Skip to main content
NCBI home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1994 Jan;93(1):286–296. doi: 10.1172/JCI116958

Short-term effects of uninephrectomy on electrical properties of the cortical collecting duct from rabbit remnant kidneys.

S Muto 1, S Ebata 1, Y Asano 1
PMCID: PMC293764  PMID: 8282799

Abstract

Microelectrode techniques were used to assess the electrical properties of the collecting duct cell in the isolated perfused cortical collecting duct from remnant kidneys 3, 6, and 24 h after uninephrectomy (UNX); results were compared with those from sham-operated kidneys. Plasma aldosterone levels did not change during the time course after UNX. The lumen-negative transepithelial voltage was elevated significantly 3 h after UNX, and was increased further 24 h after UNX. The basolateral membrane voltage (VB) was elevated 6 h after UNX, and then was increased further at 24 h. Although the tight junction conductance and the fractional apical membrane resistance (fRA) were not altered at any time points after UNX, the apical membrane conductance as well as the transepithelial (GT) and basolateral membrane conductances increased 6 and 24 h after UNX. The changes in apical membrane voltage, GT, and fRA upon addition of luminal amiloride increased just 3 h after UNX, and then remained elevated at 6 and 24 h. The changes in apical membrane voltage and GT upon addition of luminal Ba2+, the changes in VB upon addition of bath ouabain, and the changes in VB, GT, and fRA upon raising bath K+ were not influenced 3 h after UNX, but increased at 6 and 24 h. At these latter periods after UNX, the transference number of Cl- of the basolateral membrane decreased significantly, whereas the transference number of K+ of the basolateral membrane increased significantly. Simultaneously, addition of Ba2+ to the bath caused the VB to hyperpolarize in parallel with decreases in GT and fRA. We conclude: (a) the initial effect of UNX (3 h) in the collecting duct cell is an increase in apical membrane Na+ conductance; (b) the delayed effects of UNX (6 and 24 h) are increases in apical membrane K+ conductance as well as basolateral membrane Na(+)-K+ pump activity and K+ conductance; (c) the hyperpolarization of VB at 6 and 24 h after UNX may result in the decrease of the ratio of the relative Cl- conductance to the relative K+ conductance of the basolateral membrane and also may increase passive K+ entry into the cell across the basolateral membrane; (d) these time-dependent electrical changes occur independently of plasma aldosterone levels.

Full text

PDF
286

Images in this article

294Image
on p.294

Selected References

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

  1. 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]
  2. Diezi J., Michoud P., Grandchamp A., Giebisch G. Effects of nephrectomy on renal salt and water transport in the remaining kidney. Kidney Int. 1976 Dec;10(6):450–462. doi: 10.1038/ki.1976.132. [DOI] [PubMed] [Google Scholar]
  3. Ebata S., Muto S., Asano Y. Effects of uninephrectomy on electrical properties of the cortical collecting duct from rabbit remnant kidneys. J Clin Invest. 1992 Oct;90(4):1547–1557. doi: 10.1172/JCI116023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ellison D. H., Velázquez H., Wright F. S. Adaptation of the distal convoluted tubule of the rat. Structural and functional effects of dietary salt intake and chronic diuretic infusion. J Clin Invest. 1989 Jan;83(1):113–126. doi: 10.1172/JCI113847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Fine L. G., Yanagawa N., Schultze R. G., Tuck M., Trizna W. Functional profile of the isolated uremic nephron: potassium adaptation in the rabbit cortical collecting tubule. J Clin Invest. 1979 Oct;64(4):1033–1043. doi: 10.1172/JCI109540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Good D. W., Wright F. S. Luminal influences on potassium secretion: sodium concentration and fluid flow rate. Am J Physiol. 1979 Feb;236(2):F192–F205. doi: 10.1152/ajprenal.1979.236.2.F192. [DOI] [PubMed] [Google Scholar]
  7. Halliburton I. W., Thomson R. Y. Chemical aspects of compensatory renal hypertrophy. Cancer Res. 1965 Dec;25(11):1882–1887. [PubMed] [Google Scholar]
  8. Hayslett J. P. Functional adaptation to reduction in renal mass. Physiol Rev. 1979 Jan;59(1):137–164. doi: 10.1152/physrev.1979.59.1.137. [DOI] [PubMed] [Google Scholar]
  9. Kaissling B., Bachmann S., Kriz W. Structural adaptation of the distal convoluted tubule to prolonged furosemide treatment. Am J Physiol. 1985 Mar;248(3 Pt 2):F374–F381. doi: 10.1152/ajprenal.1985.248.3.F374. [DOI] [PubMed] [Google Scholar]
  10. Kaissling B., Le Hir M. Distal tubular segments of the rabbit kidney after adaptation to altered Na- and K-intake. I. Structural changes. Cell Tissue Res. 1982;224(3):469–492. doi: 10.1007/BF00213746. [DOI] [PubMed] [Google Scholar]
  11. Kaissling B., Stanton B. A. Adaptation of distal tubule and collecting duct to increased sodium delivery. I. Ultrastructure. Am J Physiol. 1988 Dec;255(6 Pt 2):F1256–F1268. doi: 10.1152/ajprenal.1988.255.6.F1256. [DOI] [PubMed] [Google Scholar]
  12. Koeppen B. M., Biagi B. A., Giebisch G. H. Intracellular microelectrode characterization of the rabbit cortical collecting duct. Am J Physiol. 1983 Jan;244(1):F35–F47. doi: 10.1152/ajprenal.1983.244.1.F35. [DOI] [PubMed] [Google Scholar]
  13. Muto S., Furuya H., Tabei K., Asano Y. Site and mechanism of action of epidermal growth factor in rabbit cortical collecting duct. Am J Physiol. 1991 Feb;260(2 Pt 2):F163–F169. doi: 10.1152/ajprenal.1991.260.2.F163. [DOI] [PubMed] [Google Scholar]
  14. Muto S., Giebisch G., Sansom S. Effects of adrenalectomy on CCD: evidence for differential response of two cell types. Am J Physiol. 1987 Oct;253(4 Pt 2):F742–F752. doi: 10.1152/ajprenal.1987.253.4.F742. [DOI] [PubMed] [Google Scholar]
  15. Muto S., Imai M., Asano Y. Effect of nafamostat mesilate on Na+ and K+ transport properties in the rabbit cortical collecting duct. Br J Pharmacol. 1993 Jul;109(3):673–678. doi: 10.1111/j.1476-5381.1993.tb13626.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Muto S., Miyata Y., Asano Y. Electrical properties of the rabbit cortical collecting duct from obstructed and contralateral kidneys after unilateral ureteral obstruction. J Clin Invest. 1993 Aug;92(2):571–581. doi: 10.1172/JCI116624. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Muto S., Sansom S., Giebisch G. Effects of a high potassium diet on electrical properties of cortical collecting ducts from adrenalectomized rabbits. J Clin Invest. 1988 Feb;81(2):376–380. doi: 10.1172/JCI113329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Muto S., Yasoshima K., Yoshitomi K., Imai M., Asano Y. Electrophysiological identification of alpha- and beta-intercalated cells and their distribution along the rabbit distal nephron segments. J Clin Invest. 1990 Dec;86(6):1829–1839. doi: 10.1172/JCI114913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. O'Neil R. G., Hayhurst R. A. Sodium-dependent modulation of the renal Na-K-ATPase: influence of mineralocorticoids on the cortical collecting duct. J Membr Biol. 1985;85(2):169–179. doi: 10.1007/BF01871269. [DOI] [PubMed] [Google Scholar]
  20. O'Neil R. G., Helman S. I. Transport characteristics of renal collecting tubules: influences of DOCA and diet. Am J Physiol. 1977 Dec;233(6):F544–F558. doi: 10.1152/ajprenal.1977.233.6.F544. [DOI] [PubMed] [Google Scholar]
  21. O'Neil R. G., Sansom S. C. Electrophysiological properties of cellular and paracellular conductive pathways of the rabbit cortical collecting duct. J Membr Biol. 1984;82(3):281–295. doi: 10.1007/BF01871637. [DOI] [PubMed] [Google Scholar]
  22. Sansom S. C., Agulian S., Muto S., Illig V., Giebisch G. K activity of CCD principal cells from normal and DOCA-treated rabbits. Am J Physiol. 1989 Jan;256(1 Pt 2):F136–F142. doi: 10.1152/ajprenal.1989.256.1.F136. [DOI] [PubMed] [Google Scholar]
  23. Sansom S. C., La B. Q., Carosi S. L. Double-barreled chloride channels of collecting duct basolateral membrane. Am J Physiol. 1990 Jul;259(1 Pt 2):F46–F52. doi: 10.1152/ajprenal.1990.259.1.F46. [DOI] [PubMed] [Google Scholar]
  24. Sansom S. C., O'Neil R. G. Effects of mineralocorticoids on transport properties of cortical collecting duct basolateral membrane. Am J Physiol. 1986 Oct;251(4 Pt 2):F743–F757. doi: 10.1152/ajprenal.1986.251.4.F743. [DOI] [PubMed] [Google Scholar]
  25. Sansom S. C., O'Neil R. G. Mineralocorticoid regulation of apical cell membrane Na+ and K+ transport of the cortical collecting duct. Am J Physiol. 1985 Jun;248(6 Pt 2):F858–F868. doi: 10.1152/ajprenal.1985.248.6.F858. [DOI] [PubMed] [Google Scholar]
  26. Sansom S. C., Weinman E. J., O'Neil R. G. Microelectrode assessment of chloride-conductive properties of cortical collecting duct. Am J Physiol. 1984 Aug;247(2 Pt 2):F291–F302. doi: 10.1152/ajprenal.1984.247.2.F291. [DOI] [PubMed] [Google Scholar]
  27. Sansom S., Muto S., Giebisch G. Na-dependent effects of DOCA on cellular transport properties of CCDs from ADX rabbits. Am J Physiol. 1987 Oct;253(4 Pt 2):F753–F759. doi: 10.1152/ajprenal.1987.253.4.F753. [DOI] [PubMed] [Google Scholar]
  28. Scherzer P., Wald H., Czaczkes J. W. Na-K-ATPase in isolated rabbit tubules after unilateral nephrectomy and Na+ loading. Am J Physiol. 1985 Apr;248(4 Pt 2):F565–F573. doi: 10.1152/ajprenal.1985.248.4.F565. [DOI] [PubMed] [Google Scholar]
  29. Scherzer P., Wald H., Popovtzer M. M. Enhanced glomerular filtration and Na+-K+-ATPase with furosemide administration. Am J Physiol. 1987 May;252(5 Pt 2):F910–F915. doi: 10.1152/ajprenal.1987.252.5.F910. [DOI] [PubMed] [Google Scholar]
  30. Shimizu T., Yoshitomi K., Taniguchi J., Imai M. Effect of high NaCl intake on Na+ and K+ transport in the rabbit distal convoluted tubule. Pflugers Arch. 1989 Sep;414(5):500–508. doi: 10.1007/BF00580984. [DOI] [PubMed] [Google Scholar]
  31. Shirley D. G., Walter S. J. Acute and chronic changes in renal function following unilateral nephrectomy. Kidney Int. 1991 Jul;40(1):62–68. doi: 10.1038/ki.1991.180. [DOI] [PubMed] [Google Scholar]
  32. Stanton B. A., Kaissling B. Adaptation of distal tubule and collecting duct to increased Na delivery. II. Na+ and K+ transport. Am J Physiol. 1988 Dec;255(6 Pt 2):F1269–F1275. doi: 10.1152/ajprenal.1988.255.6.F1269. [DOI] [PubMed] [Google Scholar]
  33. Stanton B. A., Kaissling B. Regulation of renal ion transport and cell growth by sodium. Am J Physiol. 1989 Jul;257(1 Pt 2):F1–10. doi: 10.1152/ajprenal.1989.257.1.F1. [DOI] [PubMed] [Google Scholar]
  34. Stokes J. B. Potassium secretion by cortical collecting tubule: relation to sodium absorption, luminal sodium concentration, and transepithelial voltage. Am J Physiol. 1981 Oct;241(4):F395–F402. doi: 10.1152/ajprenal.1981.241.4.F395. [DOI] [PubMed] [Google Scholar]
  35. Toback F. G., Lowenstein L. M. Thymidine metabolism during normal and compensatory renal growth. Growth. 1974 Mar;38(1):35–44. [PubMed] [Google Scholar]
  36. Vehaskari V. M., Hering-Smith K. S., Klahr S., Hamm L. L. Increased sodium transport by cortical collecting tubules from remnant kidneys. Kidney Int. 1989 Jul;36(1):89–95. doi: 10.1038/ki.1989.165. [DOI] [PubMed] [Google Scholar]
  37. Zalups R. K., Stanton B. A., Wade J. B., Giebisch G. Structural adaptation in initial collecting tubule following reduction in renal mass. Kidney Int. 1985 Apr;27(4):636–642. doi: 10.1038/ki.1985.58. [DOI] [PubMed] [Google Scholar]

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

RESOURCES