Skip to main content
NCBI home page
Immunology logoLink to Immunology
. 1990 May;70(1):11–19.

Distribution of class II major histocompatibility antigens in enterocytes of the rat jejunum and their association with organelles of the endocytic pathway.

G Mayrhofer 1, L D Spargo 1
PMCID: PMC1384075  PMID: 2354854

Abstract

The subcellular distribution of class II major histocompatibility molecules has been investigated in enterocytes in the rat jejunum. Studies have been carried out at both light microscope and ultrastructural levels using an indirect immunoperoxidase technique and monoclonal antisera against rat class II molecules. The results show that the class II molecules have also been demonstrated on the baso-lateral cell membranes of enterocytes, but are absent from the brush borders. The distribution of class II molecules has also been studied during enterocyte maturation. The results suggest that enterocytes might be capable of intracellular processing of antigens and suggest that the encounter between class II molecules and processed antigens within the endocytic pathways of cells may be a general phenomenon in both 'professional' and 'non-professional' antigen-presenting cells.

Full text

PDF
11

Images in this article

13Figure 1
on p.13
15Figure 2
on p.15
16Figure 3
on p.16
17Figure 4
on p.17

Selected References

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

  1. Arnaud-Battandier F., Cerf-Bensussan N., Amsellem R., Schmitz J. Increased HLA-DR expression by enterocytes in children with celiac disease. Gastroenterology. 1986 Nov;91(5):1206–1212. doi: 10.1016/s0016-5085(86)80018-x. [DOI] [PubMed] [Google Scholar]
  2. BARKA T. ELECTRON HISTOCHEMICAL LOCALIZATION OF ACID PHOSPHATASE ACTIVITY IN THE SMALL INTESTINE OF MOUSE. J Histochem Cytochem. 1964 Apr;12:229–238. doi: 10.1177/12.4.229. [DOI] [PubMed] [Google Scholar]
  3. Brown M. S., Anderson R. G., Goldstein J. L. Recycling receptors: the round-trip itinerary of migrant membrane proteins. Cell. 1983 Mar;32(3):663–667. doi: 10.1016/0092-8674(83)90052-1. [DOI] [PubMed] [Google Scholar]
  4. Cornell R., Walker W. A., Isselbacher K. J. Small intestinal absorption of horseradish peroxidase. A cytochemical study. Lab Invest. 1971 Jul;25(1):42–48. [PubMed] [Google Scholar]
  5. Cresswell P. Intracellular class II HLA antigens are accessible to transferrin-neuraminidase conjugates internalized by receptor-mediated endocytosis. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8188–8192. doi: 10.1073/pnas.82.23.8188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Friend D. S., Farquhar M. G. Functions of coated vesicles during protein absorption in the rat vas deferens. J Cell Biol. 1967 Nov;35(2):357–376. doi: 10.1083/jcb.35.2.357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gorvel J. P., Sarles J., Maroux S., Olive D., Mawas C. Cellular localization of class I (HLA-A, B, C) and class II (HLA-DR and DQ) MHC antigens on the epithelial cells of normal human jejunum. Biol Cell. 1984;52(3):249–252. doi: 10.1111/j.1768-322x.1985.tb00343.x. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Hart D. N., Fabre J. W. Endogenously produced Ia antigens within cells of convoluted tubules of rat kidney. J Immunol. 1981 Jun;126(6):2109–2113. [PubMed] [Google Scholar]
  10. Hermanns W., Colbatzky F., Günther A., Steiniger B. Ia antigens in plastic-embedded tissues: a post-embedding immunohistochemical study. J Histochem Cytochem. 1986 Jun;34(6):827–831. doi: 10.1177/34.6.3517152. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Hugon J. S., Borgers M. Absorption of horseradish peroxidase by the mucosal cells of the duodenum of mouse. I. The fasting animal. J Histochem Cytochem. 1968 Apr;16(4):229–236. doi: 10.1177/16.4.229. [DOI] [PubMed] [Google Scholar]
  13. Klareskog L., Forsum U., Peterson P. A. Hormonal regulation of the expression of Ia antigens on mammary gland epithelium. Eur J Immunol. 1980 Dec;10(12):958–963. doi: 10.1002/eji.1830101212. [DOI] [PubMed] [Google Scholar]
  14. Londei M., Lamb J. R., Bottazzo G. F., Feldmann M. Epithelial cells expressing aberrant MHC class II determinants can present antigen to cloned human T cells. Nature. 1984 Dec 13;312(5995):639–641. doi: 10.1038/312639a0. [DOI] [PubMed] [Google Scholar]
  15. Machamer C. E., Cresswell P. Monensin prevents terminal glycosylation of the N- and O-linked oligosaccharides of the HLA-DR-associated invariant chain and inhibits its dissociation from the alpha-beta chain complex. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1287–1291. doi: 10.1073/pnas.81.5.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Mayrhofer G., Pugh C. W., Barclay A. N. The distribution, ontogeny and origin in the rat of Ia-positive cells with dendritic morphology and of Ia antigen in epithelia, with special reference to the intestine. Eur J Immunol. 1983 Feb;13(2):112–122. doi: 10.1002/eji.1830130206. [DOI] [PubMed] [Google Scholar]
  18. Mayrhofer G., Schon-Hegrad M. A. Ia antigens in rat kidney, with special reference to their expression in tubular epithelium. J Exp Med. 1983 Jun 1;157(6):2097–2109. doi: 10.1084/jem.157.6.2097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mayrhofer G., Spargo L. D. Subcellular distribution of class II major histocompatibility antigens in enterocytes of the human and rat small intestine. Immunol Cell Biol. 1989 Aug;67(Pt 4):251–260. doi: 10.1038/icb.1989.38. [DOI] [PubMed] [Google Scholar]
  20. McMaster W. R., Williams A. F. Identification of Ia glycoproteins in rat thymus and purification from rat spleen. Eur J Immunol. 1979 Jun;9(6):426–433. doi: 10.1002/eji.1830090603. [DOI] [PubMed] [Google Scholar]
  21. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rodman J. S., Seidman L., Farquhar M. G. The membrane composition of coated pits, microvilli, endosomes, and lysosomes is distinctive in the rat kidney proximal tubule cell. J Cell Biol. 1986 Jan;102(1):77–87. doi: 10.1083/jcb.102.1.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. STRAUS W. CYTOCHEMICAL OBSERVATIONS ON THE RELATIONSHIP BETWEEN LYSOSOMES AND PHAGOSOMES IN KIDNEY AND LIVER BY COMBINED STAINING FOR ACID PHOSPHATASE AND INTRAVENOUSLY INJECTED HORSERADISH PEROXIDASE. J Cell Biol. 1964 Mar;20:497–507. doi: 10.1083/jcb.20.3.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Schwartz R. H. T-lymphocyte recognition of antigen in association with gene products of the major histocompatibility complex. Annu Rev Immunol. 1985;3:237–261. doi: 10.1146/annurev.iy.03.040185.001321. [DOI] [PubMed] [Google Scholar]
  25. Scott H., Solheim B. G., Brandtzaeg P., Thorsby E. HLA-DR-like antigens in the epithelium of the human small intestine. Scand J Immunol. 1980;12(1):77–82. doi: 10.1111/j.1365-3083.1980.tb00043.x. [DOI] [PubMed] [Google Scholar]
  26. Steinman R. M., Mellman I. S., Muller W. A., Cohn Z. A. Endocytosis and the recycling of plasma membrane. J Cell Biol. 1983 Jan;96(1):1–27. doi: 10.1083/jcb.96.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Unanue E. R. Antigen-presenting function of the macrophage. Annu Rev Immunol. 1984;2:395–428. doi: 10.1146/annurev.iy.02.040184.002143. [DOI] [PubMed] [Google Scholar]
  28. Walker W. A., Cornell R., Davenport L. M., Isselbacher K. J. Macromolecular absorption. Mechanism of horseradish peroxidase uptake and transport in adult and neonatal rat intestine. J Cell Biol. 1972 Aug;54(2):195–205. doi: 10.1083/jcb.54.2.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Werdelin O. Determinant protection. A hypothesis for the activity of immune response genes in the processing and presentation of antigens by macrophages. Scand J Immunol. 1986 Dec;24(6):625–636. doi: 10.1111/j.1365-3083.1986.tb02181.x. [DOI] [PubMed] [Google Scholar]
  30. Wiman K., Curman B., Forsum U., Klareskog L., Malmnäs-Tjernlund U., Rask L., Trägårdh L., Peterson P. A. Occurrence of Ia antigens on tissues on non-lymphoid origin. Nature. 1978 Dec 14;276(5689):711–713. doi: 10.1038/276711a0. [DOI] [PubMed] [Google Scholar]

Articles from Immunology are provided here courtesy of British Society for Immunology

RESOURCES