Skip to main content
NCBI home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1993 Oct;92(4):1881–1888. doi: 10.1172/JCI116780

Cellular heterogeneity of ammonium ion transport across the basolateral membrane of the hamster medullary thick ascending limb of Henle's loop.

S Tsuruoka 1, M Takeda 1, K Yoshitomi 1, M Imai 1
PMCID: PMC288353  PMID: 8408639

Abstract

The epithelia of the medullary thick ascending limb (MAL) consists of two cell types, high (HBC) and low basolateral conductance (LBC) cell, depending on the K+ conductance of the basolateral membrane. The NH4+ conductance distinct from the K+ conductance has been suggested to exist in the proximal tubule, MAL cell, and Xenopus oocyte. The present study was designed to examine whether there is a conductive NH4+ transport system distinct from K+ conductance in two different cell types of the hamster MAL perfused in vitro. The basolateral membrane voltage (VB) was measured by impaling cells with conventional microelectrodes. Addition of NH4+ to the bath depolarized VB in a dose-dependent manner in both cell types. The response was maintained in the absence of HCO3-. When the VB deflection elicited upon 50 mM KCl or NH4Cl in the bath (delta VBK+ or delta VBNH4+) were compared, delta VBNH4+ was almost the same as delta VBK+ in the HBC cell, whereas the former was greater than the latter in the LBC. In the HBC cell, 10 mM Ba2+ in the bath equally suppressed both delta VBK+ and delta VBNH4+, whereas in the LBC cell it suppressed delta VBK+ with a small effect on delta VBNH4+, indicating that NH4+ is transported via a pathway distinct from Ba(2+)-sensitive K+ conductance. The VB deflection by NH4+ was unaffected by addition of 0.1 mM ouabain or 10 microM 5-nitro-2-(3-phenylpropylamino)-benzoate (a Cl- channel blocker) to the bath, excluding the contribution of the Na+, K+ pump or Cl- channel. An abrupt reduction of Na+ in the bath from 200 to 20 mM did not cause any changes in VB, suggesting that a nonselective cation channel may not account for the NH4+ transport. Amiloride at 10 microM inhibited delta VBNH4+ with a higher efficacy in the LBC cell. We conclude that a rheogenic NH4+ transport system independent from the K+ conductance exists in the basolateral membrane of the LBC cell of the hamster MAL, and may play some roles in the regulation of NH4+ transport.

Full text

PDF
1881

Images in this article

1884Image
on p.1884

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. 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]
  2. Burckhardt B. C., Frömter E. Pathways of NH3/NH4+ permeation across Xenopus laevis oocyte cell membrane. Pflugers Arch. 1992 Jan;420(1):83–86. doi: 10.1007/BF00378645. [DOI] [PubMed] [Google Scholar]
  3. Burg M., Grantham J., Abramow M., Orloff J. Preparation and study of fragments of single rabbit nephrons. Am J Physiol. 1966 Jun;210(6):1293–1298. doi: 10.1152/ajplegacy.1966.210.6.1293. [DOI] [PubMed] [Google Scholar]
  4. Discala F., Hulin P., Belachgar F., Planelles G., Edelman A., Anagnostopoulos T. Millimolar amiloride concentrations block K conductance in proximal tubular cells. Br J Pharmacol. 1992 Oct;107(2):532–538. doi: 10.1111/j.1476-5381.1992.tb12779.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Garvin J. L., Burg M. B., Knepper M. A. Active NH4+ absorption by the thick ascending limb. Am J Physiol. 1988 Jul;255(1 Pt 2):F57–F65. doi: 10.1152/ajprenal.1988.255.1.F57. [DOI] [PubMed] [Google Scholar]
  6. Good D. W. Active absorption of NH4+ by rat medullary thick ascending limb: inhibition by potassium. Am J Physiol. 1988 Jul;255(1 Pt 2):F78–F87. doi: 10.1152/ajprenal.1988.255.1.F78. [DOI] [PubMed] [Google Scholar]
  7. Good D. W., Knepper M. A. Ammonia transport in the mammalian kidney. Am J Physiol. 1985 Apr;248(4 Pt 2):F459–F471. doi: 10.1152/ajprenal.1985.248.4.F459. [DOI] [PubMed] [Google Scholar]
  8. Good D. W., Knepper M. A., Burg M. B. Ammonia and bicarbonate transport by thick ascending limb of rat kidney. Am J Physiol. 1984 Jul;247(1 Pt 2):F35–F44. doi: 10.1152/ajprenal.1984.247.1.F35. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Guggino W. B. Functional heterogeneity in the early distal tubule of the Amphiuma kidney: evidence for two modes of Cl- and K+ transport across the basolateral cell membrane. Am J Physiol. 1986 Mar;250(3 Pt 2):F430–F440. doi: 10.1152/ajprenal.1986.250.3.F430. [DOI] [PubMed] [Google Scholar]
  11. Kikeri D., Azar S., Sun A., Zeidel M. L., Hebert S. C. Na(+)-H+ antiporter and Na(+)-(HCO3-)n symporter regulate intracellular pH in mouse medullary thick limbs of Henle. Am J Physiol. 1990 Mar;258(3 Pt 2):F445–F456. doi: 10.1152/ajprenal.1990.258.3.F445. [DOI] [PubMed] [Google Scholar]
  12. Kikeri D., Sun A., Zeidel M. L., Hebert S. C. Cell membranes impermeable to NH3. Nature. 1989 Jun 8;339(6224):478–480. doi: 10.1038/339478a0. [DOI] [PubMed] [Google Scholar]
  13. Kinne R., Kinne-Saffran E., Schütz H., Schölermann B. Ammonium transport in medullary thick ascending limb of rabbit kidney: involvement of the Na+,K+,Cl(-)-cotransporter. J Membr Biol. 1986;94(3):279–284. doi: 10.1007/BF01869723. [DOI] [PubMed] [Google Scholar]
  14. Knepper M. A. NH4+ transport in the kidney. Kidney Int Suppl. 1991 Jul;33:S95–102. [PubMed] [Google Scholar]
  15. Krapf R. Basolateral membrane H/OH/HCO3 transport in the rat cortical thick ascending limb. Evidence for an electrogenic Na/HCO3 cotransporter in parallel with a Na/H antiporter. J Clin Invest. 1988 Jul;82(1):234–241. doi: 10.1172/JCI113576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Sasaki S., Ishibashi K., Nagai T., Marumo F. Regulation mechanisms of intracellular pH of Xenopus laevis oocyte. Biochim Biophys Acta. 1992 Oct 6;1137(1):45–51. doi: 10.1016/0167-4889(92)90098-v. [DOI] [PubMed] [Google Scholar]
  17. Völkl H., Lang F. Electrophysiology of ammonia transport in renal straight proximal tubules. Kidney Int. 1991 Dec;40(6):1082–1089. doi: 10.1038/ki.1991.318. [DOI] [PubMed] [Google Scholar]
  18. Wangemann P., Wittner M., Di Stefano A., Englert H. C., Lang H. J., Schlatter E., Greger R. Cl(-)-channel blockers in the thick ascending limb of the loop of Henle. Structure activity relationship. Pflugers Arch. 1986;407 (Suppl 2):S128–S141. doi: 10.1007/BF00584942. [DOI] [PubMed] [Google Scholar]
  19. Yoshitomi K., Koseki C., Taniguchi J., Imai M. Functional heterogeneity in the hamster medullary thick ascending limb of Henle's loop. Pflugers Arch. 1987 May;408(6):600–608. doi: 10.1007/BF00581162. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES