energy-loss spectroscopy (EELS). (Na+, K+)-ATPase activity was predominantly observed on the oolemma as well as on the membranes of the columnar follicle cells covering the oocyte, whereas on the membranes of the nurse cells and of the squamous follicle cells covering the nurse cells the activity was vary low. The highset activity of the (Na+ K+)-pump was found at the anterior and posterior ends of the oocute, and this on the oolemma as well as on the membranes of the follicle cells located here. Strong activity of ouabain-insensitive K+-pumps was observed on most of the oolemma (except at the anterior of the oocyte) and on the membranes of some nurse cells located next to the oocyte, whereas less activity was found on the other nurse cell membranes and on the membranes of all follicle cells. The suitability of the differnet methods nurse cell membranes and on the membrances of all follicle cells. The suitability of th different methods used for determining the localisation as well as the activity of K+-pumps is discussed. We further discuss the nature of the ouabain-insensitive K+ pumps and the relevance of the observed distribution of K+-pumps for K+ uptake, extrafollicular ionic current flow intercelluar signalling and other developmental processes in Drosophila oogenesis.

Keywords

AnthroylouabainElectron spectroscopic imaging (ESI)Ionic currentsNa+, K+-ATPaseOogenesis
Type
Article
Information
Zygote , Volume 2 , Issue 3 , August 1994 , pp. 189 - 200
Copyright
Copyright © Cambridge University Press 1994

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References

Al-Awqati, Q. (1986). Proton-translocating ATPases. Annu Rev. Cell Biol. 2 179–99.CrossRefGoogle ScholarPubMed
Bauer, R. (1988). Electron spectroscopic imaging: an advanced technique for imaging and analysis in transmission electron microscapy. In Methods in Microbiology vol. 20, ed. Meyer, F., pp. 113–46. New York: Academic Press.Google Scholar
Bohrmann, J.. (1991 a). In vitro culture of Drosophila ovarian follicles: the influence of different media on development, RNA synthesis, protein synthesis and potassium uptake. Rouxs Arch. Dev Bio. 199, 315–26.CrossRefGoogle ScholarPubMed
Bohrmann, J. (1991 b). Potassium uptake into Drosophila ovarian follicles relevance to physiological and developmental processes. J. Insect Physiol. 37, 937–46.CrossRefGoogle Scholar
Bohrmann, J. (1993). Antisera against a channel-forming 16 kDa protein inhibit dye-coupling and bind to cell membranes in Drosophila ovarian follicles. J. Cell Sci. 105, 513–18.CrossRefGoogle ScholarPubMed
Bohrmann, J. & Gutzeit, H.O. (1987). Evidence against electrophoresis as the principal mode of protein transport in vitellogenic ovarian follicles of Drosophila. Development 101, 279–88.CrossRefGoogle ScholarPubMed
Bohrmann, J. & Haas-Assenbaum, A. (1993). Gap junctions in ovarian follicles of Drosophila melanogaster: inhibition and promotion of dye-coupling between oocyte and follicle cells. Cell Tissue Res. 273, 163–73.CrossRefGoogle ScholarPubMed
Bohrmann, J., Dorn, A., Sander, K. & Gutzeit, H.O. (1986 a). The extracellular electrical current pattern and its variability in vitellogenic Drosophila follicles. J. Cell. Sci. 81, 189–206.CrossRefGoogle ScholarPubMed
Bohrmann, J., Huebner, E., Sander, K. & Gutzeit, H.O. (1986 b). Intracellular electrical potential measurements in Drosophila follicles. J. Cell. Sci. 81, 207–21.CrossRefGoogle ScholarPubMed
Buultjens, T.E.J., Finbow, M.E., Lane, N.J. & Pitts, J.D. (1988). Tissue and species conservation of the vertebrate and anthropod forms of the low molecular weight (16–18 000) proteins of gap junctions. Cell Tissue Res. 251, 571–80.CrossRefGoogle Scholar
Chao, A.C., Koch, A.R. & Moffett, D.F. (1990). Basal membrane uptake in potassium-secreting cells of midgut of tobacco hornworm (Manduca sexta). Am. J. Physiol. 258, R112–19.Google ScholarPubMed
Ernst, S.A. & Hootman, S.R. (1981). Microscopical methods for the localization of (Na+, K+)-ATPase. Histochem. J. 13, 397–418.CrossRefGoogle ScholarPubMed
Finbow, M.E. & Meagher, L. (1992). Connexins and the vacuolar proteolipid-like 16-kDa protein are not directly associated with each other but may be components of similar or the same gap junctional complexes. Exp. Cell Res. 203, 280–4.CrossRefGoogle ScholarPubMed
Finbow, M.E., Thompson, P., Keen, J., Jackson, P., Eliopoulos, E.E., Meagher, L. & Findlay, J.B.C. (1990). A structural analysis of the gap junctional channel and the 16K protein. In Parallels in Cell to Cell Junctions in Plants and Animals. NATO ASI series, vol. H46, ed. Robards, A.W., Lucas, W.J., Pitts, J.D., Jongsma, H.J. & Spray, D.C., pp. 13–19. BerlinSpringer.CrossRefGoogle Scholar
Findlay, J.B.C., Eliopoulos, E.E. & Finbow, M.E. (1990). Molecular modelling of integral membrane proteins. Biochem. Soc. Trans. 18, 838–40.CrossRefGoogle ScholarPubMed
Fortes, P.A.G. (1977). Anthroylouabain: a specific fluorescent probe for the cardiac glycoside receptor. Biochemistry 16, 531–40.CrossRefGoogle ScholarPubMed
Hawkins, E. & O'Donnell, M.J. (1992). Regulation of ooplasmic sodium and potassium activities in developing locust eggs. Arch. Insect Biochem. Physiol. 20, 23–34.CrossRefGoogle Scholar
Heinrich, U.-R & Gutzeit, H.O. (1985). Characterization of cation-rich follicle cells in vitellogenic follicles of Drosophila melanogaster. Differentiation 28, 237–43.CrossRefGoogle Scholar
Heinrich, U.-R, Gutzeit, H.O. & Kreutz, W. (1991 a). Elemental composition of pyroantimonate precipitates analysed by electron spectroscopic imaging (ESI) and electron energy-loss spectroscopy (EELS) in vitellogenic ovarian follicles of Drosophila. J. Microscopy. 162, 123–32.CrossRefGoogle ScholarPubMed
Heinrich, U.-R, Maurer, J., Mann, W. & Kreutz, W.. (1991 b). Progress in electron microscopic diagnostics: semi-quantitative determination of precipitable calcium in different cell types of the organ of Corti in the guinea-pig. J. Microscopy. 162, 133–40.CrossRefGoogle ScholarPubMed
Hille, B. (1984). Ionic Channels of Excitable Membranes. Sunderland: Sinauer.Google Scholar
Horisberger, J.-D, Lemas, V., Kraehenbühl, J.-P. & Rossier, B.C. (1991). Structure-function relationship of Na,K-ATPase. Annu. Rev. Physiol. 53, 565–84.CrossRefGoogle ScholarPubMed
Huebner, E. & Sigurdson, W. (1986). Extracellular currents during insect oogenesis: special emphasis on telotrophic ovarioles. Prog. Clin. Biol. Res. 20, 155–63.Google Scholar
Ilenchuk, T.T. & Davey, K.G. (1987). Effects of various compounds on Na/K-ATPase activity, JH I binding capacity and patency response in follicles of Rhodnius prolixus. Insect Biochem. 17, 1085–8.CrossRefGoogle Scholar
Inoué, S. (1986). Video Microscopy. New York: Plenum Press.CrossRefGoogle Scholar
King, R.C. (1970). Ovarian Development in Drosophila melanogaster. New York: Academic Press.Google Scholar
Klein, U. (1992). The insect V-ATPase, a plasma membrane proton pump energizing secondary active transport: immunological evidence for the occurrence of a V-ATPase in insect ion-transporting epithelia. J. Exp. Biol. 172, 345–54.CrossRefGoogle ScholarPubMed
Klein, U., Löffelmann, G. & Wieczorek, H. (1991). The midgut as a model system for insect K+-transporting epithelia: immunocytochemical localization of a vacuolartype H+ pump. J. Exp. Biol. 161, 61–75.CrossRefGoogle Scholar
Klein, U., Löffelmann, G. & Wieczorek, H. (1991). The midgut as a model system for insect K+-transporting epithelia: immunocytochemical localization of a vacuolartype H+ pump. J. Exp. Biol. 161, 61–75.CrossRefGoogle Scholar
Komnick, H. & Achenbach, U. (1979). Comparative biochemical, histochemical and autoradiographic studies of Na+/K+-ATPase in the rectum of dragonfly larvae (Odonata, Aeshnidae). Eur. J. Cell Biol. 20, 92–100.Google ScholarPubMed
Körtje, K.H., Freihöfer, D. & Rahmann, H. (1990). Cytochemical localization of high-affinity Ca2+-ATPase activity in synaptic terminals. J. Histochem. Cytochem. 38, 895–900.CrossRefGoogle ScholarPubMed
Körtje, K.H., Körtje, D. & Rahmann, H. (1991). The application of energy-filtering electron microscopy for the cytochemical localization of Ca2+-ATPase activity in synaptic terminals. J. Microscopy. 162, 105–14.CrossRefGoogle ScholarPubMed
Lebovitz, R.M., Takeyasu, K. & Fambrough, D.M. (1989). Molecular characterization and expression of the (Na++ K+)-ATPase alpha subunit in Drosophila melanogaster. EMBO. J. 8, 193–202.CrossRefGoogle ScholarPubMed
Mayahara, H., Fujimoto, K., Ando, H. & Ogawa, K. (1980). A new one-step method for the cytochemical localization of ouabain-sensitive, potassium-dependent p-nitrophenyl-phosphatase activity. Histochemistry 67, 125–38.CrossRefGoogle Scholar
McCormick, S.D. (1990). Fluorescent labelling of (Na+, K+)-ATPase in intact cells by use of a fluorescent derivative of ouabain: salinity and teleost chloride cells. Cell Tissue Res. 260, 529–33.CrossRefGoogle ScholarPubMed
Miledi, R. & Woodward, R.M. (1989). Effects of defolliculation on membrane current responses of Xenopus oocytes. J. Physiol. (Lond.) 416, 601–21.CrossRefGoogle ScholarPubMed
Miyazaki, S. & Hagiwara, S. (1976). Electrical properties of the Drosophila egg membrane. Dev. Biol. 53, 91–100.CrossRefGoogle ScholarPubMed
Moczydlowski, E.G. & Fortes, P.A.G. (1980). Kinetics of cardiac glycoside binding to sodium, potassium adenosine triphosphatase studied with a fluorescent derivative of ouabain. Biochemistry 19, 969–77.CrossRefGoogle ScholarPubMed
O'Donnell, M.J. (1988). Potassium channel blockers unmask electrical excitability of insect follicles. J. Exp. Zool. 245, 137–43.CrossRefGoogle Scholar
Ogawa, K.S., Fujimoto, K. & Ogawa, K. (1987). Cytochemical localization of Ca++-ATPase, H+, K+-ATPase and Na+, K+-ATPase in acid-secreting parietal cell and non-secreting parietal cell. Acta Histochem. Cytochem. 20, 197–216.CrossRefGoogle Scholar
Overall, R. & Jaffe, L.F. (1985). Patterns of ionic current through Drosophila follicles and eggs. Dev. Biol. 108, 102–19.CrossRefGoogle ScholarPubMed
Reimer, L. (1989). Transmission Electron Microscopy. Berlin: Springer.CrossRefGoogle Scholar
Robb, J.A. (1969). Maintenance of imaginal discs of Drosophila melanogaster in chemically defined media. J. Cell Biol. 41, 876–85.CrossRefGoogle ScholarPubMed
Robinson, J.M. & Karnovsky, M.J. (1983). Ultrastructural localization of several phosphatases with cerium. J. Histochem. Cytochem. 31, 1197–208.CrossRefGoogle ScholarPubMed
Russell, V.E.W., Klein, U., Reuveni, M., Spaeth, D.D., Wolfersberger, M.G. & Harvey, W.R. (1992). Antibodies to mammalian and plant V-ATPases cross react with the V-ATPase of insect cation-transporting plasma membranes. J. Exp. Biol. 166, 131–43.CrossRefGoogle ScholarPubMed
Shotton, D.M. (1988). Review: video-enhanced light microscopy and its applications in cell biology. J. Cell Sci. 89, 129–50.CrossRefGoogle ScholarPubMed
Singleton, K. & Woodruff, R.I.. (1994). The osmolarity of adult Drosophila hemolymph and its effect on oocyte-nurse cell electrical polarity. Dev. Biol. 161, 154–67.CrossRefGoogle ScholarPubMed
Skobis, E. & Bereiter-Hahn, J.. (1991). Inhibition of the Na/K-ATPase by levamisole. Naturwissenschaften 78, 226–29.CrossRefGoogle ScholarPubMed
St Johnston, D. & Nüsslein-Volhard, C. (1992). The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201–19.CrossRefGoogle ScholarPubMed
Sun, Y.-A. & Wyman, R.J. (1989). The Drosophila egg chamber: external ionic currents and the hypothesis of electrophoretic transport. Biol. Bull. (Suppl.) 176, 79–85.CrossRefGoogle ScholarPubMed
Sun, Y.-A & Wyman, R.J. (1993). Re-evaluation of electrophoresis in the Drosophila egg chamber. Dev. Biol. 155, 206–15.CrossRefGoogle Scholar
Supplisson, S., Kado, R.T. & Bergman, C. (1991). A possible Na/Ca exchange in the follicle cells of Xenopus oocyte. Dev. Biol. 145, 231–40.CrossRefGoogle ScholarPubMed
Wieczorek, H. (1992). The insect V-ATPase, a plasma membrane proton pump energizing secondary active transport: molecular analysis of electrogenic potassium transport in the tobacco hornworm midgut. J. Exp. Biol. 172, 335–43.CrossRefGoogle ScholarPubMed
Woodruff, R.I. (1989). Charge-dependent molecular movement through intercellular bridges in Drosophila follicles. Biol. Bull. (Suppl.) 176, 71–8.CrossRefGoogle ScholarPubMed
Woodruff, R.I., Kulp, J.H. & La Gaccia, L.D. (1988). Electrically mediated protein movement in Drosophila follicles. Rouxs Arch. Dev. Biol. 197, 231–8.CrossRefGoogle Scholar
Yoda, A. & Yoda, S. (1988). Interaction between ouabain and the phosphorylated intermediate of Na, K-ATPase. Mol. Pharmacol. 22, 700–8.Google Scholar