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. 1994 Jun 1;103(6):1055–1070. doi: 10.1085/jgp.103.6.1055

Basic properties and potential regulators of the apical K+ channel in macula densa cells

PMCID: PMC2216885  PMID: 7931137

Abstract

These studies examine the properties of an apical potassium (K+) channel in macula densa cells, a specialized group of cells involved in tubuloglomerular feedback signal transmission. To this end, individual glomeruli with thick ascending limbs (TAL) and macula densa cells were dissected from rabbit kidney and the TAL covering macula densa cells was removed. Using patch clamp techniques, we found a high density (up to 54 channels per patch) of K+ channels in the apical membrane of macula densa cells. An inward conductance of 41.1 +/- 4.8 pS was obtained in cell-attached patches (patch pipette, 140 mM K+). In inside- out patches (patch pipette, 140 mM; bath, 5 mM K+), inward currents of 1.1 +/- 0.1 pA (n = 11) were observed at 0 mV and single channel current reversed at a pipette potential of -84 mV giving a permeability ratio (PK/PNa) of over 100. In cell-attached patches, mean channel open probability (N,Po, where N is number of channels in the patch and Po is single channel open probability) was unaffected by bumetanide, but was reduced from 11.3 +/- 2.7 to 1.6 +/- 1.3 (n = 5, p < 0.02) by removal of bath sodium (Na+). Simultaneous removal of bath Na+ and calcium (Ca2+) prevented the Na(+)-induced decrease in N.Po indicating that the effect of Na+ removal on N.Po was probably mediated by stimulation of Ca2+ entry. This interpretation was supported by studies where ionomycin, which directly increases intracellular Ca2+, produced a fall in N.Po from 17.8 +/- 4.0 to 5.9 +/- 4.1 (n = 7, p < 0.02). In inside- out patches, the apical K+ channel was not sensitive to ATP but was directly blocked by 2 mM Ca2+ and by lowering bath pH from 7.4 to 6.8. These studies constitute the first single channel observations on macula densa cells and establish some of the characteristics and regulators of this apical K+ channel. This channel is likely to be involved in macula densa transepithelial Cl- transport and perhaps in the tubuloglomerular feedback signaling process.

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Selected References

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  1. Beck J. S., Hurst A. M., Lapointe J. Y., Laprade R. Regulation of basolateral K channels in proximal tubule studied during continuous microperfusion. Am J Physiol. 1993 Mar;264(3 Pt 2):F496–F501. doi: 10.1152/ajprenal.1993.264.3.F496. [DOI] [PubMed] [Google Scholar]
  2. Bell P. D. Calcium antagonists and intrarenal regulation of glomerular filtration rate. Am J Nephrol. 1987;7 (Suppl 1):24–31. doi: 10.1159/000167539. [DOI] [PubMed] [Google Scholar]
  3. Bell P. D. Cyclic AMP-calcium interaction in the transmission of tubuloglomerular feedback signals. Kidney Int. 1985 Nov;28(5):728–732. doi: 10.1038/ki.1985.191. [DOI] [PubMed] [Google Scholar]
  4. Bell P. D., Lapointe J. Y., Cardinal J. Direct measurement of basolateral membrane potentials from cells of the macula densa. Am J Physiol. 1989 Sep;257(3 Pt 2):F463–F468. doi: 10.1152/ajprenal.1989.257.3.F463. [DOI] [PubMed] [Google Scholar]
  5. Bleich M., Schlatter E., Greger R. The luminal K+ channel of the thick ascending limb of Henle's loop. Pflugers Arch. 1990 Jan;415(4):449–460. doi: 10.1007/BF00373623. [DOI] [PubMed] [Google Scholar]
  6. Briggs J. P., Schnermann J. The tubuloglomerular feedback mechanism: functional and biochemical aspects. Annu Rev Physiol. 1987;49:251–273. doi: 10.1146/annurev.ph.49.030187.001343. [DOI] [PubMed] [Google Scholar]
  7. Briggs J. The macula densa sensing mechanism for tubuloglomerular feedback. Fed Proc. 1981 Jan;40(1):99–103. [PubMed] [Google Scholar]
  8. Greger R. Ion transport mechanisms in thick ascending limb of Henle's loop of mammalian nephron. Physiol Rev. 1985 Jul;65(3):760–797. doi: 10.1152/physrev.1985.65.3.760. [DOI] [PubMed] [Google Scholar]
  9. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  10. Hurst A. M., Duplain M., Lapointe J. Y. Basolateral membrane potassium channels in rabbit cortical thick ascending limb. Am J Physiol. 1992 Aug;263(2 Pt 2):F262–F267. doi: 10.1152/ajprenal.1992.263.2.F262. [DOI] [PubMed] [Google Scholar]
  11. Hurst A. M., Hunter M. Apical K+ channels of frog diluting segment: inhibition by acidification. Pflugers Arch. 1989 Oct;415(1):115–117. doi: 10.1007/BF00373148. [DOI] [PubMed] [Google Scholar]
  12. Hurst A. M., Hunter M. Apical membrane potassium channels in frog diluting segment: stimulation by furosemide. Am J Physiol. 1992 Apr;262(4 Pt 2):F606–F614. doi: 10.1152/ajprenal.1992.262.4.F606. [DOI] [PubMed] [Google Scholar]
  13. Kirk K. L., Bell P. D., Barfuss D. W., Ribadeneira M. Direct visualization of the isolated and perfused macula densa. Am J Physiol. 1985 Jun;248(6 Pt 2):F890–F894. doi: 10.1152/ajprenal.1985.248.6.F890. [DOI] [PubMed] [Google Scholar]
  14. Lapointe J. Y., Bell P. D., Cardinal J. Direct evidence for apical Na+:2Cl-:K+ cotransport in macula densa cells. Am J Physiol. 1990 May;258(5 Pt 2):F1466–F1469. doi: 10.1152/ajprenal.1990.258.5.F1466. [DOI] [PubMed] [Google Scholar]
  15. Lapointe J. Y., Bell P. D., Hurst A. M., Cardinal J. Basolateral ionic permeabilities of macula densa cells. Am J Physiol. 1991 Jun;260(6 Pt 2):F856–F860. doi: 10.1152/ajprenal.1991.260.6.F856. [DOI] [PubMed] [Google Scholar]
  16. Pirie S. C., Potts D. J. Application of cold flush preservation to in vitro microperfusion studies of kidney tubules. Kidney Int. 1985 Dec;28(6):982–984. doi: 10.1038/ki.1985.227. [DOI] [PubMed] [Google Scholar]
  17. Rasmussen H., Barrett P. Q. Calcium messenger system: an integrated view. Physiol Rev. 1984 Jul;64(3):938–984. doi: 10.1152/physrev.1984.64.3.938. [DOI] [PubMed] [Google Scholar]
  18. Salomonsson M., Gonzalez E., Kornfeld M., Persson A. E. The cytosolic chloride concentration in macula densa and cortical thick ascending limb cells. Acta Physiol Scand. 1993 Mar;147(3):305–313. doi: 10.1111/j.1748-1716.1993.tb09503.x. [DOI] [PubMed] [Google Scholar]
  19. Salomonsson M., Gonzalez E., Westerlund P., Persson A. E. Intracellular cytosolic free calcium concentration in the macula densa and in ascending limb cells at different luminal concentrations of sodium chloride and with added furosemide. Acta Physiol Scand. 1991 Jun;142(2):283–290. doi: 10.1111/j.1748-1716.1991.tb09158.x. [DOI] [PubMed] [Google Scholar]
  20. Schlatter E. Effect of various diuretics on membrane voltage of macula densa cells. Whole-cell patch-clamp experiments. Pflugers Arch. 1993 Apr;423(1-2):74–77. doi: 10.1007/BF00374963. [DOI] [PubMed] [Google Scholar]
  21. Schlatter E., Salomonsson M., Persson A. E., Greger R. Macula densa cells sense luminal NaCl concentration via furosemide sensitive Na+2Cl-K+ cotransport. Pflugers Arch. 1989 Jul;414(3):286–290. doi: 10.1007/BF00584628. [DOI] [PubMed] [Google Scholar]
  22. Schnermann J., Ploth D. W., Hermle M. Activation of tubulo-glomerular feedback by chloride transport. Pflugers Arch. 1976 Apr 6;362(3):229–240. doi: 10.1007/BF00581175. [DOI] [PubMed] [Google Scholar]
  23. Skøtt O., Briggs J. P. Direct demonstration of macula densa-mediated renin secretion. Science. 1987 Sep 25;237(4822):1618–1620. doi: 10.1126/science.3306925. [DOI] [PubMed] [Google Scholar]
  24. Wang W. H., White S., Geibel J., Giebisch G. A potassium channel in the apical membrane of rabbit thick ascending limb of Henle's loop. Am J Physiol. 1990 Feb;258(2 Pt 2):F244–F253. doi: 10.1152/ajprenal.1990.258.2.F244. [DOI] [PubMed] [Google Scholar]
  25. Wright F. S. Characteristics of feedback control of glomerular filtration rate. Fed Proc. 1981 Jan;40(1):87–92. [PubMed] [Google Scholar]
  26. Wright F. S., Schnermann J. Interference with feedback control of glomerular filtration rate by furosemide, triflocin, and cyanide. J Clin Invest. 1974 Jun;53(6):1695–1708. doi: 10.1172/JCI107721. [DOI] [PMC free article] [PubMed] [Google Scholar]

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