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Clinical and Experimental Immunology logoLink to Clinical and Experimental Immunology
. 1995 Jul;101(1):157–163. doi: 10.1111/j.1365-2249.1995.tb02292.x

Adhesion molecules intercellular adhesion molecule-1 (ICAM-1), ICAM-3 and B7 are not expressed by epithelium in normal or inflamed colon.

S Bloom 1, D Simmons 1, D P Jewell 1
PMCID: PMC1553302  PMID: 7542573

Abstract

Adhesion molecules are involved in facilitating cell-mediated immune events. Because lymphocyte-epithelial cell interaction has been implicated in the pathogenesis of colonic inflammation, we analysed expression of a range of adhesion molecules on colonic epithelium in vitro and in vivo using flow cytometry, immunohistochemistry and in situ hybridization. Expression of ICAM-1 by cell lines HT29 and int407 was increased by proinflammatory cytokines interferon-gamma (IFN-gamma), tumour necrosis factor-alpha (TNF-alpha) and IL-1 but not by IL-6. Vascular cell adhesion molecule (VCAM) and E-selectin were not expressed. Immunohistochemistry using sections of inflamed colon from 16 patients with ulcerative colitis (UC), five patients with Crohn's disease (CD) and seven patients with normal colonoscopic biopsies, showed no expression of ICAM-1 on colonic epithelium. VCAM was seen in isolated lymphoid aggregates and E-selectin was expressed on endothelium. In situ hybridization showed no ICAM-1 or ICAM-3 mRNA in colonic epithelium. B7, the ligand for CD28, was not found on normal or inflamed colonic epithelium. The adhesion molecules ICAM-1, ICAM-3 and B7 are not involved in lymphocyte-epithelial cell interaction in the normal or inflamed colon. This may have implications for the development of T cell tolerance to intestinal luminal antigens.

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Selected References

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  1. Aruffo A., Seed B. Molecular cloning of a CD28 cDNA by a high-efficiency COS cell expression system. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8573–8577. doi: 10.1073/pnas.84.23.8573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bevilacqua M. P., Stengelin S., Gimbrone M. A., Jr, Seed B. Endothelial leukocyte adhesion molecule 1: an inducible receptor for neutrophils related to complement regulatory proteins and lectins. Science. 1989 Mar 3;243(4895):1160–1165. doi: 10.1126/science.2466335. [DOI] [PubMed] [Google Scholar]
  3. Bland P. W., Warren L. G. Antigen presentation by epithelial cells of the rat small intestine. I. Kinetics, antigen specificity and blocking by anti-Ia antisera. Immunology. 1986 May;58(1):1–7. [PMC free article] [PubMed] [Google Scholar]
  4. Bland P. W., Warren L. G. Antigen presentation by epithelial cells of the rat small intestine. II. Selective induction of suppressor T cells. Immunology. 1986 May;58(1):9–14. [PMC free article] [PubMed] [Google Scholar]
  5. Brynskov J., Tvede N., Andersen C. B., Vilien M. Increased concentrations of interleukin 1 beta, interleukin-2, and soluble interleukin-2 receptors in endoscopical mucosal biopsy specimens with active inflammatory bowel disease. Gut. 1992 Jan;33(1):55–58. doi: 10.1136/gut.33.1.55. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cominelli F., Dinarello C. A. Interleukin-1 in the pathogenesis of and protection from inflammatory bowel disease. Biotherapy. 1989;1(4):369–375. doi: 10.1007/BF02171013. [DOI] [PubMed] [Google Scholar]
  7. Dippold W., Wittig B., Schwaeble W., Mayet W., Meyer zum Büschenfelde K. H. Expression of intercellular adhesion molecule 1 (ICAM-1, CD54) in colonic epithelial cells. Gut. 1993 Nov;34(11):1593–1597. doi: 10.1136/gut.34.11.1593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dustin M. L., Rothlein R., Bhan A. K., Dinarello C. A., Springer T. A. Induction by IL 1 and interferon-gamma: tissue distribution, biochemistry, and function of a natural adherence molecule (ICAM-1). J Immunol. 1986 Jul 1;137(1):245–254. [PubMed] [Google Scholar]
  9. Dustin M. L., Springer T. A. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature. 1989 Oct 19;341(6243):619–624. doi: 10.1038/341619a0. [DOI] [PubMed] [Google Scholar]
  10. Fais S., Capobianchi M. R., Pallone F., Di Marco P., Boirivant M., Dianzani F., Torsoli A. Spontaneous release of interferon gamma by intestinal lamina propria lymphocytes in Crohn's disease. Kinetics of in vitro response to interferon gamma inducers. Gut. 1991 Apr;32(4):403–407. doi: 10.1136/gut.32.4.403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fawcett J., Holness C. L., Needham L. A., Turley H., Gatter K. C., Mason D. Y., Simmons D. L. Molecular cloning of ICAM-3, a third ligand for LFA-1, constitutively expressed on resting leukocytes. Nature. 1992 Dec 3;360(6403):481–484. doi: 10.1038/360481a0. [DOI] [PubMed] [Google Scholar]
  12. Freeman G. J., Gray G. S., Gimmi C. D., Lombard D. B., Zhou L. J., White M., Fingeroth J. D., Gribben J. G., Nadler L. M. Structure, expression, and T cell costimulatory activity of the murine homologue of the human B lymphocyte activation antigen B7. J Exp Med. 1991 Sep 1;174(3):625–631. doi: 10.1084/jem.174.3.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gimmi C. D., Freeman G. J., Gribben J. G., Sugita K., Freedman A. S., Morimoto C., Nadler L. M. B-cell surface antigen B7 provides a costimulatory signal that induces T cells to proliferate and secrete interleukin 2. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6575–6579. doi: 10.1073/pnas.88.15.6575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hoang P., Crotty B., Dalton H. R., Jewell D. P. Epithelial cells bearing class II molecules stimulate allogeneic human colonic intraepithelial lymphocytes. Gut. 1992 Aug;33(8):1089–1093. doi: 10.1136/gut.33.8.1089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kaiserlian D., Rigal D., Abello J., Revillard J. P. Expression, function and regulation of the intercellular adhesion molecule-1 (ICAM-1) on human intestinal epithelial cell lines. Eur J Immunol. 1991 Oct;21(10):2415–2421. doi: 10.1002/eji.1830211018. [DOI] [PubMed] [Google Scholar]
  16. Kaiserlian D., Vidal K., Revillard J. P. Murine enterocytes can present soluble antigen to specific class II-restricted CD4+ T cells. Eur J Immunol. 1989 Aug;19(8):1513–1516. doi: 10.1002/eji.1830190827. [DOI] [PubMed] [Google Scholar]
  17. Kemler B. J., Alpert E. Inflammatory bowel disease: study of cell mediated cytotoxicity for isolated human colonic epithelial cells. Gut. 1980 May;21(5):353–359. doi: 10.1136/gut.21.5.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Koizumi M., King N., Lobb R., Benjamin C., Podolsky D. K. Expression of vascular adhesion molecules in inflammatory bowel disease. Gastroenterology. 1992 Sep;103(3):840–847. doi: 10.1016/0016-5085(92)90015-q. [DOI] [PubMed] [Google Scholar]
  19. Kvale D., Krajci P., Brandtzaeg P. Expression and regulation of adhesion molecules ICAM-1 (CD54) and LFA-3 (CD58) in human intestinal epithelial cell lines. Scand J Immunol. 1992 Jun;35(6):669–676. doi: 10.1111/j.1365-3083.1992.tb02973.x. [DOI] [PubMed] [Google Scholar]
  20. Linsley P. S., Brady W., Grosmaire L., Aruffo A., Damle N. K., Ledbetter J. A. Binding of the B cell activation antigen B7 to CD28 costimulates T cell proliferation and interleukin 2 mRNA accumulation. J Exp Med. 1991 Mar 1;173(3):721–730. doi: 10.1084/jem.173.3.721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Linsley P. S., Clark E. A., Ledbetter J. A. T-cell antigen CD28 mediates adhesion with B cells by interacting with activation antigen B7/BB-1. Proc Natl Acad Sci U S A. 1990 Jul;87(13):5031–5035. doi: 10.1073/pnas.87.13.5031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Malizia G., Calabrese A., Cottone M., Raimondo M., Trejdosiewicz L. K., Smart C. J., Oliva L., Pagliaro L. Expression of leukocyte adhesion molecules by mucosal mononuclear phagocytes in inflammatory bowel disease. Gastroenterology. 1991 Jan;100(1):150–159. doi: 10.1016/0016-5085(91)90595-c. [DOI] [PubMed] [Google Scholar]
  23. Mayer L., Eisenhardt D., Salomon P., Bauer W., Plous R., Piccinini L. Expression of class II molecules on intestinal epithelial cells in humans. Differences between normal and inflammatory bowel disease. Gastroenterology. 1991 Jan;100(1):3–12. doi: 10.1016/0016-5085(91)90575-6. [DOI] [PubMed] [Google Scholar]
  24. Mayer L., Shlien R. Evidence for function of Ia molecules on gut epithelial cells in man. J Exp Med. 1987 Nov 1;166(5):1471–1483. doi: 10.1084/jem.166.5.1471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Norton J., Sloane J. P., al-Saffar N., Haskard D. O. Expression of adhesion molecules in human intestinal graft-versus-host disease. Clin Exp Immunol. 1992 Feb;87(2):231–236. doi: 10.1111/j.1365-2249.1992.tb02980.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Okazaki K., Morita M., Nishimori I., Sano S., Toyonaga M., Nakazawa Y., Yamamoto Y., Yamamoto Y. Major histocompatibility antigen-restricted cytotoxicity in inflammatory bowel disease. Gastroenterology. 1993 Feb;104(2):384–391. doi: 10.1016/0016-5085(93)90405-2. [DOI] [PubMed] [Google Scholar]
  27. Olsberg C., Pelka A., Miller S., Waltenbaugh C., Creighton T. M., Dal Canto M. C., Lipton H., Melvold R. Induction of Theiler's murine encephalomyelitis virus (TMEV)-induced demyelinating disease in genetically resistant mice. Reg Immunol. 1993 Jan-Feb;5(1):1–10. [PubMed] [Google Scholar]
  28. Osborn L., Hession C., Tizard R., Vassallo C., Luhowskyj S., Chi-Rosso G., Lobb R. Direct expression cloning of vascular cell adhesion molecule 1, a cytokine-induced endothelial protein that binds to lymphocytes. Cell. 1989 Dec 22;59(6):1203–1211. doi: 10.1016/0092-8674(89)90775-7. [DOI] [PubMed] [Google Scholar]
  29. Phillips M. L., Nudelman E., Gaeta F. C., Perez M., Singhal A. K., Hakomori S., Paulson J. C. ELAM-1 mediates cell adhesion by recognition of a carbohydrate ligand, sialyl-Lex. Science. 1990 Nov 23;250(4984):1130–1132. doi: 10.1126/science.1701274. [DOI] [PubMed] [Google Scholar]
  30. Pober J. S., Gimbrone M. A., Jr, Lapierre L. A., Mendrick D. L., Fiers W., Rothlein R., Springer T. A. Overlapping patterns of activation of human endothelial cells by interleukin 1, tumor necrosis factor, and immune interferon. J Immunol. 1986 Sep 15;137(6):1893–1896. [PubMed] [Google Scholar]
  31. Roberts A. I., O'Connell S. M., Ebert E. C. Intestinal intraepithelial lymphocytes bind to colon cancer cells by HML-1 and CD11a. Cancer Res. 1993 Apr 1;53(7):1608–1611. [PubMed] [Google Scholar]
  32. Rothlein R., Czajkowski M., O'Neill M. M., Marlin S. D., Mainolfi E., Merluzzi V. J. Induction of intercellular adhesion molecule 1 on primary and continuous cell lines by pro-inflammatory cytokines. Regulation by pharmacologic agents and neutralizing antibodies. J Immunol. 1988 Sep 1;141(5):1665–1669. [PubMed] [Google Scholar]
  33. Salmi M., Jalkanen S. Regulation of lymphocyte traffic to mucosa-associated lymphatic tissues. Gastroenterol Clin North Am. 1991 Sep;20(3):495–510. [PubMed] [Google Scholar]
  34. Sanderson I. R., Ouellette A. J., Carter E. A., Walker W. A., Harmatz P. R. Differential regulation of B7 mRNA in enterocytes and lymphoid cells. Immunology. 1993 Jul;79(3):434–438. [PMC free article] [PubMed] [Google Scholar]
  35. Scheynius A., Engstrand L. Gastric epithelial cells in Helicobacter pylori-associated gastritis express HLA-DR but not ICAM-1. Scand J Immunol. 1991 Feb;33(2):237–241. doi: 10.1111/j.1365-3083.1991.tb03755.x. [DOI] [PubMed] [Google Scholar]
  36. Schwartz R. H. A cell culture model for T lymphocyte clonal anergy. Science. 1990 Jun 15;248(4961):1349–1356. doi: 10.1126/science.2113314. [DOI] [PubMed] [Google Scholar]
  37. Selby W. S., Janossy G., Mason D. Y., Jewell D. P. Expression of HLA-DR antigens by colonic epithelium in inflammatory bowel disease. Clin Exp Immunol. 1983 Sep;53(3):614–618. [PMC free article] [PubMed] [Google Scholar]
  38. Senior P. V., Critchley D. R., Beck F., Walker R. A., Varley J. M. The localization of laminin mRNA and protein in the postimplantation embryo and placenta of the mouse: an in situ hybridization and immunocytochemical study. Development. 1988 Nov;104(3):431–446. doi: 10.1242/dev.104.3.431. [DOI] [PubMed] [Google Scholar]
  39. Shorter R. G., McGill D. B., Bahn R. C. Cytotoxicity of mononuclear cells for autologous colonic epithelial cells in colonic diseases. Gastroenterology. 1984 Jan;86(1):13–22. [PubMed] [Google Scholar]
  40. Simmons D., Makgoba M. W., Seed B. ICAM, an adhesion ligand of LFA-1, is homologous to the neural cell adhesion molecule NCAM. Nature. 1988 Feb 18;331(6157):624–627. doi: 10.1038/331624a0. [DOI] [PubMed] [Google Scholar]
  41. Smart C. J., Calabrese A., Oakes D. J., Howdle P. D., Trejdosiewicz L. K. Expression of the LFA-1 beta 2 integrin (CD11a/CD18) and ICAM-1 (CD54) in normal and coeliac small bowel mucosa. Scand J Immunol. 1991 Sep;34(3):299–305. doi: 10.1111/j.1365-3083.1991.tb01550.x. [DOI] [PubMed] [Google Scholar]
  42. Smith M. E., Thomas J. A. Cellular expression of lymphocyte function associated antigens and the intercellular adhesion molecule-1 in normal tissue. J Clin Pathol. 1990 Nov;43(11):893–900. doi: 10.1136/jcp.43.11.893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Staunton D. E., Dustin M. L., Springer T. A. Functional cloning of ICAM-2, a cell adhesion ligand for LFA-1 homologous to ICAM-1. Nature. 1989 May 4;339(6219):61–64. doi: 10.1038/339061a0. [DOI] [PubMed] [Google Scholar]
  44. Sturgess R. P., Macartney J. C., Makgoba M. W., Hung C. H., Haskard D. O., Ciclitira P. J. Differential upregulation of intercellular adhesion molecule-1 in coeliac disease. Clin Exp Immunol. 1990 Dec;82(3):489–492. doi: 10.1111/j.1365-2249.1990.tb05477.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Watson D. W., Quigley A., Bolt R. J. Effect of lymphocytes from patients with ulcerative colitis on human adult colon epithelial cells. Gastroenterology. 1966 Dec;51(6):985–993. [PubMed] [Google Scholar]

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