Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1988 Jan;395:271–284. doi: 10.1113/jphysiol.1988.sp016918

Epithelial transport in guinea-pig proximal colon: influence of enteric neurones.

A Kuwahara 1, H J Radowicz-Cooke 1
PMCID: PMC1191993  PMID: 3411479

Abstract

1. The effects of electrical field stimulation and aminophylline on sodium and chloride transport in the guinea-pig proximal colon were examined. 2. Under basal conditions, both sodium and chloride were actively absorbed and the net fluxes of these ions accounted for the short-circuit current. 3. Basal short-circuit current was reduced by furosemide, unchanged by amiloride and increased by aminophylline. The aminophylline-evoked increase in short-circuit current resulted from a reduction in net sodium absorption and abolishment of chloride absorption without a significant effect on residual flux. 4. Electrical field stimulation evoked a tetrodotoxin-sensitive increase in short-circuit current and total tissue conductance. The stimulus-evoked response was unaltered by mucosal amiloride, but was reduced by serosal furosemide. Electrical stimulation of submucosal neurones reduced both sodium and chloride absorption without any effect on residual flux. 5. Atropine had no effect on the basal short-circuit current; however, it reduced, but did not abolish, the neurally evoked response. Carbachol evoked a dose-dependent increase in short-circuit current that was reduced by tetrodotoxin. 6. These results suggest that electrical field stimulation activates submucosal neurones that innervate the epithelium. Release of acetylcholine and other neurotransmitters leads to excitation of receptors on epithelial cells, and an increase in short-circuit current that reflects inhibition of sodium and chloride absorption.

Full text

PDF
271

Selected References

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

  1. Andres H., Rock R., Bridges R. J., Rummel W., Schreiner J. Submucosal plexus and electrolyte transport across rat colonic mucosa. J Physiol. 1985 Jul;364:301–312. doi: 10.1113/jphysiol.1985.sp015746. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Binder H. J., Stange G., Murer H., Stieger B., Hauri H. P. Sodium-proton exchange in colon brush-border membranes. Am J Physiol. 1986 Sep;251(3 Pt 1):G382–G390. doi: 10.1152/ajpgi.1986.251.3.G382. [DOI] [PubMed] [Google Scholar]
  3. Christofides N. D., Polak J. M., Bloom S. R. Studies on the distribution of PHI in mammals. Peptides. 1984 Mar-Apr;5(2):261–266. doi: 10.1016/0196-9781(84)90216-x. [DOI] [PubMed] [Google Scholar]
  4. Clauss W., Dürr J., Rechkemmer G. Characterization of conductive pathways in guinea pig distal colon in vitro. Am J Physiol. 1985 Feb;248(2 Pt 1):G176–G183. doi: 10.1152/ajpgi.1985.248.2.G176. [DOI] [PubMed] [Google Scholar]
  5. Clauss W., Schäfer H., Horch I., Hörnicke H. Segmental differences in electrical properties and Na-transport of rabbit caecum, proximal and distal colon in vitro. Pflugers Arch. 1985 Mar;403(3):278–282. doi: 10.1007/BF00583600. [DOI] [PubMed] [Google Scholar]
  6. Cooke H. J. Influence of enteric cholinergic neurons on mucosal transport in guinea pig ileum. Am J Physiol. 1984 Mar;246(3 Pt 1):G263–G267. doi: 10.1152/ajpgi.1984.246.3.G263. [DOI] [PubMed] [Google Scholar]
  7. Cooke H. J. Neurobiology of the intestinal mucosa. Gastroenterology. 1986 Apr;90(4):1057–1081. doi: 10.1016/0016-5085(86)90889-9. [DOI] [PubMed] [Google Scholar]
  8. Cooke H. J., Shonnard K., Wood J. D. Effects of neuronal stimulation on mucosal transport in guinea pig ileum. Am J Physiol. 1983 Aug;245(2):G290–G296. doi: 10.1152/ajpgi.1983.245.2.G290. [DOI] [PubMed] [Google Scholar]
  9. Dharmsathaphorn K., Pandol S. J. Mechanism of chloride secretion induced by carbachol in a colonic epithelial cell line. J Clin Invest. 1986 Feb;77(2):348–354. doi: 10.1172/JCI112311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Foster E. S., Budinger M. E., Hayslett J. P., Binder H. J. Ion transport in proximal colon of the rat. Sodium depletion stimulates neutral sodium chloride absorption. J Clin Invest. 1986 Jan;77(1):228–235. doi: 10.1172/JCI112281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Foster E. S., Dudeja P. K., Brasitus T. A. Na+-H+ exchange in rat colonic brush-border membrane vesicles. Am J Physiol. 1986 Jun;250(6 Pt 1):G781–G787. doi: 10.1152/ajpgi.1986.250.6.G781. [DOI] [PubMed] [Google Scholar]
  12. Furness J. B., Costa M., Gibbins I. L., Llewellyn-Smith I. J., Oliver J. R. Neurochemically similar myenteric and submucous neurons directly traced to the mucosa of the small intestine. Cell Tissue Res. 1985;241(1):155–163. doi: 10.1007/BF00214637. [DOI] [PubMed] [Google Scholar]
  13. Furness J. B., Costa M., Keast J. R. Choline acetyltransferase- and peptide immunoreactivity of submucous neurons in the small intestine of the guinea-pig. Cell Tissue Res. 1984;237(2):329–336. doi: 10.1007/BF00217152. [DOI] [PubMed] [Google Scholar]
  14. Furness J. B., Costa M. Types of nerves in the enteric nervous system. Neuroscience. 1980;5(1):1–20. doi: 10.1016/0306-4522(80)90067-6. [DOI] [PubMed] [Google Scholar]
  15. Hubel K. A. Electrical stimulus-secretion coupling in rabbit ileal mucosa. J Pharmacol Exp Ther. 1984 Dec;231(3):577–582. [PubMed] [Google Scholar]
  16. Hubel K. A., Renquist K., Shirazi S. Ion transport in human cecum, transverse colon, and sigmoid colon in vitro. Baseline and response to electrical stimulation of intrinsic nerves. Gastroenterology. 1987 Feb;92(2):501–507. doi: 10.1016/0016-5085(87)90148-x. [DOI] [PubMed] [Google Scholar]
  17. Hubel K. A. The effects of electrical field stimulation and tetrodotoxin on ion transport by the isolated rabbit ileum. J Clin Invest. 1978 Nov;62(5):1039–1047. doi: 10.1172/JCI109208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kuwahara A., Bowen S., Wang J., Condon C., Cooke H. J. Epithelial responses evoked by stimulation of submucosal neurons in guinea pig distal colon. Am J Physiol. 1987 May;252(5 Pt 1):G667–G674. doi: 10.1152/ajpgi.1987.252.5.G667. [DOI] [PubMed] [Google Scholar]
  19. Luciano L., Reale E., Rechkemmer G., von Engelhardt W. Structure of zonulae occludentes and the permeability of the epithelium to short-chain fatty acids in the proximal and the distal colon of guinea pig. J Membr Biol. 1984;82(2):145–156. doi: 10.1007/BF01868939. [DOI] [PubMed] [Google Scholar]
  20. Lübcke R., Haag K., Berger E., Knauf H., Gerok W. Ion transport in rat proximal colon in vivo. Am J Physiol. 1986 Jul;251(1 Pt 1):G132–G139. doi: 10.1152/ajpgi.1986.251.1.G132. [DOI] [PubMed] [Google Scholar]
  21. Mainoya J. R. Effect of prolactin on fluid and NaCl absorption by the rat proximal and distal colon. Experientia. 1979 Aug 15;35(8):1060–1061. doi: 10.1007/BF01949941. [DOI] [PubMed] [Google Scholar]
  22. Mei N. Intestinal chemosensitivity. Physiol Rev. 1985 Apr;65(2):211–237. doi: 10.1152/physrev.1985.65.2.211. [DOI] [PubMed] [Google Scholar]
  23. Melander T., Hökfelt T., Rökaeus A., Fahrenkrug J., Tatemoto K., Mutt V. Distribution of galanin-like immunoreactivity in the gastro-intestinal tract of several mammalian species. Cell Tissue Res. 1985;239(2):253–270. doi: 10.1007/BF00218003. [DOI] [PubMed] [Google Scholar]
  24. NARAHASHI T., MOORE J. W., SCOTT W. R. TETRODOTOXIN BLOCKAGE OF SODIUM CONDUCTANCE INCREASE IN LOBSTER GIANT AXONS. J Gen Physiol. 1964 May;47:965–974. doi: 10.1085/jgp.47.5.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rimele T. J., O'Dorisio M. S., Gaginella T. S. Evidence for muscarinic receptors on rat colonic epithelial cells: binding of [3H]quinuclidinyl benzilate. J Pharmacol Exp Ther. 1981 Aug;218(2):426–434. [PubMed] [Google Scholar]
  26. Sellin J. H., DeSoignie R. C. Steroids alter ion transport and absorptive capacity in proximal and distal colon. Am J Physiol. 1985 Jul;249(1 Pt 1):G113–G119. doi: 10.1152/ajpgi.1985.249.1.G113. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Tapper E. J., Powell D. W., Morris S. M. Cholinergic-adrenergic interactions on intestinal ion transport. Am J Physiol. 1978 Oct;235(4):E402–E409. doi: 10.1152/ajpendo.1978.235.4.E402. [DOI] [PubMed] [Google Scholar]
  29. Venglarik C. J., Dawson D. C. Cholinergic regulation of Na absorption by turtle colon: role of basolateral K conductance. Am J Physiol. 1986 Oct;251(4 Pt 1):C563–C570. doi: 10.1152/ajpcell.1986.251.4.C563. [DOI] [PubMed] [Google Scholar]
  30. Zimmerman T. W., Binder H. J. Effect of tetrodotoxin on cholinergic agonist-mediated colonic electrolyte transport. Am J Physiol. 1983 Apr;244(4):G386–G391. doi: 10.1152/ajpgi.1983.244.4.G386. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES