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. 1993 Jun;91(6):2776–2784. doi: 10.1172/JCI116519

Renal bicarbonate reabsorption in the rat. IV. Bicarbonate transport mechanisms in the early and late distal tubule.

T Wang 1, G Malnic 1, G Giebisch 1, Y L Chan 1
PMCID: PMC443344  PMID: 8390489

Abstract

Bicarbonate transport was studied in vivo by separate microperfusion experiments of early and late distal tubules. Total CO2 was measured by microcalorimetry and fluid absorption by 3H-inulin. Significant bicarbonate absorption was observed in all experimental conditions. Bicarbonate transport was load-dependent upon increasing the luminal bicarbonate concentration from 15 to 50 mM in both early and late distal tubule segments and remained constant at higher concentrations at a maximum rate of 100-110 pmol/min per mm. At low lumen bicarbonate concentrations (15 mM), higher rates of bicarbonate absorption were observed in early (32.9 +/- 4.57 pmol/min per mm) as compared to late distal tubules (10.7 +/- 3.1 pmol/min per mm). Amiloride and ethyl-isopropylamiloride both inhibited early but not late distal tubule bicarbonate absorption whereas acetazolamide blocked bicarbonate transport in both tubule segments. Fluid absorption was significantly reduced in both tubule segments by amiloride but only in early distal tubules by ethyl-isopropylamiloride. Substitution of lumen chloride by gluconate increased bicarbonate absorption in late but not in early distal tubules. Bafilomycin A1, an inhibitor of H-ATPase, inhibited late and also early distal tubule bicarbonate absorption, the latter at higher concentration. After 8 d on a low K diet, bicarbonate absorption increased significantly in both early and late distal tubules. Schering compound 28080, a potent H-K ATPase inhibitor, completely blocked this increment of bicarbonate absorption in late but not in early distal tubule. The data suggest bicarbonate absorption via Na(+)-H+ exchange and H-ATPase in early, but only by amiloride-insensitive H+ secretion (H-ATPase) in late distal tubules. The study also provides evidence for activation of K(+)-H+ exchange in late distal tubules of K depleted rats. Indirect evidence implies a component of chloride-dependent bicarbonate secretion in late distal tubules and suggests that net bicarbonate transport at this site results from bidirectional bicarbonate movement.

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Selected References

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  1. Alpern R. J., Cogan M. G., Rector F. C., Jr Effect of luminal bicarbonate concentration on proximal acidification in the rat. Am J Physiol. 1982 Jul;243(1):F53–F59. doi: 10.1152/ajprenal.1982.243.1.F53. [DOI] [PubMed] [Google Scholar]
  2. Alpern R. J., Cogan M. G., Rector F. C., Jr Flow dependence of proximal tubular bicarbonate absorption. Am J Physiol. 1983 Oct;245(4):F478–F484. doi: 10.1152/ajprenal.1983.245.4.F478. [DOI] [PubMed] [Google Scholar]
  3. Aronson P. S. Mechanisms of active H+ secretion in the proximal tubule. Am J Physiol. 1983 Dec;245(6):F647–F659. doi: 10.1152/ajprenal.1983.245.6.F647. [DOI] [PubMed] [Google Scholar]
  4. Barfuss D. W., Schafer J. A. Rate of formation and composition of absorbate from proximal nephron segments. Am J Physiol. 1984 Jul;247(1 Pt 2):F117–F129. doi: 10.1152/ajprenal.1984.247.1.F117. [DOI] [PubMed] [Google Scholar]
  5. Berry C. A. Water permeability and pathways in the proximal tubule. Am J Physiol. 1983 Sep;245(3):F279–F294. doi: 10.1152/ajprenal.1983.245.3.F279. [DOI] [PubMed] [Google Scholar]
  6. Bichara M., Mercier O., Houillier P., Paillard M., Leviel F. Effects of antidiuretic hormone on urinary acidification and on tubular handling of bicarbonate in the rat. J Clin Invest. 1987 Sep;80(3):621–630. doi: 10.1172/JCI113114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brown D., Hirsch S., Gluck S. Localization of a proton-pumping ATPase in rat kidney. J Clin Invest. 1988 Dec;82(6):2114–2126. doi: 10.1172/JCI113833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Capasso G., Jaeger P., Giebisch G., Guckian V., Malnic G. Renal bicarbonate reabsorption in the rat. II. Distal tubule load dependence and effect of hypokalemia. J Clin Invest. 1987 Aug;80(2):409–414. doi: 10.1172/JCI113087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Capasso G., Kinne R., Malnic G., Giebisch G. Renal bicarbonate reabsorption in the rat. I. Effects of hypokalemia and carbonic anhydrase. J Clin Invest. 1986 Dec;78(6):1558–1567. doi: 10.1172/JCI112748. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Capasso G., Unwin R., Giebisch G. Role of the loop of Henle in urinary acidification. Kidney Int Suppl. 1991 Jul;33:S33–S35. [PubMed] [Google Scholar]
  11. Chan Y. L., Malnic G., Giebisch G. Renal bicarbonate reabsorption in the rat. III. Distal tubule perfusion study of load dependence and bicarbonate permeability. J Clin Invest. 1989 Sep;84(3):931–938. doi: 10.1172/JCI114255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Costanzo L. S. Localization of diuretic action in microperfused rat distal tubules: Ca and Na transport. Am J Physiol. 1985 Apr;248(4 Pt 2):F527–F535. doi: 10.1152/ajprenal.1985.248.4.F527. [DOI] [PubMed] [Google Scholar]
  13. Crayen M. L., Thoenes W. Architecture and cell structures in the distal nephron of the rat kidney. Cytobiologie. 1978 Jun;17(1):197–211. [PubMed] [Google Scholar]
  14. Garg L. C., Narang N. Effects of low-potassium diet on N-ethylmaleimide-sensitive ATPase in the distal nephron segments. Ren Physiol Biochem. 1990 May-Jun;13(3):129–136. doi: 10.1159/000173359. [DOI] [PubMed] [Google Scholar]
  15. Gifford J. D., Rome L., Galla J. H. H(+)-K(+)-ATPase activity in rat collecting duct segments. Am J Physiol. 1992 Apr;262(4 Pt 2):F692–F695. doi: 10.1152/ajprenal.1992.262.4.F692. [DOI] [PubMed] [Google Scholar]
  16. Good D. W. Sodium-dependent bicarbonate absorption by cortical thick ascending limb of rat kidney. Am J Physiol. 1985 Jun;248(6 Pt 2):F821–F829. doi: 10.1152/ajprenal.1985.248.6.F821. [DOI] [PubMed] [Google Scholar]
  17. Hersey S. J., Steiner L., Mendlein J., Rabon E., Sachs G. SCH28080 prevents omeprazole inhibition of the gastric H+/K+-ATPase. Biochim Biophys Acta. 1988 Aug 31;956(1):49–57. doi: 10.1016/0167-4838(88)90296-8. [DOI] [PubMed] [Google Scholar]
  18. Iacovitti M., Nash L., Peterson L. N., Rochon J., Levine D. Z. Distal tubule bicarbonate accumulation in vivo. Effect of flow and transtubular bicarbonate gradients. J Clin Invest. 1986 Dec;78(6):1658–1665. doi: 10.1172/JCI112759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Khadouri C., Cheval L., Marsy S., Barlet-Bas C., Doucet A. Characterization and control of proton-ATPase along the nephron. Kidney Int Suppl. 1991 Jul;33:S71–S78. [PubMed] [Google Scholar]
  20. Kriz W., Bankir L. A standard nomenclature for structures of the kidney. The Renal Commission of the International Union of Physiological Sciences (IUPS). Kidney Int. 1988 Jan;33(1):1–7. doi: 10.1038/ki.1988.1. [DOI] [PubMed] [Google Scholar]
  21. Kunau R. T., Jr, Walker K. A. Total CO2 absorption in the distal tubule of the rat. Am J Physiol. 1987 Mar;252(3 Pt 2):F468–F473. doi: 10.1152/ajprenal.1987.252.3.F468. [DOI] [PubMed] [Google Scholar]
  22. Kurtz I. Apical Na+/H+ antiporter and glycolysis-dependent H+-ATPase regulate intracellular pH in the rabbit S3 proximal tubule. J Clin Invest. 1987 Oct;80(4):928–935. doi: 10.1172/JCI113184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Levine D. Z. An in vivo microperfusion study of distal tubule bicarbonate reabsorption in normal and ammonium chloride rats. J Clin Invest. 1985 Feb;75(2):588–595. doi: 10.1172/JCI111735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Levine D. Z., Iacovitti M., Nash L., Vandorpe D. Secretion of bicarbonate by rat distal tubules in vivo. Modulation by overnight fasting. J Clin Invest. 1988 Jun;81(6):1873–1878. doi: 10.1172/JCI113533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Levine D. Z., Jacobson H. R. The regulation of renal acid secretion: new observations from studies of distal nephron segments. Kidney Int. 1986 Jun;29(6):1099–1109. doi: 10.1038/ki.1986.114. [DOI] [PubMed] [Google Scholar]
  26. Levine D. Z., Vandorpe D., Iacovitti M. Luminal chloride modulates rat distal tubule bidirectional bicarbonate flux in vivo. J Clin Invest. 1990 Jun;85(6):1793–1798. doi: 10.1172/JCI114637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lucci M. S., Pucacco L. R., Carter N. W., DuBose T. D., Jr Evaluation of bicarbonate transport in rat distal tubule: effects of acid-base status. Am J Physiol. 1982 Oct;243(4):F335–F341. doi: 10.1152/ajprenal.1982.243.4.F335. [DOI] [PubMed] [Google Scholar]
  28. Malnic G., Berliner R. W., Giebisch G. Distal perfusion studies: transport stimulation by native tubule fluid. Am J Physiol. 1990 Jun;258(6 Pt 2):F1523–F1527. doi: 10.1152/ajprenal.1990.258.6.F1523. [DOI] [PubMed] [Google Scholar]
  29. Malnic G., De Mello Aires M., Giebisch G. Micropuncture study of renal tubular hydrogen ion transport in the rat. Am J Physiol. 1972 Jan;222(1):147–158. doi: 10.1152/ajplegacy.1972.222.1.147. [DOI] [PubMed] [Google Scholar]
  30. Mattsson J. P., Vänänen K., Wallmark B., Lorentzon P. Omeprazole and bafilomycin, two proton pump inhibitors: differentiation of their effects on gastric, kidney and bone H(+)-translocating ATPases. Biochim Biophys Acta. 1991 Jun 18;1065(2):261–268. doi: 10.1016/0005-2736(91)90238-4. [DOI] [PubMed] [Google Scholar]
  31. McKinney T. D., Burg M. B. Bicarbonate secretion by rabbit cortical collecting tubules in vitro. J Clin Invest. 1978 Jun;61(6):1421–1427. doi: 10.1172/JCI109061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Okusa M. D., Unwin R. J., Velázquez H., Giebisch G., Wright F. S. Active potassium absorption by the renal distal tubule. Am J Physiol. 1992 Mar;262(3 Pt 2):F488–F493. doi: 10.1152/ajprenal.1992.262.3.F488. [DOI] [PubMed] [Google Scholar]
  33. Planelles G., Anagnostopoulos T., Cheval L., Doucet A. Biochemical and functional characterization of H(+)-K(+)-ATPase in distal amphibian nephron. Am J Physiol. 1991 Jun;260(6 Pt 2):F806–F812. doi: 10.1152/ajprenal.1991.260.6.F806. [DOI] [PubMed] [Google Scholar]
  34. Preisig P. A., Ives H. E., Cragoe E. J., Jr, Alpern R. J., Rector F. C., Jr Role of the Na+/H+ antiporter in rat proximal tubule bicarbonate absorption. J Clin Invest. 1987 Oct;80(4):970–978. doi: 10.1172/JCI113190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schwartz G. J., Al-Awqati Q. Carbon dioxide causes exocytosis of vesicles containing H+ pumps in isolated perfused proximal and collecting tubules. J Clin Invest. 1985 May;75(5):1638–1644. doi: 10.1172/JCI111871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Schwartz G. J., Al-Awqati Q. Regulation of transepithelial H+ transport by exocytosis and endocytosis. Annu Rev Physiol. 1986;48:153–161. doi: 10.1146/annurev.ph.48.030186.001101. [DOI] [PubMed] [Google Scholar]
  37. Star R. A., Burg M. B., Knepper M. A. Bicarbonate secretion and chloride absorption by rabbit cortical collecting ducts. Role of chloride/bicarbonate exchange. J Clin Invest. 1985 Sep;76(3):1123–1130. doi: 10.1172/JCI112067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Velázquez H., Ellison D. H., Wright F. S. Chloride-dependent potassium secretion in early and late renal distal tubules. Am J Physiol. 1987 Sep;253(3 Pt 2):F555–F562. doi: 10.1152/ajprenal.1987.253.3.F555. [DOI] [PubMed] [Google Scholar]
  39. Velázquez H., Ellison D. H., Wright F. S. Chloride-dependent potassium secretion in early and late renal distal tubules. Am J Physiol. 1987 Sep;253(3 Pt 2):F555–F562. doi: 10.1152/ajprenal.1987.253.3.F555. [DOI] [PubMed] [Google Scholar]
  40. Wang T., Chan Y. L. Neural control of distal tubular bicarbonate and fluid transport. Am J Physiol. 1989 Jul;257(1 Pt 2):F72–F76. doi: 10.1152/ajprenal.1989.257.1.F72. [DOI] [PubMed] [Google Scholar]
  41. Wingo C. S. Active proton secretion and potassium absorption in the rabbit outer medullary collecting duct. Functional evidence for proton-potassium-activated adenosine triphosphatase. J Clin Invest. 1989 Jul;84(1):361–365. doi: 10.1172/JCI114165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wingo C. S., Madsen K. M., Smolka A., Tisher C. C. H-K-ATPase immunoreactivity in cortical and outer medullary collecting duct. Kidney Int. 1990 Nov;38(5):985–990. doi: 10.1038/ki.1990.302. [DOI] [PubMed] [Google Scholar]
  43. Yoshimori T., Yamamoto A., Moriyama Y., Futai M., Tashiro Y. Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J Biol Chem. 1991 Sep 15;266(26):17707–17712. [PubMed] [Google Scholar]

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