Luminal cholera toxin alters motility in isolated guinea-pig jejunum via a pathway independent of 5-HT3

Frontiers in Neuroscience

Volumn 4, Issue SEP, 2010, Pages

  Fung, Candice ^a   Ellis, Melina ^a   Bornstein, Joel C ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

5 HT3 receptors; Cholera toxin; Intestinal motility; Peristalsis; Segmentation; Serotonin

Indexed keywords

EID: 84856570308     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2010.00162     Document Type: Article

References (43)

1. Abdu, F., Hicks, G. A., Hennig, G., Allen, J. P., and Grundy, D. (2002). Somatostatin sst2 receptors inhibit peristalsis in the rat and mouse jejunum. Am. J. Physiol. 282, G624-G633.
2. Argenzio, R. A., and Whipp, S. C. (1981). Effect of Escherichia coli heat-stable enterotoxin, cholera toxin and theophylline on ion transport in porcine colon. J. Physiol. (Lond.) 320, 469-487.
3. Bertrand, P. P., and Bornstein, J. C. (2002). ATP as a putative sensory mediator: activation of intrinsic sensory neurons of the myenteric plexus via P2X receptors. J. Neurosci. 22, 4767-4775.
4. Bertrand, P. P., Kunze, W. A. A., Furness, J. B., and Bornstein, J. C. (2000). The terminals of myenteric intrinsic primary afferent neurons of the guinea-pig ileum are excited by 5-HT acting at 5-HT3 receptors. Neuroscience 101, 459-469.
5. Buchheit, K.-H. (1989). Inhibition of cholera toxin-induced intestinal secretion by the 5-HT3 receptor antagonist ICS 205-930. Naunyn Schmiedebergs Arch. Pharmacol. 339, 704-705.
6. Burns, T. W., Mathias, J. R., Carlson, G. M., Martin. J. L., and Shields, R. P. (1978). Effect of toxigenic Escherichia coli on myoelectric activity of small intestine. Am. J. Physiol. 238, E311-E315.
7. Chambers, J. D., Bornstein, J. C., and Thomas, E. A. (2008). Insights into mechanisms of intestinal segmentation in guinea pigs: a combined computational modeling and in vitro study. Am. J. Physiol. Gastrointest. Liver Physiol. 295, G534-G541.
8. Cowles, V. E., and Sarna, S. (1990a). Relation between small intestinal motor activity and transit in secretory diarrhea. Am. J. Physiol. 259, G420-G429.
9. Cowles, V. E., and Sarna, S. K. (1990b). Effect of cholera toxin on small intestinal motor activity in the fed state. Dig. Dis. Sci. 35, 353-359.
10. Ellis, M., Gwynne, R. M., and Bornstein, J. C. (2009) Nutrient induced segmentation is mediated by serotonin and cholecystokinin in isolated guinea-pig small intestine. Auton. Neurosci. 149, 42.
11. Endo, T., Minami, M., Kitamura, N., Teramoto, Y., Ogawa, T., Nemoto, M., Hamaue, N., Hirafuji, M., Yasuda, E., and Blower, P. R. (1999). Effects of various 5-HT3 receptor antagonists, granisetron, ondansetron, ramosetron and azasetron on serotonin (5-HT) release from the ferret isolated ileum. Res. Commun. Mol. Pathol. Pharmacol. 104, 145-155.
12. Farthing, M. J. (2000). Enterotoxins and the enteric nervous system-a fatal attraction. Int. J. Med. Microbiol. 290, 491-496.
13. Farthing, M. J. (2002). Novel targets for the control secretory diarrhoea. Gut 50(Suppl. 3), III15-III18.
14. Field, M., Fromm, D., Al-Awqati, Q., and Greenough, W. B., III. (1972). Effect of cholera enterotoxin on ion transport across isolated ileal mucosa. J. Clin. Invest. 51, 796-804.
15. Gebauer, A., Merger, M., and Kilbinger, H. (1993). Modulation by 5-HT3 and 5-HT4 receptors of the release of 5-hydroxytryptamine from the guinea-pig small intestine. Naunyn Schmiedebergs Arch Pharmacol. 347, 137-140.
16. Gwynne, R. M., and Bornstein, J. C. (2007a). Local inhibitory reflexes excited by mucosal application of nutrient amino acids in guinea-pig jejunum. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G1660-G1670.
17. Gwynne, R. M., and Bornstein, J. C. (2007b). Mechanisms underlying nutrient induced segmentation in isolated guinea-pig small intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G1162-G1172.
18. Gwynne, R. M., Ellis, M., Sjövall, H., and Bornstein, J. C. (2009). Cholera toxin induces sustained hyperexcitability in submucosal secretomotor neurons in guinea pig jejunum. Gastroenterology 136, 299-308.
19. Gwynne, R. M., Thomas, E. A., Goh, S. M., Sjövall, H., and Bornstein, J. C. (2004). Segmentation induced by intraluminal fatty acid in isolated guinea-pig duodenum and jejunum. J. Physiol. (Lond.) 556, 557-569.
20. Hennig, G. W., Costa, M., Chen, B. G., and Brookes, S. J. H. (1999). Quantitative analysis of peristalsis in the guinea-pig small intestine using spatio-temporal maps. J. Physiol. (Lond.) 517, 575-590.
21. Janssen, P. W., Lentle, R. G., Hulls, C., Ravindran, V., and Amerah, A. M. (2009). Spatiotemporal mapping of the motility of the isolated chicken caecum. J. Comp. Physiol. B, Biochem. Syst. Environ. Physiol. 179, 593-604.
22. Keating, D. J., and Spencer, N. J. (2009). Release of 5-hydroxytryptamine from the mucosa is not required for the generation or propagation of colonic migrating motor complexes. Gastroenterology 138, 659-670, e652.
23. Kordasti, S., Sapnara, M., Thomas, E. A., Lindstrom, E., Forsman, M., Bornstein, J. C., and Sjövall, H. (2006). Effects of cholera toxin on the potential difference and motor responses induced by distension in the rat proximal small intestine in vivo. Am. J. Physiol. Gastrointest. Liver Physiol. 290, G948-G958.
24. Lentle, R. G., Janssen, P. W., Asvarujanon, P., Chambers, P., Stafford, K. J., and Hemar, Y. (2008). High-definition spatiotemporal mapping of contractile activity in the isolated proximal colon of the rabbit. J. Comp. Physiol. B, Biochem. Syst. Environ. Physiol. 178, 257-268.
25. Lentle, R. G., Janssen, P. W., Goh, K., Chambers, P., and Hulls, C. (2010). Quantification of the effects of the volume and viscosity of gastric contents on antral and fundic activity in the rat stomach maintained ex vivo. Dig. Dis. Sci. doi: 10.1007/s10620-010-1164-y.
26. Lundgren, O., and Jodal, M. (1997). The enteric nervous system and cholera toxin-induced secretion. Comp. Biochem. Physiol. A Physiol. 118, 319-327.
27. Mathias, J. R., Carlson, G. M., Bertiger, G., Martin, J.-L., and Cohen, S. (1977). Migrating action potential complex of cholera: a possible prostaglandin-induced response. Am. J. Physiol. 232, G529-G534.
28. Mathias, J. R., Nogueira, J., Martin, J. L., Carlson, G. M., and Giannella, R. A. (1982). Escherichia coli heat-stable toxin: its effect on motility of the small intestine. Am. J. Physiol. 242, G360-G363.
29. Minami, M., Taguchi, S., Kikuchi, T., Endo, T., Hamaue, N., Hiroshige, T., Liu, Y., Yue, W., and Hirafuji, M. (2003). Effects of fluvoxamine, a selective serotonin re-uptake inhibitor, on serotonin release from the mouse isolated ileum. Res. Commun. Mol. Pathol. Pharmacol. 113-114, 115-131.
30. Monro, R. L., Bertrand, P. P., and Bornstein, J. C. (2002). ATP and 5-HT are the principal neurotransmitters in the descending excitatory reflex pathway of the guinea-pig ileum. Neurogastroenterol. Motil. 14, 255-264.
31. Monro, R. L., Bertrand, P. P., and Bornstein, J. C. (2004). ATP participates in three excitatory post-synaptic potentials in the submucous plexus of the guinea-pig ileum. J. Physiol. (Lond.) 556, 571-584.
32. Mourad, F. H., O'Donnell, L. J., Dias, J. A., Ogutu, E., Andre, E. A., Turvill, J. L., and Farthing, M. J. G. (1995). Role of 5-hydroxytryptamine type 3 receptors in rat intestinal fluid and electrolyte secretion induced by cholera and Escherichia coli enterotoxins. Gut 37, 340-345.
33. Neal, K. B., and Bornstein, J. C. (2007). Mapping serotonin inputs to enteric neurons of the guinea pig small intestine. Neuroscience 145, 556-567.
34. Neal, K. B., Parry, L. J., and Bornstein, J. C. (2009). Strain-specific genetics, anatomy and function of entericneural serotonergic pathways in inbred mice. J. Physiol. (Lond.) 587, 567-586.
35. Reeves-Darby, V. G., Turner, J. A., Prasad, R., Chopra, A. K., Chary, P., Clench, M. H., Peterson, J. W., and Mathias, J. R. (1995). Effect of cloned Salmonella typhimurium enterotoxin on rabbit intestinal motility. FEMS Microbiol. Lett. 134, 239-244.
36. Roberts, R. R., Bornstein, J. C., Bergner, A. J., and Young, H. M. (2008). Disturbances of colonic motility in mouse models of Hirschprung's disease. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G996-G1008.
37. Roberts, R. R., Ellis, M., Gwynne, R. M., Bergner, A. J., Lewis, M., Beckett, E. A. H., Bornstein, J. C., and Young, H. M. (2010). The first intestinal motility patterns in fetal mice are not mediated by neurons or interstitial cells of Cajal. J. Physiol. (Lond.) 588, 1153-1169.
38. Tuladhar, B. R., Kaisar, M., and Naylor, R. J. (1997). Evidence for a 5-HT3 receptor involvement in the facilitation of peristalsis on mucosal application of 5-HT in the guinea-pig isolated ileum. Br. J. Pharmacol. 122, 1174-1178.
39. Turvill, J. L., Connor, P., and Farthing, M. J. G. (2000a). Neurokinin 1 and 2 receptors mediate cholera toxin secretion in rat jejunum. Gastroenterology 119, 1037-1044.
40. Turvill, J. L., Connor, P., and Farthing, M. J. G. (2000b). The inhibition of cholera toxin-induced 5-HT release by the 5-HT(3) receptor antagonist, granisetron, in the rat. Br. J. Pharmacol. 130, 1031-1036.
41. Turvill, J. L., Wapnir, R. A., Wingertzahn, M. A., Teichberg, S., and Farthing, M. J. G. (2000c). Cholera toxin-induced secretion in rats is reduced by a soluble fiber, gum arabic. Dig. Dis. Sci. 45, 946-951.
42. Turvill, J. L., Mourad, F. H., and Farthing, M. J. G. (1998). Crucial role for 5-HT in cholera toxin but not Escherichia coli heat-labile enterotoxin-intestinal secretion in rats. Gastroenterology 115, 883-890.
43. Zhou, X., and Galligan, J. J. (1999). Synaptic activation and properties of 5-hydroxytryptamine3 receptors in myenteric neurons of guinea-pig intestine. J. Pharmacol. Exp. Ther. 290, 803-810.