Skip to main content
PMC home page
Clinical and Experimental Immunology logoLink to Clinical and Experimental Immunology
. 1989 Dec;78(3):424–430.

Possible role of vascular endothelial cells in immune responses in colonic mucosa examined immunocytochemically in subjects with and without ulcerative colitis.

T Matsumoto 1, A Kitano 1, S Nakamura 1, N Oshitani 1, A Obata 1, M Hiki 1, H Hashimura 1, K Okawa 1, K Kobayashi 1, H Nagura 1
PMCID: PMC1534821  PMID: 2692886

Abstract

Phenotypic characteristics of vascular endothelial cells of the colonic mucosa in patients with ulcerative colitis and healthy controls were studied with immunoperoxidase staining by light and electron microscopy. The cells could be classified into two groups according to their phenotypes; one was positive for von Willebrand factor and the other had an antigen detected by a monoclonal antibody, OKM5. The endothelial cells positive for von Willebrand factor were usually in relatively large blood vessels, and OKM5-positive cells were mostly located in small capillaries along the glandular epithelium. OKM5-positive endothelial cells also expressed HLA-DR and interleukin-1 (IL-1). In patients with ulcerative colitis, OKM5-positive endothelial cells and spindle-shaped cells that might be precursors of endothelial cells were more numerous in the lamina propria than in the other subjects. Thus, OKM5-positive endothelial cells may be important as antigen-presenting cells and immunoregulatory cells in the intramucosal immune system. Furthermore, colonic epithelial cells in patients with ulcerative colitis synthesized HLA-DR and IL-1, and may have a close relation to immune responses, such as antigen processing and presentation to immunocompetent cells. It was suggested that these cells have a close relation to the pathogenesis of the impaired immune responses in situ in ulcerative colitis.

Full text

PDF
424

Images in this article

426Fig. 1
on p.426
427Fig. 2
on p.427
428Fig. 3
on p.428
428Fig. 4
on p.428

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aiso S., Watanabe M., Hibi T., Yoshida T., Tsuchiya M., Tsuru S. Characterization of immunoregulatory T cells and lymphocytophilic antibodies in ulcerative colitis: analysis with monoclonal antibodies. J Clin Lab Immunol. 1982 Nov;9(2):109–112. [PubMed] [Google Scholar]
  2. BROBERGER O., PERLMANN P. Autoantibodies in human ulcerative colitis. J Exp Med. 1959 Nov 1;110:657–674. doi: 10.1084/jem.110.5.657. [DOI] [PMC free article] [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. Buckley P. J., Dickson S. A., Walker W. S. Human splenic sinusoidal lining cells express antigens associated with monocytes, macrophages, endothelial cells, and T lymphocytes. J Immunol. 1985 Apr;134(4):2310–2315. [PubMed] [Google Scholar]
  5. Butcher E. C., Scollay R. G., Weissman I. L. Lymphocyte adherence to high endothelial venules: characterization of a modified in vitro assay, and examination of the binding of syngeneic and allogeneic lymphocyte populations. J Immunol. 1979 Nov;123(5):1996–2003. [PubMed] [Google Scholar]
  6. Challacombe S. J., Tomasi T. B., Jr Systemic tolerance and secretory immunity after oral immunization. J Exp Med. 1980 Dec 1;152(6):1459–1472. doi: 10.1084/jem.152.6.1459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chin Y. H., Carey G. D., Woodruff J. J. Lymphocyte recognition of lymph node high endothelium. IV. Cell surface structures mediating entry into lymph nodes. J Immunol. 1982 Nov;129(5):1911–1915. [PubMed] [Google Scholar]
  8. Das K. M., Dubin R., Nagai T. Isolation and characterization of colonic tissue-bound antibodies from patients with idiopathic ulcerative colitis. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4528–4532. doi: 10.1073/pnas.75.9.4528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Durum S. K., Schmidt J. A., Oppenheim J. J. Interleukin 1: an immunological perspective. Annu Rev Immunol. 1985;3:263–287. doi: 10.1146/annurev.iy.03.040185.001403. [DOI] [PubMed] [Google Scholar]
  10. Elson C. O., Heck J. A., Strober W. T-cell regulation of murine IgA synthesis. J Exp Med. 1979 Mar 1;149(3):632–643. doi: 10.1084/jem.149.3.632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Freemont A. J., Jones C. J. Light microscopic, histochemical and ultrastructural studies of human lymph node paracortical venules. J Anat. 1983 Mar;136(Pt 2):349–362. [PMC free article] [PubMed] [Google Scholar]
  12. Green N., Hiai H., Elder J. H., Schwartz R. S., Khiroya R. H., Thomas C. Y., Tsichlis P. N., Coffin J. M. Expression of leukemogenic recombinant viruses associated with a recessive gene in HRS/J mice. J Exp Med. 1980 Aug 1;152(2):249–264. doi: 10.1084/jem.152.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hirata I., Austin L. L., Blackwell W. H., Weber J. R., Dobbins W. O., 3rd Immunoelectron microscopic localization of HLA-DR antigen in control small intestine and colon and in inflammatory bowel disease. Dig Dis Sci. 1986 Dec;31(12):1317–1330. doi: 10.1007/BF01299810. [DOI] [PubMed] [Google Scholar]
  14. Hirschberg H., Evensen S. A., Henriksen T., Thorsby E. The human mixed lymphocyte-endothelium culture interaction. Transplantation. 1975 Jun;19(6):495–504. doi: 10.1097/00007890-197506000-00008. [DOI] [PubMed] [Google Scholar]
  15. Iizuka M., Chiba M., Ohta H., Kodama K., Igarashi K., Arakawa H., Masamune O. Expression of HLA-DR antigens on colonic epithelium in ulcerative colitis. Gastroenterol Jpn. 1987 Oct;22(5):571–577. doi: 10.1007/BF02776716. [DOI] [PubMed] [Google Scholar]
  16. Jalkanen S., Bargatze R. F., de los Toyos J., Butcher E. C. Lymphocyte recognition of high endothelium: antibodies to distinct epitopes of an 85-95-kD glycoprotein antigen differentially inhibit lymphocyte binding to lymph node, mucosal, or synovial endothelial cells. J Cell Biol. 1987 Aug;105(2):983–990. doi: 10.1083/jcb.105.2.983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jalkanen S., Steere A. C., Fox R. I., Butcher E. C. A distinct endothelial cell recognition system that controls lymphocyte traffic into inflamed synovium. Science. 1986 Aug 1;233(4763):556–558. doi: 10.1126/science.3726548. [DOI] [PubMed] [Google Scholar]
  18. Jeurissen S. H., Duijvestijn A. M., Sontag Y., Kraal G. Lymphocyte migration into the lamina propria of the gut is mediated by specialized HEV-like blood vessels. Immunology. 1987 Oct;62(2):273–277. [PMC free article] [PubMed] [Google Scholar]
  19. Knowles D. M., 2nd, Tolidjian B., Marboe C., D'Agati V., Grimes M., Chess L. Monoclonal anti-human monocyte antibodies OKM1 and OKM5 possess distinctive tissue distributions including differential reactivity with vascular endothelium. J Immunol. 1984 May;132(5):2170–2173. [PubMed] [Google Scholar]
  20. MATTS S. G. The value of rectal biopsy in the diagnosis of ulcerative colitis. Q J Med. 1961 Oct;30:393–407. [PubMed] [Google Scholar]
  21. Matsumoto T., Kitano A., Oshitani N., Obata A., Hiki M., Hashimura H., Okawa K., Nagura H., Kobayashi K. Immunoglobulin-containing cells in the colonic mucosa of rabbits with carrageenan-induced colitis. Dis Colon Rectum. 1988 Sep;31(9):723–729. doi: 10.1007/BF02552594. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Nagura H., Brandtzaeg P., Nakane P. K., Brown W. R. Ultrastructural localization of J chain in human intestinal mucosa. J Immunol. 1979 Sep;123(3):1044–1050. [PubMed] [Google Scholar]
  24. Nagura H., Koshikawa T., Fukuda Y., Asai J. Hepatic vascular endothelial cells heterogenously express surface antigens associated with monocytes, macrophages and T lymphocytes. Virchows Arch A Pathol Anat Histopathol. 1986;409(4):407–416. doi: 10.1007/BF00705413. [DOI] [PubMed] [Google Scholar]
  25. Nagura H., Nakane P. K., Brown W. R. Breast milk IgA binds to jejunal epithelium in suckling rats. J Immunol. 1978 Apr;120(4):1333–1339. [PubMed] [Google Scholar]
  26. Nagura H., Nakane P. K., Brown W. R. Translocation of dimeric IgA through neoplastic colon cells in vitro. J Immunol. 1979 Nov;123(5):2359–2368. [PubMed] [Google Scholar]
  27. Nunez G., Ball E. J., Stastny P. Accessory cell function of human endothelial cells. I. A subpopulation of Ia positive cells is required for antigen presentation. J Immunol. 1983 Aug;131(2):666–673. [PubMed] [Google Scholar]
  28. Roche J. K., Fiocchi C., Youngman K. Sensitization to epithelial antigens in chronic mucosal inflammatory disease. Characterization of human intestinal mucosa-derived mononuclear cells reactive with purified epithelial cell-associated components in vitro. J Clin Invest. 1985 Feb;75(2):522–530. doi: 10.1172/JCI111728. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rosekrans P. C., Meijer C. J., van der Wal A. M., Cornelisse C. J., Lindeman J. Immunoglobulin containing cells in inflammatory bowel disease of the colon: a morphometric and immunohistochemical study. Gut. 1980 Nov;21(11):941–947. doi: 10.1136/gut.21.11.941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Shen H. H., Talle M. A., Goldstein G., Chess L. Functional subsets of human monocytes defined by monoclonal antibodies: a distinct subset of monocytes contains the cells capable of inducing the autologous mixed lymphocyte culture. J Immunol. 1983 Feb;130(2):698–705. [PubMed] [Google Scholar]
  32. Shioda Y., Nagura H., Tsutsumi Y., Shimamura K., Tamaoki N. Distribution of Leu 7 (HNK-1) antigen in human digestive organs: an immunohistochemical study with monoclonal antibody. Histochem J. 1984 Aug;16(8):843–854. doi: 10.1007/BF01002790. [DOI] [PubMed] [Google Scholar]
  33. Stamper H. B., Jr, Woodruff J. J. Lymphocyte homing into lymph nodes: in vitro demonstration of the selective affinity of recirculating lymphocytes for high-endothelial venules. J Exp Med. 1976 Sep 1;144(3):828–833. doi: 10.1084/jem.144.3.828. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Streefkerk J. G. Inhibition of erythrocyte pseudoperoxidase activity by treatment with hydrogen peroxide following methanol. J Histochem Cytochem. 1972 Oct;20(10):829–831. doi: 10.1177/20.10.829. [DOI] [PubMed] [Google Scholar]
  35. Takahashi F., Das K. M. Isolation and characterization of a colonic autoantigen specifically recognized by colon tissue-bound immunoglobulin G from idiopathic ulcerative colitis. J Clin Invest. 1985 Jul;76(1):311–318. doi: 10.1172/JCI111963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Yamamoto M., Shimokata K., Nagura H. An immunohistochemical study on phenotypic heterogeneity of human pulmonary vascular endothelial cells. Virchows Arch A Pathol Anat Histopathol. 1988;412(5):479–486. doi: 10.1007/BF00750582. [DOI] [PubMed] [Google Scholar]

Articles from Clinical and Experimental Immunology are provided here courtesy of British Society for Immunology

RESOURCES