Protease-resistant human GAD-derived altered peptide ligands decrease TNF-α and IL-17 production in peripheral blood cells from patients with type 1 diabetes mellitus

Molecular Immunology

Volumn 46, Issue 13, 2009, Pages 2576-2584

  Boehm, Bernhard O ^a   Rosinger, Silke ^a   Sauer, Guido ^b   Manfras, Burkhard J ^a   Palesch, David ^a   Schiekofer, Stefan ^a   Kalbacher, Hubert ^c   Burster, Timo ^a  

^a UNIVERSITY HOSPITAL ULM   (Germany)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Altered peptide ligands; Antigen presentation processing; Cathepsin; Diabetes; GAD65

Indexed keywords

CATHEPSIN; GLUTAMATE DECARBOXYLASE 65; HLA DR ANTIGEN; INTERLEUKIN 17; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN PRESENTATION; ARTICLE; BINDING AFFINITY; CELL CLONING; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HUMAN; HUMAN CELL; INSULIN DEPENDENT DIABETES MELLITUS; LYSOSOME; PERIPHERAL LYMPHOCYTE; PLASMA HALF LIFE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN BLOOD LEVEL; PROTEIN CLEAVAGE; PROTEIN MODIFICATION; PROTEIN TARGETING; T LYMPHOCYTE; TH17 CELL;

CATHEPSINS; CELL LINE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DIABETES MELLITUS, TYPE 1; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLUTAMATE DECARBOXYLASE; HUMANS; INTERLEUKIN-2; INTERLEUKIN-6; INTERLEUKIN-7; LEUKOCYTES, MONONUCLEAR; MASS SPECTROMETRY; PEPTIDE FRAGMENTS; PEPTIDE HYDROLASES; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 67650441499     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2009.05.007     Document Type: Article

References (43)

1. Adorini L., Muller S., Cardinaux F., Lehmann P.V., Falcioni F., and Nagy Z.A. In vivo competition between self peptides and foreign antigens in T-cell activation. Nature 334 (1988) 623-625
2. Baekkeskov S., Aanstoot H.J., Christgau S., Reetz A., Solimena M., Cascalho M., Folli F., Richter-Olesen H., and De Camilli P. Identification of the 64K autoantigen in insulin-dependent diabetes as the GABA-synthesizing enzyme glutamic acid decarboxylase. Nature 347 (1990) 151-156
3. Balasa B., Boehm B.O., Fortnagel A., Karges W., Van Gunst K., Jung N., Camacho S.A., Webb S.R., and Sarvetnick N. Vaccination with glutamic acid decarboxylase plasmid DNA protects mice from spontaneous autoimmune diabetes and B7/CD28 costimulation circumvents that protection. Clin Immunol 99 (2001) 241-252
4. Bettelli E., Korn T., Oukka M., and Kuchroo V.K. Induction and effector functions of T(H)17 cells. Nature 453 (2008) 1051-1057
5. Bielekova B., Goodwin B., Richert N., Cortese I., Kondo T., Afshar G., Gran B., Eaton J., Antel J., Frank J.A., McFarland H.F., and Martin R. Encephalitogenic potential of the myelin basic protein peptide (amino acids 83-99) in multiple sclerosis: results of a phase II clinical trial with an altered peptide ligand. Nat Med 6 (2000) 1167-1175
6. Boehm B.O., and Bluestone J.A. Differential roles of costimulatory signaling pathways in type 1 diabetes mellitus. Rev Diabet Stud 1 (2004) 156-164
7. Bolin D.R., Swain A.L., Sarabu R., Berthel S.J., Gillespie P., Huby N.J., Makofske R., Orzechowski L., Perrotta A., Toth K., Cooper J.P., Jiang N., Falcioni F., Campbell R., Cox D., Gaizband D., Belunis C.J., Vidovic D., Ito K., Crowther R., Kammlott U., Zhang X., Palermo R., Weber D., Guenot J., Nagy Z., and Olson G.L. Peptide and peptide mimetic inhibitors of antigen presentation by HLA-DR class II MHC molecules. Design, structure-activity relationships, and X-ray crystal structures. J Med Chem 43 (2000) 2135-2148
8. Burster T., Beck A., Tolosa E., Marin-Esteban V., Rotzschke O., Falk K., Lautwein A., Reich M., Brandenburg J., Schwarz G., Wiendl H., Melms A., Lehmann R., Stevanovic S., Kalbacher H., and Driessen C. Cathepsin G, and not the asparagine-specific endoprotease, controls the processing of myelin basic protein in lysosomes from human B lymphocytes. J Immunol 172 (2004) 5495-5503
9. Burster T., Marin-Esteban V., Boehm B.O., Dunn S., Rotzschke O., Falk K., Weber E., Verhelst S.H., Kalbacher H., and Driessen C. Design of protease-resistant myelin basic protein-derived peptides by cleavage site directed amino acid substitutions. Biochem Pharmacol 74 (2007) 1514-1523
10. Chao C.C., Sytwu H.K., Chen E.L., Toma J., and McDevitt H.O. The role of MHC class II molecules in susceptibility to type I diabetes: identification of peptide epitopes and characterization of the T cell repertoire. Proc Natl Acad Sci U S A 96 (1999) 9299-9304
11. Chapman H.A. Endosomal proteases in antigen presentation. Curr Opin Immunol 18 (2006) 78-84
12. Crowe P.D., Qin Y., Conlon P.J., and Antel J.P. NBI-5788, an altered MBP83-99 peptide, induces a T-helper 2-like immune response in multiple sclerosis patients. Ann Neurol 48 (2000) 758-765
13. Eisenbarth G.S. Update in type 1 diabetes. J Clin Endocrinol Metab 92 (2007) 2403-2407
14. Eizirik D.L., and Mandrup-Poulsen T. A choice of death--the signal-transduction of immune-mediated beta-cell apoptosis. Diabetologia 44 (2001) 2115-2133
15. Endl J., Otto H., Jung G., Dreisbusch B., Donie F., Stahl P., Elbracht R., Schmitz G., Meinl E., Hummel M., Ziegler A.G., Wank R., and Schendel D.J. Identification of naturally processed T cell epitopes from glutamic acid decarboxylase presented in the context of HLA-DR alleles by T lymphocytes of recent onset IDDM patients. J Clin Invest 99 (1997) 2405-2415
16. Endl J., Rosinger S., Schwarz B., Friedrich S.O., Rothe G., Karges W., Schlosser M., Eiermann T., Schendel D.J., and Boehm B.O. Coexpression of CD25 and OX40 (CD134) receptors delineates autoreactive T-cells in type 1 diabetes. Diabetes 55 (2006) 50-60
17. Falcioni F., Ito K., Vidovic D., Belunis C., Campbell R., Berthel S.J., Bolin D.R., Gillespie P.B., Huby N., Olson G.L., Sarabu R., Guenot J., Madison V., Hammer J., Sinigaglia F., Steinmetz M., and Nagy Z.A. Peptidomimetic compounds that inhibit antigen presentation by autoimmune disease-associated class II major histocompatibility molecules. Nat Biotechnol 17 (1999) 562-567
18. Fenalti G., and Rowley M.J. GAD65 as a prototypic autoantigen. J Autoimmun 31 (2008) 228-232
19. Hsing L.C., and Rudensky A.Y. The lysosomal cysteine proteases in MHC class II antigen presentation. Immunol Rev 207 (2005) 229-241
20. Jain R., Tartar D.M., Gregg R.K., Divekar R.D., Bell J.J., Lee H.H., Yu P., Ellis J.S., Hoeman C.M., Franklin C.L., and Zaghouani H. Innocuous IFNgamma induced by adjuvant-free antigen restores normoglycemia in NOD mice through inhibition of IL-17 production. J Exp Med 205 (2008) 207-218
21. Jasinski J.M., and Eisenbarth G.S. Insulin as a primary autoantigen for type 1A diabetes. Clin Dev Immunol 12 (2005) 181-186
22. Kappos L., Comi G., Panitch H., Oger J., Antel J., Conlon P., and Steinman L. Induction of a non-encephalitogenic type 2 T helper-cell autoimmune response in multiple sclerosis after administration of an altered peptide ligand in a placebo-controlled, randomized phase II trial. The altered peptide ligand in Relapsing MS Study Group. Nat Med 6 (2000) 1176-1182
23. Lamont A.G., Powell M.F., Colon S.M., Miles C., Grey H.M., and Sette A. The use of peptide analogs with improved stability and MHC binding capacity to inhibit antigen presentation in vitro and in vivo. J Immunol 144 (1990) 2493-2498
24. Larsen C.M., Faulenbach M., Vaag A., Volund A., Ehses J.A., Seifert B., Mandrup-Poulsen T., and Donath M.Y. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med 356 (2007) 1517-1526
25. Ludvigsson J. Therapy with GAD in diabetes. Diabetes Metab Res Rev 25 (2009) 307-315
26. Ludvigsson J., Faresjo M., Hjorth M., Axelsson S., Cheramy M., Pihl M., Vaarala O., Forsander G., Ivarsson S., Johansson C., Lindh A., Nilsson N.O., Aman J., Ortqvist E., Zerhouni P., and Casas R. GAD treatment and insulin secretion in recent-onset type 1 diabetes. N Engl J Med 359 (2008) 1909-1920
27. Lutgens S.P., Cleutjens K.B., Daemen M.J., and Heeneman S. Cathepsin cysteine proteases in cardiovascular disease. FASEB J 21 (2007) 3029-3041
28. Max H., Halder T., Kalbus M., Gnau V., Jung G., and Kalbacher H. A 16mer peptide of the human autoantigen calreticulin is a most prominent HLA-DR4Dw4-associated self-peptide. Hum Immunol 41 (1994) 39-45
29. Maynard J., Petersson K., Wilson D.H., Adams E.J., Blondelle S.E., Boulanger M.J., Wilson D.B., and Garcia K.C. Structure of an autoimmune T cell receptor complexed with class II peptide-MHC: insights into MHC bias and antigen specificity. Immunity 22 (2005) 81-92
30. Nerup J., Mandrup-Poulsen T., Molvig J., Helqvist S., Wogensen L., and Egeberg J. Mechanisms of pancreatic beta-cell destruction in type I diabetes. Diabetes Care 11 Suppl. 1 (1988) 16-23
31. Nicholson L.B., Greer J.M., Sobel R.A., Lees M.B., and Kuchroo V.K. An altered peptide ligand mediates immune deviation and prevents autoimmune encephalomyelitis. Immunity 3 (1995) 397-405
32. Oukka M. Interplay between pathogenic Th17 and regulatory T cells. Ann Rheum Dis 66 Suppl. 3 (2007) iii87-iii90
33. Raz I., Eldor R., and Naparstek Y. Immune modulation for prevention of type 1 diabetes mellitus. Trends Biotechnol 23 (2005) 128-134
34. Richter W., Mertens T., Schoel B., Muir P., Ritzkowsky A., Scherbaum W.A., and Boehm B.O. Sequence homology of the diabetes-associated autoantigen glutamate decarboxylase with coxsackie B4-2C protein and heat shock protein 60 mediates no molecular mimicry of autoantibodies. J Exp Med 180 (1994) 721-726
35. Sakai K., Zamvil S.S., Mitchell D.J., Hodgkinson S., Rothbard J.B., and Steinman L. Prevention of experimental encephalomyelitis with peptides that block interaction of T cells with major histocompatibility complex proteins. Proc Natl Acad Sci U S A 86 (1989) 9470-9474
36. Teitelbaum D., Aharoni R., Arnon R., and Sela M. Specific inhibition of the T-cell response to myelin basic protein by the synthetic copolymer Cop 1. Proc Natl Acad Sci U S A 85 (1988) 9724-9728
37. Travis J. Structure, function, and control of neutrophil proteinases. Am J Med 84 (1988) 37-42
38. Ueda H., Howson J.M., Esposito L., Heward J., Snook H., Chamberlain G., Rainbow D.B., Hunter K.M., Smith A.N., Di Genova G., Herr M.H., Dahlman I., Payne F., Smyth D., Lowe C., Twells R.C., Howlett S., Healy B., Nutland S., Rance H.E., Everett V., Smink L.J., Lam A.C., Cordell H.J., Walker N.M., Bordin C., Hulme J., Motzo C., Cucca F., Hess J.F., Metzker M.L., Rogers J., Gregory S., Allahabadia A., Nithiyananthan R., Tuomilehto-Wolf E., Tuomilehto J., Bingley P., Gillespie K.M., Undlien D.E., Ronningen K.S., Guja C., Ionescu-Tirgoviste C., Savage D.A., Maxwell A.P., Carson D.J., Patterson C.C., Franklyn J.A., Clayton D.G., Peterson L.B., Wicker L.S., Todd J.A., and Gough S.C. Association of the T-cell regulatory gene CTLA4 with susceptibility to autoimmune disease. Nature 423 (2003) 506-511
39. Watts C., Matthews S.P., Mazzeo D., Manoury B., and Moss C.X. Asparaginyl endopeptidase: case history of a class II MHC compartment protease. Immunol Rev 207 (2005) 218-228
40. *0401. J Clin Invest 98 (1996) 2597-2603
41. Wraith D.C., Smilek D.E., Mitchell D.J., Steinman L., and McDevitt H.O. Antigen recognition in autoimmune encephalomyelitis and the potential for peptide-mediated immunotherapy. Cell 59 (1989) 247-255
42. Wysocka M., Legowska A., Bulak E., Jaskiewicz A., Miecznikowska H., Lesner A., and Rolka K. New chromogenic substrates of human neutrophil cathepsin G containing non-natural aromatic amino acid residues in position P(1) selected by combinatorial chemistry methods. Mol Divers 11 (2007) 93-99
43. Zavasnik-Bergant T., and Turk B. Cysteine cathepsins in the immune response. Tissue Antigens 67 (2006) 349-355