Abstract
The membrane potential response of proximal tubular cells to changing HCO −3 concentrations was measured in micro-puncture experiments on rat kidney in vivo. No significant effect was noticed when luminal bicarbonate concentration was changed. Changing peritubular HCO −3 by substitution with Cl− resulted in conspicuous membrane potential transients, which reached peak values after 100–200 ms and decayed towards near control with time constants of ∼2s. The polarity of the potential changes and the dependence of the initial potential deflections on the logarithm of HCO −3 concentration suggest a high conductance of the peritubular cell membrane for HCO −3 buffer, but not for Cl−, SO 2−4 , or isethionate. At constant pH\(t_{{\text{HCO}}_{\text{3}}^ - } \) was estimated to amount to ∼0.68. At constant\(p_{{\text{CO}}_{\text{2}} } \),\(t_{{\text{HCO}}_{\text{3}}^ - } \) was even greater because of an additional effect of OH− or respectively H+ gradients across the cell membrane. The secondary repolarization may be explained by passive net movements of K+ and HCO −3 across the peritubular cell membrane, which result in a readjustment of intracellular HCO −3 to the altered peritubular HCO −3 concentration. Application of carbonic anhydrase inhibitors in the tubular lumen reduced the initial potential response by one half and doubled the repolarization time constant. The same effect occurred instantaneously when the inhibitor was applied—together with the HCO −3 concentration step—in the peritubular perfusate. This observation demonstrates that membrane bound carbonic anhydrase is somehow involved in passive rheogenic bicarbonate transfer across the peritubular cell membrane, and suggests that HCO −3 permeation might occur in form of CO2 and OH− (or H+ in opposite direction).
Similar content being viewed by others
References
Amorena C, Malnic G (1983) Peritubular buffering power and luminal acidification in proximal convoluted tubules of the rat. Pflügers Arch 398:331–336
Bello-Reuss E (1982) Electrical properties of the basolateral membrane of the straight portion of the rabbit proximal renal tubule. J Physiol 326:49–63
Bichara M, Paillard M, Leviel F, Gardin JP (1980) Hydrogen transport in rabbit kidney proximal tubules—Na∶H exchange. Am J Physiol 238:F445–451
Bichara M, Paillard M, Leviel F, Prigent A, Gardin JP (1983) Na∶H exchange and the primary H pump in the proximal tubule. Am J Physiol 244:F165–171
Boron WF (1983) Transport of H+ and of ionic weak acids and bases. J Membr Biol 72:1–16
Boron WF, Boulpaep EL (1983) Intracellular pH regulation in the renal proximal tubule of the salamander. Basolateral HCO3 transport. J Gen Physiol 81:53–94
Burckhardt BCH, Frömter E (1980) Bicarbonate transport across the peritubular membrane of rat kidney proximal tubule. In: Schulz I, Sachs G, Forte JG, Ullrich KJ (eds) Hydrogen ion transport in epithelia. Elsevier, Amsterdam, pp 277–285
Burckhardt BCH, Cassola AC, Frömter E (1984) Electrophysiological analysis of bicarbonate permeation across the peritubular cell membrane of rat kidney proximal tubule. II. Exclusion of HCO −3 effects on other ion permeabilities and of coupled electroneutral HCO −3 transport. Pflügers Arch 401:43–51
Burg M, Green N (1977) Bicarbonate transport by isolated perfused rabbit proximal convoluted tubules. Am J Physiol 233:F307–314
Burg M, Schwartz G (1980) Carbon dioxide permeability of renal proximal convoluted tubules. In: Schulz I, Sachs G, Forte JG, Ullrich KJ (eds) Hydrogen ion transport in epithelia. Elsevier, Amsterdam, pp 287–294
Cabantchik ZI, Knauf PA, Rothstein A (1978) The anion transport system of the red blood cell. The role of membrane protein evaluated by the use of probes. Biochim Biophys Acta 515:239–302
Conway EJ (1957) Nature and significance of concentration relations of potassium and sodium ions in skeletal muscle. Physiol Rev 37:84–132
Du Bose TD, Pucacco LR, Seldin DW, Carter NW, Kokko JP (1978) Direct determination of\(p_{{\text{CO}}_{\text{2}} } \) in the renal cortex. J Clin Invest 62:338–348
Edelman A, Teulon J, Anagnostopoulos T (1978) The effect of a disulfonic acid stilbene on proximal cell membrane potential in Necturus kidney. Biochim Biophys Acta 514:137–144
Edelman AA, Bouthier M, Anagnostopoulos T (1981) Chloride distribution in the proximal convoluted tubule of necturus kidney. J Membr Biol 62:7–17
Flemström G, Sachs G (1975) Ion transport by amphibian antrum in vitro. I. General characteristics. Am J Physiol 228(4):1188–1198
Frömter E (1982) Electrophysiological analysis of rat renal sugar and amino acid transport. I. Basic phenomena. Pflügers Arch 393:179–189
Frömter E, Geßner K (1974) Active transport potentials, membrane diffusion potentials, and streaming potentials across rat kidney proximal tubule. Pflügers Arch 351:85–98
Frömter E, Sato K (1976) Electrical events in active H+/HCO −3 transport across rat kidney proximal tubular epithelium. In: Kasbekar DK, Sachs G, Rehm WS (eds) Gastric hydrogen ion secretion. Dekker, New York, pp 382–403
Frömter E, Müller CW, Wick T (1971) Permeability properties of the proximal tubular epithelium of the rat kidney studied with electrophysiological methods. In: Giebisch G (ed) Electrophysiology of epithelia. Schattauer, Stuttgart, pp. 119–146
Frömter E, Rumrich G, Ullrich KJ (1973) Phenomenologic description of Na+, Cl− and HCO −3 absorption from proximal tubules of rat kidney. Pflügers Arch 343:189–220
Guggino WB, London R, Boulpaep EL, Giebisch G (1983) Chloride transport across the basolateral cell membrane of the Necturus proximal tubule: Dependence on bicarbonate and sodium. J Membr Biol 71:227–240
Hegel U, Frömter E, Wick T (1967) Der elektrische Wandwiderstand des proximalen Konvolutes der Rattenniere. Pflügers Arch 294:274–290
Hodgkin AL, Horowicz P (1959) The influence of potassium and chloride ions on the membrane potential of single muscle fibers. J Physiol 148:127–160
Hülser DF (1971) Elektrophysiologische Untersuchungen an Säugerzellkulturen: Der Einfluß von Bicarbonat und pH auf das Membranpotential. Pflügers Arch 325:174–187
Husted RF, Cohen LH, Steinmetz PR (1979) Pathway for bicarbonate transfer across the serosal membrane of turtle urinary bladder: Studies with a disulfonic stilbene. J Membr Biol 47:27–37
Jacobson HR, Kokko JP (1980) Bicarbonate reabsorption in the proximal tubule. In: Schulz I, Sachs G, Forte, JG, Ullrich KJ (eds) Hydrogen ion transport in epithelia. Elsevier, Amsterdam, pp 295–301
Kinne-Saffran E, Beauwens R, Kinne R (1982) An ATP-driven proton pump in brush-border membranes from rat renal cortex. J Membr Biol 64:67–76
Kinsella JL, Aronson PS (1980) Properties of the Na+−H+ exchanger in renal microvillus membrane vesicles. Am J Physiol 238: F461–469
Kleinman JG, Ware RA, Schwartz JH (1981) Anion transport regulates intracellular pH in renal cortical tissue. Biochim Biophys Acta 648:87–92
Kubota T, Biagi BA, Giebisch G (1983) Effects of acid base disturbances on basolateral membrane potential and intracellular potassium activity in the proximal tubule of Necturus. J Membr Biol 73:61–68
Murer H, Hopfer U, Kinne R (1976) Sodium/proton antiport in brush-border membrane vesicles isolated from rat small intestine and kidney. Biochim J 154:597–604
Rehm WS, Sanders SS (1975) Implications of the neutral carrier Cl−−HCO −3 exchange mechanism in gastric mucosa. Ann NY Acad Science 264:442–455
Reuss L (1979) Electrical properties of the cellular transepithelial pathway in Necturus gallbladder. III. Ionic permeability of the basolateral cell membrane. J Membr Biol 47:239–259
Sanyal G, Pessah NI, Maren TH (1981) Kinetics and inhibition of membrane-boud carbonic anhydrase from canine renal cortex. Biochim Biophys Acta 657:128–137
Struyvenberg A, Morrison RB, Relman AS (1968) Acid-base behavior of separated canine renal tubule cells. Am J Physiol 214:1155–1162
Suzuki K, Frömter E (1977) The potential and resistance profile of Necturus gallbladder cells. Pflügers Arch 371:109–117
Ullrich KJ, Frömter E, Baumann K (1969) Micropuncture and microanalysis in kidney physiology. In: Passow H, Stampfli R (eds) Laboratory techniques in membrane biophysics. Springer, Berlin Heidelberg New York, pp 106–109
Ullrich KJ, Rumrich G, Baumann K (1975) Renal proximal tubular buffer-(glycodiazine) transport. Inhomogenity of local transport rate, dependence on sodium, effect of inhibitors and chronic adaption. Pflügers Arch 357:149–163
Wistrand PJ, Kinne R (1977) Carbonic anhydrase activity of isolated brush border and basal-lateral membrane of renal tubular cells. Pflügers Arch 370:121–126
Woodbury JW, Miles PR (1972) Anion conductance of frog muscle membranes: One channel, two kinds of pH dependence. J Gen Physiol 62:324–353
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Burckhardt, B.C., Sato, K. & Frömter, E. Electrophysiological analysis of bicarbonate permeation across the peritubular cell membrane of rat kidney proximal tubule. Pflugers Arch. 401, 34–42 (1984). https://doi.org/10.1007/BF00581530
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00581530