The role of smooth muscle in intestinal inflammation

  • S. M. Collins
  • I. Khan
  • B. Vallance
  • C. Hogaboam

Abstract

The observation that active ulcerative colitis is accompanied by a reduction in motor activity in the distal colon1–3 suggests that the contractility of colonic smooth muscle may be impaired as a result of inflammation. this has been confirmed in an in-vitro study of human colonic circular muscle in which contraction induced by either bethanechol or KC1 was significantly reduced in comparison to muscle obtained from patients without inflammatory bowel disease (IBD)4, suggesting that the underlying mechanism is located at the postreceptor level in the excitation—contraction coupling of the muscle cell. Similar observations have been made in animal models of colitis5. In our study5, a similar decrease in colonic smooth muscle contractility was observed in colitis induced by chemical injury (acetic acid or trinitrobenzene sulfonic acid, TNB), as well as infection (Trichinella spiralis) These results also illustrate that inflammation-induced changes in smooth muscle are nonspecific in that they do not appear to be influenced by the manner in which colitis is induced.

Keywords

Intestinal Smooth Muscle Trinitrobenzene Sulfonic Acid Intestinal Muscle Colonic Smooth Muscle Inflame Intestine 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Rao SSC, Read NW, Brown C, Bruce C, Holdsworth CD. Studies on the mechanism of bowel disturbance in ulcerative colitis. Gastroenterology. 1987; 93: 934–40.PubMedGoogle Scholar
  2. 2.
    Kern FJ, Almy TP, Abbot FK, Bogdonoff MD. Motility of the distal colon in nonspecific ulcerative colitis. Gastroenterology. 1951; 19: 492–503.PubMedGoogle Scholar
  3. 3.
    Snape WJ, Matarazzo SA, Cohen S. Abnormal gastrocolonic response in patients with ulcerative colitis. Gut. 1980; 21: 392–6.PubMedCrossRefGoogle Scholar
  4. 4.
    Snape WI, Williams R, Hyman PE. Defect in colonic muscle contraction in patients with ulcerative colitis. Am J Physiol. 1991; 261: G987–91.PubMedGoogle Scholar
  5. 5.
    Grossi L, McHugh K, Collins SM. On the specificity of altered muscle function in experimental colitis in rats. Gastroenterology. 1993; 104: 1049–56.PubMedGoogle Scholar
  6. 6.
    Vermillion DL, Huizinga JD, Ridell RH, Collins SM. Altered small intestinal smooth muscle function in Crohn’s disease. Gastroenterology. 1993; 104: 1692–700.PubMedGoogle Scholar
  7. 7.
    Vermillion DL, Collins SM. Increased responsiveness of jejuna] longitudinal muscle in Trichinella-infected rats. Am J Physiol. 1988; 254: G124–9.Google Scholar
  8. 8.
    Russell DA, Castro GA. Physiology of the gastrointestinal tract in the parasitized host. In: Johnson LR, editor. Physiology of the gastrointestinal tract, 2nd edn. New York: Raven Press; 1987: 1749–80.Google Scholar
  9. 9.
    Muller MJ, Huizinga JD, Collins SM. Altered smooth muscle contraction and sodium pump activity in the inflamed rat intestine. Am J Physiol. 1989; 257: G570–7.PubMedGoogle Scholar
  10. 10.
    Khan I, Collins SM. Altered sodium pump gene expression in the inflamed intestine of the nematode-infected rat. Am J Physiol. 1993; 264: G1160–8.PubMedGoogle Scholar
  11. 11.
    Bowers RL, Castro GA, Lai M, Harari Y, Weisbrodt NW. Actin mRNA expression in intestinal smooth muscle of rats infected with Trichinella spiralis. Gastroenterology. 1990; 99: 1236 (abstr.).Google Scholar
  12. 12.
    Graham MF, Diegelmann RF, Elson CO et al Collagen content and types in the intestinal strictures of Crohn’s disease. Gastroenterology. 1988; 94: 257–65.PubMedGoogle Scholar
  13. 13.
    Dvorak AM, Connell AB, Dickersin GR. Crohn’s disease, a scanning electron microscopic study. Hum Pathol. 1979; 10: 165–77.PubMedCrossRefGoogle Scholar
  14. 14.
    Shah M, Willey A, Graham MP. Inflammatory bowel disease induces changes in the in vitro phenotype of human intestinal muscle cells. Gastroenterology. 1993; 104: 779 (abstr.).Google Scholar
  15. 15.
    Blennerhassett MG, Vignjevic P, Vermillion DL, Collins SM. Inflammation causes hyperplasia and hypertrophy in smooth muscle of rat small intestine. Am J Physiol. 1992; 262: G1041–6.PubMedGoogle Scholar
  16. 16.
    Scheinfeld BA, Collins SM, Blennerhassett MG. Verapamil inhibits interleukin-lß-mediated hyperplasia of human intestinal smooth muscle. Gastroenterology. 1994; 106: A768.Google Scholar
  17. 17.
    Marzio L, Blennerhassett P, Chiverton S, Vermillion DL, Langer J, Collins SM. Altered smooth muscle function in worm-free gut regions of Trichinella-infected rats. Am J Physiol. 1990; 259: G306–13.PubMedGoogle Scholar
  18. 18.
    Vermillion DL, Ernst PB, Collins SM. T-lymphocyte modulation of intestinal muscle function in the Trichinella-infected rat. Gastroenterology. 1991; 101: 31–8.PubMedGoogle Scholar
  19. 19.
    Dzwonkowski P, Stead RH, Blennerhassett MG, Collins SM. Induction of class II major histocompatibility complex (MHCII) in enteric smooth muscle. Gastroenterology. 1991; 100: A577 (abstr.).Google Scholar
  20. 20.
    Valiance BA, Blennerhassett PA, Collins SM. T lymphocyte dependence of persistent intestinal muscle function post infection by Trichinella spiralis in the mouse. Gastroenterology. 1994; 106: A1054.Google Scholar
  21. 21.
    Else KJ, Hultner L, Grencis RK. Cellular immune responses to the murine nematode parasite Trichuris muris. II. Differential induction of Th-cell subsets in resistant versus susceptible mice. Immunology. 1992; 75: 232–7.PubMedGoogle Scholar
  22. 22.
    Else KJ, Grencis RK. Cellular immune responses to the murine nematode parasite Trichuris muris. I. Differential cytokine production during acute or chronic infection. Immunology. 1991; 72: 508–13.PubMedGoogle Scholar
  23. 23.
    Zhu DH, Bell RG. IL-2 production, IL-2 receptor expression, and IL-2 responsiveness of spleen and mesenteric lymph node cells from inbred mice infected with Trichinella spiralis. J Immunol. 1989; 142: 3262–7.PubMedGoogle Scholar
  24. 24.
    Wakelin D. Allergic inflammation as a hypothesis for the expulsion of worms from tissues. Parasitol Today. 1993; 9: 115–16.PubMedCrossRefGoogle Scholar
  25. 25.
    Blennerhassett G, Vignjevic P, Vermillion DL, Ernst PB, Collins SM. Intestinal inflammation induces T-lymphocyte-dependent hyperplasia of jejunal smooth muscle. Gastroenterology. 1990; 98: A328 (abstr.).Google Scholar
  26. 26.
    Hogaboam CM, Jacobson K, Collins SM, Blennerhassett MG. The selective beneficial effects of nitric oxide inhibition in experimental colitis. Gastroenterology. 1994; 106: A700.Google Scholar
  27. 27.
    Dvorak AM, Osage JE, Monahan RA, Dickersin GR. Crohn’s disease: transmission electron microscopic studies. III. Target tissues. Proliferation of and injury to smooth muscle and the autonomic nervous system. Hum Pathol. 1980; 11: 620–34.PubMedCrossRefGoogle Scholar
  28. 28.
    Graham MF, Drucker DE, Diegelmann RF, Elson CO. Collagen synthesis by human intestinal smooth muscle cells in culture. Gastroenterology. 1987; 92: 400–5.PubMedGoogle Scholar
  29. 29.
    Graham MF, Bryson GR, Diegelmann RF. Transforming growth factor beta 1 selectively augments collagen synthesis by human intestinal smooth muscle cells. Gastroenterology. 1990; 99: 447–53.PubMedGoogle Scholar
  30. 30.
    Kao HW, Zipser RD. Exaggerated prostaglandin production by colonic smooth muscle in rabbit colitis. Dig Dis Sci. 1988; 33: 697–704.PubMedCrossRefGoogle Scholar
  31. 31.
    Khan I, Blennerhassett P, Gauldie J, Collins SM. Cytokine mRNA profile in smooth muscle from the inflamed intestine of the nematode-infected rat. Gastroenterology. I992;102:A645 (abstract).Google Scholar
  32. 32.
    Khan I, Kataeva G, Blennerhassett MG, Collins SM. Auto-induction of interleukin-lß gene expression in enteric smooth muscle cells. Gastroenterology. 1993; 104: A534 (abstr.).Google Scholar
  33. 33.
    Khan I, Collins SM. Interleukin-lß induces the expression of interleukin-6 in intestinal smooth muscle cells. Gastroenterology. 1994; 106: A710.Google Scholar
  34. 34.
    Hogaboam CM, Hewlett B, Stead RH, Snider DP, Collins SM. Cytokine-induced class II major histocompatibility antigen and intracellular adhesion molecular expression on murine intestinal smooth muscle cells. Gastroenterology. 1994; 106: A700.Google Scholar
  35. 35.
    Goebels N, Michaelis D, Wekerle H, Hohfeld R. Human myoblasts as antigen presenting cells. J Immunol. 1992; 149: 661–7.PubMedGoogle Scholar
  36. 36.
    Hart MN, Waldschmidt MM, Hanley-Hyde JH, Moore SA, Kemp JD, Schelper RL. Brain microvascular smooth muscle expresses Class II antigens. J Immunol. 1987; 138: 2960–3.PubMedGoogle Scholar
  37. 37.
    Blennerhassett MG, Catallo D. Dexamethasone blocks vascular leakage, but not endothelial activation, in smooth muscle of inflamed rat jejunum. Gastroenterology. 1993; 104: A670 (abstr.).Google Scholar
  38. 38.
    Isgar B, Harman M, Kaye MD, Whorwell PJ. Symptoms of irritable bowel syndrome in ulcerative colitis in remission. Gut. 1983; 24: 190–2.PubMedCrossRefGoogle Scholar
  39. 39.
    Rao SSC, Read NW, Stobart JAH, Haynes WG, Benjamin S, Holdsworth CD. Anorectal contractility under basal conditions and during rectal infusion of saline in ulcerative colitis. Gut. 1988; 29: 769–77.PubMedCrossRefGoogle Scholar
  40. 40.
    Valiance BA, Blennerhassett PA, Collins SM. Murine trichinosis: a model of post-infective smooth muscle dysfunction. Gastroenterology. 1994; 106: A584.Google Scholar
  41. 41.
    Beasley D, Cohen RA, Levinsky NG. Interleukin-1 inhibits contraction of vascular smooth muscle. J Clin Invest. 1989; 83: 331–5.PubMedCrossRefGoogle Scholar
  42. 42.
    Collins SM, Hurst SM, Main C et al Effect of inflammation of enteric nerves. Cytokine-induced changes in neurotransmitter content and release. Ann NY Acad Sci. 1992; 664: 4 1524.Google Scholar

Copyright information

© Kluwer Academic Publishers and Axcan Pharma, Inc. 1994

Authors and Affiliations

  • S. M. Collins
  • I. Khan
  • B. Vallance
  • C. Hogaboam

There are no affiliations available

Personalised recommendations