Skip to main content
PMC home page
Gut logoLink to Gut
. 1999 May;44(5):615–619. doi: 10.1136/gut.44.5.615

Vagotomy inhibits the jejunal fluid secretion activated by luminal ileal Escherichia coli STa in the rat in vivo

V Rolfe 1, R Levin 1
PMCID: PMC1727489  PMID: 10205195

Abstract

BACKGROUND—Escherichia coli heat stable enterotoxin (STa) is a major cause of secretory diarrhoea in humans. 
AIMS—To assess the effects of instilling STa into the ileum on remote fluid secretion in the jejunum and colon in rats in vivo by a gravimetric technique. 
METHODS AND RESULTS—Ileal STa (55 ng/ml) stimulated fluid secretion in both ileal and jejunal loops but not in the colon. The fluid secretion induced by ileal STa was inhibited by L-NAME (N -nitro-L-arginine methyl ester, 40 mg/kg intraperitoneally) but not by D-NAME (N -nitro-D-arginine methyl ester). Ileal carbachol (183 mg/ml) instilled into the lumen stimulated ileal secretion but not jejunal secretion, and was unaffected by L-NAME. Capsaicin (10 µM), instilled luminally with STa in the ileum, blocked both the ileal and jejunal fluid secretion. Acute bilateral vagotomy prevented luminal ileal STa from inducing jejunal fluid secretion but not from activating ileal fluid secretion. 
CONCLUSION—Ileal E coli STa stimulates remote secretion in the rat jejunum but not in the colon, probably by a nitrinergic, vagal reflex mediated by C fibres. This neural pathway will amplify the action of the toxin in its generation of secretory diarrhoea. 



Keywords: intestinal fluid secretion; Escherichia coli STa; vagus; nitric oxide; C fibres

Full Text

The Full Text of this article is available as a PDF (125.3 KB).

Selected References

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

  1. Bornstein J. C., Furness J. B., Costa M. Sources of excitatory synaptic inputs to neurochemically identified submucous neurons of guinea-pig small intestine. J Auton Nerv Syst. 1987 Jan;18(1):83–91. doi: 10.1016/0165-1838(87)90137-8. [DOI] [PubMed] [Google Scholar]
  2. Castagliuolo I., LaMont J. T., Letourneau R., Kelly C., O'Keane J. C., Jaffer A., Theoharides T. C., Pothoulakis C. Neuronal involvement in the intestinal effects of Clostridium difficile toxin A and Vibrio cholerae enterotoxin in rat ileum. Gastroenterology. 1994 Sep;107(3):657–665. doi: 10.1016/0016-5085(94)90112-0. [DOI] [PubMed] [Google Scholar]
  3. Eklund S., Jodal M., Lundgren O. The enteric nervous system participates in the secretory response to the heat stable enterotoxins of Escherichia coli in rats and cats. Neuroscience. 1985 Feb;14(2):673–681. doi: 10.1016/0306-4522(85)90318-5. [DOI] [PubMed] [Google Scholar]
  4. Field M., Graf L. H., Jr, Laird W. J., Smith P. L. Heat-stable enterotoxin of Escherichia coli: in vitro effects on guanylate cyclase activity, cyclic GMP concentration, and ion transport in small intestine. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2800–2804. doi: 10.1073/pnas.75.6.2800. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Gaginella T. S., Mascolo N., Izzo A. A., Autore G., Capasso F. Nitric oxide as a mediator of bisacodyl and phenolphthalein laxative action: induction of nitric oxide synthase. J Pharmacol Exp Ther. 1994 Sep;270(3):1239–1245. [PubMed] [Google Scholar]
  6. Holzer P. Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience. 1988 Mar;24(3):739–768. doi: 10.1016/0306-4522(88)90064-4. [DOI] [PubMed] [Google Scholar]
  7. Hubel K. A., Renquist K. S., Varley G. Secretory reflexes in ileum and jejunum: absence of remote effects. J Auton Nerv Syst. 1991 Jul;35(1):53–62. doi: 10.1016/0165-1838(91)90038-5. [DOI] [PubMed] [Google Scholar]
  8. Izzo A. A., Sautebin L., Rombolà L., Capasso F. The role of constitutive and inducible nitric oxide synthase in senna- and cascara-induced diarrhoea in the rat. Eur J Pharmacol. 1997 Mar 26;323(1):93–97. doi: 10.1016/s0014-2999(97)00023-x. [DOI] [PubMed] [Google Scholar]
  9. Jodal M., Holmgren S., Lundgren O., Sjöqvist A. Involvement of the myenteric plexus in the cholera toxin-induced net fluid secretion in the rat small intestine. Gastroenterology. 1993 Nov;105(5):1286–1293. doi: 10.1016/0016-5085(93)90130-5. [DOI] [PubMed] [Google Scholar]
  10. Jodal M., Lundgren O. Do intestinal villi secrete? Acta Physiol Scand. 1996 Oct;158(2):115–118. doi: 10.1046/j.1365-201X.1996.538302000.x. [DOI] [PubMed] [Google Scholar]
  11. Jodal M. Neuronal influence on intestinal transport. J Intern Med Suppl. 1990;732:125–132. doi: 10.1111/j.1365-2796.1990.tb01484.x. [DOI] [PubMed] [Google Scholar]
  12. Martin K., Kong T. H., Renehan W., Schurr A., Dong W., Zhang X., Fogel R. Identification and function of brain stem neurons regulating rat ileal water absorption. Am J Physiol. 1989 Aug;257(2 Pt 1):G266–G273. doi: 10.1152/ajpgi.1989.257.2.G266. [DOI] [PubMed] [Google Scholar]
  13. Nocerino A., Iafusco M., Guandalini S. Cholera toxin-induced small intestinal secretion has a secretory effect on the colon of the rat. Gastroenterology. 1995 Jan;108(1):34–39. doi: 10.1016/0016-5085(95)90005-5. [DOI] [PubMed] [Google Scholar]
  14. Nzegwu H. C., Levin R. J. Luminal capsaicin inhibits fluid secretion induced by enterotoxin E. coli STa, but not by carbachol, in vivo in rat small and large intestine. Exp Physiol. 1996 Mar;81(2):313–315. doi: 10.1113/expphysiol.1996.sp003935. [DOI] [PubMed] [Google Scholar]
  15. Perkins A., Goy M. F., Li Z. Uroguanylin is expressed by enterochromaffin cells in the rat gastrointestinal tract. Gastroenterology. 1997 Sep;113(3):1007–1014. doi: 10.1016/s0016-5085(97)70198-7. [DOI] [PubMed] [Google Scholar]
  16. Qiu B., Pothoulakis C., Castagliuolo I., Nikulasson Z., LaMont J. T. Nitric oxide inhibits rat intestinal secretion by Clostridium difficile toxin A but not Vibrio cholerae enterotoxin. Gastroenterology. 1996 Aug;111(2):409–418. doi: 10.1053/gast.1996.v111.pm8690206. [DOI] [PubMed] [Google Scholar]
  17. Rolfe V. E., Brand M. P., Heales S. J., Lindley K. J., Milla P. J. Tetrahydrobiopterin regulates cyclic GMP-dependent electrogenic Cl- secretion in mouse ileum in vitro. J Physiol. 1997 Sep 1;503(Pt 2):347–352. doi: 10.1111/j.1469-7793.1997.347bh.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rolfe V., Levin R. J. Enterotoxin Escherichia coli STa activates a nitric oxide-dependent myenteric plexus secretory reflex in the rat ileum. J Physiol. 1994 Mar 15;475(3):531–537. doi: 10.1113/jphysiol.1994.sp020091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Schirgi-Degen A., Beubler E. Significance of nitric oxide in the stimulation of intestinal fluid absorption in the rat jejunum in vivo. Br J Pharmacol. 1995 Jan;114(1):13–18. doi: 10.1111/j.1476-5381.1995.tb14899.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Song Z. M., Brookes S. J., Costa M. Projections of specific morphological types of neurons within the myenteric plexus of the small intestine of the guinea-pig. Cell Tissue Res. 1996 Jul;285(1):149–156. doi: 10.1007/s004410050630. [DOI] [PubMed] [Google Scholar]
  21. de Sauvage F. J., Keshav S., Kuang W. J., Gillett N., Henzel W., Goeddel D. V. Precursor structure, expression, and tissue distribution of human guanylin. Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):9089–9093. doi: 10.1073/pnas.89.19.9089. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Gut are provided here courtesy of BMJ Publishing Group

RESOURCES