Abstract
To elucidate the route of transepithelial Cl transport across amphibian skins, electrolyte concentrations and uptake of Br in different epithelial cell types of toad skin were determined using electron microprobe analysis. Under short-circuited conditions, Cl concentrations were about 10 mmol/kg ww lower in MR-cells (23.9±9.6 mmol/kg ww) than in principal cells and showed a large scatter. After unitateral substitution of Br for Cl in the bathing solutions, principal cells exchanged Br for Cl only from the serosal side, whereas variable amounts of Br were gained in MR-cells from either side. The ratio of Br to Cl concentrations in MR-cells averaged 0.35 and 0.81 after incubation with NaBr-Ringer's on the apical or serosal side, respectively. After activation of transepithelial anion conductance by serosa-positive voltage-clamping to 100 mV, uptake of Br from the apical side was increased in MR-cells compared with short-circuited conditions. On the average, the ratio of cellular Br to Cl concentrations was 1.38, but the variation among individual MR-cells from the same tissue was considerable. In MR-cells with large uptake of Br and voltageactivated conditions, the sum of Br and Cl concentrations was higher than the Cl concentration under control conditions. The increase of anion content was associated by increase of the Na and corresponding decrease of the K concentrations. The MR-cells were swollen as indicated by the decrease in the cellular dry weight content from 22.2±2.5 to 17.1±4.2 g/100 g. The principal cells contained 3.5±2.6 mmol/kg ww Br after voltage activation of anion conductance which appears to be taken up from the lateral intercellular spaces across the basolateral membrane.
The data indicate that principal cells are not involved in transepithelial Cl transport. The MR-cells, although representing a heterogeneous cell population, might be a site for electrodiffusional transepithelial Cl movement.
Similar content being viewed by others
References
Bauer R, Rick R (1978) Computer analysis of X-ray spectra (EDS) from thin biological specimens.X-Ray Spectrom 7:63–69
Biber TUL, Drewnowska K, Baumgarten CM, Fisher RS (1985) Intracellular Cl activity changes of frog skin. Am J Physiol 249:F432-F438
Bruus K, Kristensen P, Larsen EH (1976) Pathways for chloride and sodium transport across toad skin. Acta Physiol Scand 97:31–47
Dörge A, Rick R, Gehring K, Thurau K (1978) Preparation of freeze-dried cryosections for quantitative X-ray microanalysis for electrolytes in biological soft tissues. Pflügers Arch 373:85–97
Dörge A, Rick R, Beck F, Thurau K (1985) Cl transport across the basolateral membrane in frog skin epithelium. Pflügers Arch 405:S8-S11
Drewnowska K, Biber TUL (1985) Active transport and exchange diffusion of Cl across the isolated skin ofRana pipiens. Am J Physiol 249:F424-F431
Duranti E, Ehrenfeld J, Harvey BJ (1986) Acid secretion through the Rana esculenta skin: involvement of an anionexchange mechanism at the basolateral membrane. J Physiol 378:195–211
Foskett JK, Ussing HH (1986) Localization of chloride conductance to mitochondria-rich cells in frog skin epithelium. J Membr Biol 91:251–258
Harck AF, Larsen EH (1986) Concentration dependence of halide fluxes and selectivity of the anion pathway in toad skin. Acta Physiol Scand 128:289–304
Helman SI, Fisher RS (1977) Microelectrode studies of the active Na transport pathway of frog skin. J Gen Physiol 69:571–604
Katz U, Scheffey C (1986) The voltage-dependent chloride current conductance of toad skin is localized to mitochondriarich cells. Biochim Biophys Acta 861:480–482
Koefoed-Johnsen V, Levi H, Ussing HH (1952) The mode of passage of chloride ions through the isolated frog skin. Acta Physiol Scand 25:150–163
Kristensen P (1981) Is chloride transfer in frog skin localized to a special cell type? Acta Physiol Scand 113:123–124
Kristensen P, Larsen EH (1978) Relationship between chloride exchange diffusion and a conductive chloride pathway across the isolated skin of the toad (Bufo bufo). Acta Physiol Scand 102:22–34
Kristensen P, Ussing HH (1985) Epithelial organization. In: Seldin DW, Giebisch G (eds) The kidney: physiology and pathophysiology. Raven Press, New York, pp 173–188
Larsen EH, Kristensen P (1978) Properties of a conductive cellular chloride pathway in the skin of the toad (Bufo bufo). Acta Physiol Scand 102:1–21
Larsen EH, Rasmussen BE (1985) A mathematical model of amphibian skin epithelium with two types of transporting cellular units. Pflügers Arch 405:S50-S58
McRobbie EA, Ussing HH (1961) Osmotic behaviour of the epithelial cells of frog skin. Acta Physiol Scand 53:348–365
Nagel W (1976) The intracellular electrical potential profile of the frog skin epithelium. Pflügers Arch 365:135–143
Nagel W (1978) Effects of ADH upon electrical potential and resistance of apical and basolateral membranes of frog skin. J Membr Biol 42:99–122
Nagel W, Garcia-Diaz JF, Essig A (1983) Contribution of junctional conductance to the cellular voltage-divider ratio in frog skins. Pflügers Arch 399:336–341
Ques-Von Petery MV, Rotunno CA, Cereijido M (1978) Studies on chloride permeability of the skin of Leptodactyllus ocellatus: Io Na+ and Cl− effect on passive movements of Cl−. J Membr Biol 42:317–330
Rick R, Dörge A, Arnim EV, Thurau K (1978) Electron microprobe analysis of frog skin epithelium: Evidence for a syncytial sodium transport compartment. J Membr Biol 39:313–331
Rick R, Dörge A, Katz U, Bauer R, Thurau K (1980) The osmotic behaviour of toad skin epithelium (Bufo viridis). Pflügers Arch 385:1–10
Rick R, Dörge A, Thurau K (1982) Quantitative analysis of electrolytes in frozen dried sections. J Microsc 125:239–247
Rick R, Dörge A, Beck FX, Thurau K (1986) Electron-probe X-ray microanalysis of transepithelial ion transport. Ann NY Acad Sci 483:245–258
Schneider W (1975) Chloride transport in isolated skin of Rana esculenta. Pflügers Arch 355:107–124
Spring KR, Ussing HH (1986) The volume of mitochondria-rich cells of frog skin epithelium. J Membr Biol 92:21–26
Ussing HH (1985) Volume regulation and basolateral cotransport of sodium, potassium, and chloride ions in frog skin epithelium. Pflügers Arch 405:S2-S7
Voute CL, Meier W (1978) The mitochondria-rich cell of frog skin as hormone-sensitive “shunt-path”. J Membr Biol (Special issue) 40:151–165
Watlington CO, Sessee FJr (1973) Chloride flux across frog skins of low potential difference. Biochim Biophys Acta 330:102–107
Whitear M (1975) Flask cells and epidermal dynamics in frog skin. J Zool 175:107–149
Willumsen NJ, Larsen EH (1986) Membrane potentials and intracellular Cl activity of toad skin epithelium in relation to activation of the transepithelial Cl conductance. J Membr Biol 94:173–190
Zadunaisky JA, DeFisch FW (1964) Active and passive chloride movements across isolated amphibian skin. Am J Physiol 207:1010–1014
Author information
Authors and Affiliations
Additional information
Dedicated to Prof. Dr. med. Dr. h.c. Klaus Thurau on the occasion of his 60th birthday
Rights and permissions
About this article
Cite this article
Dörge, A., Rick, R., Beck, F.X. et al. Uptake of Br in mitochondria-rich and principal cells of toad skin epithelium. Pflugers Arch. 412, 305–313 (1988). https://doi.org/10.1007/BF00582513
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00582513