SpringerLink
Log in

Role of histamine in a rat model of colitis

  • Original Research Papers
  • Published:
Inflammation Research Aims and scope Submit manuscript

Abstract

We examined the possible involvement of mast cells in a rat model of colitis, by monitoring levels of histamine at various times after inducing inflammation with intrarectal trinitrobenzene sulfonic acid in 50% ethanol. The ability of a histamine H1 antagonist, diphenhydramine, to modify colitis was also assessed. As expected, trinitrobenzene sulfonic acid in 50% ethanol induced a sustained colitis. Myeloperoxidase levels in macroscopically damaged tissue peaked at one week, and declined thereafter. In contrast, tissue histamine levels were normal at one week, then increased in damaged tissue to approximately four times normal levels at four weeks. Indices of inflammation were markedly suppressed at one week by diphenhydramine, while tissue histamine levels were unaffected. Chronic colitis in rats is thus apparently accompanied by a local mast cell hyperplasia or influx. Moreover, antagonism of a major mast cell mediator, histamine, significantly reduces the severity of inflammation in this model.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

MPO:

myeloperoxidas

SCF:

stem cell factor

TNB:

trinitrobenzene sulfonic acid

References

  1. Barrett KE, Metcalfe DD. The mucosal mast cell and its role in gastrointestinal allergic disease. Clin Rev Allergy 1984;2:39–53.

    Google Scholar 

  2. McAuley RL, Sommers SC. Mast cells in nonspecific ulcerative colitis. Am J Dig Dis 1961;6:233–6.

    Google Scholar 

  3. Dvorak AM, Monahan RA, Osage JE, Dickersin GR. Crohn's disease: Transmission electron microscopic studies. II. Immunologic inflammatory response. Alterations of mast cells, basophils, eosinophils and the microvasculature. Hum Pathol 1980;11:606–19.

    Google Scholar 

  4. Dvorak AM, McLeod RS, Onderdonk A, Monahan-Earley RA, Cullen JB, Antonioli DA et al. Ultrastructural evidence for piecemeal and anaphylactic degranulation of human gut mucosal mast cells in vivo. Int Archs Allergy Appl Immunol 1992;99:74–83.

    Google Scholar 

  5. Nolte H, Spjeldnaes N, Kruse A and Windelborg B. Histamine release from gut mast cells from patients with inflammatory bowel diseases. Gut 1990;31:791–4.

    Google Scholar 

  6. King T, Biddle W, Bhatia P, Moore J and Miner Jr PB. Colonic mucosal mast cell distribution at line of demarcation of active ulcerative colitis. Dig Dis Sci 1992;37:490–5.

    Google Scholar 

  7. Balaz M, Illyes G and Vadasz G. Mast cells in ulcerative colitis. Quantitative and ultrastructural studies. Virchows Archiv. B Cell Pathol. 1989;57:353–60.

    Google Scholar 

  8. Eliakim R, Rachmilewitz D, Ligumsky M and Razin E. Pathogenesis of ulcerative colitis: increased colonic chondroitin sulfate E synthesis indicates possible involvement of E-mast cells. Gastroenterol 1986;90:1404.

    Google Scholar 

  9. Fox CC, Lazenby AJ, Moore WC, Yardley JH, Bayless TM, Lichtenstein LM. Enhancement of human intestinal mast cell mediator release in active ulcerative colitis. Gastroenterol 1990;99:119–24

    Google Scholar 

  10. Fox CC, Lichtenstein LM, Roche JK. Intestinal mast cell responses in idiopathic inflammatory bowel disease. Histamine release from human intestinal mast cells in response to gut epithelial proteins. Dig Dis Sci 1993;38:1105–12.

    Google Scholar 

  11. Fox CC, Moore WC, Lichtenstein LM. Modulation of mediator release from human intestinal mast cells by sulfasalazine and 5-amino-salicyclic acid. Dig Dis Sci 1991;36:179–84.

    Google Scholar 

  12. Barrett KE, Pearce FL. Mast cell heterogeneity. In: Foreman JC, editor. Immunopharmacology of Mast Cells and Basophils. London: Academic Press 1993:29–42.

    Google Scholar 

  13. Thompson H, Buchmann P. Mast cell population in rectal biopsies from patients with Crohn's disease. In: Pepys J, Edwards AM, editors. The Mast Cell: its Role in Health and Disease. Tunbridge Wells: Pitman Medical Publishing, 1979:697–701.

    Google Scholar 

  14. Sanderson IR, Leung KBP, Pearce FL, Walker-Smith JA. Lamina propria mast cells in biopsies from children with Crohn's disease. J Clin Pathol 1986;39:279–83.

    Google Scholar 

  15. Soda K, Kawabori S, Perdue MH, Bienenstock J. Macrophage engulfment of mucosal mast cells in rats treated with dexamethasone. Gastroenterol 1991;100:929–37.

    Google Scholar 

  16. Riley JF, West GB. The presence of histamine in tissue mast cells. J Physiol 1953;120:528–37.

    Google Scholar 

  17. Saavedra-Delgado AMP, Turpin S, Metcalfe DD. Typical and atypical mast cells of the rat gastrointestinal system: distribution and correlation with tissue histamine. Agents Actions 1984;14:1–7.

    Google Scholar 

  18. Raithel A, Horauf AM, Matek M, Baenkler HW. Kinetics of histamine released from rectal mucosa. Agents Actions 1989;28:164–7.

    Google Scholar 

  19. Knutson L, Ahrenstedt O, Odlind B, Hallgren R. The jejunal secretion of histamine is increased in active Crohn's disease. Gastroenterol 1990;98:849–54.

    Google Scholar 

  20. Schmidt WU, Sattler J, Hesterberg R, Roher HD, Zoedler T, Sitter H, et al. Human intestinal diamine oxidase (DAO) activity in Crohn's disease: a new marker for disease assessment? Agents Actions 1990;30:267–70.

    Google Scholar 

  21. Morris GP, Beck PL, Herridge MS, Depew WT, Szewczuk MR, Wallace JL. A hapten-induced model of chronic inflammation and ulceration in the rat colon. Gastroenterol 1989;96:795–803.

    Google Scholar 

  22. Lindstrom CG, Rosengren JE, Fork FT. Colon of the rat. An anatomic, histologic and radiographic investigation. Acta Radiol Diagn 1979;20:523–36.

    Google Scholar 

  23. Bradley PP, Priebat DA, Christensen RD, Rothstein G. Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol 1982;78:206–9.

    Google Scholar 

  24. Shore PA, Burkhalter A, Cohn VH. A method for the fluorimetric assay of histamine in tissues. J Pharmacol Exp Ther 1959;127:182–6.

    Google Scholar 

  25. Aldenborg F, Nilsson K, Jarlshammar B, Bjermer L, Enerback L. Mast cells and biogenic amines in radiation-induced pulmonary fibrosis. Am J Resp Cell Mol Biol 1993;8:112–7.

    Google Scholar 

  26. Kitamura Y, Kasugai T, Nomura S, Matsuda H. Development of mast cells and basophils. In: Foreman JC, editor. Immunopharmacology of Mast Cells and Basophils. London: Academic Press, 1993;5–27.

    Google Scholar 

  27. Hirschowitz BI, Molina E. Anticholinergic potency of diphenhydramine (Benadryl) measured against bethanechol in the gastric fistula dog. J Pharmacol Exp Ther 1983;226:171–3.

    Google Scholar 

  28. Weinstock JV, Chensue SW, Boros DL. Modulation of granulomatous hypersensitivity. V. Participation of histamine receptor positive and negative lymphocytes in the granulomatous response of Schistosoma mansoni-infected mice. J Immunol 1983;130:423–7.

    Google Scholar 

  29. Rangachari PK. Histamine: mercurial messenger in the gut. Am J Physiol 1992;262:G1–13.

    Google Scholar 

  30. Stanciu L. Immunomodulation by histamine. Ann Biol Clin 1990;48:623–5.

    Google Scholar 

  31. Owen DAA. Inflammation — histamine and 5-hydroxytryptamine. Brit Med Bull 1987;43:256–69.

    Google Scholar 

  32. Fujisaki J, Fujimoto K, Oohara A, Sakata T, Hirano M, Ohyama T, et al. Roles of histamine and diamine oxidase in mucosa of rat small intestine after ischemia-reperfusion. Dig Dis Sci 1993;38:1195–200.

    Google Scholar 

  33. Wolf DJ, Lubeski A. Aminoguanidine is an isoform-selective, mechanism-based inactivator of nitric oxide synthase. Arch Biochem Biophys 1995;316:290–301.

    Google Scholar 

  34. Bradding P, Feather IH, Wilson S, Bardin PG, Heusser CH, Holgate ST, et al. Immunolocalization of cytokines in the nasal mucosa of normal and perennial rhinitic subjects. The mast cell as a source of IL-4, IL-5, and IL-6 in human allergic mucosal inflammation. J Immunol 1993;151:3853–65.

    Google Scholar 

  35. Smith CW. Endothelial adhesion molecules and their role in inflammation. Can J Physiol Pharmacol 1993;71:76–87.

    Google Scholar 

  36. Marshall JS. Repeated antigen challenge in rats induces a mucosal mast cell hyperplasia. Gastroenterol 1993;105:391–8.

    Google Scholar 

  37. Chin KW, Barrett KE. Mast cells are not essential to inflammation in murine model of colitis. Dig Dis Sci 1994;39:513–25.

    Google Scholar 

  38. Gelbmann CM, Schteingart CD, Thompson SM, Hofmann AF, Barrett KE. Mast cells and histamine contribute to bile acidstimulated secretion in the mouse colon. J Clin Invest 1995;95:2831–9.

    Google Scholar 

Download references

Author information

Author notes

  1. C. M. Gelbmann

    Present address: Medizinische Klinik und Poliklinik I, University of Regensburg, Franz-Josef-Strauss-Allee 11, D-93053, Regensburg, Germany

Authors and Affiliations

  1. Department of Medicine, University of California, San Diego, School of Medicine, 200 West Arbor Drive, 92103-8414, San Diego, CA, USA

    C. M. Gelbmann & K. E. Barrett

Authors
  1. C. M. Gelbmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. E. Barrett
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gelbmann, C.M., Barrett, K.E. Role of histamine in a rat model of colitis. Inflamm Res 44, 386–392 (1995). https://doi.org/10.1007/BF01797866

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01797866

Keywords

Search

Navigation