Highly polarized HLA class II antigen processing and presentation by human intestinal epithelial cells

Journal of Clinical Investigation

Volumn 102, Issue 4, 1998, Pages 792-803

  Hershberg, Robert M ^a,b   Cho, Diane H ^a   Youakim, Adel ^c   Bradley, M Brigid ^d   Lee, Janet S ^d   Framson, Paul E ^a   Nepom, Gerald T ^a,b  

^a BENAROYA RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c AMGEN INC   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Cell polarity; HLA class II; Inflammatory bowel disease; Intestinal epithelium; Oral tolerance

Indexed keywords

HLA ANTIGEN CLASS 2;

ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; CONTROLLED STUDY; ENTERITIS; HLA SYSTEM; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; INTESTINE EPITHELIUM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING;

EID: 0032528838     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI3201     Document Type: Article

References (45)

1. Jung, H.C., L. Eckmann, S.-K. Yang, A. Panja, J. Fierer, E. Morzycka-Wroblewska, and M.F. Kagnoff. 1995. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J. Clin. Invest. 95:55-65.
2. Cepek, K.L., S.K. Shaw, C.M. Parker, G.J. Russell, J.S. Morrow, D.L. Rimm, and M.B. Brenner. 1994. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature. 372: 190-193.
3. + cells mediate active suppression. J. Immunol. 155:910-916.
4. + T cells are required for the induction of oral tolerance. Int. Immunol. 7: 501-504.
5. + cells on the induction and maintenance of oral tolerance. Cell. Immunol. 163:19-29.
6. Powrie, F. 1995. T cells in inflammatory bowel disease: protective and pathogenic roles. Immunity. 3:171-174.
7. Germain, R.N. 1994. MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell. 76:287-299.
8. Mayer, L., D. Eisenhardt, P. Salomon, W. Bauer, R. Plous, and L. Piccinini. 1991. Expression of class II molecules on intestinal epithelial cells in humans. Differences between normal and inflammatory bowel disease. Gastroenterology. 100:3-12.
9. Bland, P.W., and C.V. Whiting. 1992. Induction of MHC class II gene products in rat intestinal epithelium during graft-versus-host disease and effects on the immune function of the epithelium. Immunology. 75:366-371.
10. Ciclitira, P.J., J.M. Nelufer, H.J. Ellis, and D.J. Evans. 1986. The effect of gluten on HLA-DR in the small intestinal epithelium of patients with Coeliac disease. Clin. Exp. Immunol. 63:101-104.
11. Wolf, P.R., and H.L. Ploegh. 1995. How MHC class II molecules acquire peptide cargo: biosynthesis and trafficking through the endocytic pathway. Annu. Rev. Cell Dev. Biol. 11:267-306.
12. Cresswell, P. 1994. Assembly, transport, and function of MHC class II molecules. Annu. Rev. Immunol. 12:259-293.
13. + T cells. Eur. J. Immunol. 19:1513-1516.
14. Hershberg, R.M., P.E. Framson, D.H. Cho, L.Y. Lee, S. Kovats, J. Beitz, J.S. Blum, and G.T. Nepom. 1997. Intestinal epithelial cells utilize two distinct pathways for HLA class II antigen processing. J. Clin. Invest. 100:204-215.
15. Hirata, I., L.L. Austin, W.H. Blackwell, J.R. Weber, and W.O. Dobbins, III. 1986. Immunoelectron microscopic localization of HLA-DR antigen in control small intestine and colon and in inflammatory bowel disease. Dig. Dis. Sci. 31:1317-1330.
16. Sarles, J., J.P. Gorvel, D. Olive, S. Maroux, C. Mawas, and F. Giraud. 1987. Subcellular localization of class I (A,B,C) and class II (DR and DQ) MHC antigens in jejunal epithelium of children with coelic disease. J. Pediatr. Gastroenterol. Nutr. 6:51-56.
17. Mayrhofer, G., and L.D. Spargo. 1990. Distribution of class II major histocompatibility antigens in enterocytes of the rat jejunum and their association with organelles of the endocytic pathway. Immunology. 70:11-19.
18. Madara, J.L., and J. Stafford. 1989. Interferon-γ directly affects barrier function of cultured intestinal epithelial monolayers. J. Clin. Invest. 83:724-727.
19. Bradley, M.B., J.M. Fernandez, G. Ungers, T. Diaz-Barrientos, V. Steimle, B. Mach, R. O'Reilly, and J.S. Lee. 1997. Correction of defective expression in MHC class II deficiency (bare lymphocyte syndrome) cells by retroviral transduction of CIITA. J. Immunol. 159:1086-1095.
20. Hughson, E.J., and R.P. Hirt. 1996. Assessment of cell polarity. In Epithelial Cell Culture. A.J. Shaw, editor. IRL Press, Oxford, UK. 37-66.
21. Planchon, S.M., C.A. Martins, R.L. Guerrant, and J.K. Roche. 1994. Regulation of intestinal epithelial barrier function by TGF-β 1. Evidence for its role in abrogating the effect of a T cell cytokine. J. Immunol. 153:5730-5739.
22. Woods, A., H.Y. Chen, M.E. Trumbauer, A. Sirotina, R. Cummings, and D.M. Zaller. 1994. Human major histocompatibility complex class II-restricted T cell responses in transgenic mice. J. Exp. Med. 180:173-181.
23. Genevée, C., A. Diu, J. Nierat, A. Caignard, P.-Y. Dietrich, L. Ferradini, S. Roman-Roman, F. Triebel, and T. Hercend. 1992. An experimentally validated panel of subfamily-specific oligonucleotide primers (Val-w29/Vb1-w24) for the study of human T cell receptor variable V gene segment usage by polymerase chain reaction. Eur. J. Immunol. 22:1261-1269.
24. Colgan, S.P., C.A. Parkos, J.B. Matthews, L. D'Andrea, C.S. Awtrey, A.H. Lichtman, C. Delp-Archer, and J.L. Madara. 1994. Interferon-γ induces a cell surface phenotype switch on T84 intestinal epithelial cells. Am. J. Physiol. 36:C402-C410.
25. Gottardi, C.J., L.A. Dunbar, and M.J. Caplan. 1995. Biotinylation and assessment of membrane polarity: caveats and methodological concerns. Am. J. Physiol. 268:F285-F295.
26. Strohmeier, G.R., W.I. Lencer, T.W. Patapoff, L.F. Thompson, S.L. Carlson, S.J. Moe, D.K. Carnes, R.J. Mrsny, and J.L. Madara. 1997. Surface expression, polarization, and functional significance of CD73 in human intestinal epithelia. J. Clin. Invest. 99:2588-2601.
27. Chang, C.-H., and R.A. Flavell. 1995. Class II transactivator regulates the expression of multiple genes involved in antigen presentation. J. Exp. Med. 181:765-767.
28. Gottlieb, T.A., I.E. Ivanov, M. Adesnik, and D.D. Sabatini. 1993. Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J. Cell Biol. 120:695-710.
29. Jackman, M.R., W. Shurety, J.A. Ellis, and J.P. Luzio. 1994. Inhibition of apical but not basolateral endocytosis of ricin and folate in Caco-2 cells by cytochalasin D. J. Cell Sci. 107:2547-2556.
30. Lencer, W.I., G. Strohmeier, S. Moe, S.L. Carlson, C.T. Constable, and J.L. Madara. 1995. Signal transduction by cholera toxin: processing in vesicular compartments does not require acidification. Am. J. Physiol. 269:G548-G557.
31. Pociot, F., A.G. Wilson, J. Nerup, and G.W. Duff. 1993. No independent association between a tumor necrosis factor-α promoter region polymorphism and insulin-dependent diabetes mellitus. Eur. J. Immunol. 23:3050-3053.
32. Simonsen, A., E. Stang, B. Bremnes, M. Roe, K. Prydz, and O. Bakke. 1997. Sorting of MHC class II molecules and the associated invariant chain (li) in polarized MDCK cells. J. Cell Sci. 110:597-609.
33. Odorizzi, G., and I.S. Trowbridge. 1997. Structural requirements for major histocompatibility complex class II invariant chain trafficking in polarized Madin-Darby canine kidney cells. J. Biol. Chem. 272:11757-11762.
34. Zhong, G., P. Romagnoli, and R.N. Germain. 1997. Related leucine-based cytoplasmic targeting signals in invariant chain and major histocompatibility complex class II molecules control endocytic presentation of distinct determinants in a single protein. J. Exp. Med. 185:429-438.
35. Pinet, V., M. Vergelli, R. Martin, O. Bakke, and E.O. Long. 1995. Antigen presentation mediated by recycling of surface HLA-DR molecules. Nature. 375:603-604.
36. Hunziker, W., and C. Fumey. 1994. A di-leucine motif mediates endocytosis and basolateral sorting of macrophage IgG Fc receptors in MDCK cells. EMBO (Eur. Mol. Biol. Organ.) J. 13:2963-2969.
37. Mellman, I. 1995. Molecular sorting of membrane proteins in polarized and nonpolarized cells. Cold Spring Harbor Symp. Quant. Biol. LX:745-752.
38. Siegrist, C.A., E. Martinez-Soria, I. Kern, and B. Mach. 1995. A novel antigen-processing-defective phenotype in major histocompatibility complex class !!-positive CIITA transfectants is corrected by interferon-γ. J. Exp. Med. 182:1793-1799.
39. Knight, A., E. Hughson, C.R. Hopkins, and D.F. Cutler. 1995. Membrane protein trafficking through the common apical endosome compartment of polarized caco-2 cells. Mol. Biol. Cell. 6:597-610.
40. Odorizzi, G., A. Pearse, D. Domingo, I.S. Trowbridge, and C.R. Hopkins. 1996. Apical and basolateral endosomes of MDCK cells are interconnected and contain a polarized sorting mechanism. J. Cell Biol. 135:139-152.
41. Momburg, F., S. Fuchs, J. Drexler, R. Busch, M. Post, G.J. Hammerling, and L. Adorini. 1993. Epitope-specific enhancement of antigen presentation by invariant chain. J. Exp. Med. 178:1453-1458.
42. Pinet, V., M.S. Malnati, and E.O. Long. 1994. Two processing pathways for the MHC class II-restricted presentation of exogenous influenza virus antigen. J. Immunol. 152:4852-4860.
43. Ceman, S., and A.J. Sant. 1995. The function of invariant chain in class II-restricted antigen presentation. Semin. Immunol. 7:373-387.
44. Zhang, Z., and J.G. Michael. 1990. Orally inducible immune unresponsiveness is abrogated by IFN-γ treatment. J. Immunol. 144:4163-4165.
45. Kjerrulf, M., D. Grdic, L. Ekman, K. Schon, M. Vajdy, and N.Y. Lycke. 1997. Interferon-γ receptor-deficient mice exhibit impaired gut mucosal immune responses but intact oral tolerance. Immunology. 92:60-68.