Skip to main content
SpringerLink
Log in

High-conductance K+ channel in apical membranes of principal cells cultured from rabbit renal cortical collecting duct anlagen

  • Transport Processes, Metabolism and Endocrinology; Kidney, Gastrointestinal Tract, and Exocrine Glands
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

Using the patch clamp technique, one type of K+ channel was identified in the apical cell membrane of cultured principal cells of rabbit renal collecting ducts in the cell-attached or excised-patch configuration. The channel was highly selective for K+ over Na+ (typically 30-70-fold) and had a conductance of 180, SD±39 pS (n=6), referred to a situation of 140 mmolar K+-Ringer solution present on either surface of the patch membrane. Channel activity was completely blocked by Ba2+ (5 mmol/l) and partially inhibited by Na+. The latter was evidenced by a deviation from Goldman rectification at high cytoplasm-positive membrane potentials, which was observed when Na+ competed with K+ for channel entrace from the cytoplasmic surface. Channel open probability depended strongly on membrane voltage and cytoplasmic Ca2+ concentration. Open-close kinetics exhibited double exponential behaviour, with a strong voltage dependence of the slow open time constant. Infrequently also a substate conductance level was identified. The voltage and calcium dependence suggest that the channel plays a role in adjusting K+ secretion to Na+ absorption in the fine regulation of cation excretion in renal collecting ducts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Adams PR, Constanti A, Brown PA, Clark BB (1982) Intracellular Ca++ activates a fast voltage-sensitive K+-current in vertebrate sympathetic neurons. Nature 296:746–749

    Google Scholar 

  2. Barrett JN, Magleby KL, Palotta BS (1982) Properties of single calcium-activated potassium channels in cultured rat muscle. J Physiol (Lond) 331:211–230

    Google Scholar 

  3. Bergman C (1970) Increase in sodium concentration near the inner surface of model membranes. Pflügers Arch 317:287–302

    Google Scholar 

  4. Bezanilla F (1986) A high capacity data recording device based on a digital audio processor and a video cassette recorder. Biophysical J 47:437–441

    Google Scholar 

  5. Bezanilla F, Armstrong CM (1972) Negative conductance caused by entry of sodium and cesium ions into the potassium channels of squid axons. J Gen Physiol 60:588–608

    Google Scholar 

  6. Findlay I, Dunne MJ, Petersen OH (1985) High conductance K+-channel in pancreatic islet cells can be activated and inactivated by internal calcium. J Membr Biol 83:169–175

    Google Scholar 

  7. Garg LC, Knepper HA, Burg M (1981) Mineralocorticoid effects on Na-K-ATPase individual nephron segments. Am J Physiol 240:F536-F544

    Google Scholar 

  8. Gitter A, Theis J (1987) A low cost voltage stepper device for use in patch clamp experiments. Pflügers Arch 408 (in press)

  9. Gögelein H, Greger R (1984) Single channel recordings from basolateral and apical membranes of renal proximal tubules. Pflügers Arch 401:424–426

    Google Scholar 

  10. Goldman DE (1943) Potential, impedance and rectification in membranes. J Gen Physiol 27:37–60

    Google Scholar 

  11. Grantham JJ, Burg MB, Orloff J (1970) The nature of transtubular Na and K transport in isolated rabbit renal collecting tubules. J Clin Invest 49:1815–1826

    Google Scholar 

  12. Gross P, Minuth WW, Frömter E (1986) Ionic conductances of apical and basal cell membranes of collecting duct principal cells in culture. Kidney Int 29:396

    Google Scholar 

  13. Gross P, Minuth WW, Kriz W, Frömter E (1986) Electrical properties of renal collecting duct principal cell epithelium in tissue culture. Pflügers Arch 406:380–386

    Google Scholar 

  14. Guggino SE, Suarez-Isla BA, Guggino W, Sacktor B (1985) Porskolin and antidiuretic hormone stimulate Ca++-activated K+ channel in cultured kidney cells. Am J Physiol 249:F448-F455

    Google Scholar 

  15. 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

    Google Scholar 

  16. Heeswijk van MPE, Geertsen JAM, Os van CH (1984) Kinetic properties of the ATP-dependent Ca2+ pump and the Na+/Ca2+ exchange system in basolateral membranes from rat kidney cortex. J Membrane Biol 79:19–31

    Google Scholar 

  17. Helman SI, O'Neil RG (1977) Model of active transepithelial Na and K transport of renal collecting tubule. Am J Physiol 233:F559-F571

    Google Scholar 

  18. Hille B (1984) Ionic channels of excitable membranes. Sinauer Assoc., Sunderland, Mass, USA

    Google Scholar 

  19. Hunter M, Lopes AG, Boulpaep EC, Giebisch GH (1984) Single channel recordings of calcium-activated potassium channels in the apical membrane of rabbit cortical collecting tubules. Proc Natl Acad Sci USA 81:4237–4239

    Google Scholar 

  20. Hunter M, Lopes AG, Boulpaep E, Giebisch G (1986) Regulation of single potassium ion channels from apical membrane of rabbit collecting tubule. Am J Physiol 251:F725-F733

    Google Scholar 

  21. Koeppen BM, Giebisch G (1985) Mineralocorticoid regulation of sodium and potassium transport by the cortical collecting duct. In: Graves JS (ed) Regulation and development of membrane transport processes. John Wiley, New York, pp 89–103

    Google Scholar 

  22. Koeppen BM, Biagi BA, Giebisch G (1983) Intracellular microelectrode characterisation of the rabbit cortical collecting duct. Am J Physiol 244:F35-F47

    Google Scholar 

  23. Latorre R, Miller C (1983) Conduction and selectivity in potassium channels. J Membr Biol 71:11–30

    Google Scholar 

  24. Madsen KM, Tisher CC (1986) Structural-functional relationships along the distal nephron. Am J Physiol 250 (Renal Fluid Electrolyte Physiol 19): F1-F15

    Google Scholar 

  25. Magleby KL, Palotta BS (1983) Calcium dependence of open and shut interval distributions from calcium-activated potassium channels in cultured rat muscle. J Physiol 344:585–604

    Google Scholar 

  26. Magleby KL, Palotta BS (1983) Burst kinetics of single calcium-activated potassium channels in cultured rat muscle. J Physiol 344:605–623

    Google Scholar 

  27. Marquardt DC (1963) An algorithm for least squares estimates of non-linear parameters. J SIAM 11:431–441

    Google Scholar 

  28. Marty A (1981) Ca++-dependent K+-channels with large unitary conductance in chromaffin cell membranes. Nature 291:497–500

    Google Scholar 

  29. Marty A (1983) Blocking of large unitary calcium-dependent potassium currents by internal sodium ions. Pflügers Arch 396:179–181

    Google Scholar 

  30. Marty A, Tan YP, Trautman A (1984) Three types of calcium-dependent channel in rat lacrimal glands. J Physiol 357:293–325

    Google Scholar 

  31. Maruyama Y, Petersen OH, Flanagan P, Pearson GT (1983) Quantification of Ca2+-activated K+ channels under hormonal control in pig pancreas acinar cells. Nature 305:228–232

    Google Scholar 

  32. Maruyama Y, Matsunaga H, Hoshi T (1986) Ca++- and voltage activated K+-channel in apical cell membrane of gallbladder epithelium fromTriturus. Pflügers Arch 406:563–567

    Google Scholar 

  33. McKinney TD, Burg MB (1978) Bicarbonate secretion by rabbit cortical collecting tubules in vitro. J Clin Invest 61:1421–1427

    Google Scholar 

  34. Minuth WW (1983) Induction and inhibition of outgrowth and development of renal collecting duct epithelium. Lab Invest 48:543–548

    Google Scholar 

  35. Minuth WW, Kriz W (1982) Renal collecting duct cells cultured as globular bodies and as monolayers. J Tiss Cult Meth 1:93–96

    Google Scholar 

  36. O'Neil RG, Helman SI (1977) Transport characteristics of renal collecting tubules: Influences of DOCA and diet. Am J Physiol 233:F544-F558

    Google Scholar 

  37. O'Neil RG, Sansom SC (1984) Characterisation of apical cell membrane Na+ and K+ conductances of cortical collecting duct using microclectrode technique. Am J Physiol 247:F14-F24

    Google Scholar 

  38. Palmer LE (1986) Patch clamp technique in renal physiology. Am J Physiol 250:F379-F385

    Google Scholar 

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

    Google Scholar 

  40. Schwartz GJ, Al-Awqati Q (1985) Carbon dioxide causes exocytosis of vesicles containing H+ pumps in isolated perfused proximal and collecting tubules. J Clin Invest 75:1638–1644

    Google Scholar 

  41. Schwartz GJ, Burg MG (1978) Mineralocorticoid effects on cation transport by cortical collecting tubules in vitro. Am J Physiol 235:F576-F585

    Google Scholar 

  42. Stokes JB (1981) Potassium secretion by cortical collecting tubule: Relation to sodium absorption, luminal sodium concentration, and transepithelial voltage. Am J Physiol 241:F395-F402

    Google Scholar 

  43. Stokes JB (1982) Ion transport by cortical and outer medullary collecting duct tubule. Kidney Int 22:473–484

    Google Scholar 

  44. Trautmann A, Marty A (1984) Activation of Ca-dependent K+ channels by carbamoylcholine in rat lacrimal glands. Proc Natl Acad Sci USA 81:611–615

    Google Scholar 

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

    Google Scholar 

  46. Windhager EE, Taylor A, Maack T, Lee CO, Lorenzen M (1982) Studies on renal tubular function. In: Corradina RA (ed) Functional regulation at the cellular and molecular levels. Elsevier/North-Holland, Amsterdam, pp 299–316

    Google Scholar 

  47. Wong DS, Lecar H, Adler M (1982) Single calcium-dependent potassium channels in clonal anterior pituitary cells. Biophys J 39:313–317

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Zentrum der Physiologie, Klinikum der J. W. Goethe-Universität, Theodor-Stern-Kai 7, D-6000, Frankfurt/M. 70, Federal Republic of Germany

    Alfred H. Gitter, Chadwick W. Christine & Ebrhard Frömter

  2. Section Physiology, VRT 826, Cornell University, 14853, Ithaca, NY, USA

    Klaus W. Beyenbach

  3. Medizinische Universitätsklinik, Universität Heidelberg, D-6900, Heidelberg, Federal Republic of Germany

    Peter Gross

  4. Anatomie I, Universität Heidelberg, D-6900, Heidelberg, Federal Republic of Germany

    Will W. Minuth

Authors
  1. Alfred H. Gitter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Klaus W. Beyenbach
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chadwick W. Christine
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Peter Gross
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Will W. Minuth
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ebrhard Frömter
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gitter, A.H., Beyenbach, K.W., Christine, C.W. et al. High-conductance K+ channel in apical membranes of principal cells cultured from rabbit renal cortical collecting duct anlagen. Pflugers Arch. 408, 282–290 (1987). https://doi.org/10.1007/BF02181471

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02181471

Key words

Search

Navigation