Summary
Necturus urinary bladders were mounted between half chambers filled with Ringer's solution and the electrical potential difference was measured across the luminal and basal membrane of the epithelial cells under open circuit conditions. The measurements were complicated by leak artifacts, which developed at the puncture site during impalements from the mucosal surface, but not during impalements from the serosal surface, probably because the resistance of the mucosal cell membrane was on the average 13 times higher than that of the serosal membrane. In contrast to previous reports on potential profiles in amphibian urinary bladders, in which the possible influence of leak artifacts was neglected, it was observed that the serosal membrane potential was constant at ∼ −90 mV in all bladders, irrespective of the spontaneous transepithelial potential difference. In low potential bladders (bladders with low transepithelial Na+ transport, mainly from female animals) the potential profile was trough-like with −30 mV in the mucosal bath, and −90 mV inside the cells, the serosal bath being taken as zero. In high potential bladders (bladders with high rates of Na+ transport from male animals) it was stairstep-like from −150 mV in the mucosal bath to −90 mV inside the cells and to zero in the serosal bath. Luminal application of amiloride produced similar changes of the potential profile as caused the transition from high to low potential bladders. In agreement with resistance data reported in the subsequent paper, we conclude that the polarity change of the luminal membrane potential with increasing transepithelial Na+ transport reflects an increase of the luminal Na+ conductance following the incorporation of Na+-selective, amiloride sensitive passive transport channels into the luminal cell membrane in response to hormonal stimuli from androgens and aldosterone.
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References
Bentley, P. J.: Sodium and water movement across the urinary bladder of a urodele amphibian (the Mudpuppy Necturus maculosus): Studies with vasotocin and aldosterone. Gen. Comp. Endocr.16, 356–362 (1971)
Choi, J. K.: The fine structure of the urinary bladder of the toad, bufo marinus. J. Cell Biol.16, 53–72 (1963)
Chowdhury, T. K., Snell, F. M.: A microelectrode study of electrical potentials in frog skin and toad bladder. Biochim. Biophys. Acta94, 461–471 (1965)
Civan, M. M., Frazier, H. S.: The site of the stimulatory action of vasopressin on sodium transport in toad bladder. J. Gen. Physiol.51, 589–606 (1968)
Civan, M. M., Hoffman, R. E.: Effect of aldosterone on electrical resistance of toad bladder. Am. J. Physiol.220, 324–328 (1971)
Frazier, H. S.: The electrical potential profile of the isolated toad bladder. J. Gen. Physiol.45, 515–528 (1962)
Frazier, H. S., Leaf, A.: The electrical characteristics of active sodium transport in the toad bladder. J. Gen. Physiol.46, 491–503 (1963)
Frömter, E.: The route of passive ion movement through the epithelium of Necturus gall bladder. J. Membr. Biol.8, 259–301 (1972)
Frömter, E.: Progress in microelectrode techniques for kidney tubules. Yale J. Biol. Med.45, 414–425 (1972)
Frömter, E., Gebler, B.: Electrical properties of amphibian urinary bladder epithelia. III. The cell membrane resistances and the effect of amiloride. Pflügers Arch.371, 99–108 (1977)
Gruber, W. D., Knauf, H., Frömter, E.: The action of aldosterone on Na+- and K+-transport in the rat submaxillary main duct. Pflügers Arch.344, 33–49 (1973)
Higgins, J. T., Jr., Cesaro, L., Gebler, B., Frömter, E.: Electrical properties of amphibian urinary bladder epithelia. Pflügers Arch.358, 41–56 (1975)
Higgins, J. T., Jr., Frömter, E.: Potential profile in Necturus urinary bladder. Pflügers Arch.347, R32 (1974)
Higgins, J. T., Jr., Frömter, E.: Cell membrane potential in amphibian urinary bladder. Physiologist17, 247 (1974)
Hirschhorn, N., Frazier, H. S.: Intracellular electrical potential of the epithelium of turtle bladder. Am. J. Physiol.220, 1158–1161 (1971)
Hladky, S. B., Haydon, D. A.: Ion transfer across lipid membranes in the presence of gramicidin A. I. Studies of the unit conductance channel. Biochim. Biophys. Acta274, 294–312 (1972)
Janácek, K., Morel, F., Bourguet, J.: Étude experimentale des potentiels électriques et des activités ioniques dans les cellules épithéliales de la vessie de Grenouille. J. Physiol. (Paris)60, 51–66 (1968)
Lassen, U. V., Nielsen, A.-M., Pape, L., Simonsen, L.: The membrane potential of Ehrlich ascites tumor cells. Microelectrode measurements and their critical evaluation. J. Membr. Biol.6, 269–288 (1971)
Lassen, U. V., Sten-Knudsen, O.: Direct measurements of membrane potential and membrane resistance of human red cells. J. Physiol. (Lond.)195, 681–696 (1968)
Leaf, A.: Transepithelial transport and its hormonal control in the toad bladder. Ergebn. Physiol.56, 216–263 (1965)
Lefevre, M. E., Norris, J., Hammer, R.: Sex differences in Necturus urinary bladders. Anat. Rec.187, 47–62 (1977)
Lewis, S. A., Eaton, D. C., Diamond, J. M.: The mechanism of Na+ transport by rabbit urinary bladder. J. Membr. Biol.28, 41–70 (1976)
Lewis, S. A., Diamond, J. M.: Na+ transport by rabbit urinary bladder, a tight epithelium. J. Membr. Biol.28, 1–40 (1976)
Nagel, W.: The intracellular electrical potential profile of the frog skin epithelium. Pflügers Arch.365, 135–143 (1976)
Peachey, L. D., Rasmussen, H.: Structure of the toad's urinary bladder as related to its physiology. J. Biophys. Biochem. Cytol.10, 529–553 (1961)
Ramsay, A. G., Gallagher, D. L., Shoemaker, R. L., Sachs, G.: Barium inhibition of sodium ion transport in toad bladder. Biochim. Biophys. Acta436, 617–627 (1976)
Reuss, L., Finn, A. L.: Passive electrical properties of toad urinary bladder epithelium. J. Gen. Physiol.64, 1–25 (1974)
Reuss, L., Finn, A. L.: Effects of changes in the composition of the mucosal solution on the electrical properties of the toad urinary bladder epithelium. J. Membr. Biol.20, 191–204 (1975)
Reuss, L., Finn, A. L.: Dependence of serosal membrane potential on mucosal membrane potential in toad urinary bladder. Biophys. J.15, 71–75 (1975)
Spooner, P. M., Edelman, I. S.: Further studies on the effect of aldosterone on electrical resistance of toad bladder. Biochim. Biophys. Acta406, 304–314 (1975)
Ussing, H. H.: The alkali metal ions in isolated systems and tissues. In: Handbuch der Experimentellen Pharmakologie, pp. 1–195. Berlin-Göttingen-Heidelberg: Springer 1960
Voûte, C. L., Møllgard, K., Ussing, H. H.: Quantitative relationship between active Na+ transport, expansion of endoplamatic reticulum and specialized vacuoles (“scalloped sacs”) in the outermost living cell layer of the frog skin epithelium (rana temporaria). J. Membr. Biol.21, 273–289 (1975)
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Higgins, J.T., Gebler, B. & Frömter, E. Electrical properties of amphibian urinary bladder epithelia. Pflugers Arch. 371, 87–97 (1977). https://doi.org/10.1007/BF00580776
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DOI: https://doi.org/10.1007/BF00580776