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The Brain-Gut Axis and the Mucosal Immunoinflammatory Response

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Neuroendocrinology of Gastrointestinal Ulceration

Part of the book series: Hans Selye Symposia on Neuroendocrinology and Stress ((HSSN,volume 2))

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Abstract

The concept of a brain-gut axis is now well established, although it is usually discussed in the context of neuroendocrine regulation of gastrointestinal secretory and motor function. That there might also be a neuroendocrine controlling effect on gastrointestinal mucosal immune function seems intuitively correct, but has only recently been investigated. While most investigators have examined systemic neuroimmune interactions1–4, it is becoming evident that the mucosal immune system may respond to distinct neuroregulatory influences5–8. The intent here is to present a brief overview of the evidence for a mucosal neuroimmune axis and to discuss its potential relevance to mucosal inflammatory disease.

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References

  1. J.E. Blalock, A molecular basis for bidirectional communication between the immune system and neuroendocrine systems. Physiol Rev. 69:1 (1989).

    PubMed  CAS  Google Scholar 

  2. B.S. Rabin, S. Cohen, R. Ganguli, D.T. Lysle, and J.E. Cunnick, Bidirectional interaction between the central nervous system and the immune system, Crit Rev Immunol 9:279 (1989).

    PubMed  CAS  Google Scholar 

  3. S. Reichlin, Neuroendocrine-immune interactions, N Engl J Med. 329:1246 (1993).

    Article  PubMed  CAS  Google Scholar 

  4. E.J. Goetzl, D.C. Adelman, and S.P. Sreedharan, Neuroimmunology, Adv Immunol. 48:161 (1990).

    Article  PubMed  CAS  Google Scholar 

  5. F. Shanahan, and P. Anton, Role of peptides in the regulation of the mucosal immune and inflammatory response, in: “Gut Peptides: Biochemistry and Physiology,” J.H. Walsh, G.J. Dockray, eds., Raven Press, New York (1994).

    Google Scholar 

  6. F. Shanahan, and P. Anton, Neuroendocrine modulation of the immune system. Possible implications for inflammatory bowel disease, Dig Dis Sci. 33:41S (1988).

    Article  PubMed  CAS  Google Scholar 

  7. K. Croitoru, P.B. Ernst, A.M. Stanisz, R.H. Stead, and J. Bienenstock, Neuroendocrine regulation of the mucosal immune system, in: “Immunology and Immunopathology of the Liver and Gastrointestinal Tract,” S.R. Targan, F. Shanahan, eds., Igaku-Shoin Press, New York, Tokyo (1989).

    Google Scholar 

  8. J. Bienenstock, M. Perdue, A. Stanisz, and R. Stead, Neurohormonal regulation of gastrointestinal immunity, Gastroenterology. 93:1431 (1987).

    PubMed  CAS  Google Scholar 

  9. R. Ader, “Psychoneuroimmunology,” Academic Press, London (1981).

    Google Scholar 

  10. G. MacQueen, J. Marshall, M. Perdue, S. Siegel, and J. Bienenstock, Conditional secretion of rat mast cell protease II by mucosal mast cells, Science. 243:83, (1989).

    Article  PubMed  CAS  Google Scholar 

  11. U.K. Olness, T. Culbert, and D. Uden, Self-regulation of salivary immunoglobulin A by children, Pediatrics. 83:66 (1989).

    PubMed  CAS  Google Scholar 

  12. H.J. Cooke, Neurobiology of the intestinal mucosa, Gastroenterology. 90:1057 (1986).

    PubMed  CAS  Google Scholar 

  13. D.L. Bellinger, D. Lorton, T.D. Romano, J.A. Olschowka, S.Y. Felten, and D.L. Felten, Neuropeptide innervation of lymphoid organs, Ann NY Acad Sci. 594:17 (1990).

    Article  PubMed  CAS  Google Scholar 

  14. C.A. Ottaway, D.L. Lewis, and S.L. Asa, Vasoactive intestinal peptide-containing nerves in Peyer’s patches, Brain Behav Immun. 1:148 (1987).

    Article  PubMed  CAS  Google Scholar 

  15. E. Ekblad, C. Winther, R. Ekman, R. Hakanson, and F. Sundler, Projections of peptide-containing neurons in rat small intestine, Neuroscience. 20:169 (1987).

    Article  PubMed  CAS  Google Scholar 

  16. L. Probert, J. Demey, and J.M. Polak, Distinct subpopulations of enteric p-type neurons contain substance P and vasoactive intestinal polypeptide, Nature. 294:470 (1981).

    Article  PubMed  CAS  Google Scholar 

  17. R.H. Stead, M. Tomioka, G. Quinonez, G. Simon, S.Y. Felten, and J. Bienenstock, Intestinal mucosal mast cells in normal and nematode-infected rat intestines are in intimate contact with peptidergic nerves, Proc Natl Acad Sci USA. 2975 (1987).

    Google Scholar 

  18. R.H. Stead, M.F. Dixon, N.H. Bramwell, R.H. Ridell, and J. Bienenstock, Mast cells are closely apposed to nerves in the human gastrointestinal mucosa, Gastroenterology. 97:575 (1989).

    PubMed  CAS  Google Scholar 

  19. N. Arizono, S. Natsuda, T. Hattori, Y. Kojima, T. Maeda, and S.J. Galli, Anatomical variation in mast cell nerve associations in the rat small intestine, heart, lung, and skin: similarities of distances between neural processes and mast cells, eosinophils, or plasma cells in the jejunal lamina propria, Lab Invest. 62:626 (1990).

    PubMed  CAS  Google Scholar 

  20. J.C. Foreman, Peptides and neurogenic inflammation, Br Med Bull. 43:386 (1987).

    PubMed  CAS  Google Scholar 

  21. B Pernow, Role of tachykinins in neurogenic inflammation, J Immunol. 135:812S (1985).

    PubMed  CAS  Google Scholar 

  22. S.D. Brain, and T.J. Williams, Substance P regulates the vasodilator activity of calcitonin gene related peptide, Nature. 335:73 (1988).

    Article  PubMed  CAS  Google Scholar 

  23. M.L. Kowalski, and M.A. Kaliner, Neurogenic inflammation, vascular permeability and mast cells,J Immunol. 140:3905 (1988).

    PubMed  CAS  Google Scholar 

  24. T. Bani-Sacchi, M. Barattini, S. Bianchi et al., The release of histamine by parasympathetic stimulation in guinea pig auricle and rat ileum, J Physiol., 371:29 (1986).

    PubMed  CAS  Google Scholar 

  25. G.A. Castro, Immunophysiology of enteric parasitism, Parasitology Today. 5:11 (1989).

    Article  PubMed  CAS  Google Scholar 

  26. A.M. Stanisz, D. Befus, and J. Bienenstock, Differential effects of vasoactive intestinal polypeptide, substance P, and somatostatin on immunoglobulin synthesis and proliferations by lymphocytes from Peyer’s Patches, mesenteric lymph nodes, and spleen, J Immunol 136:152 (1986).

    PubMed  CAS  Google Scholar 

  27. A.M. Stanisz, R. Scicchitano, P. Dazin, J. Bienenstock, D.G. Payan, Distribution of substance P receptors in murine spleen and Peyer’s patch T and B cells, J Immunol. 139:749 (1987).

    PubMed  CAS  Google Scholar 

  28. R. Scicchitano, P. Dazin, J. Bienenstock, D.G. Payan, and A.M. Stanisz, Distribution of somatostatin receptors on murine spleen and Peyer’s patch T and B lymphocytes, Brain Behav Immunol. 1:173 (1987).

    Article  CAS  Google Scholar 

  29. A.A. Irani, and L.B. Schwartz, Mast cell heterogeneity, Clin Exp Allergy. 19:143 (1989).

    Article  PubMed  CAS  Google Scholar 

  30. Y. Kitamura, Heterogeneity of mast cells and phenotypic change between subpopulations, Ann Rev Immunol. 7:59 (1989).

    Article  CAS  Google Scholar 

  31. F. Shanahan, J.A. Denburg, J. Fox, J. Bienenstock, and D. Befus, Mast cell heterogeneity: effect of neuroenteric peptides on histamine release, J Immunol. 135:1331 (1985).

    PubMed  CAS  Google Scholar 

  32. F. Shanahan, T.D.G. Lee, J. Bienenstock, and A.D. Befus, The influence of endorphins on peritoneal and mucosal mast cell secretion, J Allergy Clin Immunol. 74:499 (1984).

    Article  PubMed  CAS  Google Scholar 

  33. E.J. Goetzl, T. Chernov-Rogan, K. Furuichi, L.M. Goetzl, J.Y. Lee, and F. Renold,Neuromodulation of mast cell and basophil function, in: “Mast Cell Differentiation and Heterogeneity,” A.D. Befus, J. Bienenstock, J.A. Denburg, eds., Raven Press, New York (1986).

    Google Scholar 

  34. H. Repke, and M. Bienert, Mast cell activation-a receptor-independent mode of substance P action, FEBS Lett. 221:236 (1987).

    Article  PubMed  CAS  Google Scholar 

  35. M. Mousli, J.L. Bueb, C. Bronner, B. Rouot, and Y. Landry, G protein activation: a receptor independent mode of action for cationic amphiphilic neuropeptides and venom peptides, Trends Pharmacol Sci. 11:358 (1990).

    Article  PubMed  CAS  Google Scholar 

  36. C.A. Ottaway, Migration of lymphocytes within the mucosal immune system, in: “Immunology and Immunopathology of the Liver and Gastrointestinal Tract,” S.R. Targan, F. Shanahan, eds., Igaku-Shoin Press, New York, Tokyo (1989).

    Google Scholar 

  37. C.A. Ottaway, In vitro alteration of receptors for vasoactive intestinal peptide changes the in vivo localization of mouse T cells, J Exp Med. 160:1054 (1984).

    Article  PubMed  CAS  Google Scholar 

  38. D.N. Khansari, A.J. Murgo, and R.E. Faith. Effects of stress on the immune system, Immunol Today. 11:170 (1990).

    Article  PubMed  CAS  Google Scholar 

  39. D. Mason, Genetic variation in the stress response: susceptibility to experimental allergic encephalomyelitis and implications for human inflammatory disease, Immunol Today. 12:57 (1991).

    Article  PubMed  CAS  Google Scholar 

  40. S. Cohen, D.A.J. Tyrell, and A.P. Smith, Psychological stress and susceptibility to the common cold,N Engl J Med. 325:606 (1991).

    Article  PubMed  CAS  Google Scholar 

  41. S. Meyers, and H.D. Janowitz, “Natural history” of Crohn’s disease. An analytical review of the placebo lession, Gastroenterology. 87:1189 (1984).

    PubMed  CAS  Google Scholar 

  42. F. Shanahan, and S. Targan, Mechanisms of tissue injury in inflammatory bowel disease, in:“Inflammatory Bowel Disease: From Bench to Bedside,” S. Targan, F. Shanahan, eds., Williams & Wilkins, Baltimore (1994).

    Google Scholar 

  43. V.E. Eysselein, and C.C. Nast, Neuropeptides and inflammatory bowel disease, in: “Inflammatory bowel diseases. Progress in basic research and clinical implications,” H. Goebell, K. Ewe, H. Malchow, C.H. Koelbel., eds., Kluwer Academic Publishers, Dordrecht (1991).

    Google Scholar 

  44. C.R. Mantyh, T.S. Gates, R.P. Zimmerman, M.L. Welton, E.P. Passaro, S.R. Vigna, R. Maggio,L. Kurger, and P.W. Mantyh, Receptor binding sites for substance P, but not substance K or neuromedin K, are expressed in high concentrations by arterioles, venules, and lymph nodules in surgical specimens obtained from patients with ulcerative colitis and Crohn’s disease, Proc Natl Acad Sci USA. 85:3235 (1988).

    Article  PubMed  CAS  Google Scholar 

  45. P.W. Mantyh, M.D. Catton, C.G. Boehmer, M.L. Welton, E.P. Passaro, J.E. Maggio, and S.R.Vigna, Receptors for sensory neuropeptides in human inflammatory bowel diseases: implications for the effector role of sensory neurons, Peptides. 10:627 (1989).

    Article  PubMed  CAS  Google Scholar 

  46. P.A. Anton, J.R. Reeve, A. Vidrich, E. Mayer and F. Shanahan, Development of a biotinylatedanalog of substance P for use as a receptor probe, Lab Invest. 64:703 (1991).

    PubMed  CAS  Google Scholar 

  47. P.W. Mantyh, D.J. Johnson, C.G. Boehmer, M.D. Catton, H.V. Vinters, J.E. Maggio, H.-P. Too, and S.R. Vigna, Substance P receptor binding sites are expressed by glia in vivo after neuronal injury, Proc Natl Acad Sci USA. 86:5193 (1989).

    Article  PubMed  CAS  Google Scholar 

  48. J. Nilsson, A.M. von Euler, and C.-J. Dalsgaard, Stimulation of connective tissue cell growth by substance P and substance K, Nature. 315:61 (1985).

    Article  PubMed  CAS  Google Scholar 

  49. E.S. Kimball, and M.C. Fisher, Potentiation of IL-1-induced BALB/3T3 fibroblast proliferation by neuropeptides, I Immunol. 141:4203 (1988).

    CAS  Google Scholar 

  50. P. Holzer, M.A. Pabst, I. Th. Lippe, Intragastric capsaicin protects against aspirin-induced lesion formation and bleeding in the rat gastric mucosa, Gastroenterology. 96:1425 (1989).

    PubMed  CAS  Google Scholar 

  51. S. Evangelista, and A. Meli, Influence of capsaicin-sensitive fibres on experimentally-induced colitis in rats, I Pharm Pharmacol. 41:574 (1989).

    CAS  Google Scholar 

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Authors
  1. Fergus Shanahan
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Editor information

Editors and Affiliations

  1. Harvard Medical School, Boston, Massachusetts, USA

    Sandor Szabo

  2. Irvine VA Medical Center, University of California, Long Beach, California, USA

    Sandor Szabo

  3. Center for Ulcer Research and Education, University of California, Los Angeles, California, USA

    Yvette Taché

  4. University of Manitoba, Winnipeg, Manitoba, Canada

    Gary B. Glavin

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© 1995 Springer Science+Business Media New York

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Shanahan, F. (1995). The Brain-Gut Axis and the Mucosal Immunoinflammatory Response. In: Szabo, S., Taché, Y., Glavin, G.B. (eds) Neuroendocrinology of Gastrointestinal Ulceration. Hans Selye Symposia on Neuroendocrinology and Stress, vol 2. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-1867-9_10

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  • DOI: https://doi.org/10.1007/978-1-4615-1867-9_10

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-5759-9

  • Online ISBN: 978-1-4615-1867-9

  • eBook Packages: Springer Book Archive

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