HLA-DR15-derived self-peptides are involved in increased autologous T cell proliferation in multiple sclerosis

Brain

Volumn 136, Issue 6, 2013, Pages 1783-1798

  Mohme, Malte ^a   Hotz, Christian ^b   Stevanović, Stefan ^b   Binder, Thomas ^a   Lee, Jar How ^c   Okoniewski, Michal ^d,e   Eiermann, Thomas ^a   Sospedra, Mireia ^a,d   Rammensee, Hans Georg ^b   Martin, Roland ^a,d  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c One Lambda Inc   (United States)

^d UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^e FUNCTIONAL GENOMICS CENTER ZURICH   (Switzerland)

Author keywords

autologous T cell proliferation; HLA DR15; homeostatic proliferation; multiple sclerosis; self peptides

Indexed keywords

HLA DR15 ANTIGEN;

AGED; ARTICLE; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; ELUTION; GENETIC ASSOCIATION; GENETIC RISK; HAPLOTYPE; HUMAN; HUMAN CELL; IN VITRO STUDY; MAJOR CLINICAL STUDY; MULTIPLE SCLEROSIS; PRIORITY JOURNAL; T LYMPHOCYTE;

EID: 84878841826     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt108     Document Type: Article

References (67)

1. Amel Kashipaz MR, Huggins ML, Powell RJ, Todd I. Human autologous mixed lymphocyte reaction as an in vitro model for autoreactivity to apoptotic antigens. Immunology 2002; 107: 358-65.
2. Ashton-Rickardt PG, Bandeira A, Delaney JR, Van Kaer L, Pircher HP, Zinkernagel RM, et al. Evidence for a differential avidity model of T cell selection in the thymus. Cell 1994; 76: 651-63.
3. Baccala R, Theofilopoulos AN. The new paradigm of T-cell homeostatic proliferation-induced autoimmunity. Trends Immunol 2005; 26: 5-8.
4. Barcellos LF, Oksenberg JR, Begovich AB, Martin ER, Schmidt S, Vittinghoff E, et al. HLA-DR2 dose effect on susceptibility to multiple sclerosis and influence on disease course. Am J Hum Genet 2003; 72: 710-16.
5. Bielekova B, Muraro PA, Golestaneh L, Pascal J, McFarland HF, Martin R. Preferential expansion of autoreactive T lymphocytes from the memory T-cell pool by IL-7. J Neuroimmunol 1999; 100: 115-23.
6. Bielekova B, Sung MH, Kadom N, Simon R, McFarland H, Martin R. Expansion and functional relevance of high-avidity myelin-specific CD4 + T cells in multiple sclerosis. J Immunol 2004; 172: 3893-904.
7. Burns J, Bartholomew B, Lobo S. Isolation of myelin basic protein-specific T cells predominantly from the memory T-cell compartment in multiple sclerosis. Ann Neurol 1999; 45: 33-9.
8. Burroughs AK, Butler P, Sternberg MJ, Baum H. Molecular mimicry in liver disease. Nature 1992; 358: 377-8.
9. Cai G, Hafler DA. Multispecific responses by T cells expanded by endogenous self-peptide/MHC complexes. Eur J Immunol 2007; 37: 602-12.
10. Caillier SJ, Briggs F, Cree BA, Baranzini SE, Fernandez-Vina M, Ramsay PP, et al. Uncoupling the roles of HLA-DRB1 and HLADRB5 genes in multiple sclerosis. J Immunol 2008; 181: 5473-80.
11. Cella M, Engering A, Pinet V, Pieters J, Lanzavecchia A. Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature 1997; 388: 782-7.
12. Cournu-Rebeix I, Genin E, Leray E, Babron MC, Cohen J, Gout C, et al. HLA-DRB1 15 allele influences the later course of relapsing remitting multiple sclerosis. Genes Immun 2008; 9: 570-4.
13. Cox AL, Thompson SA, Jones JL, Robertson VH, Hale G, Waldmann H, et al. Lymphocyte homeostasis following therapeutic lymphocyte depletion in multiple sclerosis. Eur J Immunol 2005; 35: 3332-42.
14. Dengjel J, Schoor O, Fischer R, Reich M, Kraus M, Muller M, et al. Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc Natl Acad Sci USA 2005; 102: 7922-7.
15. Duszczyszyn DA, Beck JD, Antel J, Bar-Or A, Lapierre Y, Gadag V, et al. Altered naive CD4 and CD8 T cell homeostasis in patients with relapsing-remitting multiple sclerosis: thymic versus peripheral (non-thymic) mechanisms. Clin Exp Immunol 2006; 143: 305-13.
16. Duszczyszyn DA, Williams JL, Mason H, Lapierre Y, Antel J, Haegert DG. Thymic involution and proliferative T-cell responses in multiple sclerosis. J Neuroimmunol 2010; 221: 73-80.
17. Falk K, Rotzschke O, Stevanovic S, Jung G, Rammensee HG. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 1991; 351: 290-6.
18. Falk K, Rotzschke O, Stevanovic S, Jung G, Rammensee HG. Pool sequencing of natural HLA-DR, DQ, and DP ligands reveals detailed peptide motifs, constraints of processing, and general rules. Immunogenetics 1994; 39: 230-42.
19. Gronski MA, Boulter JM, Moskophidis D, Nguyen LT, Holmberg K, Elford AR, et al. TCR affinity and negative regulation limit autoimmunity. Nat Med 2004; 10: 1234-9.
20. Haegert DG. Multiple sclerosis: a disorder of altered T-cell homeostasis. Mult Scler Int 2011; 2011: 461304.
21. Haegert DG, Hackenbroch JD, Duszczyszyn D, Fitz-Gerald L, Zastepa E, Mason H, et al. Reduced thymic output and peripheral naive CD4 T-cell alterations in primary progressive multiple sclerosis (PPMS). J Neuroimmunol 2011; 233: 233-9.
22. Hafler DA, Buchsbaum M, Weiner HL. Decreased autologous mixed lymphocyte reaction in multiple sclerosis. J Neuroimmunol 1985; 9: 339-47.
23. Hao Y, Legrand N, Freitas AA. The clone size of peripheral CD8 T cells is regulated by TCR promiscuity. J Exp Med 2006; 203: 1643-9.
24. Hensiek AE, Sawcer SJ, Feakes R, Deans J, Mander A, Akesson E, et al. HLA-DR 15 is associated with female sex and younger age at diagnosis in multiple sclerosis. J Neurol Neurosurg Psychiatry 2002; 72: 184-7.
25. Hug A, Korporal M, Schroder I, Haas J, Glatz K, Storch-Hagenlocher B, et al. Thymic export function and T cell homeostasis in patients with relapsing remitting multiple sclerosis. J Immunol 2003; 171: 432-7.
26. Jersild C, Fog T, Hansen GS, Thomsen M, Svejgaard A, Dupont B. Histocompatibility determinants in multiple sclerosis, with special reference to clinical course. Lancet 1973; 2: 1221-5.
27. Kakalacheva K, Munz C, Lunemann JD. Viral triggers of multiple sclerosis. Biochim Biophys Acta 2011; 1812: 132-40.
28. Kieper WC, Burghardt JT, Surh CD. A role for TCR affinity in regulating naive T cell homeostasis. J Immunol 2004; 172: 40-4.
29. Klein L, Klugmann M, Nave KA, Tuohy VK, Kyewski B. Shaping of the autoreactive T-cell repertoire by a splice variant of self protein expressed in thymic epithelial cells. Nat Med 2000; 6: 56-61.
30. Kondo T, Cortese I, Markovic-Plese S, Wandinger KP, Carter C, Brown M, et al. Dendritic cells signal T cells in the absence of exogenous antigen. Nat Immunol 2001; 2: 932-8.
31. Krogsgaard M, Juang J, Davis MM. A role for "self" in T-cell activation. Semin Immunol 2007; 19: 236-44.
32. Lang HL, Jacobsen H, Ikemizu S, Andersson C, Harlos K, Madsen L, et al. A functional and structural basis for TCR cross-reactivity in multiple sclerosis. Nat Immunol 2002; 3: 940-3.
33. Laplaud DA, Ruiz C, Wiertlewski S, Brouard S, Berthelot L, Guillet M, et al. Blood T-cell receptor beta chain transcriptome in multiple sclerosis. Characterization of the T cells with altered CDR3 length distribution. Brain 2004; 127 (Pt 5): 981-95.
34. Lo WL, Felix NJ, Walters JJ, Rohrs H, Gross ML, Allen PM. An endogenous peptide positively selects and augments the activation and survival of peripheral CD4 + T cells. Nat Immunol 2009; 10: 1155-61.
35. Madsen LS, Andersson EC, Jansson L, krogsgaard M, Andersen CB, Engberg J, et al. A humanized model for multiple sclerosis using HLA-DR2 and a human T-cell receptor. Nat Genet 1999; 23: 343-7.
36. Markovic-Plese S, Cortese I, Wandinger KP, McFarland HF, Martin R. CD4 + CD28-costimulation-independent T cells in multiple sclerosis. J Clin Invest 2001; 108: 1185-94.
37. Martin R, Howell MD, Jaraquemada D, Flerlage M, Richert J, Brostoff S, et al. A myelin basic protein peptide is recognized by cytotoxic T cells in the context of four HLA-DR types associated with multiple sclerosis. J Exp Med 1991; 173: 19-24.
38. Martin R, Jaraquemada D, Flerlage M, Richert J, Whitaker J, Long EO, et al. Fine specificity and HLA restriction of myelin basic proteinspecific cytotoxic T cell lines from multiple sclerosis patients and healthy individuals. J Immunol 1990; 145: 540-8.
39. Massa M, Mazzoli F, Pignatti P, De Benedetti F, Passalia M, Viola S, et al. Proinflammatory responses to self HLA epitopes are triggered by molecular mimicry to Epstein-Barr virus proteins in oligoarticular juvenile idiopathic arthritis. Arthritis Rheum 2002; 46: 2721-9.
40. McFarland HF, Martin R. Multiple sclerosis: a complicated picture of autoimmunity. Nat Immunol ,2007, 8, 913-19.
41. Min B, Foucras G, Meier-Schellersheim M, Paul WE. Spontaneous proliferation, a response of naive CD4 T cells determined by the diversity of the memory cell repertoire. Proc Natl Acad Sci USA 2004; 101: 3874-9.
42. Muraro PA, Pette M, Bielekova B, McFarland HF, Martin R. Human autoreactive CD4 + T cells from naive CD45RA + and memory CD45RO + subsets differ with respect to epitope specificity and functional antigen avidity. J Immunol 2000; 164: 5474-81.
43. Naylor K, Li G, Vallejo AN, Lee WW, Koetz K, Bryl E, et al. The influence of age on T cell generation and TCR diversity. J Immunol 2005; 174: 7446-52.
44. Oksenberg JR, Baranzini SE, Sawcer S, Hauser SL. The genetics of multiple sclerosis: SNPs to pathways to pathogenesis. Nat Rev Genet 2008; 9: 516-26.
45. Olsen JV, de Godoy LM, Li G, Macek B, Mortensen P, Pesch R, et al. Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol Cell Proteomics 2005; 4: 2010-21.
46. Ota K, Matsui M, Milford EL, Mackin GA, Weiner HL, Hafler DA. T-cell recognition of an immunodominant myelin basic protein epitope in multiple sclerosis. Nature 1990; 346: 183-7.
47. Pette M, Fujita K, Kitze B, Whitaker JN, Albert E, Kappos L, et al. Myelin basic protein-specific T lymphocyte lines from MS patients and healthy individuals. Neurology 1990; 40: 1770-6.
48. Prat E, Tomaru U, Sabater L, Park DM, Granger R, Kruse N, et al. HLADRB5 0101 and-DRB1 1501 expression in the multiple sclerosisassociated HLA-DR15 haplotype. J Neuroimmunol 2005; 167: 108-19.
49. Quandt JA, Huh J, Baig M, Ito N, Bryan M, Kawamura K, et al. Myelin basic protein-specific TCR/HLA-DRB5 01:01 transgenic mice support the etiologic role of DRB5 01:01 in multiple sclerosis. J Immunol 2012; 189: 2897-908.
50. Ramagopalan SV, Morris AP, Dyment DA, Herrera BM, DeLuca GC, Lincoln MR, et al. The inheritance of resistance alleles in multiple sclerosis. PLoS Genet 2007; 3: 1607-13.
51. Rudd BD, Venturi V, Li G, Samadder P, Ertelt JM, Way SS, et al. Nonrandom attrition of the naive CD8 + T-cell pool with aging governed by T-cell receptor:pMHC interactions. Proc Natl Acad Sci USA 2011; 108: 13694-9.
52. Sawcer S, Hellenthal G, Pirinen M, Spencer CC, Patsopoulos NA, Moutsianas L, et al. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 2011; 476: 214-19.
53. Schild H, Rotzschke O, Kalbacher H, Rammensee HG. Limit of T cell tolerance to self proteins by peptide presentation. Science 1990; 247: 1587-9.
54. Sospedra M, Martin R. Immunology of multiple sclerosis. Annu Rev Immunol 2005; 23: 683-747.
55. Sospedra M, Muraro PA, Stefanova I, Zhao Y, Chung K, Li Y, et al. Redundancy in antigen-presenting function of the HLA-DR and-DQ molecules in the multiple sclerosis-associated HLA-DR2 haplotype. J Immunol 2006; 176: 1951-61.
56. Sospedra M, Zhao Y, zur Hausen H, Muraro PA, Hamashin C, de Villiers EM, et al. Recognition of conserved amino acid motifs of common viruses and its role in autoimmunity. PLoS Pathog 2005; 1: e41.
57. Sprent J, Surh CD. Normal T cell homeostasis: the conversion of naive cells into memory-phenotype cells. Nat Immunol 2011; 12: 478-84.
58. Sundberg EJ, Deng L, Mariuzza RA. TCR recognition of peptide/MHC class II complexes and superantigens. Semin Immunol 2007; 19: 262-71.
59. Valli A, Sette A, Kappos L, Oseroff C, Sidney J, Miescher G, et al. Binding of myelin basic protein peptides to human histocompatibility leukocyte antigen class II molecules and their recognition by T cells from multiple sclerosis patients. J Clin Invest 1993; 91: 616-28.
60. Viglietta V, Baecher-Allan C, Weiner HL, Hafler DA. Loss of functional suppression by CD4 + CD25 + regulatory T cells in patients with multiple sclerosis. J Exp Med 2004; 199: 971-9.
61. Vogt AB, Kropshofer H, Kalbacher H, Kalbus M, Rammensee HG, Coligan JE, et al. Ligand motifs of HLA-DRB5 0101 and DRB1 1501 molecules delineated from self-peptides. J Immunol 1994; 153: 1665-73.
62. Wang P, Sidney J, Dow C, Mothe B, Sette A, Peters B. A systematic assessment of MHC class II peptide binding predictions and evaluation of a consensus approach. PLoS Comput Biol 2008; 4: e1000048.
63. Wucherpfennig KW, Gagnon E. Positively selecting peptides: their job does not end in the thymus. Nat Immunol 2009; 10: 1143-4.
64. Wucherpfennig KW, Sette A, Southwood S, Oseroff C, Matsui M, Strominger JL, et al. Structural requirements for binding of an immunodominant myelin basic protein peptide to DR2 isotypes and for its recognition by human T cell clones. J Exp Med 1994; 179: 279-90.
65. Wucherpfennig KW, Strominger JL. Molecular mimicry in T cell-mediated autoimmunity: viral peptides activate human T cell clones specific for myelin basic protein. Cell 1995; 80: 695-705.
66. Yousef S, Planas R, Chakroun K, Hoffmeister-Ullerich S, Binder TM, Eiermann TH, et al. TCR bias and HLA cross-restriction are strategies of human brain-infiltrating JC virus-specific CD4 + T cells during viral infection. J Immunol 2012; 189: 3618-30.
67. Zipp F, Windemuth C, Pankow H, Dichgans J, Wienker T, Martin R, et al. Multiple sclerosis associated amino acids of polymorphic regions relevant for the HLA antigen binding are confined to HLA-DR2. Hum Immunol 2000; 61: 1021-30.