Functional inhibition related to structure of a highly potent insulin-specific CD8 T cell clone using altered peptide ligands

European Journal of Immunology

Volumn 38, Issue 1, 2008, Pages 240-249

  de Marquesini, Liliana G Petrich ^a   Moustakas, Antonis K ^b   Thomas, Ian J ^a   Wen, Li ^c   Papadopoulos, George K ^d   Wong, F Susan ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b IONIAN UNIVERSITY   (Greece)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Faculty of Agricultural Technology   (Greece)

Author keywords

Antigens peptides epitopes; Autoimmunity; Cytotoxic; T cell receptors

Indexed keywords

AMINO ACID; EPITOPE; GAMMA INTERFERON; INSULIN; LEUCYLTYROSYLLEUCYLVALYLCYSTYLGLYCYLGLUTAMYLARGINYLGLYCINE; LIGAND; PEPTIDE DERIVATIVE; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CD8+ T LYMPHOCYTE; CELL ASSAY; CELL CLONE; CELL LINE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; DRUG EFFECT; INHIBITION KINETICS; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR MODEL; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CLONE CELLS; DIABETES MELLITUS, TYPE 1; EPITOPES, T-LYMPHOCYTE; INSULIN; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED NOD; MODELS, MOLECULAR; PEPTIDES; PROTEIN STRUCTURE, TERTIARY;

EID: 38349079848     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200737762     Document Type: Article

References (57)

1. Evavold, B. D., Sloan-Lancaster, J. and Allen, P. M., Tickling the TCR: Selective T-cell functions stimulated by altered peptide ligands. Immunol. Today 1993. 14: 602-609.
2. Sloan-Lancaster, J. and Allen, P. M., Altered peptide ligand-induced partial T cell activation: Molecular mechanisms and role in T cell biology. Annu. Rev. Immunol. 1996. 14: 1-27.
3. Kalergis, A. M. and Nathenson, S. G., Altered peptide ligand-mediated TCR antagonism can be modulated by a change in a single amino acid residue within the CDR3 beta of an MHC class I-restricted TCR. J. Immunol. 2000. 165: 280-285.
4. Ford, M. L. and Evavold, B. D., An MHC anchor-substituted analog of myelin oligodendrocyte glycoprotein 35-55 induces IFN-gamma and autoantibodies in the absence of experimental autoimmume encephalomyelitis and optic neuritis. Eur. J. Immunol. 2004. 34: 388-397.
5. Ryan, K. R., McNeil, L. K., Dao, C., Jensen, P. E. and Evavold, B. D., Modification of peptide interaction with MHC creates TCR partial agonists. Cell. Immunol. 2004. 227: 70-78.
6. Kersh, G. J. and Allen, P. M., Structural basis for Tcell recognition of altered peptide ligands: A single T cell receptor can productively recognize a large continuum of related ligands. J. Exp. Med. 1996. 184: 1259-1268.
7. Windhagen, A., Scholz, C., Hollsberg, P., Fukaura, H., Sette, A. and Hafler, D. A., Modulation of cytokine patterns of human autoreactive T cell clones by a single amino acid substitution of their peptide ligand. Immunity 1995. 2: 373-380.
8. Sloan-Lancaster, J., Evavold, B. D. and Allen, P. M., Induction of T-cell anergy by altered T-cell-receptor ligand on live antigen-presenting cells. Nature 1993. 363: 156-159.
9. De Magistris, M. T., Alexander, J., Coggeshall, M., Altman, A., Gaeta, F. C., Grey, H. M. and Sette, A., Antigen analog-major histocompatibility complexes act as antagonists of the T cell receptor. Cell 1992. 68: 625-634.
10. Jameson, S. C., Carbone, F. R. and Bevan, M. J., Clone-specific T cell receptor antagonists of major histocompatibility complex class I-restricted cytotoxic T cells. J. Exp. Med. 1993. 177: 1541-1550.
11. Ostrov, D., Krieger, J., Sidney, J., Sette, A. and Concannon, P., T cell receptor antagonism mediated by interaction between T cell receptor junctional residues and peptide antigen analogues. J. Immunol. 1993. 150: 4277-4283.
12. Ruppert, J., Alexander, J., Snoke, K., Coggeshall, M., Herbert, E., McKenzie, D., Grey, H. M. et al., Effect of T-cell receptor antagonism on interaction between T cells and antigen-presenting cells and on T-cell signaling events. Proc. Natl. Acad. Sci. USA 1993. 90: 2671-2675.
13. Evavold, B. D., Sloan-Lancaster, J. and Allen, P. M., Antagonism of superantigen-stimulated helper T-cell clones and hybridomas by altered peptide ligand. Proc. Natl. Acad. Sci. USA 1994. 91: 2300-2304.
14. Wong, F. S., Visintin, I., Wen, L., Flavell, R. A. and Janeway, C. A., Jr., CD8 T cell clones from young nonobese diabetic (NOD) islets can transfer rapid onset of diabetes in NOD mice in the absence of CD4 cells. J. Exp. Med. 1996. 183: 67-76.
15. Wong, F. S., Karttunen, J., Dumont, C., Wen, L., Visintin, I., Pilip, I. M., Shastri, N. et al., Identification of an MHC class I-restricted autoantigen in type 1 diabetes by screening an organ-specific cDNA library. Nat Med 1999. 5: 1026-1031.
16. Alleva, D. G., Crowe, P. D., Jin, L., Kwok, W. W., Ling, N., Gottschalk, M., Conlon, P. J. et al., A disease-associated cellular immune response in type 1 diabetics to an immunodominant epitope of insulin. J. Clin. Invest. 2001. 107: 173-180.
17. Daniel, D., Gill, R. G., Schloot, N. and Wegmann, D., Epitope specificity, cytokine production profile and diabetogenic activity of insulin-specific T cell clones isolated from NOD mice. Eur. J. Immunol. 1995. 25: 1056-1062.
18. Alleva, D. G., Maki, R. A., Putnam, A. L., Robinson, J. M., Kipnes, M. S., Dandona, P., Marks, J. B. et al., Immunomodulation in type 1 diabetes by NBI-6024, an altered peptide ligand of the insulin B epitope. Scand. J. Immunol. 2006. 63: 59-69.
19. Rammensee, H. G., Friede, T. and Stevanoviic, S., MHC ligands and peptide motifs: First listing. Immunogenetics 1995. 41: 178-228.
20. Bouvier, M. and Wiley, D. C., Importance of peptide amino and carboxyl termini to the stability of MHC class I molecules. Science 1994. 265: 398-402.
21. Wong, F. S., Moustakas, A. K., Wen, L., Papadopoulos, G. K. and Janeway, C. A., Jr., Analysis of structure and function relationships of an autoantigenic peptide of insulin bound to H-2K(d) that stimulates CD8 T cells in insulin-dependent diabetes mellitus. Proc. Natl. Acad. Sci. USA 2002. 99: 5551-5556.
22. Matsumura, M., Fremont, D. H., Peterson, P. A. and Wilson, I. A., Emerging principles for the recognition of peptide antigens by MHC class I molecules. Science 1992. 257: 927-934.
23. Rudolph, M. G. and Wilson, I. A., The specificity of TCR/pMHC interaction. Curr. Opin. Immunol. 2002. 14: 52-65.
24. Ding, Y. H., Smith, K. J., Garboczi, D. N., Utz, U., Biddison, W. E. and Wiley, D. C., Two human T cell receptors bind in a similar diagonal mode to the HLA-A2/Tax peptide complex using different TCR amino acids. Immunity 1998. 8: 403-411.
25. Ding, Y. H., Baker, B. M., Garboczi, D. N., Biddison, W. E. and Wiley, D. C., Four A6-TCR/peptide/HLA-A2 structures that generate very different T cell signals are nearly identical. Immunity 1999. 11: 45-56.
26. Garcia, K. C., Degano, M., Stanfield, R. L., Brunmark, A., Jackson, M. R., Peterson, P. A., Teyton, L. et al., An alphabeta T cell receptor structure at 2.5 A and its orientation in the TCR-MHC complex. Science 1996. 274: 209-219.
27. Stewart-Jones, G. B., McMichael, A. J., Bell, J. L, Stuart, D. I. and Jones, E. Y., A structural basis for immunodominant human T cell receptor recognition. Nat. Immunol. 2003. 4: 657-663.
28. Teng, M. K., Smolyar, A., Tse, A. G., Liu, J. H., Liu, J., Hussey, R. E., Nathenson, S. G. et al., Identification of a common docking topology with substantial variation among different TCR-peptide-MHC complexes. Curr. Biol. 1998. 8: 409-412.
29. d peptide-binding motif. J. Biol. Chem. 2006. 281: 10618-10625.
30. Baker, B. M., Gagnon, S. J., Biddison, W. E. and Wiley, D. C., Conversion of a T cell antagonist into an agonist by repairing a defect in the TCR/peptide/MHC interface: Implications for TCR signaling. Immunity 2000. 13: 475-484.
31. Starr, T. K., Jameson, S. C. and Hogquist, K. A., Positive and negative selection of T cells. Annu. Rev. Immunol. 2003. 21: 139-176.
32. Siggs, O. M., Makaroff, L. E. and Liston, A., The why and how of thymocyte negative selection. Curr. Opin. Immunol. 2006. 18: 175-183.
33. Wong, F. S. and Janeway, C. A., Jr., Insulin-dependent diabetes mellitus and its animal models. Curr. Opin. Immunol. 1999. 11: 643-647.
34. Trudeau, J. D., Kelly-Smith, C., Verchere, C. B., Elliott, J. F., Dutz, J. P., Finegood, D. T., Santamaria, P. et al., Prediction of spontaneous autoimmune diabetes in NOD mice by quantification of autoreactive T cells in peripheral blood. J. Clin. Invest. 2003. 111: 217-223.
35. Velloso, L. M., Michaelsson, J., Ljunggren, H. G., Schneider, G. and Achour, A., Determination of structural principles underlying three different modes of lymphocytic choriomeningitis virus escape from CTL recognition. J. Immunol. 2004. 172: 5504-5511.
36. Housset, D. and Malissen, B., What do TCR-pMHC crystal structures teach us about MHC restriction and alloreactivity? Trends Immunol. 2003. 24: 429-437.
37. Rudolph, M. G., Stanfield, R. L. and Wilson, I. A., How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol. 2006. 24: 419-466.
38. Reis e Sousa, C., Levine, E. H. and Germain, R. N., Partial signaling by CD8+ T cells in response to antagonist ligands. J. Exp. Med. 1996. 184: 149-157.
39. Hahn, M., Nicholson, M. J., Pyrdol, J. and Wucherpfennig, K. W., Unconventional topology of self peptide-major histocompatibility complex binding by a human autoimmune T cell receptor. Nat. Immunol. 2005. 6: 490-496.
40. Li, Y., Huang, Y., Lue, J., Quandt, J. A., Martin, R. and Mariuzza, R. A., Structure of a human autoimmune TCR bound to a myelin basic protein self-peptide and a multiple sclerosis-associated MHC class II molecule. EMBO J. 2005. 24: 2968-2979.
41. Maynard, J., Petersson, K., Wilson, D. H., Adams, E. J., Blondelle, S. E., Boulanger, M. J., Wilson, D. B. et al., Structure of an autoimmune T cell receptor complexed with class II peptide-MHC: Insights into MHC bias and antigen specificity. Immunity 2005. 22: 81-92.
42. Nakayama, M., Abiru, N., Moriyama, H., Babaya, N., Liu, E., Miao, D., Yu, L. et al., Prime role for an insulin epitope in the development of type 1 diabetes in NOD mice. Nature 2005. 435: 220-223.
43. Lee, K. H., Wucherpfennig, K. W. and Wiley, D. C., Structure of a human insulin peptide-HLA-DQ8 complex and susceptibility to type 1 diabetes. Nat. Immunol. 2001. 2: 501-507.
44. Levisetti, M. G., Suri, A., Petzold, S. J. and Unanue, E. R., The insulin-specific T cells of nonobese diabetic mice recognize a weak MHC-binding segment in more than one form. J. Immunol. 2007 178: 6051-6057.
45. Martinez, N. R., Augstein, P., Moustakas, A. K., Papadopoulos, G. K., Gregori, S., Adorini, L., Jackson, D. C. et al., Disabling an integral CTL epitope allows suppression of autoimmune diabetes by intranasal proinsulin peptide. J. Clin. Invest. 2003. 111: 1365-1371.
46. Hassainya, Y., Garcia-Pons, F., Kratzer, R., Linda, V., Greer, F., Lemonnier, F. A., Niedermann, G. et al, identification of naturally processed HLA-A2-restricted proinsulin epitopes by reverse immunology. Diabetes 2005. 54: 2053-2059.
47. Pinkse, G. G., Tysma, O. H., Bergen, C. A., Kester, M. G., Ossendorp, F., van Veelen, P. A., Keymeulen, B. et al., Autoreactive CD8 T cells associated with beta cell destruction in type 1 diabetes. Proc. Natl. Acad. Sci. USA 2005. 102: 18425-18430.
48. Toma, A., Haddouk, S., Briand, J. P., Camoin, L., Gahery, H., Connan, F., Dubois-Laforgue, D. et al., Recognition of a subregion of human proinsulin by class I-restricted T cells in type 1 diabetic patients. Proc. Natl. Acad. Sci. USA 2005. 102: 10581-10586.
49. Krishnamurthy, B., Dudek, N. L., McKenzie, M. D., Purcell, A. W., Brooks, A. G., Gellert, S., Colman, P. G. et al., Responses against islet antigens in NOD mice are prevented by tolerance to proinsulin but not IGRP. J. Clin. Invest. 2006. 116: 3258-3265.
50. Amrani, A., Verdaguer, J., Serra, P., Tafuro, S., Tan, R. and Santamaria, P., Progression of autoimmune diabetes driven by avidity maturation of a T-cell population. Nature 2000. 406: 739-742.
51. Agnes, M. C., Tan, A., Jordens, R., Geluk, A., Roep, B. O., Ottenhoff, T., Drijfhout, J. W. et al., Strongly increased efficiency of altered peptide ligands by mannosylation. Int. Immunol. 1998. 10: 1299-1304.
52. Cresswell, P., Ackerman, A. L., Giodini, A., Peaper, D. R. and Wearsch, P. A., Mechanisms of MHC class I-restricted antigen processing and cross-presentation. Immunol. Rev. 2005. 207: 145-157.
53. Ljunggren, H. G., Chien, C., Hoglund, P., Franksson, L. and Karre, K., The RMA-S lymphoma mutant; consequences of a peptide loading defect on immunological recognition and graft rejection. Int. J. Cancer Suppl. 1991. 6: 38-44.
54. Ljunggren, H. G., Stam, N. J., Ohlen, C., Neefjes, J. J., Hoglund, P., Heemels, M. T., Bastin, J. et al., Empty MHC class I molecules come out in the cold. Nature 1990. 346: 476-480.
55. Moustakas, A. K., Routsias, J. and Papadopoulos, G. K., Modelling of the MHC II allele FA(g7) of NOD mouse: PH-dependent changes in specificity at pockets 9 and 6 explain several of the unique properties of this molecule. Diabetologia 2000. 43: 609-624.
56. Ettinger, R. A., Papadopoulos, G. K., Moustakas, A. K., Nepom, G. T. and Kwok, W. W., Allelic variation in key peptide-binding pockets discriminates between closely related diabetes-protective and diabetes-susceptible HLA-DQB1*06 alleles. J. Immunol. 2006. 176: 1988-1998.
57. Stepniak, D., Vader, L. W., Kooy, Y., van Veelen, P. A., Moustakas, A., Papandreou, N. A., Eliopoulos, E. et al., T-cell recognition of HLA-DQ2-bound gluten peptides can be influenced by an N-terminal proline at p-1. Immunogenetics 2005. 57: 8-15.