Molecular mimicry and multiple sclerosis: Degenerate T-cell recognition and the induction of autoimmunity

Annals of Neurology

Volumn 45, Issue 5, 1999, Pages 559-567

  Gran, Bruno ^a   Hemmer, Bernhard ^b   Vergelli, Marco ^c   McFarland, Henry F ^a   Martin, Roland ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MYELIN BASIC PROTEIN; PROTEOLIPID PROTEIN; T LYMPHOCYTE RECEPTOR;

ALLERGIC ENCEPHALOMYELITIS; ANTIGEN RECOGNITION; ARTICLE; AUTOIMMUNITY; CELL CLONING; CROSS REACTION; HUMAN; IMMUNOPATHOGENESIS; LYMPHOCYTE COUNT; MOLECULAR DYNAMICS; MOLECULAR MIMICRY; MULTIPLE SCLEROSIS; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; T LYMPHOCYTE;

EID: 0032915806     PISSN: 03645134     EISSN: None     Source Type: Journal    
DOI: 10.1002/1531-8249(199905)45:5<559::AID-ANA3>3.0.CO;2-Q     Document Type: Article

References (93)

1. Martin R, McFarland HF, McFarlin DE. Immunological aspects of demyelinating diseases. Annu Rev Immunol 1992;10: 153-187
2. Fujinami RS, Oldstone MBA. Amino acid homology between the encephalitogenic site of myelin basic protein and virus: mechanism for autoimmunity. Science 1985;230:1043-1045
3. Oldstone MBA. Molecular mimicry and autoimmune disease. Cell 1987;50:819-820
4. Traugott U, Reinherz EL, Raine CS. Multiple sclerosis. Distribution of T cells, T cell subsets and Ia-positive macrophages in lesions of different ages. J Neuroimmunol 1983;4:201-221
5. Hvas J, Oksenberg JR, Fernando R, et al. Gamma delta T cell receptor repertoire in brain lesions of patients with multiple sclerosis. J Neuroimmunol 1993;46:225-234
6. Esiri MM. Multiple sclerosis: a quantitative and qualitative study of immunoglobulin-containing cells in the central nervous system. Neuropathol Appl Neurobiol 1980;6:9-21
7. Vartdal F, Sollid LM, Vandvik B, et al. Patients with multiple sclerosis carry DQB1 genes which encode shared polymorphic aminoacid sequences. Hum Immunol 1989;25:103-110
8. Naito S, Kuroiwa Y, Itoyama T, et al. HLA and Japanese MS. Tissue Antigens 1978;12:19-24
9. Marrosu HG, Muntoni F, Murru MR, et al. Sardinian multiple sclerosis is associated with HLA-DR4: a serological and molecular analysis. Neurology 1988;38:1749-1753
10. Sawcer S, Jones HB, Feakes R, et al. A genome screen in multiple sclerosis reveals susceptibility loci on chromosome 6p21 and 17q22. Nat Genet 1996;13:464-468
11. Haines JL, Ter-Minassian M, Bazyk A, et al. A complete genomic screen for multiple sclerosis underscores a role for the major histocompatibility complex. The Multiple Sclerosis Genetics Group. Nat Genet 1996;13:469-471
12. Ebers GC, Kukay K, Bulman DE, et al. A full genome search in multiple sclerosis. Nat Genet 1996;13:472-476
13. Paty DW, Li DKB, UBC MS/MRI Study Group and the IFNB Multiple Sclerosis Study Group. Interferon beta-1b is effective in relapsing-remitting multiple sclerosis. II. MRI analysis results of a multicenter, randomized, double-blind, placebo-controlled trial. Neurology 1993;43:662-667
14. The Interferon-Beta Multiple Sclerosis Study Group. Interferon beta-1b is effective in relapsing-remitting multiple sclerosis. I. Clinical results of a multicenter, randomized, double-blind, placebo-controlled trial. Neurology 1993;43:655-661
15. Weiner HL, Mackin GA, Orav EJ, the NCMST. Intermittent cyclophosphamide pulse therapy in progressive multiple sclerosis: final report of the Northeast Cooperative Multiple Sclerosis Treatment Group. Neurology 1993;43:910-918
16. Panitch HS, Hirsch RL, Schindler J, Johnson KP. Treatment of multiple sclerosis with gamma interferon: exacerbations associated with activation of the immune system. Neurology 1987; 37:1097-1102
17. Lucchinetti CF, Bruck W, Rodriguez M, Lassmann H. Distinct patterns of multiple sclerosis pathology indicates heterogeneity on pathogenesis. Brain Pathol 1996;6:259-274
18. Raine CS. The neuropathology of multiple sclerosis. In: Raine CS, McFarland HF, Tourtellotte WW, eds. Multiple sclerosis: clinical and pathogenetic basis. London, Chapman and Hall, 1997:151-171
19. Raine CS. The lesion in multiple sclerosis and chronic relapsing experimental allergic encephalomyelitis: a structural comparison. In: Raine CS, McFarland HF, Tourtellotte WW, eds. Multiple sclerosis: clinical and pathogenetic basis. London, Chapman and Hall, 1997:243-286
20. Schlüsener H, Wekerle H. Autoaggressive T lymphocyte lines recognize the encephalitogenic region of myelin basic protein; in vitro selection from unprimed rat T lymphocyte populations. J Immunol 1985;135:3128-3133
21. Fritz RB, Skeen MJ, Jen-Chou CH, et al. Major histocompatibitity complex-linked control of the murine immune response to myelin basic protein. J Immunol 1985;134:2328-2332
22. Wekerle H, Linington C, Lassmann H, Meyermann R. Cellular immune reactivity within the CNS. Trends Neurosci 1986;9: 271-277
23. Burns J, Rosenzweig A, Zweiman B, Lisak RP. Isolation of myelin basic protein-reactive T-cell lines from normal human blood. Cell Immunol 1983;81:435-440
24. Martin R, Jaraquemada D, Flerlage M, et al. Fine specificity and HLA restriction of myelin basic protein-specific cytotoxic T cell lines from multiple sclerosis patients and healthy individuals. J Immunol 1990;145:540-548
25. Pette M, Fujita K, Kitze B, et al. Myelin basic protein-specific T lymphocyte lines from MS patients and healthy individuals. Neurology 1990;40:1770-1776
26. Zhang J, Markovic-Plese S, Lacet B, et al. Increased frequency of interleukin-2-responsive T cells specific for myelin basic protein in peripheral blood and cerebrospinal fluid of patients with multiple sclerosis. J Exp Med 1994;179:973-984
27. Ota K, Matsui M, Milford EL, et al. T-cell recognition of an immunodominant myelin basic protein epitope in multiple sclerosis. Nature 1990;346:183-187
28. Sibley WA, Bamford CR, Clark K. Clinical viral infections and multiple sclerosis. Lancet 1985;1:1313-1315
29. Panitch HS. Influence of infection on exacerbations of multiple sclerosis. Ann Neurol 1994;36(Suppl):S25-28
30. Kurtzke JF. Epidemiologic evidence for multiple sclerosis as an infection. Clin Microbiol Rev 1993;6:382-427
31. Talbot PJ, Paquette J-S, Ciurli C, et al. Myelin basic protein and human coronavirus 229E cross-reactive T cells in multiple sclerosis. Ann Neurol 1996;39:233-240
32. Zinkernagel RM, Doherty PC. Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature 1974;248:701-702
33. Germain RN. MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell 1994;76:287-299
34. Croft M. Activation of naive, memory and effector T cells. Curr Opin Immunol 1994;6:431-437
35. Olsson T. Cytokine-producing cells in experimental autoimmune encephalomyelitis and multiple sclerosis. Neurology 1995; 45(Suppl 6):S11-S15
36. Dubey C, Croft M, Swain SL. Naive and effector CD4 T cells differ in their requirements for T cell receptor versus costimulatory signals. J Immunol 1996;157:3280-3289
37. Gautam AM, Liblau R, Chelvanayagam G, et al. A viral peptide with limited homology to a self peptide can induce clinical signs of experimental autoimmune encephalomyelitis. J Immunol 1998;161:60-64
38. van Eden W, Hogervorst EJ, Hensen EJ, et al. A cartilage-mimicking T-cell epitope on a 65K mycobacterial heat-shock protein: adjuvant arthritis as a model for human rheumatoid arthritis. Curr Top Microbiol Immunol 1989;145:27-43
39. Davies JM. Molecular mimicry: can epitope mimicry induce autoimmune disease? Immunol Cell Biol 1997;75:113-126
40. Hammer J, Valsasnini P, Tolba K, et al. Promiscuous and allele-specific anchors in HLA-DR binding peptides. Cell 1993; 74:197-203
41. Evavold BD, Sloan-Lancaster J, Hsu BL, Allen PM. Separation of T helper 1 clone cytolysis from proliferation and lymphokine production using analog peptides. J Immunol 1993;150:3131-3140
42. Kersh GJ, Allen PM. Structural basis for T cell 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
43. von Boehmer H, Kisielow P. Self-nonself discrimination by T cells. Science 1990;248:1369-1373
44. Vogt AB, Kropshofer H, Kalbacher H, et al. Ligand motifs of HLA-DRB5*0101 and DRB1*1501 molecules delineated from self-peptides. J Immunol 1994;153:1665-1673
45. Wucherpfennig KW, Sette A, Southwood S, 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;179:279-290
46. 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
47. Vergelli M, Hemmer B, Utz U, et al. Differential activation of human autoreactive T cell clones by altered peptide ligands derived from myelin basic protein peptide (87-99). Eur J Immunol 1996;26:2624-2634
48. Vergelli M, Hemmer B, Kalbus M, et al. Modifications of peptide ligands enhancing T cell responsiveness imply large numbers of stimulatory ligands for autoreactive T cells. J Immunol 1997;158:3746-3752
49. Hemmer B, Vergelli M, Gran B, et al. Predictable TCR antigen recognition based on peptide scans leads to the identification of agonise ligands with no sequence homology. J Immunol 1998; 160:3631-3636
50. Ausubel LJ, Kwan CK, Sette A, et al. Complementary mutations in an antigenic peptide allow for crossreactivity of autoreactive T-cell clones. Proc Natl Acad Sci USA 1996;93:15317-15322
51. Houghten RA, Pinilla C, Blondelle SE, et al. Generation and use of synthetic peptide combinatorial libraries for basic research and drug discovery. Nature 1991;354:84-86
52. Udaka K, Wiesmüller K-H, Kienle S, et al. Decrypting the structure of major histocompatibility complex class 1-restricted cytotoxic T lymphocyte epitopes with complex peptide libraries. J Exp Med 1995;181:2097-2108
53. Hemmer B, Vergelli M, Pinilla C, et al. Probing degeneracy in T-cell recognition using combinatorial peptide libraries. Immunol Today 1998;19:163-168
54. Hemmer B, Fleckenstein B, Vergelli M, et al. Identification of high potency microbial and self ligands for a human autoreactive class II-restricted T cell clone. J Exp Med 1997;185:1651-1659
55. Mason D. A very high level of crossreactivity is an essential feature of the T-cell receptor. Immunol Today 1998;19:395-404
56. Evavold BD, Allen PM. Separation of IL-4 production from Th cell proliferation by an altered T cell receptor ligand. Science 1991;252:1308-1310
57. Hemmer B, Stefanova I, Vergelli M, et al. Relationships among TCR ligand potency, thresholds for effector function elicitation, and the quality of early signaling events in human T cells. J Immunol 1998;160:5807-5814
58. Sloan-Lancaster J, Allen PM. Altered peptide ligand-induced partial T cell activation: molecular mechanisms and role in T cell biology. Annu Rev Immunol 1996;14:1-27
59. Wekerle H, Bradl M, Linington C, et al. The shaping of the brain-specific T lymphocyte repertoire in the thymus. Immunol Rev 1996;149:231-243
60. Nossal GJ. Negative selection of lymphocytes. Cell 1994;76: 229-239
61. von Boehmer H. Positive selection of lymphocytes. Cell 1994; 76:219-228
62. Ashton-Rickardt PG, Bandeira A, Delaney JR, et al. Evidence for a differential avidity model of T cell selection in the thymus. Cell 1994;76:651-663
63. Ashton-Rickardt PG, Tonegawa S. A differential-avidity model for T-cell selection. Immunol Today 1994;15:362-366
64. Jameson SC, Bevan MJ. T-cell selection. Curr Opin Immunol 1998;10:214-219
65. Rudensky AY. Endogenous peptides associated with MHC class II and selection of CD4 T cells. Semin Immunol 1995;7:399-409
66. Fritz RB, Zhao M-L. Thymic expression of myelin basic protein (MBP). Activation of MBP-specific T cells by thymic cells in the absence of exogenous MBP. J Immunol 1996;157:5249-5253
67. Mor F, Boccaccio GL, Unger T. Expression of autoimmune disease-related antigens by cells of the immune system. J Neurosci Res 1998;54:254-262
68. Sospedra M, Ferrer-Francesch X, Dominguez O, et al. Transcription of a broad range of self-antigens in human thymus suggests a role for central mechanisms in tolerance toward peripheral antigens. J Immunol 1998;161:5918-5929
69. Egwuagu CE, Charukamnoetkanok P, Gery I. Thymic expression of autoantigens correlates with resistance to autoimmune disease. J Immunol 1997;159:3109-3112
70. Heath VL, Moore NC, Parnell SM, Mason DW. Intrathymic expression of genes involved in organ specific autoimmune disease. J Autoimmun 1998;11:309-318
71. Heath VL, Saoudi A, Seddon BP, et al. The role of the thymus in the control of autoimmunity. J Autoimmun 1996;9:241-246
72. Fairchild PJ, Wildgoose R, Atherton E, et al. An autoantigenic T cell epitope forms unstable complexes with class II MHC: a novel route for escape from tolerance induction. Int Immunol 1993;5:1151-1158
73. Zal T, Volkmann A, Stockinger B. Mechanisms of tolerance induction in major histocompatibility complex class II-restricted T cells specific for a blood-borne self-antigen. J Exp Med 1994;180:2089-2099
74. Bevan MJ. In thymic selection, peptide diversity gives and takes away. Immunity 1997;7:175-178
75. Ignatowicz L, Kappler J, Marrack P. The repertoire of T cells shaped by a single MHC/peptide ligand. Cell 1996;84:521-529
76. Hu Q, Bazemore Walker CR, Girao C, et al. Specific recognition of thymic self-peptides induces the positive selection of cytotoxic T lymphocytes. Immunity 1997;7:221-231
77. Kirberg J, Berns A, von Boehmer H. Peripheral T cell survival requires continual ligation of the T cell receptor to major histocompatibility complex-encoded molecules. J Exp Med 1997; 186:1269-1275
78. Lohse AW, Dinkelmann M, Kimmig M, et al. Estimation of the frequency of self-reactive T cells in health and inflammatory diseases by limiting dilution analysis and single cell cloning. J Autoimmun 1996;9:667-675
79. Dutton RW, Bradley LM, Swain SL. T cell memory. Annu Rev Immunol 1998;16:201-223
80. Traugott U, Scheinberg LC, Raine CS. On the presence of Ia-positive endothelial cells and astrocytes in multiple sclerosis lesions and its relevance to antigen presentation. J Neuroimmunol 1985;8:1-14
81. De Simone R, Giampaolo A, Giometto B, et al. The costimulatory molecule B7 is expressed on human microglia in culture and in multiple sclerosis acute lesions. J Neuropathol Exp Neurol 1995;54:175-187
82. Horwitz MS, Bradley LM, Harbertson J, et al. Diabetes induced by Coxsackie virus: initiation by bystander damage and not molecular mimicry. Nat Med 1998;4:781-785
83. Evans CF, Horwitz MS, Hobbs MV, Oldstone MBA. Viral infection of transgenic mice expressing a viral protein in oligodendrocytes leads to chronic central nervous system autoimmune disease. J Exp Med 1996;184:2371-2384
84. Targoni OS, Lehmann PV. Endogenous myelin basic protein inactivates the high avidity T cell repertoire. J Exp Med 1998; 187:2055-2063
85. Lee SC, Raine CS. Multiple sclerosis: oligodendrocytes in active lesions do not express class II major histocompatibility complex molecules. J Neuroimmunol 1989;25:261-266
86. Ohashi PS, Oehen S, Buerki K, et al. Ablation of "tolerance" and induction of diabetes by virus infection in viral antigen transgenic mice. Cell 1991;65:305-317
87. Oldstone MBA, Nerenberg M, Southern P, et al. Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: role of anti-self (virus) immune response. Cell 1991;65: 319-331
88. Johnson RT. The virology of demyelinating diseases. Ann Neurol 1994;36(Suppl):S54-S60
89. Sobel RA, Hafler DA, Castro EE, et al. The 2H4 (CD45R) antigen is selectively decreased in multiple sclerosis lesions. J Immunol 1988;140:2210-2214
90. Bevilacqua MP. Endothelial-leukocyte adhesion molecules. Annu Rev Immunol 1993;11:767-804
91. Cannella B, Cross AH, Raine CS. Adhesion-related molecules in the central nervous system. Upregulation correlates with inflammatory cell influx during relapsing experimental autoimmune encephalomyelitis. Lab Invest 1991;65:23-31
92. Lehmann PV, Forsthuber T, Miller A, Sercarz EE. Spreading of T-cell autoimmunity to cryptic determinants of an autoantigen. Nature 1992;358:155-157
93. Vanderlugt CJ, Miller SD. Epitope spreading. Curr Opin Immunol 1996;8:831-836