Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T cells in celiac disease

Nature Medicine

Volumn 4, Issue 6, 1998, Pages 713-717

  Molberg, Øyvind ^a   Mcadam, Stephen N ^a   Körner, Roman ^b   Quarsten, Hanne ^a   Kristiansen, Christel ^a   Madsen, Lars ^c   Fugger, Lars ^c,d   Scott, Helge ^a   Norën, Ove ^d   Roepstorff, Peter ^b   Lundin, Knut E A ^a,e   Sjöström, Hans ^d   Sollid, Ludvig M ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c AARHUS UNIVERSITY HOSPITAL   (Denmark)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e ULLEVÅL UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

GLIADIN; HLA DQ ANTIGEN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

AMINO ACID SEQUENCE; ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; CELIAC DISEASE; CONTROLLED STUDY; DEAMINATION; HUMAN; HUMAN TISSUE; PRIORITY JOURNAL; T LYMPHOCYTE;

AMINO ACID SEQUENCE; BINDING SITES; CELIAC DISEASE; CELLS, CULTURED; CHROMATOGRAPHY, ION EXCHANGE; COAGULANTS; EPITOPES; GLIADIN; HLA-DQ ANTIGENS; HUMANS; INTESTINES; MOLECULAR SEQUENCE DATA; OLIGOPEPTIDES; PROTEIN BINDING; SEQUENCE HOMOLOGY, AMINO ACID; T-LYMPHOCYTES; TRANSGLUTAMINASES;

TRITICUM AESTIVUM;

EID: 0031779478     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/nm0698-713     Document Type: Article

References (33)

1. Folk, J. E. Mechanism and basis for specificity of transglutaminase-catalyzed ε-(γ-glutamyl) lysine bond formation. Adv. Enzymol. Relat. Areas Mol. Biol. 54, 1-56 (1983).
2. Kahlem, P., Terre, C., Green, H. & Djian, P. Peptides containing glutamine repeats as substrates for transglutaminase-catalyzed cross-linking: relevance to diseases of the nervous system Proc. Natl. Acad. Sci. USA 93, 14580-14585 (1996).
3. Aeschlimann, D. & Paulsson, M. Transglutaminases: protein cross-linking enzymes in tissues and body fluids. Thromb. Haemost. 71, 402-415 (1994).
4. Davies, P. J. et al. Transglutaminase is essential in receptor-mediated endocytosis of α2-macroglobulin and polypeptide hormones. Nature 283, 162-167 (1980).
5. Teshigawara, K., Kannagi, R., Noro, N. & Masuda, T. Possible involvement of transglutaminase in endocytosis and antigen presentation. Microbiol. Immunol. 29, 737-750 (1985).
6. Sollid, L. M. & Thorsby, E. HLA susceptibility genes in celiac disease: genetic mapping and role in pathogenesis. Gastroenterology 105, 910-922 (1993).
7. Trier, J. S. Celiac sprue. N. Engl. J. Med. 325, 1709-1719 (1991).
8. Bruce, S. E., Bjarnason, I. & Peters, T.J. Human jejunal transglutaminase: demonstration of activity, enzyme kinetics and substrate specificity with special relation to gliadin and coeliac disease. Clin. Sci. (Colch.) 68, 573-579 (1985).
9. Dieterich, W. et al. Identification of tissue transglutaminase as the autoantigen of celiac disease. Nature Med. 3, 797-801 (7-1997).
10. Larre, C. et al. Gliadin modifications catalysed by guinea pig liver transglutaminase. J. Food. Biochem 267-282 (1993).
11. Lundin, K. E.A. et al. Gliadin-specific, HLA-DQ(α1*0501,β1*0201) restricted T cells isolated from the small intestinal mucosa of celiac disease patients. J. Exp. Med. 178, 187-196 (1993).
12. MacDonald, T. T. In Coeliac Disease (ed. Marsh, M. N.) 283-304 (Blackwell Scientific, Oxford, 1992).
13. Frazer, A. C. Gluten-induced enteropathy, the effect of partially digested gluten. Lancet 252-255 (1959).
14. Wieser, H. In Coeliac disease (ed. Howdle, P. D.) 191-208 (Bailliere Tindall, London, 1995).
15. Watts, C. Capture and processing of exogenous antigens for presentation on MHC molecules. Ann. Rev. Immunol. 15, 821-850 (1997).
16. Gjertsen, H. A. et al. T cells from the peripheral blood of coeliac disease patients recognize gluten antigens when presented by HLA-DR, -DQ, or -DP molecules. Scand. J. Immunol. 39, 567-574 (1994).
17. Hamada, J. S. Deamidation of food proteins to improve functionality. Crit. Rev. Food Sci. Nutr. 34, 283-292 (1994).
18. Johansen, B. H. et al. Identification of a putative motif for binding of peptides to HLA-DQ2. Int. Immunol. 8, 177-182 (1996).
19. van de Wal, Y. et al. Peptide binding characteristics of the coeliac disease-associated DQ(α1*0501, β1*0201) molecule. Immunogenetics 44, 246-253 (1996).
20. Halstensen, T. S. et al. In situ two- and three-color immunofluorescence staining of mucosal T-cells in celiac disease. Increase of TCR γ/δ+CD8- and TCR α/β+CD45RO+ intraepithelial lymphocytes and IL2R+ TCR α/β+CD4+CD45RO+lamina propria lymphocytes. Prog. Histochem. Cytochem. 26, 201-210 (1992).
21. Sollid, L. M., Molberg, O., McAdam, S. & Lundin, K.E.A. Autoantibodies in coeliac disease,. Tissue transglutaminase - guilty by association. Gut 41, 851-852 (1997).
22. Kwok, W. W. et al. HLA-DQB1 codon 57 is critical for peptide binding and recognition. J. Exp. Med. 183, 1253-1258 (1996).
23. Meadows, L. et al. The HLA-A*0201-restricted H-Y antigen contains a posttranslationally modified cysteine that significantly affects T cell recognition. Immunity 6, 273-281 (1997).
24. Skipper, J. C. et al. An HLA-A2-restricted tyrosinase antigen on melanoma cells results from posttranslational modification and suggests a novel pathway for processing of membrane proteins. J. Exp. Med. 183, 527-534 (1996).
25. Michaelsson, E. et al. T cell recognition of carbohydrates on type II collagen. J. Exp. Med. 180, 745-749 (1994).
26. Molberg, Ø. et al. CD4+ T cells with specific reactivity against astrovirus isolated from normal human small intestine. Gastroenterology 114, 115-122 (1998).
27. Lundin, K. E. A. et al. T cells from the small intestinal mucosa of a DR4, DQ7/DR4, DQ8 celiac disease patient preferentially recognize gliadin when presented by DQ8. Hum. Immunol. 41, 285-291 (1994).
28. Kouskoff, V., Signorelli, K., Benoist, C. & Mathis, D. Cassette vectors directing expression of T cell receptor genes in transgenic mice. J. Immunol. Methods 180, 273-280 (1995).
29. Letourneur, F. & Malissen, B. Derivation of a T cell hybridoma variant deprived of functional T cell receptor α/β chain transcripts reveals a nonfunctional alpha-mRNA of BW5147 origin. Eur. J. Immunol. 19, 2269-2274 (1989).
30. Hunt, D. F. et al. Protein sequencing by tandem mass spectrometry. Proc. Natl. Acad. Sci. USA 83, 6233-6237 (1986).
31. Karas, M. & Hillenkamp, F. Laser desorption ionization of proteins with molecular masses exceeding 10,000 daltons. Anal. Chem. 60, 2299-2301 (1988).
32. Fenn, J. B. et al. Electrospray ionization for mass spectrometry of large biomolecules. Science 246, 64-71 (1989).
33. Cooks, G. L., Glish, G.L., McLuskey, S.A. & Kaiser, R.E. Ion trap mass spectrometry. Chem. Eng. News 25, 26-41 (1991).