Skip to main content

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 473))

Summary

The close anatomic juxtaposition of epithelial cells with lymphocytes lining the intestinal tract facilitates communication between the two cell types. This intercellular dialogue is important for mucosal development and has a conditioning effect on mucosal structure, function, and response to tissue injury. Lymphoepithelial communication is bi-directional, and mediated in large part, by shared ligands and receptors. The chemical messengers involved include cytokines, growth factors, local hormones, and products of arachidonate metabolism. The interdependency between the epithelium and adjacent lymphoid cells is such that the epithelium is considered to have a central role in the mucosal immune system and is an active participant in both the afferent and efferent limbs of the mucosal immune response. The molecular crosstalk between the epithelium and adjacent lymphocytes is just one aspect of a more complex network of intercellular signalling within the intestinal mucosa and upon which the integrity of the mucosa is dependent. Thus, there are extensive interactions between nerve and immune cells and between the enteric flora and the epithelium and amongst intestinal mesenchymal cells including fibroblasts and vascular endothelial cells. Disruption of any aspect of the mucosal microenvironment, as has been achieved with selective genetically engineered murine models, is associated with impaired mucosal defence and inflammation.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Andoh, A., Fujiyama, Y., Sumiyoshi, K.-I., Sakumoto, H., and Bamba, T., 1996, Interleukin 4 acts as an inducer of decay-accelerating factor gene expression in human intestinal epithelial cells. Gastroenterology 111:911–918.

    Article  PubMed  CAS  Google Scholar 

  • Baird, A.W., Coombs, R.R.A., McLaughlan, P., and Cuthbert, A.W., 1984, Immediate hypersensitivity reactions to cow milk proteins in isolated epithelium from ileum of milk-drinking guinea pigs: comparisons with colonic epithelia. Int. Arch. Allergy Appl. Immunol. 75:255–263.

    Article  PubMed  CAS  Google Scholar 

  • Baird, A.W., Cuthbert, A.W., and MacVinish, L.J., 1987, Type 1 hypersensitivity reactions in reconstructed tissues using syngeneic cell types. Br. J. Pharmacol. 91:857–869.

    Article  PubMed  CAS  Google Scholar 

  • Barrett, K.E., 1991, Immune-related intestinal chloride secretion. III. Acute and chronic effects of mast cell mediators on chloride secretion by a human colonic epithelial cell line. J. Immunol. 147:959–964.

    PubMed  CAS  Google Scholar 

  • Befus, A.D., 1990, Immunophysiology: influence of the mucosal immune system on intestinal function, In: Immunology and immunopathology of the liver and gastrointestinal tract., Targan, S.R. and Shanahan, F. (editors), Igaku-Shoin, New York, Tokyo, pp. 205–229.

    Google Scholar 

  • Bennett, M.W., O’Connell, J., O’Sullivan, G.C., Brady, C., Roche, D., Collins, J.K., and Shanahan, F., 1998, The Fas counterattack in vivo: apoptotic depletion of tumor-infiltrating lymphocytes (TIL) associated with Fas ligand (FasL) expression by human esophageal carcinoma. J. Immunol. 160:5669–5675.

    PubMed  CAS  Google Scholar 

  • Bennett, M.W., O’Connell, J., O’Sullivan, G.C., Roche, R., Brady, C., Kelly, J., Collins, J.K., and Shanahan, F., 1999, Fas ligand and Fas receptor are coexpressed in normal human esophageal epithelium; a potential mechanism of apoptotic epithelial turnover. Diseases of the Esophagus (in press).

    Google Scholar 

  • Bern, J.M., Sturbaum, C.W., Karayalcin, S.S., Berschneider, H.M., Wachsman, J.T., and Powell, D.W., 1989, Immune system control of rat and rabbit colonie electrolye transport. Role of prostaglandins and enteric nervous system. J. Clin. Invest. 83:1810–1820.

    Article  PubMed  CAS  Google Scholar 

  • Boismenu, R. and Havran, W.L., 1994, Modulation of epithelial cell growth by intraepithelial γδ T cells. Science 266:1253–1255.

    Article  PubMed  CAS  Google Scholar 

  • Brandtzaeg, P., Halstensen, T.S., Kett, K., Karjci, P., Kvale, D., Rognum, T.O., Scott, H., and Sollid, L.M., 1989, Immunobiology and immunopathology of human gut mucosa: humoral immunity and intraepithelial lymphocytes. Gastroenterology 97:1562–1584.

    PubMed  CAS  Google Scholar 

  • Bush, T.G, Savidge, T.C., Freeman, T.C., Cox, H.J., Campbell, E.A., Mucke, L., Johnson, M.H., and Sofroniew, M.V., 1998, Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell 93:189–221.

    Article  PubMed  CAS  Google Scholar 

  • Castro, G.A., 1982, Immunological regulation of epithelial function. Am. J. Physiol. 243 (Gastrointest. Liver Physiol. 6):G321–G329.

    PubMed  CAS  Google Scholar 

  • Castro, G.A. and Arntzen, C.J., 1993, Immunophysiology of the gut: a research frontier for integrative studies of the common mucosal immune system, Am. J. Physiol. 265 (Gastrointest. Liver Physiol. 28):G599–G610.

    PubMed  CAS  Google Scholar 

  • Crowe, S.E., Sestini, P., and Perdue, M.H., 1990, Allergic reactions of rat jejunal mucosa. Ion transport responses to luminal antigenand inflammatory mediators. Gastroenterology 99:74–82.

    PubMed  CAS  Google Scholar 

  • Fritsch, C., Simon-Assmann, P., Kedinger, M., and Evans, G.S., 1997, Cytokines modulate fibroblast phenotype and epithelial-stroma interactions in rat intestine. Gastroenterology 112:826–838.

    Article  PubMed  CAS  Google Scholar 

  • Goode, T., O’Connell, J., Sternini, C., Anton, P., O’Sullivan, G.C., Collins, J.K., and Shanahan, E, 1998a, Substance P (NK-1) receptor is a marker of human mucosal but not peripheral mononuclear cells: molecular quantitation and localization. J. Immunol.161::2232–2240.

    PubMed  CAS  Google Scholar 

  • Goode, T., O’Connell, J., O’Sullivan, G.C., Collins, J.K., and Shanahan, F., 1998b, Cytokine induced expression of substance P (NK-1) receptors in human colonic epithelial cells. Gastroenterology 114:A373.

    Article  Google Scholar 

  • Griffith, T.S. and Ferguson, T.A., 1997, The role of FasL-induced apoptosis in immune privilege. Immunol. Today 18:240–244.

    CAS  Google Scholar 

  • Hershberg, R.M., Framson, P.E., Cho, D.H., Lee, L.Y., Kovats, S., Beitz, J., Blum, J.S., and Nepom, G.T., 1997, Intestinal epithelial cells use two distinct pathways for HLA class II antigen processing. J. Clin. Invest. 11:204–215.

    Article  Google Scholar 

  • Kagnoff, M.E and Eckmann, L, 1997, Epithelial cells as sensors for microbial infection. J. Clin. Invest. 100:6–10.

    Article  PubMed  CAS  Google Scholar 

  • Kernéis, S., Bogdanova, A., Kraehenbuhlm J.-P, and Pringault, E, 1997, Conversion by Peyer’s Patch lymphocytes of human enterocytes into M cells that transport bacteria. Science 277:949–952.

    Article  PubMed  Google Scholar 

  • Klein, J.R., 1996, Whence the intestinal intraepithelial lymphocyte? J. Exp. Med. 184:1203–1206.

    Article  PubMed  CAS  Google Scholar 

  • Komano, H., Fujiura, Y., Kawaguchi, M., Matsumoto, S., Hashimoto, Y., Obano, S., Mombaerts, P., Tonegawa, S., Yamamoto, H., Itohara, S., Nanno, M., and Ishikawa, H., 1995, Homeostasis regulation of intestinal epithelia by intraepithelial γδ T-cells. Proc. Natl. Acad. Sci. USA 92:6147–6151.

    Article  PubMed  CAS  Google Scholar 

  • Kraehenbuhl, J.-P. and Neutra, M.R., 1992, Molecular and cellular basis of immune protection at mucosal surfaces. Physiological Reviews 72:853–879.

    PubMed  CAS  Google Scholar 

  • Lefrançois, L. and Puddington, L., 1995, Extrathymic intestinal T-cell development: virtual reality? Immunol. Today 16:16–21.

    Article  PubMed  Google Scholar 

  • Madara, J.L. and Stafford, J., 1989, Interferon-g directly affects barrier function of cultured intestinal epithelial monolayers. J. Clin. Invest. 83:724–727.

    Article  PubMed  CAS  Google Scholar 

  • Mak, T.W. and Ferrick, D.A., 1998, The γδ T-cell bridge: linking innate and acquired immunity. Nature Medicine 4:764–765.

    Article  PubMed  CAS  Google Scholar 

  • Mayer, L. and Shlien, R., 1987, Evidence for function of Ia molecules on gut epithelial cells in man. J. Exp. Med. 166:1471–1483.

    Article  PubMed  CAS  Google Scholar 

  • Mayer, L. and Eisenhardt, D., 1990, Lack of induction of suppressor T cells by intestinal epithelial cells from patients with inflammatory bowel disease. J. Clin. Invest. 86:1255–1260.

    Article  PubMed  CAS  Google Scholar 

  • Mostov, K.E., 1994, Transepithelial transport of immunoglobulins. Annu. Rev. Immunol. 12:63–84.

    Article  PubMed  CAS  Google Scholar 

  • Nagura, H., Kubota, M., and Kimura, N, 1996, Neuroendocrine regulation of mucosal immune responses. In: Essentials of Mucosal Immunology, editors, Kagnoff, M.F. and Kiyono, H., Academic Press, San Diego, pp. 125–139.

    Chapter  Google Scholar 

  • O’Connell, J., O’Sullivan, G.C., Collins, J.K., and Shanahan, F., 1996, The Fas counter attack: Fas-mediated T cell killing by colon cancer cells expressing Fas ligand. J. Exp. Med. 184:1075–1082.

    Article  PubMed  Google Scholar 

  • O’Connell, J., Bennett, M.W., O’Sullivan, G.C., Collins, J.K., and Shanahan, F., 1999, The Fas counterattack: cancer as a site of immune privilege. Immunol. Today 20:46–52.

    Article  PubMed  Google Scholar 

  • Perdue, M.H. and McKay, D.M., 1994, Integrative immunophysiology in the intestinal mucosa. Am. J. Physiol. 267 (Gastrointest Liver Physiol. 30):G151–G165.

    PubMed  CAS  Google Scholar 

  • Phipps, R.P., Stein, S.H., and Roper, R.L., 1991, A new view of prostaglandin E regulation of the immune response. Immunol. Today 12:349–351.

    Article  PubMed  CAS  Google Scholar 

  • Podolsky, D.K., 1993, Regulation of intestinal epithelial proliferation: a few answers, many questions. Am. J. Physiol. 264 (Gastrointest. Liver Physiol. 27):G179–G186.

    PubMed  CAS  Google Scholar 

  • Puddington, L., Olson, S., and Lefrançois, L., 1994, Interactions between stem cell factor and c-kit are required for intestinal immune system homeostasis. Immunity 1:733–739.

    Article  PubMed  CAS  Google Scholar 

  • Reinecker, H.-C. and Podolsky, D.K., 1995, Human intestinal epithelial cells express functional cytokine receptors sharing the common γc chain of the interleukin-2 receptor. Proc. Natl. Acad. Sci. USA 92:8353–8357.

    Article  PubMed  CAS  Google Scholar 

  • Reinecker, H.-C., MacDermott, R.P., Mirau, S., Dignass, A., and Podolsky, D.K., 1996, Intestinal epithelial cells both express and respond to interleukin 15. Gastroenterology 111:1706–1713.

    Article  PubMed  CAS  Google Scholar 

  • Saito, H., Kanamori, Y., Takemori, T., Nariuchi, H., Kubota, E., Takahashi-Iwanaga, H., Iwanaga, T., and Ishikawa, H., 1998, Generation of intestinal T cells from progenitors residing in gut cryptopatches. Science 280:275–278.

    Article  PubMed  CAS  Google Scholar 

  • Shanahan, F., 1994, The intestinal immune system. In: Physiology of the Gastrointestinal Tract, Editor, Johnson, L.R., Raven Press, New York, pp. 643–684.

    Google Scholar 

  • Shanahan, F., 1994b, Gene-targeted immunologic knockouts: new models of inflammatory bowel disease. Gastroenterology 107:312–314.

    Google Scholar 

  • Shanahan, F. and Anton, P., 1994, Role of peptides in the regulation of the mucosal immune and inflammatory response. In: Gut peptides: Biochemistry and Physiology, edited by Walsh, J.H. and Dockray, G.J., Raven Press, New York, pp. 851–867.

    Google Scholar 

  • Shanahan, F., 1997, A gut reaction: lymphoepithelial communication in the intestine. Science 275:1897–1898.

    Article  PubMed  CAS  Google Scholar 

  • Shanahan, F. and O’Sullivan, G.C., 1999, Glial cells, mucosal integrity, and inflammatory bowel disease. Gastroenterology (in press).

    Google Scholar 

  • Shannon, V.R., Stenson, W.F., and Holtzman, M.J., 1993, Induction of epithelial arachidonate 12-lipoxygenase at active stites of inflammatory bowel disease. Am. J. Physiol. 264:G104–G111.

    PubMed  CAS  Google Scholar 

  • Singer, I.I., Kawka, D.W., Scott, S., Weidner, J.R., Mumford, R.A., Riehl, T.E., and Stenson, WE, 1996, Expression of inducible nitric oxide synthase and nitrotyrosine in colonic epithelium in inflammatory bowel disease. Gastroenterology 111:871–885.

    Article  PubMed  CAS  Google Scholar 

  • Stadnyk, A.W. and Waterhouse, C.M., 1997, Epithelial cytokines in intestinal inflammation and mucosal immunity. Curr. Opin. Gastroenterol 13:510–517.

    Article  CAS  Google Scholar 

  • Stenson, W.F. and Alpers, D.H., 1994, A parable on the dangers of overclassification: can an enterocyte assume immune functions? Curr. Opinion Gastroenterology 10:121–124.

    Article  Google Scholar 

  • Taylor, C.T., Dzus, A.L., and Colgan, S.P., 1998, Autocrine regulation of epithelial permeability by hypoxia: role of polarized release of tumor necrosis factor a. Gastroenterology 114:657–668.

    Article  PubMed  CAS  Google Scholar 

  • Vidrich, A., Anton, P., and Shanahan, F., 1998, Immunoepithelial interactions: Cytokine modulation of colonie epithelial growth. In Vitro (in press Nov/Dec 1998).

    Google Scholar 

  • Walker, P.R., Saas, P., and Dietrich, P.-Y., 1998, Tumor expression of Fas ligand (CD95L) and the consequences. Curr. Opin. Immunol. 10:564–572.

    Article  PubMed  CAS  Google Scholar 

  • Wang, J., Whetsell, M., and Klein, J.R., 1997, Local hormone networks and intestinal T cell homeostasis. Science 275:1937–1939.

    Article  PubMed  CAS  Google Scholar 

  • Watanabe, M., Ueno, Y., Yajima, T., Iwao, Y., Tsuchiya, M., Ishikawa, H., Aiso, S., Hibi, T., and Ishii, H., 1995, Interleukin 7 is produced by human intestinal epithelial cells and regulates the proliferation of intestinal mucosal lymphocytes. J. Clin. Invest. 95:2945–2953.

    Article  PubMed  CAS  Google Scholar 

  • Williams, N., 1998, T cells on the mucosal frontline. Science 280:198–200.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1999 Springer Science+Business Media New York

About this chapter

Cite this chapter

Shanahan, F. (1999). Intestinal Lymphoepithelial Communication. In: Paul, P.S., Francis, D.H. (eds) Mechanisms in the Pathogenesis of Enteric Diseases 2. Advances in Experimental Medicine and Biology, vol 473. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-4143-1_1

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-4143-1_1

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-6858-8

  • Online ISBN: 978-1-4615-4143-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics