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The role of enteric glia in gut inflammation

Published online by Cambridge University Press:  21 July 2011

Georg von Boyen  and
Martin Steinkamp
Georg von Boyen*
Affiliation:
Department of Internal Medicine I (Gastroenterology), University of Ulm, Ulm, Germany
Martin Steinkamp
Affiliation:
Department of Gastroenterology, Endocrinology and Metabolism, University of Marburg, Marburg, Germany
*
Correspondence should be addressed to: Georg von Boyen, Klinik für Innere Medizin I, Universitätsklinikum Ulm, Albert-Einstein Allee 23, 89081 Ulm, Germany phone: +49 731 500 44603 fax: +49 731 500 44610 email: [email protected]
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Abstract

A neuro-glia interaction is part of gut inflammation and essential for the integrity of the bowel. A loss of enteric glia cells (EGCs) led to a fatal haemorrhagic jejuno-ileitis and death in a few days. Although a diminished EGC network is postulated in inflammatory bowel disease and enteric glia pathology is described in Chagas' disease the role of EGCs in the onset of these disease complexes is not definitely clear. Several lines of evidence implicate that the secretion of different factors by enteric glia may be the key for modulating gut homeostasis. As mucosal integrity might be important for remission in Crohn's disease and inflammation of the enteric nervous system is part of the pathology in Chagas' disease, the role of EGCs during gut inflammation could be part of the key to understand these diseases.

Keywords

Enteric glia cellsintegrity of the bowelgut inflammationChagas’ disease
Type
Research Article
Information
Neuron Glia Biology , Volume 6 , Issue 4 , November 2010 , pp. 231 - 236
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Abdo, H., Derkinderen, P., Gomes, P., Chevalier, J., Aubert, P., Masson, D. et al. (2010) Enteric glial cells protect neurons from oxidative stress in part via reduced gluthatione. FASEB Journal 24, 1082–1094.CrossRefGoogle Scholar
Baert, F., Moortgat, L., Van Assche, G., Caenepeel, P., Vergauwe, P., De Vos, M. et al. (2010) Belgian inflammatory bowel disease research group; North-Holland Gut Club. Mucosal healing predicts sustained clinical remission in patients with early-stage Crohn's disease. Gastroenterology 138, 463–468.CrossRefGoogle Scholar
Bush, T.G. (2002) Enteric glial cells. An upstream target for induction of necrotizing enterocolitis and Crohn's disease? Bioessays 24, 130–140.CrossRefGoogle ScholarPubMed
Bush, T.G., Savidge, T.C., Freeman, T.C., Cox, H.J., Campbell, E.A., Mucke, L. et al. (1998) Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell 93, 189–201.CrossRefGoogle ScholarPubMed
Cabarrocas, J., Savidge, T. and Liblau, R. (2003) Role of enteric glial cells in inflammatory bowel disease. Glia 41, 81–93.CrossRefGoogle ScholarPubMed
Colombel, J.F., Sandborn, W.J., Reinisch, W., Mantzaris, G.J., Kornbluth, A., Rachmilewitz, D., et al. ; SONIC Study Group (2010) Infliximab, azathioprine or combination therapy for Crohn's disease. New England Journal of Medicine 362, 1383–1395.CrossRefGoogle ScholarPubMed
Cornet, A., Savidge, T.C., Cabarrocas, J., Deng, W.L., Colombel, J.F., Lassmann, H. et al. (2001) Enterocolitis induced by autoimmune targeting of enteric glial cells: a possible mechanism in Crohn's disease? Proceedings of the National Academy of Sciences of the U.S.A. 98, 13306–13311.CrossRefGoogle ScholarPubMed
Daperno, M., D'Haens, G., Van Assche, G., Baert, F., Bulois, P., Maunoury, V. et al. (2004) Development and validation of a new, simplified endoscopic activity score for Crohn's disease: the SES-CD. Gastrointestinal Endoscopy 60, 505–512.CrossRefGoogle ScholarPubMed
da Silveira, A.B., de Oliveira, E.C., Neto, S.G., Luquetti, A.O., Fujiwara, R.T., Oliveira, R.C. et al. (2011) Enteroglial cells act as antigen-presenting cells in chagasic megacolon. Human Pathology 42, 522–532.CrossRefGoogle ScholarPubMed
da Silveira, A.B., Freitas, M.A., de Oliveira, E.C., Neto, S.G., Luquetti, A.O., Furness, J.B. et al. (2009) Glial fibrillary acidic protein and S-100 colocalization in the enteroglial cells in dilated and nondilated portions of colon from chagasic patients. Human Pathology 40, 244–251.CrossRefGoogle ScholarPubMed
da Silveira, A.B., Lemos, E.M., Adad, S.J., Correa-Oliveira, R., Furness, J.B. and D'Avila Reis, D. (2007) Megacolon in Chagas disease: a study of inflammatory cells, enteric nerves, and glial cells. Human Pathology 38, 1256–1264.CrossRefGoogle ScholarPubMed
de Souza, W., de Carvalho, T.M. and Barrias, E.S. (2010) Review on Trypanosoma cruzi: host cell interaction. International Journal of Cell Biology 2010, 1–12CrossRefGoogle ScholarPubMed
D'Haens, G.R., Noman, M., Baert, F., Vermeire, S. and Van Assche, G. (2002) Endoscopic healing after infliximab treatment for Crohn's disease provides a longer time to relapse. Gastroenterology 122, A776.Google Scholar
Dias, J.C. (1989) The indeterminate form of human chronic Chagas' disease. A clinical epidemiological review. Revista da Sociedade Brasileira de Medicina Tropical 22, 147–156.CrossRefGoogle ScholarPubMed
Ferri, G.L., Probert, L., Cocchia, D., Michetti, F., Marangos, P.J. and Polak, J.M. (1982) Evidence for the presence of S-100 protein in the glial component of the human enteric nervous system. Nature 297, 409–410.CrossRefGoogle ScholarPubMed
Frøslie, K.F., Jahnsen, J., Moum, B.A. and Vatn, M.H.; IBSEN Group (2007) Mucosa healing in inflammatory bowel disease: results from a Norwegian population-based cohort. Gastroenterology 133, 412–422.CrossRefGoogle ScholarPubMed
Gabella, G. (1981) Ultrastructure of the nerve plexuses of the mammalian intestine: the enteric glial cells. Neuroscience 6, 425–436.CrossRefGoogle ScholarPubMed
Geboes, K., Rutgeerts, P., Ectors, N., Mebis, J., Penninckx, F., Vantrappen, G. et al. (1992) Major histocompatibility class II expression on the small intestinal nervous system in Crohn's disease. Gastroenterology 103, 439–447.CrossRefGoogle ScholarPubMed
Gershon, M.D. and Rothman, T.P. (1991) Enteric glia. Glia 4, 195–204.CrossRefGoogle ScholarPubMed
Hollenbach, E., Rühl, A., Zoller, M. and Stremmel, W. (2000) T cell activation by enteric glia: a novel pathway for the amplification of inflammatory responses in the enteric nervous system. Gastroenterology 118, A184.CrossRefGoogle Scholar
Irvine, E.J. and Marshall, J.K. (2000) Increased intestinal permeability precedes the onset of Crohn's disease in a subject with familial risk. Gastroenterology 119, 1740–1744.CrossRefGoogle Scholar
Jessen, K.R. and Mirsky, R. (1980) Glial cells in the enteric nervous system contain glial fibrillary acidic protein. Nature 286, 736–737.CrossRefGoogle ScholarPubMed
Koretz, K., Momburg, F., Otto, H.F. and Moller, P. (1984) Sequential induction of MHC antigens on autochtonous cells of ileum affected by Crohn's disease. American Journal of Pathology 129, 493–502.Google Scholar
Krammer, H.J. and Kühnel, W. (1993) Topography of the enteric nervous system in Peyer's patches of the porcine small intestine. Cell Tissue Research 272, 267–272.CrossRefGoogle ScholarPubMed
Krammer, H.J., Süss, A., Singer, M.V. and Wedel, T. (2002) Neurogastroenterology – from the basics to the clinics. Romanian Journal of Gastroenterology 11, 313–319.Google Scholar
Nascimento, R.D., de Souza Lisboa, A., Fujiwara, R.T., de Freitas, M.A., Adad, S.J., Oliveira, R.C. et al. (2010) Characterization of enteroglial cells and denervation process in chagasic patients with and without megaesophagus. Human Pathology 41, 528–534.CrossRefGoogle ScholarPubMed
Neunlist, M., Aubert, P., Bonnaud, S., Van Landeghem, L., Coron, E., Wedel, T. et al. (2007) Enteric glia inhibit intestinal epithelial cell proliferation partly through a TGF-beta1-dependent pathway. American Journal of Physiology – Gastrointestinal and Liver Physiology 292, G231–G241.CrossRefGoogle ScholarPubMed
Neunlist, M., Van Landeghem, L., Bourreille, A. and Savidge, T. (2008) Neuro-glial crosstalk in inflammatory bowel disease. Journal of Internal Medicine 263, 577–583.CrossRefGoogle ScholarPubMed
Oliveira, E.C., Fujisawa, M.M., Hallal Longo, D.E., Farias, A.S., Contin Moraes, J, Guariento, M.E. et al. (2009) Neuropathy of gastrointestinal Chagas' disease: immune response to myelin antigens. Neuroimmunomodulation 16, 54–62.CrossRefGoogle ScholarPubMed
Radke, R. and Krammer, H.J. (1996) Enteric nervous system similarities and differences in the gastrointestinal tract, gallbladder and pancreas. Neurogastroenterologia 3, 93–105.Google Scholar
Reed, S.G. (1998) Immunology of Trypanosoma cruzi infections. Chemical Immunology 70, 124–143.Google ScholarPubMed
Reinshagen, M., Rohm, H., Steinkamp, M., Lieb, K., Geerling, I., Von Herbay, A. et al. (2000) Protective role of neurotrophins in experimental inflammation of the rat gut. Gastroenterology 119, 368–376.CrossRefGoogle ScholarPubMed
Rühl, A., Franzke, S., Collins, S.M. and Stremmel, W. (2001) Interleukin-6 expression and regulation in rat enteric glia cells. American Journal of Physiology – Gastrointestinal and Liver Physiology 280, G1163–1171.CrossRefGoogle Scholar
Rutgeerts, P., Geboes, K., Vantrappen, G., Beyls, J., Kerremans, R. and Hiele, M. (1990) Predictability of the postoperative course of Crohn's disease. Gastroenterology 99, 956–963.CrossRefGoogle ScholarPubMed
Rutgeerts, P., Geboes, K., Vantrappen, G., Kerremans, R., Coenegrachts, J.L., and Coremans, G. (1984) Natural history of recurrent Crohn's disease at the ileocolonic anastomosis after curative surgery. Gut 25, 665–672.CrossRefGoogle ScholarPubMed
Savidge, T.C., Newman, P., Pothoulakis, C., Ruhl, A., Neunlist, M., Bourreille, A. et al. (2007a) Enteric glia regulate intestinal barrier function and inflammation via release of S-nitrosoglutathione. Gastroenterology 132, 1344–1358.CrossRefGoogle ScholarPubMed
Savidge, T.C., Sofroniew, M.V. and Neunlist, M. (2007b) Starring roles for astroglia in barrier pathologies of gut and brain. Laboratory Investigation 87, 731–736.CrossRefGoogle ScholarPubMed
Shanahan, F. (2001) Inflammatory bowel disease: immunodiagnostics, immunotherapeutics, and ecotherapeutics. Gastroenterology 120, 622–635.CrossRefGoogle ScholarPubMed
Sokol, H., Polin, V., Lavergne-Slove, A., Panis, Y., Treton, X., Dray, X. et al. (2009) Plexitis as a predictive factor of early postoperative clinical recurrence in Crohn's disease. Gut 58, 1218–1225.CrossRefGoogle ScholarPubMed
Steinkamp, M., Geerling, I., Seufferlein, T., von Boyen, G., Egger, B., Grossmann, J. et al. (2003) Glial-derived neurotrophic factor regulates apoptosis in colonic epithelial cells. Gastroenterology 124, 1748–1757.CrossRefGoogle ScholarPubMed
von Boyen, G.B., Degenkolb, N., Hartmann, C., Adler, G. and Steinkamp, M. (2010) The endothelin axis influences enteric glia cell functions. Medical Science Monitor 16, BR161–BR167.Google ScholarPubMed
von Boyen, G.B., Reinshagen, M., Steinkamp, M., Adler, G. and Kirsch, J. (2002a) Gut inflammation modulated by the enteric nervous system and neurotrophic factors. Scandinavian Journal of Gastroenterology 37, 621–625.CrossRefGoogle ScholarPubMed
von Boyen, G.B., Reinshagen, M., Steinkamp, M., Adler, G. and Kirsch, J. (2002b) Enteric nervous plasticity and development: dependence on neurotrophic factors. Journal of Gastroenterology 37, 583–588.CrossRefGoogle ScholarPubMed
von Boyen, G.B., Schulte, N., Pfluger, C., Spaniol, U., Hartmann, C. and Steinkamp, M. (2011) Distribution of enteric glia and GDNF during gut inflammation. BMC Gastroenterology 11, 3. [Epub ahead of print]CrossRefGoogle ScholarPubMed
von Boyen, G.B., Steinkamp, M., Geerling, I., Reinshagen, M., Schäfer, K.H., Adler, G. et al. (2006a) Proinflammatory cytokines induce neurotrophic factor expression in enteric glia: a key to the regulation of epithelial apoptosis in Crohn's disease. Inflammatory Bowel Disease 12, 346–354.CrossRefGoogle Scholar
von Boyen, G.B., Steinkamp, M., Reinshagen, M., Schäfer, K.H., Adler, G. and Kirsch, J. (2004) Proinflammatory cytokines increase glial fibrillary acidic protein expression in enteric glia. Gut 53, 222–228.CrossRefGoogle ScholarPubMed
von Boyen, G.B., Steinkamp, M., Reinshagen, M., Schäfer, K.H., Adler, G. and Kirsch, J. (2006b) Nerve growth factor secretion in cultured enteric glia cells is modulated by proinflammatory cytokines. Journal of Neuroendocrinology 18, 820–825.CrossRefGoogle ScholarPubMed
Walz, W. (2000) Controversy surrounding the existence of discrete functional classes of astrocytes in adult gray matter. Glia 31, 95–103.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Walz, W. and Lang, M.K. (1998) Immunocytochemical evidence for a distinct GFAPnegative subpopulation of astrocytes in the adult rat hippocampus. Neuroscience Letters 257, 127–130.CrossRefGoogle ScholarPubMed
Wedel, T., Roblick, U., Gleiss, J., Schiedeck, T., Bruch, H.P., Kühnel, W. et al. (1999) Organization of the enteric nervous system in the human colon demonstrated by wholemount immunohistochemistry with special reference to the submucous plexus. Annals of Anatomy 181, 327–337.CrossRefGoogle Scholar