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. 1986 Jan;77(1):228–235. doi: 10.1172/JCI112281

Ion transport in proximal colon of the rat. Sodium depletion stimulates neutral sodium chloride absorption.

E S Foster, M E Budinger, J P Hayslett, H J Binder
PMCID: PMC423331  PMID: 2418060

Abstract

The model of sodium and chloride transport proposed for the colon is based on studies performed in the distal segment and tacitly assumes that ion transport is similar throughout the colon. In rat distal colon, neutral sodium-chloride absorption accounts for the major fraction of overall sodium absorption and aldosterone stimulates electrogenic, amiloride-sensitive sodium absorption. Since we have demonstrated qualitative differences in potassium transport in proximal and distal segments of rat colon, unidirectional 22Na and 36Cl fluxes were performed under short-circuit conditions across isolated proximal colon of control and sodium-depleted rats with secondary hyperaldosteronism. In the control group, net sodium absorption (JNanet) (7.4 +/- 0.5 mu eq/h . cm2) was greater than Isc (1.4 +/- 0.1 mu eq/h . cm2), and JClnet was 0 in Ringer solution. Residual flux (JR) was -5.2 +/- 0.5 mu eq/h . cm2 consistent with hydrogen ion secretion suggesting that neutral sodium absorption may represent sodium-hydrogen exchange. 1 mM mucosal amiloride, which inhibits sodium-hydrogen exchange in other epithelia, produced comparable decreases in JNanet and JR (4.1 +/- 0.6 and 3.2 +/- 0.6 mu eq/h . cm2, respectively) without a parallel fall in Isc. Sodium depletion stimulated JNanet, JClnet, and Isc by 7.0 +/- 1.4, 6.3 +/- 1.9, and 0.8 +/- 0.2 mu eq/h . cm2, respectively, and 1 mM amiloride markedly inhibited JNanet and JClnet by 6.0 +/- 1.1 and 4.0 +/- 1.6 mu eq/h . cm2, respectively, with only a minimal reduction in Isc. Conclusions: the predominant neutral sodium-absorptive mechanism in proximal colon is sodium-hydrogen exchange. Sodium depletion stimulates electroneutral chloride-dependent sodium absorption (most likely as a result of increasing sodium-hydrogen and chloride-bicarbonate exchanges), not electrogenic chloride-independent sodium transport. The model of ion transport in the proximal colon is distinct from that of the distal colon.

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Selected References

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  1. Al-Awqati Q., Norby L. H., Mueller A., Steinmetz P. R. Characteristics of stimulation of H+ transport by aldosterone in turtle urinary bladder. J Clin Invest. 1976 Aug;58(2):351–358. doi: 10.1172/JCI108479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Benos D. J. Amiloride: a molecular probe of sodium transport in tissues and cells. Am J Physiol. 1982 Mar;242(3):C131–C145. doi: 10.1152/ajpcell.1982.242.3.C131. [DOI] [PubMed] [Google Scholar]
  3. Billich C. O., Levitan R. Effects of sodium concentration and osmolality on water and electrolyte absorption form the intact human colon. J Clin Invest. 1969 Jul;48(7):1336–1347. doi: 10.1172/JCI106100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Binder H. J., Rawlins C. L. Effect of conjugated dihydroxy bile salts on electrolyte transport in rat colon. J Clin Invest. 1973 Jun;52(6):1460–1466. doi: 10.1172/JCI107320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Binder H. J., Rawlins C. L. Electrolyte transport across isolated large intestinal mucosa. Am J Physiol. 1973 Nov;225(5):1232–1239. doi: 10.1152/ajplegacy.1973.225.5.1232. [DOI] [PubMed] [Google Scholar]
  6. Bright-Asare P., Binder H. J. Stimulation of colonic secretion of water and electrolytes by hydroxy fatty acids. Gastroenterology. 1973 Jan;64(1):81–88. [PubMed] [Google Scholar]
  7. CADE R., PERENICH T. SECRETION OF ALDOSTERONE BY RATS. Am J Physiol. 1965 May;208:1026–1030. doi: 10.1152/ajplegacy.1965.208.5.1026. [DOI] [PubMed] [Google Scholar]
  8. Devroede G. J., Phillips S. F. Conservation of sodium, chloride, and water by the human colon. Gastroenterology. 1969 Jan;56(1):101–109. [PubMed] [Google Scholar]
  9. Devroede G. J., Phillips S. F. Failure of the human rectum to absorb electrolytes and water. Gut. 1970 May;11(5):438–442. doi: 10.1136/gut.11.5.438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Edmonds C. J. Transport of sodium and secretion of potassium and bicarbonate by the colon of normal and sodium-depleted rats. J Physiol. 1967 Dec;193(3):589–602. doi: 10.1113/jphysiol.1967.sp008380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Foster E. S., Hayslett J. P., Binder H. J. Mechanism of active potassium absorption and secretion in the rat colon. Am J Physiol. 1984 May;246(5 Pt 1):G611–G617. doi: 10.1152/ajpgi.1984.246.5.G611. [DOI] [PubMed] [Google Scholar]
  12. Foster E. S., Sandle G. I., Hayslett J. P., Binder H. J. Cyclic adenosine monophosphate stimulates active potassium secretion in the rat colon. Gastroenterology. 1983 Feb;84(2):324–330. [PubMed] [Google Scholar]
  13. Foster E. S., Zimmerman T. W., Hayslett J. P., Binder H. J. Corticosteroid alteration of active electrolyte transport in rat distal colon. Am J Physiol. 1983 Nov;245(5 Pt 1):G668–G675. doi: 10.1152/ajpgi.1983.245.5.G668. [DOI] [PubMed] [Google Scholar]
  14. Frizzell R. A., Field M., Schultz S. G. Sodium-coupled chloride transport by epithelial tissues. Am J Physiol. 1979 Jan;236(1):F1–F8. doi: 10.1152/ajprenal.1979.236.1.F1. [DOI] [PubMed] [Google Scholar]
  15. Frizzell R. A., Koch M. J., Schultz S. G. Ion transport by rabbit colon. I. Active and passive components. J Membr Biol. 1976;27(3):297–316. doi: 10.1007/BF01869142. [DOI] [PubMed] [Google Scholar]
  16. Frizzell R. A., Schultz S. G. Effect of aldosterone on ion transport by rabbit colon in vitro. J Membr Biol. 1978 Feb 6;39(1):1–26. doi: 10.1007/BF01872752. [DOI] [PubMed] [Google Scholar]
  17. Fromm M., Hegel U. Segmental heterogeneity of epithelial transport in rat large intestine. Pflugers Arch. 1978 Dec 15;378(1):71–83. doi: 10.1007/BF00581960. [DOI] [PubMed] [Google Scholar]
  18. Heintze K., Stewart C. P., Frizzell R. A. Sodium-dependent chloride secretion across rabbit descending colon. Am J Physiol. 1983 Apr;244(4):G357–G365. doi: 10.1152/ajpgi.1983.244.4.G357. [DOI] [PubMed] [Google Scholar]
  19. Hirsch D., Pace P., Binder H. J., Hayslett J. P. Evidence that aldosterone influences transport in target tissues by dissimilar mechanisms. Am J Physiol. 1985 Apr;248(4 Pt 2):F507–F512. doi: 10.1152/ajprenal.1985.248.4.F507. [DOI] [PubMed] [Google Scholar]
  20. Kinsella J. L., Aronson P. S. Properties of the Na+-H+ exchanger in renal microvillus membrane vesicles. Am J Physiol. 1980 Jun;238(6):F461–F469. doi: 10.1152/ajprenal.1980.238.6.F461. [DOI] [PubMed] [Google Scholar]
  21. Knickelbein R., Aronson P. S., Atherton W., Dobbins J. W. Sodium and chloride transport across rabbit ileal brush border. I. Evidence for Na-H exchange. Am J Physiol. 1983 Oct;245(4):G504–G510. doi: 10.1152/ajpgi.1983.245.4.G504. [DOI] [PubMed] [Google Scholar]
  22. Knickelbein R., Aronson P. S., Schron C. M., Seifter J., Dobbins J. W. Sodium and chloride transport across rabbit ileal brush border. II. Evidence for Cl-HCO3 exchange and mechanism of coupling. Am J Physiol. 1985 Aug;249(2 Pt 1):G236–G245. doi: 10.1152/ajpgi.1985.249.2.G236. [DOI] [PubMed] [Google Scholar]
  23. Liedtke C. M., Hopfer U. Mechanism of Cl- translocation across small intestinal brush-border membrane. I. Absence of Na+-Cl- cotransport. Am J Physiol. 1982 Mar;242(3):G263–G271. doi: 10.1152/ajpgi.1982.242.3.G263. [DOI] [PubMed] [Google Scholar]
  24. Liedtke C. M., Hopfer U. Mechanism of Cl- translocation across small intestinal brush-border membrane. II. Demonstration of Cl--OH- exchange and Cl- conductance. Am J Physiol. 1982 Mar;242(3):G272–G280. doi: 10.1152/ajpgi.1982.242.3.G272. [DOI] [PubMed] [Google Scholar]
  25. Martin R. S., Jones W. J., Hayslett J. P. Animal model to study the effect of adrenal hormones on epithelial function. Kidney Int. 1983 Sep;24(3):386–391. doi: 10.1038/ki.1983.171. [DOI] [PubMed] [Google Scholar]
  26. Murer H., Hopfer U., Kinne R. Sodium/proton antiport in brush-border-membrane vesicles isolated from rat small intestine and kidney. Biochem J. 1976 Mar 15;154(3):597–604. [PMC free article] [PubMed] [Google Scholar]
  27. Powell D. W., Binder H. J., Curran P. F. Electrolyte secretion by the guinea pig ileum in vitro. Am J Physiol. 1972 Sep;223(3):531–537. doi: 10.1152/ajplegacy.1972.223.3.531. [DOI] [PubMed] [Google Scholar]
  28. Sandle G. I., Hayslett J. P., Binder H. J. Effect of chronic hyperaldosteronism on the electrophysiology of rat distal colon. Pflugers Arch. 1984 May;401(1):22–26. doi: 10.1007/BF00581528. [DOI] [PubMed] [Google Scholar]
  29. Schwartz J. H. H+ current response to CO2 and carbonic anhydrase inhibition in turtle bladder. Am J Physiol. 1976 Aug;231(2):565–572. doi: 10.1152/ajplegacy.1976.231.2.565. [DOI] [PubMed] [Google Scholar]
  30. Sellin J. H., DeSoignie R. Rabbit proximal colon: a distinct transport epithelium. Am J Physiol. 1984 May;246(5 Pt 1):G603–G610. doi: 10.1152/ajpgi.1984.246.5.G603. [DOI] [PubMed] [Google Scholar]
  31. Snipes R. L., Clauss W., Weber A., Hörnicke H. Structural and functional differences in various divisions of the rabbit colon. Cell Tissue Res. 1982;225(2):331–346. doi: 10.1007/BF00214686. [DOI] [PubMed] [Google Scholar]
  32. Stone D. K., Seldin D. W., Kokko J. P., Jacobson H. R. Mineralocorticoid modulation of rabbit medullary collecting duct acidification. A sodium-independent effect. J Clin Invest. 1983 Jul;72(1):77–83. doi: 10.1172/JCI110986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Turnberg L. A., Bieberdorf F. A., Morawski S. G., Fordtran J. S. Interrelationships of chloride, bicarbonate, sodium, and hydrogen transport in the human ileum. J Clin Invest. 1970 Mar;49(3):557–567. doi: 10.1172/JCI106266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Turnberg L. A., Fordtran J. S., Carter N. W., Rector F. C., Jr Mechanism of bicarbonate absorption and its relationship to sodium transport in the human jejunum. J Clin Invest. 1970 Mar;49(3):548–556. doi: 10.1172/JCI106265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Warnock D. G., Greger R., Dunham P. B., Benjamin M. A., Frizzell R. A., Field M., Spring K. R., Ives H. E., Aronson P. S., Seifter J. Ion transport processes in apical membranes of epithelia. Fed Proc. 1984 Jul;43(10):2473–2487. [PubMed] [Google Scholar]
  36. Weinman S. A., Reuss L. Na+-H+ exchange at the apical membrane of Necturus gallbladder. Extracellular and intracellular pH studies. J Gen Physiol. 1982 Aug;80(2):299–321. doi: 10.1085/jgp.80.2.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Will P. C., Lebowitz J. L., Hopfer U. Induction of amiloride-sensitive sodium transport in the rat colon by mineralocorticoids. Am J Physiol. 1980 Apr;238(4):F261–F268. doi: 10.1152/ajprenal.1980.238.4.F261. [DOI] [PubMed] [Google Scholar]
  38. Yau W. M., Makhlouf G. M. Comparison of transport mechanisms in isolated ascending and descending rat colon. Am J Physiol. 1975 Jan;228(1):191–195. doi: 10.1152/ajplegacy.1975.228.1.191. [DOI] [PubMed] [Google Scholar]

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