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Water permeability properties of the ovarian oocytes from Bufo arenarum and Xenopus laevis: A comparative study

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Abstract

The water permeability properties of ovarian oocytes from Xenopus laevis and Bufo arenarum, a toad species found in the Buenos Aires region, were studied. We report that: (i) the water osmotic permeability (P f, cm/sec × 10−4) was significantly higher in Bufo (6°C=12.3±2.4; 18°C = 20.8±4.8) than in Xenopus oocytes (6°C=5.3±0.3; 18°C=6.2±1.6). The corresponding water diffusion permeability values (P d, cm/sec × 10−4) were: Xenopus = 2.3±0.3 (6°C) and 4.8±0.7 (18°C); Bufo=2.7±0.4 (6°C) and 6.0 ±0.5 (18°C). (ii) Amphotericin B increased the P f and P d values. The observed ΔP fΔP d ratio was not significantly different from the expected results (n=3), after amphotericin B incorporation in both species. This means that the influence of unstirred layers and other potential artifactual compounds did not significantly affect our experimental results, (iii) Preincubation with gramicidin during 12 hr induced a clear increase in the oocyte volume. After that, a hypotonic shock only slightly increased the oocyte volume. Conversely, a hypertonic challenge induced a volume change significantly higher than the one observed in control conditions, (iv) Mercury ions did not affect the osmotic permeability in Xenopus oocytes but clearly inhibited, in a reversible way, the osmotic permeability in oocytes from B. arenarum. (v) Mercury ions did not reduce P d values in either species, (vi) The ΔP fΔP d values calculated from the differences observed in these parameters between both species were 11.9±5.1 at 18°C and 15.5±2.4 at 6°C. These numbers are similar to those previously reported in the case of membranes having water channels. From these results, we propose that water channels are present in the ovarian oocyte from B. arenarum but not in the ovarian oocyte from X. laevis.

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References

  1. Bourguet, J., Chevalier, J., Parisi, M. 1981. On the role of intramembranes particle aggregates in the hydrosmotic action of antidiuretic hormone. In: Water Transport across Epithelia. A. Benzon Symposium 15, pp. 404–421. Munsksgaard, Copenhagen

    Google Scholar 

  2. Bourguet, J., Chevalier, J., Parisi, M., Ripoche, P. 1990. Water permeability of amphibian urinary bladder. In: Water Transport in Biological Membranes. G. Benzon, editor. Vol. II, pp 169–196. CRC, Boca Raton, FL

    Google Scholar 

  3. Cass, A., Finkelstein, A. 1967. Water permeability of thin lipid membranes. J. Gen. Physiol. 50:1965–1984

    Google Scholar 

  4. Dascal, N. 1987. The use of Xenopus oocytes for the study of ion channels. CRC Crit. Rev. Biochem. 22:317–373

    Google Scholar 

  5. Fettiplace, R., Haydon, D.A. 1980. Water permeability of lipid membranes. Physiol. Rev. 60:510–550

    Google Scholar 

  6. Finkelstein, A. 1974. Aqueous pores created in thin lipid membranes by the antibiotics nystatin, amphotericin B and gramicidin A: implication for pores in plasma membranes. In: Drugs and Transport Processes. B.A. Collingham, editor, pp. 241–250. Macmillan, London

    Google Scholar 

  7. Finkelstein, A. 1987. Water movement through lipid bilayers, pores and plasma membranes. Theory and reality. In: Distinguished Lecture Series of the Society of General Physiologists. Vol. 4. Wiley, New York

    Google Scholar 

  8. Fushimi, K., Uchida, S., Hara, Y., Hirata, Y., Marumo, F., Sasaki, S. 1993. Cloning and expression of apical membrane water channel of rat kidney collecting tubule. Nature 361:549–552

    Article  CAS  PubMed  Google Scholar 

  9. Gould, G.W., Lienhard, G.E. 1989. Expression of a functional glucose transporter in Xenopus oocytes. Biochemistry 28:9447–9452

    Google Scholar 

  10. Harris, H.W., Wade, J.B., Handler, J.S. 1988. Identification of specific apical membrane polypeptides associated with the antidiuretic hormone elicited water permeability increase in the toad urinary bladder. Proc. Natl. Acad. Sci. USA 85:1942–1946

    Google Scholar 

  11. Hays, R.M., Franki, N., Soberman, R. 1971. Activation energy for water diffusion across the toad bladder. J. Clin. Invest. 50:1016–1021

    Google Scholar 

  12. Hediger, M.A., Coday, M.J., Ikeda, T.S., Wright, E.M. 1987. Expression cloning and cDNA sequencing of the Na+/glucose cotransporter. Nature 330:379–381

    Google Scholar 

  13. Hoch, B.S., Gorfien, P.C., Linzer, D., Fusco, M.J., Levine, S.D. 1989. Mercurial reagents inhibit water flow through ADH induced water channels in toad bladder. Am J Physiol. 256:F948-F953

    Google Scholar 

  14. Levine, S.D., Jacoby, M., Finkelstein, A. 1984. The water permeability of toad urinary bladder: II. The value of Pf/Pd (w) for the antidiuretic hormone induced water permeation pathway. J. Gen. Physiol. 83:543–561

    Google Scholar 

  15. Macey, R.I., Karan, D.M., Farmer, R.E.L. 1972. Properties of water channels in human red cells. In: Biomembranes, Vol. 3: Passive Permeability of Cell Membranes. F. Kreuzer and J.F.G. Siegers, editors, pp. 331–340. Plenum, New York

    Google Scholar 

  16. Mayer, M.M., Verkman, A.S. 1987. Evidence for water channels in proximal tubule cell membranes. J. Membrane Biol. 96:107–119

    Google Scholar 

  17. Mild, K.H., Lovtrup, S. 1985. Movement and structure of water in animal cells. Ideas and experiments. Biochim. Biophys. Acta 822:155–167

    Google Scholar 

  18. Parisi, M., Bourguet, J. 1983. The single file hypothesis and the water channels induced by antiduretic hormones. J. Membrane Biol. 71:189–193

    Google Scholar 

  19. Parisi, M., Bourguet, J. 1985. Water channels in animal cells: a widespread structure? Biol. Cell. 55:155–158

    Google Scholar 

  20. Parisi, M., Merot, J., Bourguet, J. 1985. Glutaraldehyde fixation preserves the permeability properties of the ADH-induced water channels. J. Membrane Biol. 86:239–245

    Google Scholar 

  21. Parisi, M., Merot, J., Ripoche, P., Chevalier, J., Bourguet, J. 1985. Biophysical characterization of the ADH-induced water channel. In: Water and Ions in Biological Systems. A. Pullman, V. Vasilescu, L. Packer, editors, pp. 205–210. USMS, Bucharest

    Google Scholar 

  22. Preston, G.M., Agre, P. 1991. Isolation of the cDNA for erythrocyte integral membrane protein of a 28-Kilodaltons member of an ancient channel family. Proc. Natl. Acad. Sci. USA 88:11110–11114

    Google Scholar 

  23. Preston, G.M., Canoll, T.P., Guggino, W.B., Agre, P. 1992. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387

    CAS  PubMed  Google Scholar 

  24. Sigel, E. 1990. Use of Xenopus oocytes for the functional expression of plasma membrane proteins. J. Membrane Biol. 117:201–221

    Google Scholar 

  25. Takahashi, T., Neher, E., Sakmann, B. 1987. Rat brain serotonin receptors in Xenopus oocytes are coupled by intracellular calcium to endogenous channels. Proc. Natl. Acad. Sci. USA 84:5063–5067

    Google Scholar 

  26. Whittembury, G., Carpi-Medina, P., Gonzalez, E., Linares, H. 1984. Effect of para-chloromercuribenzenesulfonic acid and temperature on cell water osmotic permeability of proximal straight tubules. Biochim. Biophys. Acta 775:365–373

    Google Scholar 

  27. Zhang, R., Verkman, A.S. 1991. Water and urea permeability properties of Xenopus oocytes: expression of mRNA from toad urinary bladder. Am. J. Physiol. 260:C26-C34

    Google Scholar 

  28. Zhang, R., Logee, K., Verkman, A.S. 1990. Expression of mRNA coding for kidney and red cell water channels in Xenopus oocytes. J. Biol. Chem. 265:15375–15378

    Google Scholar 

  29. Zhang, R., Skach, W., Hasegawa, H., van Hoek, A., Verkman, A.S. 1993. Cloning, functional analysis and cell localization of a kidney proximal tubule water transport homologous to CHIP28. J. Cell Biol. 10:359–369

    Google Scholar 

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Authors and Affiliations

  1. Facultad de Medicina, Laboratorio de Biomembranas, Departamento de Fisiología, Universidad de Buenos Aires, C.C. 128, Suc. 53 (B), 1453, Buenos Aires, Argentina

    C. Capurro, P. Ford, C. Ibarra & M. Parisi

  2. Service de Biologie Cellulaire, Département de Biologie Cellulaire et Moléculaire, Centre D'Etudes de Saclay, France

    P. Ripoche

Authors
  1. C. Capurro
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  2. P. Ford
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  3. C. Ibarra
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  4. P. Ripoche
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  5. M. Parisi
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This work was supported by Fundación Antorchas, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina) and Universidad de Buenos Aires (UBA). It was developed in the frame of an INSERM (France)-CONICET cooperative program.

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Capurro, C., Ford, P., Ibarra, C. et al. Water permeability properties of the ovarian oocytes from Bufo arenarum and Xenopus laevis: A comparative study. J. Membarin Biol. 138, 151–157 (1994). https://doi.org/10.1007/BF00232643

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  • DOI: https://doi.org/10.1007/BF00232643

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