Immune tolerance in multiple sclerosis

Immunological Reviews

Volumn 241, Issue 1, 2011, Pages 228-240

  Goverman, Joan M ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

EAE; Multiple sclerosis; Myelin; Tolerance

Indexed keywords

HLA A2 ANTIGEN; HLA A3 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYELIN; MYELIN BASIC PROTEIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; PROTEOLIPID PROTEIN; T LYMPHOCYTE RECEPTOR;

ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; AUTOIMMUNITY; BINDING AFFINITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL INTERACTION; CELL ISOLATION; GENE LOCUS; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOPATHOGENESIS; MAJOR HISTOCOMPATIBILITY COMPLEX; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; THYMOCYTE; THYMUS;

ANIMALS; AUTOANTIGENS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CLONAL DELETION; HUMANS; IMMUNE TOLERANCE; MULTIPLE SCLEROSIS; MYELIN BASIC PROTEINS; T-LYMPHOCYTES, REGULATORY;

EID: 79954557114     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2011.01016.x     Document Type: Review

References (83)

1. Goverman J. Autoimmune T cell responses in the central nervous system. Nat Rev Immunol 2009;9:393-407.
2. Stromnes IM, Goverman JM. Active induction of experimental allergic encephalomyelitis. Nat Protocols 2006;1:1810-1819.
3. Raine C. 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.
4. Goverman J, Perchellet A, Huseby ES. The role of CD8(+) T cells in multiple sclerosis and its animal models. Curr Drug Targets Inflamm Allergy 2005;4:239-245.
5. + T cells in multiple sclerosis: a new target for therapy? Brain 2005;128:1747-1763.
6. + T cells in multiple sclerosis revealed by novel flow cytometric assay. Blood 2004;103:4222-4231.
7. Akirav EM, Ruddle NH, Herold KC. The role of AIRE in human autoimmune disease. Nat Rev Endocrinol 2011;7:25-33.
8. Gardner JM, Fletcher AL, Anderson MS, Turley SJ. AIRE in the thymus and beyond. Curr Opin Immunol 2009;21:582-589.
9. Weller RO, Engelhardt B, Phillips MJ. Lymphocyte targeting of the central nervous system: a review of afferent and efferent CNS-immune pathways. Brain Pathol 1996;6:275-288.
10. Nave KA, Milner RJ. Proteolipid proteins: structure and genetic expression in normal and myelin-deficient mutant mice. Crit Rev Neurobiol 1989;5:65-91.
11. Agrawal HC, Burton RM, Fishman MA, Mitchell RF, Prensky AL. Partial characterization of a new myelin protein component. J Neurochem 1972;19:2083-2089.
12. Nave KA, Lai C, Bloom FE, Milner RJ. Splice site selection in the proteolipid protein (PLP) gene transcript and primary structure of the DM-20 protein of central nervous system myelin. Proc Natl Acad Sci USA 1987;84:5665-5669.
13. Agrawal HC, Agrawal D. Proteolipid protein and DM-20 are synthesized by Schwann cells, present in myelin membrane, but they are not fatty acylated. Neurochem Res 1991;16:855-858.
14. Lemke G. Myelin and Myelination. In: Hall ZW ed. An Introduction to Molecular Neurobiology. Sunderland, Massachusetts: Sinauer Associates, Inc, 1992:281-309.
15. Anderson AC, Nicholson LB, Legge KL, Turchin V, Zaghouani H, Kuchroo VK. High frequency of autoreactive myelin proteolipid protein-specific T cells in the periphery of naive mice: mechanisms of selection of the self-reactive repertoire. J Exp Med 2000;191:761-770.
16. 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.
17. Waldner H, Whitters MJ, Sobel RA, Collins M, Kuchroo VK. Fulminant spontaneous autoimmunity of the central nervous system in myelin proteolipid protein specific T cell receptor transgenic mice. Proc Natl Acad Sci USA 2000;28:3412-3417.
18. Zhang H, Podojil JR, Luo X, Miller SD. Intrinsic and induced regulation of the age-associated onset of spontaneous experimental autoimmune encephalomyelitis. J Immunol 2008;181:4638-4647.
19. Iglesias A, Bauer J, Litzenburger T, Schubart A, Linington C. T- and B-cell responses to myelin oligodendrocyte glycoprotein in experimental autoimmune encephalomyelitis and multiple sclerosis. Glia 2001;36:220-234.
20. Derbinski J, Schulte A, Kyewski B, Klein L. Promiscuous gene expression in medullary thymic epithelial cells mirrors the peripheral self. Nat Immunol 2001;2:1032-1039.
21. Delarasse C, et al. Myelin/oligodendrocyte glycoprotein-deficient (MOG-deficient) mice reveal lack of immune tolerance to MOG in wildtype mice. J Clin Invest 2003;112:544-553.
22. Bettelli E, Pagany M, Weiner HL, Linington C, Sobel RA, Kuchroo VK. Myelin oligodendrocyte glycoprotein-specific T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J Exp Med 2003;197:1073-1081.
23. Pollinger B, et al. Spontaneous relapsing-remitting EAE in the SJL/J mouse: MOG-reactive transgenic T cells recruit endogenous MOG-specific B cells. J Exp Med 2009;206:1303-1316.
24. Lemke G. Unwrapping the genes of myelin. Neuron 1988;1:535-543.
25. Zelenika D, Grima B, Pessac B. A new family of transcripts of the myelin basic protein gene: expression in brain and in immune system. J Neurochem 1993;60:1574-1577.
26. Givogri MI, Bongarzone ER, Campagnoni AT. New insights on the biology of myelin basic protein gene: the neural- immune connection. J Neurosci Res 2000;59:153-159.
27. Campagnoni AT, et al. Structure and developmental regulation of Golli-mbp, a 105-kilobase gene that encompasses the myelin basic protein gene and is expressed in cells in the oligodendrocyte lineage in the brain. J Biol Chem 1993;268:4930-4938.
28. Feng JM, et al. Golli protein negatively regulates store depletion-induced calcium influx in T cells. Immunity 2006;24:717-727.
29. Paez PM, Spreuer V, Handley V, Feng JM, Campagnoni C, Campagnoni AT. Increased expression of golli myelin basic proteins enhances calcium influx into oligodendroglial cells. J Neurosci 2007;27:12690-12699.
30. Mathisen PM, Pease S, Garvey J, Hood L, Readhead C. Identification of an embryonic isoform of myelin basic protein that is expressed widely in the mouse embryo. Proc Natl Acad Sci USA 1993;90:10125-10129.
31. Barbarese E, Carson JH, Braun PE. Accumulation of the four myelin basic proteins in mouse brain during development. J Neurochem 1978;31:779-782.
32. Pitchekian-Halabi H, Campagnoni CW, Skinner E, Kampf K, Campagnoni AT, Voskuhl RR. Strain-related differences in the ability of T lymphocytes to recognize proteins encoded by the golli-myelin basic protein gene. J Neuroimmunol 1996;68:121-129.
33. Maverakis E, et al. Immunogenicity of self antigens is unrelated to MHC-binding affinity: T-cell determinant structure of Golli-MBP in the BALB/c mouse. J Autoimmun 2000;15:315-322.
34. Tranquill LR, et al. Human T lymphocytes specific for the immunodominant 83-99 epitope of myelin basic protein: recognition of golli MBP HOG 7. J Neurosci Res 1996;45:820-828.
35. Maverakis E, Beech JT, Schneider S, Sercarz EE. Presentation of a determinant by MHC class II can be prevented through competitive capture by a flanking determinant on a multideterminant peptide. J Autoimmun 2008;31:59-65.
36. Goverman J, Woods A, Larson L, Weiner LP, Hood L, Zaller DM. Transgenic mice that express a myelin basic protein-specific T cell receptor develop spontaneous autoimmunity. Cell 1993;72:551-560.
37. Liu GY, Fairchild PJ, Smith RM, Prowle JR, Kioussis D, Wraith DC. Low avidity recognition of self-antigen by T cells permits escape from central tolerance. Immunity 1995;3:407-415.
38. Lafaille JJ, Nagashima K, Katsuki M, Tonegawa S. High incidence of spontaneous autoimmune encephalomyelitis in immunodeficient anti-myelin basic protein T cell receptor transgenic mice. Cell 1994;78:399-408.
39. Fairchild PJ, Wildgoose R, Atherton E, Webb S, Wraith DC. 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.
40. Mason K, Denney DW Jr, McConnell HM. Kinetics of the reaction of a myelin basic protein peptide with soluble IAu. Biochemistry 1995;34:14874-14878.
41. Lee C, et al. Evidence that the autoimmune antigen myelin basic protein (MBP) Ac1-9 binds towards one end of the major histocompatibility complex (MHC) cleft. J Exp Med 1998;187:1505-1516.
42. He XL, Radu C, Sidney J, Sette A, Ward ES, Garcia KC. Structural snapshot of aberrant antigen presentation linked to autoimmunity: the immunodominant epitope of MBP complexed with I-Au. Immunity 2002;17:83-94.
43. Goebels N, Hofstetter H, Schmidt S, Brunner C, Wekerle H, Hohlfeld R. Repertoire dynamics of autoreactive T cells in multiple sclerosis patients and healthy subjects: epitope spreading versus clonal persistence. Brain 2000;123(Pt 3):508-518.
44. Wucherpfennig KW, et al. Clonal expansion and persistence of human T cells specific for an immunodominant myelin basic protein peptide. J Immunol 1994;152:5581-5592.
45. Wucherpfennig KW, 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. Vergelli M, et al. T cell response to myelin basic protein in the context of the multiple sclerosis-associated HLA-DR15 haplotype: peptide binding, immunodominance and effector functions of T cells. J Neuroimmunol 1997;77:195-203.
47. Manoury B, et al. Destructive processing by asparagine endopeptidase limits presentation of a dominant T cell epitope in MBP. Nat Immunol 2002;3:169-174.
48. Krogsgaard M, et al. Visualization of myelin basic protein (MBP) T cell epitopes in multiple sclerosis lesions using a monoclonal antibody specific for the human histocompatibility leukocyte antigen (HLA)-DR2-MBP 85-99 complex. J Exp Med 2000;191:1395-1412.
49. Dupouey P, Jacque C, Bourre JM, Cesselin F, Privat A, Baumann N. Immunochemical studies of myelin basic protein in shiverer mouse devoid of major dense line of myelin. Neurosci Lett 1979;12:113-118.
50. Kirschner DA, Ganser AL. Compact myelin exists in the absence of basic protein in the shiverer mutant mouse. Nature 1980;283:207-210.
51. Roach A, Takahashi N, Pravtcheva D, Ruddle F, Hood L. Chromosomal mapping of mouse myelin basic protein gene and structure and transcription of the partially deleted gene in shiverer mutant mice. Cell 1985;42:149-155.
52. Harrington CJ, et al. Differential tolerance is induced in T cells recognizing distinct epitopes of myelin basic protein. Immunity 1998;8:571-580.
53. Loftus C, Huseby E, Gopaul P, Beeson C, Goverman J. Highly cross-reactive T cell responses to myelin basic protein epitopes reveal a nonpredictable form of TCR degeneracy. J Immunol 1999;162:6451-6457.
54. Targoni OS, Lehmann PV. Endogenous myelin basic protein inactivates the high avidity T cell repertoire. J Exp Med 1998;187:2055-2063.
55. Yoshizawa I, Bronson R, Dorf ME, Abromson-Leeman S. T-cell responses to myelin basic protein in normal and MBP-deficient mice. J Neuroimmunol 1998;84:131-138.
56. Seamons A, et al. Competition between two MHC binding registers in a single peptide processed from myelin basic protein influences tolerance and susceptibility to autoimmunity. J Exp Med 2003;197:1391-1397.
57. Huseby ES, Sather B, Huseby PG, Goverman J. Age-dependent T cell tolerance and autoimmunity to myelin basic protein. Immunity 2001;14:471-481.
58. Van de Keere F, Tonegawa S. CD4(+) T cells prevent spontaneous experimental autoimmune encephalomyelitis in anti-myelin basic protein T cell receptor transgenic mice. J Exp Med 1998;188:1875-1882.
59. Olivares-Villagomez D, Wang Y, Lafaille JJ. Regulatory CD4(+) T cells expressing endogenous T cell receptor chains protect myelin basic protein-specific transgenic mice from spontaneous autoimmune encephalomyelitis. J Exp Med 1998;188:1883-1894.
60. Furtado GC, Olivares-Villagomez D, Curotto de Lafaille MA, Wensky AK, Latkowski JA, Lafaille JJ. Regulatory T cells in spontaneous autoimmune encephalomyelitis. Immunol Rev 2001;182:122-134.
61. + regulatory T cells in anti-myelin basic protein T cell receptor transgenic mice. Proc Natl Acad Sci USA 2002;99:8213-8218.
62. Furtado GC, Marcondes MC, Latkowski JA, Tsai J, Wensky A, Lafaille JJ. Swift entry of myelin-specific T lymphocytes into the central nervous system in spontaneous autoimmune encephalomyelitis. J Immunol 2008;181:4648-4655.
63. Brabb T, von Dassow P, Ordonez N, Schnabel B, Duke B, Goverman J. In situ tolerance within the central nervous system as a mechanism for preventing autoimmunity. J Exp Med 2000;192:871-880.
64. Cabbage SE, Huseby ES, Sather BD, Brabb T, Liggitt D, Goverman J. Regulatory T cells maintain long-term tolerance to myelin basic protein by inducing a novel, dynamic state of T cell tolerance. J Immunol 2007;178:887-896.
65. Seamons A, Perchellet A, Goverman J. Endogenous myelin basic protein is presented in the periphery by both dendritic cells and resting B cells with different functional consequences. J Immunol 2006;177:2097-2106.
66. Krishnamoorthy G, Lassmann H, Wekerle H, Holz A. Spontaneous opticospinal encephalomyelitis in a double-transgenic mouse model of autoimmune T cell/B cell cooperation. J Clin Invest 2006;116:2385-2392.
67. Bettelli E, Baeten D, Jager A, Sobel RA, Kuchroo VK. Myelin oligodendrocyte glycoprotein-specific T and B cells cooperate to induce a Devic-like disease in mice. J Clin Invest 2006;116:2393-2402.
68. Friese MA, Montalban X, Willcox N, Bell JI, Martin R, Fugger L. The value of animal models for drug development in multiple sclerosis. Brain 2006;129:1940-1952.
69. Junker A, et al. Multiple sclerosis: T-cell receptor expression in distinct brain regions. Brain 2007;130:2789-2799.
70. Coles AJ, et al. The window of therapeutic opportunity in multiple sclerosis: evidence from monoclonal antibody therapy. J Neurol 2006;253:98-108.
71. -/- mice. Science 1992;256:1210-1213.
72. + T cells in murine experimental allergic encephalomyelitis. Science 1992;256:1213-1215.
73. Huseby ES, Liggitt D, Brabb T, Schnabel B, Ohlen C, Goverman J. A pathogenic role for myelin-specific CD8(+) T cells in a model for multiple sclerosis. J Exp Med 2001;194:669-676.
74. + T cells are encephalitogenic and produce severe disease in C57BL/6 mice. J Immunol 2001;166:7579-7587.
75. + T cell responses during experimental autoimmune encephalomyelitis. Eur J Immunol 2005;35:76-85.
76. + T cells in multiple sclerosis. Nat Med 2008;14:1227-1235.
77. Brynedal B, et al. HLA-A confers an HLA-DRB1 independent influence on the risk of multiple sclerosis. PLoS ONE 2007;2:e664.
78. + T cells for sustained CNS inflammation during chronic EAE. J Neuroimmunol 2009;213:60-68.
79. Huseby ES, Ohlen C, Goverman J. Cutting edge: myelin basic protein-specific cytotoxic T cell tolerance is maintained in vivo by a single dominant epitope in H-2k mice. J Immunol 1999;163:1115-1118.
80. + T cells maintain tolerance to myelin basic protein by 'epitope theft'. Nat Immunol 2004;5:606-614.
81. Jacobs EC, et al. Region-specific myelin pathology in mice lacking the golli products of the myelin basic protein gene. J Neurosci 2005;25:7004-7013.
82. Perchellet A, Brabb T, Goverman JM. Crosspresentation by nonhematopoietic and direct presentation by hematopoietic cells induce central tolerance to myelin basic protein. Proc Natl Acad Sci USA 2008;105:14040-14045.
83. + T cells expressing dual TCRs. Nat Immunol 2010;11:628-634.