T cell cross-reactivity between a highly immunogenic EBV epitope and a self-peptide naturally presented by HLA-B∗18:01+ cells

Journal of Immunology

Volumn 194, Issue 10, 2015, Pages 4668-4675

  Rist, Melissa J ^a,b   Hibbert, Kelly M ^c   Croft, Nathan P ^c   Smith, Corey ^a   Neller, Michelle A ^a   Burrows, Jacqueline M ^a   Miles, John J ^a,b,d   Purcell, Anthony W ^c   Rossjohn, Jamie ^c,d   Gras, Stephanie ^c   Burrows, Scott R ^a,b  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ARGININE; EPITOPE; EPSTEIN BARR VIRUS ANTIGEN; HLA B 18:01; HLA B ANTIGEN; PEPTIDE; UNCLASSIFIED DRUG; AUTOANTIGEN; VIRUS ANTIGEN;

ANTIGEN PRESENTATION; ANTIGEN STRUCTURE; ARTICLE; CD8+ T LYMPHOCYTE; CELL SURFACE; COMPLEX FORMATION; CONTROLLED STUDY; CROSS REACTION; ELUTION; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOPATHOLOGY; MASS SPECTROMETRY; MOLECULAR MIMICRY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; T LYMPHOCYTE; T LYMPHOCYTE RECEPTOR GENE; AUTOIMMUNITY; IMMUNOLOGY; LIQUID CHROMATOGRAPHY; TANDEM MASS SPECTROMETRY;

ANTIGEN PRESENTATION; ANTIGENS, VIRAL; AUTOANTIGENS; AUTOIMMUNITY; CD8-POSITIVE T-LYMPHOCYTES; CHROMATOGRAPHY, LIQUID; CROSS REACTIONS; EPITOPES, T-LYMPHOCYTE; EPSTEIN-BARR VIRUS INFECTIONS; HERPESVIRUS 4, HUMAN; HLA-B ANTIGENS; HUMANS; MOLECULAR MIMICRY; TANDEM MASS SPECTROMETRY;

EID: 84929095999     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500233     Document Type: Article

References (55)

1. Starr, T. K., S. C. Jameson, and K. A. Hogquist. 2003. Positive and negative selection of T cells. Annu. Rev. Immunol. 21: 139-176.
2. Nikolić-Zugić, J., and M. J. Bevan. 1990. Role of self-peptides in positively selecting the T-cell repertoire. Nature 344: 65-67.
3. Hogquist, K. A., T. A. Baldwin, and S. C. Jameson. 2005. Central tolerance: learning self-control in the thymus. Nat. Rev. Immunol. 5: 772-782.
4. Zehn, D., and M. J. Bevan. 2006. T cells with low avidity for a tissue-restricted antigen routinely evade central and peripheral tolerance and cause autoimmunity. Immunity 25: 261-270.
5. Turner, S. J., P. C. Doherty, J. McCluskey, and J. Rossjohn. 2006. Structural determinants of T-cell receptor bias in immunity. Nat. Rev. Immunol. 6: 883-894.
6. Gras, S., S. R. Burrows, S. J. Turner, A. K. Sewell, J. McCluskey, and J. Rossjohn. 2012. A structural voyage toward an understanding of the MHC-I-restricted immune response: lessons learned and much to be learned. Immunol. Rev. 250: 61-81.
7. Rossjohn, J., S. Gras, J. J. Miles, S. J. Turner, D. I. Godfrey, and J. McCluskey. 2014. T cell antigen receptor recognition of antigen-presenting molecules. Annu. Rev. Immunol. DOI: 10.1146/annurev-immunol-032414-112334.
8. Oldstone, M. B. 1987. Molecular mimicry and autoimmune disease. Cell 50: 819-820.
9. Luo, A.-M., K. M. Garza, D. Hunt, and K. S. K. Tung. 1993. Antigen mimicry in autoimmune disease sharing of amino acid residues critical for pathogenic T cell activation. J. Clin. Invest. 92: 2117-2123.
10. Harkiolaki, M., S. L. Holmes, P. Svendsen, J. W. Gregersen, L. T. Jensen, R. McMahon, M. A. Friese, G. van Boxel, R. Etzensperger, J. S. Tzartos, et al. 2009. T cell-mediated autoimmune disease due to low-affinity crossreactivity to common microbial peptides. Immunity 30: 348-357.
11. Hislop, A. D., G. S. Taylor, D. Sauce, and A. B. Rickinson. 2007. Cellular responses to viral infection in humans: lessons from Epstein-Barr virus. Annu. Rev. Immunol. 25: 587-617.
12. Long, H. M., G. S. Taylor, and A. B. Rickinson. 2011. Immune defence against EBV and EBV-associated disease. Curr. Opin. Immunol. 23: 258-264.
13. Libbey, J. E., M. F. Cusick, and R. S. Fujinami. 2014. Role of pathogens in multiple sclerosis. Int. Rev. Immunol. 33: 266-283.
14. + T cell responses. J. Immunol. 191: 561-571.
15. Illing, P. T., J. P. Vivian, N. L. Dudek, L. Kostenko, Z. Chen, M. Bharadwaj, J. J. Miles, L. Kjer-Nielsen, S. Gras, N. A. Williamson, et al. 2012. Immune self-reactivity triggered by drug-modified HLA-peptide repertoire. Nature 486: 554-558.
16. Scull, K. E., N. L. Dudek, A. J. Corbett, S. H. Ramarathinam, D. G. Gorasia, N. A. Williamson, and A. W. Purcell. 2012. Secreted HLA recapitulates the immunopeptidome and allows in-depth coverage of HLA A∗02:01 ligands. Mol. Immunol. 51: 136-142.
17. Dudek, N. L., C. T. Tan, D. G. Gorasia, N. P. Croft, P. T. Illing, and A. W. Purcell. 2012. Constitutive and inflammatory immunopeptidome of pancreatic β-cells. Diabetes 61: 3018-3025.
18. Tan, C. T., N. P. Croft, N. L. Dudek, N. A. Williamson, and A. W. Purcell. 2011. Direct quantitation of MHC-bound peptide epitopes by selected reaction monitoring. Proteomics 11: 2336-2340.
19. Schittenhelm, R. B., T. C. Sian, P. G. Wilmann, N. L. Dudek, and A. W. Purcell. 2015. Revisiting the arthritogenic peptide theory: quantitative not qualitative changes in the peptide repertoire of HLA-B27 allotypes. Arthritis Rheum. (Munch) 67: 702-713.
20. Gras, S., S. R. Burrows, L. Kjer-Nielsen, C. S. Clements, Y. C. Liu, L. C. Sullivan, M. J. Bell, A. G. Brooks, A. W. Purcell, J. McCluskey, and J. Rossjohn. 2009. The shaping of T cell receptor recognition by self-tolerance. Immunity 30: 193-203.
21. Battye, T. G. G., L. Kontogiannis, O. Johnson, H. R. Powell, and A. G.W. Leslie. 2011. iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr. 67: 271-281.
22. Winn, M. D., C. C. Ballard, K. D. Cowtan, E. J. Dodson, P. Emsley, P. R. Evans, R. M. Keegan, E. B. Krissinel, A. G. Leslie, A. McCoy, et al. 2011. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67: 235-242.
23. Adams, P. D., P. V. Afonine, G. Bunkóczi, V. B. Chen, N. Echols, J. J. Headd, L. W. Hung, S. Jain, G. J. Kapral, R. W. Grosse Kunstleve, et al. 2011. The Phenix software for automated determination of macromolecular structures. Methods 55: 94-106.
24. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60: 2126-2132.
25. DeLano, W. L. 2002. The PyMOL Molecular Graphics System. DeLano Scientific, Palo Alto, CA.
26. Baillat, D.,M.-A. Hakimi, A. M. Näär, A. Shilatifard, N. Cooch, and R. Shiekhattar. 2005. Integrator, a multiprotein mediator of small nuclear RNA processing, associates with the C-terminal repeat of RNA polymerase II. Cell 123: 265-276.
27. Callebaut, I., D. Moshous, J. P. Mornon, and J. P. de Villartay. 2002. Metallo-β-lactamase fold within nucleic acids processing enzymes: the β-CASP family. Nucleic Acids Res. 30: 3592-3601.
28. Macdonald, W. A., Z. Chen, S. Gras, J. K. Archbold, F. E. Tynan, C. S. Clements, M. Bharadwaj, L. Kjer-Nielsen, P. M. Saunders, M. C. Wilce, et al. 2009. T cell allorecognition via molecular mimicry. Immunity 31: 897-908.
29. Lünemann, J. D., I. Jelcić, S. Roberts, A. Lutterotti, B. Tackenberg, R. Martin, and C. Münz. 2008. EBNA1-specific T cells from patients with multiple sclerosis cross react with myelin antigens and co-produce IFN-γ and IL-2. J. Exp. Med. 205: 1763-1773.
30. Lang, H. L., H. Jacobsen, S. Ikemizu, C. Andersson, K. Harlos, L. Madsen, P. Hjorth, L. Sondergaard, A. Svejgaard, K. Wucherpfennig, et al. 2002. A functional and structural basis for TCR cross-reactivity in multiple sclerosis. Nat. Immunol. 3: 940-943.
31. Ascherio, A., and K. L. Munger. 2007. Environmental risk factors for multiple sclerosis. Part I: the role of infection. Ann. Neurol. 61: 288-299.
32. Vento, S., L. Guella, F. Mirandola, F. Cainelli, G. Di Perri, M. Solbiati, T. Ferraro, and E. Concia. 1995. Epstein-Barr virus as a trigger for autoimmune hepatitis in susceptible individuals. Lancet 346: 608-609.
33. Pakpoor, J., G. Disanto, J. E. Gerber, R. Dobson, U. C. Meier, G. Giovannoni, and S. V. Ramagopalan. 2013. The risk of developing multiple sclerosis in individuals seronegative for Epstein-Barr virus: a meta-analysis. Mult. Scler. 19: 162-166.
34. Thacker, E. L., F. Mirzaei, and A. Ascherio. 2006. Infectious mononucleosis and risk for multiple sclerosis: a meta-analysis. Ann. Neurol. 59: 499-503.
35. Pender, M. P., and S. R. Burrows. 2014. Epstein-Barr virus and multiple sclerosis: potential opportunities for immunotherapy. Clin Transl Immunology 3: e27. Available at: http://www.nature.com/cti/journal/v3/n10/full/cti201425a.html.
36. Igoe, A., and R. H. Scofield. 2013. Autoimmunity and infection in Sjögren's syndrome. Curr. Opin. Rheumatol. 25: 480-487.
37. Mariette, X., J. Gozlan, D. Clerc, M. Bisson, and F. Morinet. 1991. Detection of Epstein-Barr virus DNA by in situ hybridization and polymerase chain reaction in salivary gland biopsy specimens from patients with Sjögren's syndrome. Am. J. Med. 90: 286-294.
38. Inoue, H., K. Mishima, S. Yamamoto-Yoshida, R. Ushikoshi-Nakayama, Y. Nakagawa, K. Yamamoto, K. Ryo, F. Ide, and I. Saito. 2012. Aryl hydrocarbon receptor-mediated induction of EBV reactivation as a risk factor for Sjögren's syndrome. J. Immunol. 188: 4654-4662.
39. James, J. A., B. R. Neas, K. L. Moser, T. Hall, G. R. Bruner, A. L. Sestak, and J. B. Harley. 2001. Systemic lupus erythematosus in adults is associated with previous Epstein-Barr virus exposure. Arthritis Rheum. 44: 1122-1126.
40. McClain, M. T., B. D. Poole, B. F. Bruner, K. M. Kaufman, J. B. Harley, and J. A. James. 2006. An altered immune response to Epstein-Barr nuclear antigen 1 in pediatric systemic lupus erythematosus. Arthritis Rheum. 54: 360-368.
41. Moon, U. Y., S. J. Park, S. T. Oh, W. U. Kim, S. H. Park, S. H. Lee, C. S. Cho, H. Y. Kim, W. K. Lee, and S. K. Lee. 2004. Patients with systemic lupus erythematosus have abnormally elevated Epstein-Barr virus load in blood. Arthritis Res. Ther. 6: R295-R302.
42. Larsen, M.,D. Sauce, C. Deback, L. Arnaud, A.Mathian, M.Miyara, D. Boutolleau, C. Parizot, K. Dorgham, L. Papagno, et al. 2011. Exhausted cytotoxic control of Epstein-Barr virus in human lupus. PLoS Pathog. 7: e1002328. Available at: http://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1002328.
43. Gross, A. J., D. Hochberg, W. M. Rand, and D. A. Thorley-Lawson. 2005. EBV and systemic lupus erythematosus: a new perspective. J. Immunol. 174: 6599-6607.
44. David-Ameline, J., A. Lim, F. Davodeau, M. A. Peyrat, J. M. Berthelot, G. Semana, C. Pannetier, J. Gaschet, H. Vie, J. Even, and M. Bonneville. 1996. Selection of T cells reactive against autologous B lymphoblastoid cells during chronic rheumatoid arthritis. J. Immunol. 157: 4697-4706.
45. Scotet, E., J. David-Ameline, M. A. Peyrat, A. Moreau-Aubry, D. Pinczon, A. Lim, J. Even, G. Semana, J. M. Berthelot, R. Breathnach, et al. 1996. T cell response to Epstein-Barr virus transactivators in chronic rheumatoid arthritis. J. Exp. Med. 184: 1791-1800.
46. Jaquiéry, E., S. Jilek, M. Schluep, P. Meylan, A. Lysandropoulos, G. Pantaleo, and R. A. Du Pasquier. 2010. Intrathecal immune responses to EBV in early MS. Eur. J. Immunol. 40: 878-887.
47. + T cells that are specific for certain viral epitopes. Arthritis Res. 2: 154-164.
48. Lossius, A., J. N. Johansen, Ø. Torkildsen, F. Vartdal, and T. Holmøy. 2012. Epstein-Barr virus in systemic lupus erythematosus, rheumatoid arthritis and multiple sclerosis-association and causation. Viruses 4: 3701-3730.
49. + T cells during the primary immune response to Epstein-Barr virus In vivo. J. Exp. Med. 187: 1395-1402.
50. Misko, I. S., S. M. Cross, R. Khanna, S. L. Elliott, C. Schmidt, S. J. Pye, and S. L. Silins. 1999. Crossreactive recognition of viral, self, and bacterial peptide ligands by human class I-restricted cytotoxic T lymphocyte clonotypes: implications for molecular mimicry in autoimmune disease. Proc. Natl. Acad. Sci. USA 96: 2279-2284.
51. Oldstone, M. B., M. Nerenberg, P. Southern, J. Price, and H. Lewicki. 1991. Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: role of anti-self (virus) immune response. Cell 65: 319-331.
52. + T-cell function in X-linked lymphoproliferative disease is restricted to SLAM family-positive B-cell targets. Blood 116: 3249-3257.
53. Burrows, S. R., S. J. Rodda, A. Suhrbier, H. M. Geysen, and D. J. Moss. 1992. The specificity of recognition of a cytotoxic T lymphocyte epitope. Eur. J. Immunol. 22: 191-195.
54. Kuwana, Y., M. Takei, M. Yajima, K. Imadome, H. Inomata, M. Shiozaki, N. Ikumi, T. Nozaki, H. Shiraiwa, N. Kitamura, et al. 2011. Epstein-Barr virus induces erosive arthritis in humanized mice. PLoS ONE 6: e26630. Available at: http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0026630.
55. Nejentsev, S., J. M. M. Howson, N. M. Walker, J. Szeszko, S. F. Field, H. E. Stevens, P. Reynolds, M. Hardy, E. King, J. Masters, et al; Wellcome Trust Case Control Consortium. 2007. Localization of type 1 diabetes susceptibility to the MHC class I genes HLA-B and HLA-A. Nature 450: 887-892.