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Enhanced tissue responsiveness in colonic ion transport of cow's milk-sensitized guinea pigs

  • Allergy and Histamine
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Abstract

The effects of leukotriene D4 (LTD4) on ion transport were investigated in submucosa/mucosa colonic segments from guinea pigs sensitized to cow's milk and in age-matched, non-immune animals. Mediators released from mast cells in immune animals challenged with β-lactoglobulin evoked an increase in short-circuit current that was reduced by SK&F 102922, a peptidoleukotriene antagonist. Serosal addition of LTD4 (0.15–1 μM) evoked a concentration-dependent, bumetanide-sensitive increase in short-circuit current which was greater in immune than non-immune controls. In the absence of ongoing neural activity, 1 μM LTD4 evoked an 8–20 μA/cm2 increase in short-circuit current which was increased 8–13-fold when ongoing neural activity was present. In tissues with ongoing activity, the response to 0.15 μM LTD4 was reduced by SK&F 102922, tetrodotoxin and atropine. LTD4 enhanced the responsiveness of the tissue to carbachol by a factor of two, but did not affect responses of T84 colonic epithelial cell monolayers to this agent. These results show enhanced secretory function for LTD4 in animals with allergy to cow's milk. They suggest that the level of ongoing neural activity in the enteric neural microc ircuits is one of the major determinants of colonic secretory capacity.

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References

  1. D. D. Metcalfe,Mast cell mediators with emphasis on intestinal mast cells. Ann Allergy53, 563–575 (1984).

    PubMed  Google Scholar 

  2. L. B. Schwartz and K. F. Austen,Structure and function of the chemical mediators of mast cells. Prog. Allergy34, 271–321 (1984).

    PubMed  Google Scholar 

  3. D. A. Russell and G. A. Castro,Immunological regulation of colonic ion transport. Am. J. Physiol.256, G396-G403 (1989).

    PubMed  Google Scholar 

  4. A. W. Cuthbert, P. Mclaughlan and R. R. A. Coombs,Immediate hypersensitivity reaction to β-lactoglobulin in the epithelium lining of the colon of guinea pigs fed cow's milk. Int. Arch. Allergy Appl. Immunol.72, 34–40 (1983).

    PubMed  Google Scholar 

  5. N. H. Javed and H. J. Cooke,Neuro-immune interaction: Role for cholinergic neurons in intestinal anaphylaxis. Am. J. Physiol.263, G847-G852 (1992).

    PubMed  Google Scholar 

  6. Y.-Z. Wang, J. M. Palmer and H. J. Cooke,Neuroimmune regulation of colonic secretion in guinea pigs. Am. J. Physiol.260, G307-G314 (1991).

    PubMed  Google Scholar 

  7. R. Moqbel, D. Wakelin, A. J. MacDonald, S. J. King, R. K. Grencis and A. B. Kay,Release of leukotrienes during rapid expulsion of Trichinella spiralis from immune rats. Immunology60, 425–430 (1987).

    PubMed  Google Scholar 

  8. R. Moqbell, S. J. King, A. J. MacDonald, H. R. Miller, O. Cromwell, R. J. Shaw and A. B. Kay,Enteral and systemic release of leukotrienes during anaphylaxis of Nippostrongylus brasiliensis primed rats. J. Immunol.137, 296–301 (1986).

    PubMed  Google Scholar 

  9. B. Samuelson,Leukotrienes: Mediators of immediate hypersensitivity reactions and inflammation Science220, 568–575 (1983).

    PubMed  Google Scholar 

  10. P. Sharon and W. F. Stenson,Enhanced synthesis of leukotriene B 4 by colonic mucosa in inflammatory bowel diseases. Gastroenterology86, 453–460 (1984).

    PubMed  Google Scholar 

  11. R. D. Zipser, C. C. Nast, M. Lee, H. W. Kao and R. Duke,In vivo production of leukotriene B 4 and leukotriene C 4 in rabbit colitis: Relationship to inflammation. Gastroenterology92, 33–39 (1987).

    PubMed  Google Scholar 

  12. D. M. Hammerbeck and D. R. Brown,Neurally mediated actions of leumotrienes on ion transport in guinea pig distal colon. J. Pharmacol. Exp. Ther.264, 384–390 (1993).

    PubMed  Google Scholar 

  13. M. F. Jett, P. Marshall, J. D. Fondacaro and P. C. Smith,Action of peptidoleukotrienes on ion tranport in rabbit distal colon in vitro. J. Pharmacol. Exp. Ther.257, 698–705 (1991).

    PubMed  Google Scholar 

  14. P. L. Smith, D. P. Montzka, G. P. Mccafferty, M. A. Wasserman and J. D. Fondacaro,Effects of sulfidopeptide leukotrienes D 4 and E 4 on ileal ion transport in vitro in rat and rabbit. Am. J. Physiol.255, G175-G183 (1988).

    PubMed  Google Scholar 

  15. P. L. Smith, D. C. Chiossone and G. P. Mccafferty,Characterization of LTC 4 effects on rabbit ileal mucosa in vitro. Nauyn-Schmiedelberg's Arch. Pharmacol.341, 94–100 (1990).

    Google Scholar 

  16. Y.-Z. Wang and H. J. Cooke,H 2 receptors mediate cyclical chloride secretion in guinea pig distal colon. Am. J. Physiol.258, G887-G893 (1990).

    PubMed  Google Scholar 

  17. M. Diener, R. J. Bridges, S. F. Knoblock and W. Rummel,Neuronally mediated and direct effects of prostaglandins on ion transport in rat colon descendents. Nauyn Schmiedeberg's Arch. Pharmacol.337, 74–78 (1989).

    Google Scholar 

  18. A. W. Baird, B. L. Blazer-Yost and A. W. Cuthbert,Affinity purified immunoglobulin G transfers immediate hypersensitivity to guinea pig colonic epithelium in vitro. Gastroenterology92, 635–642 (1987).

    PubMed  Google Scholar 

  19. T. N. Koritz, S. Sujuke and R. R. A. Coombs,Antigenic stimulation with proteins of cow's milk via the oral route in guinea pigs and rats. Measurement of antigenically intact β-lactoglobulin and casein in the gastrointestinal contents of duodenum, jejunum and ileum. Int. Arch. Allergy Appl. Immun.82, 72–75 (1987).

    Google Scholar 

  20. R. Reddix, A. Kuwahara, L. Wallace, J. Grider and H. J. Cooke,Vasoactive intestinal polypeptide: A transmitter in submucous neurons mediating secretion in guinea pig distal colon. J. Pharmacol. Exp. Ther. (submitted).

  21. K. Dharmasathaphorn, K. G. Mandel, J. A. McRoberts, C. A. Cartwright and H. Masui,Utilization of a human colonic tumor cell line as a model to study electrolyte transport in the intesine. InIntestinal Absorption and Secretion. (Ed. E. Skadhauge and K. Heintze), pp. 325–333, MIT Press, Lancaster 1984.

    Google Scholar 

  22. R. W. Mowry,Selective staining of pancreatic beta-cell granules. Evolution and present status. Arch. Pathol. Lab. Med.107, 464–468 (1983).

    PubMed  Google Scholar 

  23. A. Kuwahara, S. Bowen, J. Wang, H. J. Cooke,Epithelial responses evoked by stimulation of submucosal neurons in guinea pig distal colon. Am. J. Physiol.252, G667-G674 (1987).

    PubMed  Google Scholar 

  24. G. A. Kopia, R. E. Valocik, T. J. Torphy, L. B. Cieslinksi, H. M. Sarau, J. J. Foley and M. A. Wasserman,Inhibition of leukotriene D 4-induced coronary vasoconstriction by leukotriene antagonists in the anesthetized dog. J. Pharmacol. Exp. Ther.243, 467–473 (1987).

    PubMed  Google Scholar 

  25. W. H. Percy, S. Y. Lee, M. B. Burton, T. Tolentino and R. Burakoff,Leukotriene D 4 excitation of rabbit distal colon arises in the region of the muscularis mucosae. Am. J. Physiol.259, G753-G759 (1990).

    PubMed  Google Scholar 

  26. M. A. Waserman, R. M. Muccitelli, S. S. Tucker, L. M. Vickery, J. F. Devan, B. M. Weichman, J. Newton, C. D. Perchonock and J. G. Gleason,SK&F 102922. An effective and selective antagonist of leukotriene-mediated bronchroconstriction. Fed. Proc.44, 491 (1985).

    Google Scholar 

  27. W. Clauss, J. Durr and G. Rechkemmer,Characterization of conductive pathways in guinea pig distal colon in vitro. Am. J. Physiol. 248, G176-G183 (1985).

    PubMed  Google Scholar 

  28. H. J. Cooke,Neuro-modulation of ion secretion by inflammatory mediators. InNeuro-Immuno-Physiology of the Gastrointestinal Mucosa. Implications for Inflammatory Dieases. (Eds. R. H. Stead, M. H. Perdue, H. Cooke, D. W. Powell and K. E. Barrett) Ann. N.Y. Acad. Sci.664, 346–352 (1992).

  29. G. H. Curtis, M. K. Patrick, A. G. Catto-Smith and D. G. Gall,Intestinal anaphylaxis in the rat. Effect of chronic antigen exposure. Gastroenterology98, 1558–1566 (1990).

    PubMed  Google Scholar 

  30. S. E. Crowe, P. Sestini and M. H. Perdue,Allergic reactions of rat jejunal mucosa. Ion transport responses to luminal antigen and inflammatory mediators. Gastroenterology99, 74–82 (1990).

    PubMed  Google Scholar 

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Javed, N.H., Barrett, K.E., Wang, Y.Z. et al. Enhanced tissue responsiveness in colonic ion transport of cow's milk-sensitized guinea pigs. Agents and Actions 41, 25–31 (1994). https://doi.org/10.1007/BF01986389

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