Abstract
The membrane potential of proximal tubule cells is dominated by the potassium conductance of the basolateral membrane. In the present paper the nature of this conductance is investigated by the patch-clamp technique. Only one type of K channel was found in the basolateral membranes of freshly isolated proximal cells. In cell-attached patches, the current/voltage relationship is markedly non-linear with much larger inward (30 pS) than outward (≈ 6 pS) conductances, even in the presence of roughly symmetrical K concentrations. Thus the channels show inward rectification. The determination of the conductance for outward current flow is complicated since the current/voltage curves show an area of negative conductance. Nevertheless, taking the conductance for outward current flow and the density of the channels it is possible to account for all of the previously reported potassium conductance of amphibian proximal tubule cells. The open probability of the channels was found not to depend upon the membrane potential. However, the non-linearity of the current/voltage relationships will confer upon the channel the same voltage dependence as that seen in intact proximal tubules, i.e. the conductance decreases with depolarisation. Incubation of cells in Ringer with no substrates or in the presence of alanine and/or glucose showed no change in the activity of the channels. These findings suggest that, although these channels may represent the basolateral conductance of frog proximal tubule cells, they are not involved in the well-established coupling between transport rate and potassium conductance.
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References
Aronson PS, Sacktor B (1975) The Na gradient-dependent transport of d-glucose in renal brush border membranes. J Biol Chem 250:6032–6039
Beck JS, Potts DJ (1990) Cell swelling, co-transport activation and potassium conductance in isolated perfused rabbit kidney proximal tubules. J Physiol (Lond) 425:369–378
Biagi B, Kubota T, Sohtell M, Giebisch G (1981) Intracellular potentials in rabbit proximal tubules perfused in vitro. Am J Physiol 240:F200-F210
Biagi B, Sohtell M, Giebisch G (1981) Intracellular potassium activity in the rabbit proximal straight tubule. Am J Physiol 241:F677-F686
Bleich M, Schlatter E, Greger R (1990) The luminal potassium channel of the thick ascending limb of Henle's loop. Pflügers Arch 415:449–460
Boron WF, Boulpaep EL (1983) Intracellular pH regulation in the renal proximal tubule of the salamander. Basolateral HCO −3 -transport. J Gen Physiol 81:53–94
Cohen B, Giebisch G (1984) Relationship between potassium conductance and transport in renal tubular epithelium. In: Information and energy transduction in biological membranes. Alan R. Liss, New York, pp 391–401
Frindt G, Palmer LG (1989) Low conductance potassium channels in the apical membrane of the rat cortical collecting tubule. Am J Physiol 256:F143-F151
Fuchs W, Larsen EH, Lindemann B (1977) Current-voltage curve of sodium channels and concentration dependence of sodium permeability in frog skin. J Physiol (Lond) 267:137–166
Giebisch G, Aronson PS (1986) The proximal nephron. In: Andreoli TE, Hoffman JF, Fancstil DD, Schultz SG (eds) Physiology of membrane disorders. Plenum, London, pp 669–700
Giebisch G, Hunter M, Kawahara K (1990) Apical potassium channels in Amphiuma diluting segment: effect of barium. J Physiol (Lond) 420:313–323
Guggino SE, Guggino WB, Green N, Sacktor B (1987) Calcium-activated potassium channels in cultured medullary thick ascending limb cells. Am J Physiol 252:C121-C127
Hagiwara S (1983) Membrane potential dependent ion channels in cell membrane. Raven, New York
Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch clamp techniques for high resolution current recording from cells and cell free membrane patches. Pflügers Arch 391:85–100
Hille B (1984) Ionic channels in excitable membranes. Sinauer Associates, Massachusetts
Hunter M (1989) Isolation of single proximal cells from frog kidneys. J Physiol (Lond) 416:13P
Hunter M (1990) Stretch-activated channels in the basolateral membrane of single proximal cells of frog kidney. Pflügers Arch (in press)
Hunter M, Oberleithner H, Henderson RM, Giebisch G (1988) Whole-cell potassium currents in single early distal tubule cells. Am J Physiol 255:F669-F703
Hurst AM, Hunter M (1989) Apical channels of frog diluting segment: inhibition by acidification. Pflügers Arch 415:115–117
Kawahara K (1990) A stretch-activated K channel in the basolateral membrane of Xenopus kidney proximal tubule cells. Pflügers Arch 415:624–629
Kawahara K, Hunter M, Giebisch G (1987) Potassium channels in Necturus proximal tubule. Am J Physiol 253:F488-F494
Kawahara K, Hunter M, Giebisch G (1990) Calcium-activated potassium channels in the luminal membrane of Amphiuma diluting segment: voltage-dependent block by intracellular sodium upon depolarisation. Pflügers Arch (in press)
Kimmich GA, Randles J (1988) Na-coupled sugar transport: membrane potential-dependent K m and K i for Na. Am J Physiol 255:C486-C494
Lang F, Messner G, Wang W, Paulmichl M, Oberleithner H, Deetjen P (1984) The influence of intracellular sodium activity on the transport of glucose in the proximal tubule of frog kidney. Pflügers Arch 401:14–21
Lang F, Messner G, Rehwald W (1986) Electrophysiology of sodium-coupled transport in proximal renal tubules. Am J Physiol 250:F953-F962
Lang, F, Oberleithner H, Giebisch G (1986) Electrophysiological heterogeneity of proximal convoluted tubules in Amphiuma kidney. Am J Physiol 251:F1063-F1072
Lopes AG, Siebens AW, Giebisch G, Boron WF (1987) Electrogenic Na/HCO cotransport across basolateral membrane of isolated perfused Necturus proximal tubule. Am J Physiol 253:F340-F350
Matsuda H, Saigusa A, Irisawa H (1987) Ohmic conductance through the inwardly rectifying K channel and blocking by internal magnesium. Nature 325: 156–159
Matsumura Y, Cohen B, Guggino WB, Giebisch G (1984) Regulation of the basolateral potassium conductance of the Necturus proximal tubule. J Membr Biol 79:153–161
Maunsbach AB, Boulpaep EL (1984) Quantitative ultrastructure and functional correlates in proximal tubule of Ambystoma and Necturus. Am J Physiol 246:F710-F724
Messner G, Oberleithner H, Lang F (1985) The effect of phenylalanine on the electrical properties of proximal tubule cells in the frog kidney. Pflügers Arch 404:138–144
Messner G, Wang W, Paulmichl M, Oberleithner H, Lang F (1985) Ouabain decreases apparent potassium-conductance in proximal tubules of the amphibian kidney. Pflügers Arch 404:131–137
Messner G, Stulnig G, Rehwald W, Lang F (1986) Influence of potassium depletion on potassium conductance in proximal tubules of frog kidney. Pflügers Arch 407:153–157
Oberleithner H, Schmidt B, Dietl P (1986) Fusion of renal epithelial cells: a model for studying cellular mechanisms of ion transport. Proc Natl Acad Sci USA 83:3547–3551
Parent L, Cardinal J, Sauve R (1988) Single-channel analysis of a K channel at basolateral membrane of rabbit proximal convoluted tubule. Am J Physiol 254:F105-F113
Rehwald W, Messner G, Lang F (1986) Influence of barium on the effects of phenylalanine in proximal tubules. Pflügers Arch 406:574–577
Sackin H (1987) Stretch-activated potassium channels in renal proximal tubule. Am J Physiol 253:F1253-F1262
Sackin H (1989) A stretch-activated K channel sensitive to cell volume. Proc Natl Acad Sci USA 86:1731–1735
Sackin H, Palmer LG (1987) Basolateral potassium channels in renal proximal tubule. Am J Physiol 253:F476-F487
Sakmann B, Trube G (1984) Conductance properties of single inwardly rectifying potassium channels in ventricular cells from guinea-pig heart. J Physiol (Lond) 347:641–657
Sansom SC, O'Neil RG (1985) Mineralocorticoid regulation of apical cell membrane sodium and potassium transport of the cortical collecting duct. Am J Physiol 248:F858-F868
Schultz SG (1981) Homocellular regulatory mechanisms in Na transporting epithelia: avoidance of extinction by flushthrough. Am J Physiol 241:f579-f590
Stokes JB (1984) Cellular potassium permeation across the cortical collecting tubule: effects of sodium-potassium pump inhibition and membrane depolarization. Am J Physiol 246:F467-F475
Volkl H, Greger R, Lang F (1987) Potassium conductance in straight proximal tubule cells of the mouse. Effect of barium, verapamil and quinidine. Biochim Biophys Acta 900:275–281
Wang W, Henderson RM, Geibel J, White S, Giebisch G (1989) Mechanism of aldosterone induced increase of potassium conductance in early distal renal tubule cells of the frog. J Membr Biol 111:277–289
Wang W, White S, Geibel J, Giebisch G (1990) A potassium channel in the apical membrane of rabbit thick ascending limb of Henle's loop. Am J Physiol 258:F244-F253
Yellen G (1984) Ionic permeation and blockade in Ca-activated K channels of bovine chromaffin cells. J Gen Physiol 84:157–186
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This work was supported by the Wellcome Trust
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Hunter, M. Potassium-selective channels in the basolateral membrane of single proximal tubule cells of frog kidney. Pflügers Archiv 418, 26–34 (1991). https://doi.org/10.1007/BF00370448
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DOI: https://doi.org/10.1007/BF00370448