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The electrical basis for enhanced potassium secretion in rat distal colon during dietary potassium loading

  • Transport Processes, Metabolism and Endocrinology; Kidney, Gastrointestinal Tract, and Exocrine Glands
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Abstract

Previous studies in rat distal colon provide evidence for an active absorptive process for potassium under basal conditions, and for active potassium secretion during chronic dietary potassium loading. The present studies were performed with conventional and potassium-selective microelectrodes to determine the electrical basis for the increase in transcellular (active) potassium secretion observed during potassium loading. Compared to control tissues, potassium loading resulted in a 5-fold increase in transepithelial voltage (V T) and a 52% decrease in total resistance (R T) in the distal colon. The rise inV T was due to a decrease in apical membrane resistance and an increase in basolateral membrane voltage from −45±2 mV (cell interior negative) in control to −56±2 mV (P<0.001) in potassium loaded tissues. This difference in basolateral membrane voltage reflected in increase in intracellular potassium activity from 86±4 mM to 153±12 mM (P<0.001). In control tissues, the sequential mucosal addition of the sodium channel blocker amiloride (0.1 mM) and the potassium channel blocker tetraethylammonium chloride (TEA: 30 mM) produced no effect on the electrical measurements. However, in potassium loaded tissues, amiloride and TEA produced transepithelial changes consistent with inhibition of apical membrane conductances for sodium and potassium, respectively, reflected by increases in the resistance ratio, α (ratio of apical to basolateral membrane resistances). These data indicate that the decrease in apical membrane resistance during potassium loading was caused by an increase in apical membrane conductance for both potassium and sodium.

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References

  • Binder HJ, Rawlins CL (1973) Electrolyte transport across isolated large intestinal muscosa. Am J Physiol 225:1232–1239

    Google Scholar 

  • Boulpaep EL, Sackin H (1980) Electrical analysis of intraepithelial barriers. In: Boulpaep EL (ed) Current topics in membranes and transport, vol 13. Academic Press, New York, pp 169–197

    Google Scholar 

  • Boyd JE, Palmore WP, Mulrow PJ (1971) Role of potassium in the control of aldosterone secretion in the rat. Endocrinology 88:556–565

    Google Scholar 

  • Cassola AC, Mollenhouer M, Frömter E (1983) The intracellular chloride activity of rat kidney proximal tubular cells. Pflügers Arch 399:259–265

    Google Scholar 

  • Civan MM (1978) Intracellular activities of sodium and potassium. Am J Physiol 234:F261-F269

    Google Scholar 

  • Dawson DC (1977) Na and Cl transport across the isolated turtle colon: parallel pathways for transmural ion movement. J Membr Biol 37:213–233

    Google Scholar 

  • Duffey ME, Turnheim K, Frizzell RA, Schultz SG (1978) Intracellular chloride activities in rabbit gallbladder. Direct evidence for the role of the sodium gradient in energizing “uphill” chloride transport. J Membr Biol 42:229–245

    Google Scholar 

  • Edmonds CJ (1967) Transport of potassium by the colon of normal and sodium-depeleted rats. J Physiol (Lond) 193:603–617

    Google Scholar 

  • Edmonds CJ, Nielsen OE (1968) Transmembrane electrical potential differences and ionic-composition of mucosal cells of rat colon. Acta Physiol Scand 72:338–349

    Google Scholar 

  • Fine LG, Yanagawa N, Schultze RG, Tuck M, Trizna W (1979) Functional profile of the isolated uremic nephron. J Clin Invest 64:1033–1043

    Google Scholar 

  • Fisher KA, Binder HJ, Hayslett JP (1976) Potassium secretion by colonic mucosal cells after potassium adaptation. Am J Physiol 231:987–994

    Google Scholar 

  • Foster ES, Sandle GI, Hayslett JP, Binder HJ (1983) Cyclic adenosine monophosphate stimulates active potassium secretion in the rat colon. Gastroenterology 84:324–330

    Google Scholar 

  • Foster ES, Hayslett JP, Binder HJ (1984) Mechanism of active potassium absorption and secretion in the rat colon. Am J Physiol 246:G611-G617

    Google Scholar 

  • Foster ES, Jones WJ, Hayslett JP, Binder HJ (1985) Role of aldosterone and dietary potassium in potassium adaptation in the distal colon of the rat. Gastroenterology 88:41–46

    Google Scholar 

  • Hayslett JP, Binder HJ (1982) Mechanism of potassium adaptation. Am J Physiol 243:F103-F112

    Google Scholar 

  • Hayslett JP, Halevy J, Pace PE, Binder HJ (1982) Demonstration of net potassium absorption in mammalian colon. Am J Physiol 242:G209-G214

    Google Scholar 

  • Hayslett JP, Myketey N, Binder HJ, Aronson PS (1980) Mechanism of increased potassium secretion in potassium loading and sodium deprivation. Am J Physiol 239:F378-F382

    Google Scholar 

  • Kashgarian M, Taylor CR, Binder HJ, Hayslett JP (1980) Amplification of cell membrane surface in potassium adaptation. Lab Invest 42:581–588

    Google Scholar 

  • Khuri RN, Agulian SK, Kalloghlian A (1972) Intracellular potassium in cells of the distal tubule. Pflügers Arch 335:297–308

    Google Scholar 

  • Kliger AS, Binder HJ, Bastl C, Hayslett JP (1981) Demonstration of active potassium transport in the mammalian colon. J Clin Invest 67:1189–1196

    Google Scholar 

  • Lewis SA, Eaton DC, Clausen C, Diamond JM (1977) Nystatin as a probe for investigating the electrical properties of a tight epithelium. J Gen Physiol 70:427–440

    Google Scholar 

  • Lewis SA, Eaton DC, Diamond JM (1976) The mechanism of Na transport by rabbit urinary bladder. J Membr Biol 28:41–70

    Google Scholar 

  • Lewis SA, Wills NK, Eaton DC (1978) Basolateral membrane potential of a tight epithelium: Ionic diffusion and electrogenic pumps. J Membr Biol 41:117–148

    Google Scholar 

  • Mandel LJ (1975) Actions of external hypertonic urea, ADH and theophylline on transcellular and extracellular solute permeabilities in frog skin. J Gen Physiol 65:599–615

    Google Scholar 

  • Martin RS, Jones WJ, Hayslett JP (1983) Animal model to study the effects of adrenal hormones on epithelial function. Kidney Int 24:386–391

    Google Scholar 

  • Mello-Aires M, Giebisch G, Malnic G (1973) Kinetics of potassium transport across single distal tubules of rat kidney. J Physiol (Lond) 232:47–70

    Google Scholar 

  • Nagel W, Garcia-Diaz JF, Armstrong WMcD (1981) Intracellular ionic activities in frog skin. J Membr Biol 61:127–134

    Google Scholar 

  • Narvarte J, Finn AL (1980) Microelectrode studies in toad urinary bladder epithelium. Effects of Na concentration changes in the mucosal solution on equivalent electromotive forces. J Gen Physiol 75:323–344

    Google Scholar 

  • Oberleithner H, Giebisch G (1981) Mechanism of potassium transport across distal tubular epithelium of Amphiuma. In: Macknight ADC, Leader JP (eds) Epithelial ion and water transport. Raven Press, New York, pp 97–105

    Google Scholar 

  • Oehme M, Simon W (1976) Microelectrode for potassium ions based on a neutral carrier and comparison of its characteristics with a cation exchange sensor. Anal Chim Acta 86:21–25

    Google Scholar 

  • Petersen OH, Maruyama Y (1984) Calcium-activated potassium channels and their role in secretion. Nature 307:693–696

    Google Scholar 

  • Rastegar A, Biemesderfer D, Kashgarian M, Hayslett JP (1980) Changes in membrane surfaces of collecting duct cells in potassium adaptation. Kidney Int 18:293–301

    Google Scholar 

  • Reuss L, Grady TP (1979) Effects of external sodium and cell membrane potantial on intracellular chloride activity in gallbladder epithelium. J Membr Biol 51:15–31

    Google Scholar 

  • Russell JM, Eaton DC, Brodwick MS (1977) Effects of nystatin on membrane conductance and internal ion activities in Aplysia neurons. J Membr Biol 37:137–156

    Google Scholar 

  • Sandle GI, Hayslett JP, Binder HJ (1984) Effect of chronic hyperaldosteronism on the electrophysiology of rat distal colon. Pflügers Arch 401:22–26

    Google Scholar 

  • Sandle GI, Lewis SA, Hayslett JP, Binder HJ (1982) Comparison of the effects of K loading and Na depletion on barriers and forces which mediate K secretion in colon. Gastroenterology 82:1169 (abstr)

    Google Scholar 

  • Snedecor GW, Cochran WG (1967) Statistical methods, 6th edn. Iowa State University Press, Ames, Iowa, p 549

    Google Scholar 

  • Thatcher JC, Radike AW (1947) Tolerance to potassium intoxication in the albino rat. Am J Physiol 151:138–146

    Google Scholar 

  • Van Driessche W, Gogelein H (1978) Potassium channels in the apical membrane of the toad gallbladder. Nature (Lond) 275:655–667

    Google Scholar 

  • Van Driessche W, Zeiske W (1980) Spontaneous fluctuations of potassium channels in the apical membrane of frog skin. J Physiol (Lond) 299:101–116

    Google Scholar 

  • Wade JB, O'Neil RG, Pryor JL, Boulpaep EL (1979) Modulation of cell membrane area in renal collecting tubules by corticosteroid hormones. J Cell Biol 81:439–445

    Google Scholar 

  • Wade JB, Revel J-P, DiScala VA (1973) Effect of osmotic gradients on intracellular junctions of the toad bladder. Am J Physiol 224:407–415

    Google Scholar 

  • Will PC, Lebowitz JL, Hopfer U (1980) Induction of amiloridesensitive sodium transport in the rat colon by mineralocorticoids. Am J Physiol 238:F261-F268

    Google Scholar 

  • Wills NK, Biagi B (1982) Active potassium transport by rabbit descending colon epithelium. J Membr Biol 64:195–203

    Google Scholar 

  • Wills NK, Lewis SA, Eaton DC (1979) Active and passive properties of rabbit descending colon. A microelectrode and nystatin study. J Membr Biol 45:81–108

    Google Scholar 

  • Wills NK, Zeiske W, Van Driessche W (1982) Noise analysis reveals K+ channel conductance fluctuations in the apical membrane of rabbit colon. J Membr Biol 69:187–197

    Google Scholar 

  • Wright FS, Strieder N, Fowler NB, Giebisch G (1971) Potassium secretion by distal tubule after potassium adaptation. Am J Physiol 221:437–448

    Google Scholar 

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Author notes

  1. G. I. Sandle

    Present address: Department of Medicine (University of Manchester, School of Medicine), Hope Hospital, Eccles Old Road, M6 8HD, Salford, UK

Authors and Affiliations

  1. Department of Internal Medicine, Yale University School of Medicine, 333 Cedar Street, 06510, New Haven, Connecticut, USA

    G. I. Sandle, E. S. Foster, S. A. Lewis, H. J. Binder & J. P. Hayslett

  2. Department of Physiology, Yale University School of Medicine, 333 Cedar Street, 06510, New Haven, Connecticut, USA

    G. I. Sandle, E. S. Foster, S. A. Lewis, H. J. Binder & J. P. Hayslett

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  1. G. I. Sandle
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  2. E. S. Foster
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  3. S. A. Lewis
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  4. H. J. Binder
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  5. J. P. Hayslett
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Sandle, G.I., Foster, E.S., Lewis, S.A. et al. The electrical basis for enhanced potassium secretion in rat distal colon during dietary potassium loading. Pflugers Arch. 403, 433–439 (1985). https://doi.org/10.1007/BF00589258

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  • DOI: https://doi.org/10.1007/BF00589258

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