Molecular mimicry as an inducing trigger for CNS autoimmune demyelinating disease

Immunological Reviews

Volumn 245, Issue 1, 2012, Pages 227-238

  Chastain, Emily M L ^a   Miller, Stephen D ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Autoimmunity; Cytotoxic T cells; Dendritic cells; Neuroimmunology; T cell receptors; Th1 Th2 Th17 cells

Indexed keywords

HLA DR2 ANTIGEN; MYELIN BASIC PROTEIN; PROTEOLIPID PROTEIN;

ARENAVIRUS INFECTION; AUTOIMMUNITY; BACILLUS SUBTILIS; BRAIN INFECTION; CANDIDA ALBICANS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONFORMATIONAL TRANSITION; COXSACKIE VIRUS B3; CROSS REACTION; CYTOTOXIC T LYMPHOCYTE; DELAYED HYPERSENSITIVITY; DISEASE COURSE; ESCHERICHIA COLI; GENE DELETION; GENE INSERTION; GRAY MATTER; HAEMOPHILUS INFLUENZAE; HEPATITIS B VIRUS; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; LYMPHOCYTIC INFILTRATION; MOLECULAR MIMICRY; MOUSE STRAIN; MULTIPLE SCLEROSIS; MURINE ENCEPHALOMYELITIS VIRUS; MURINE HEPATITIS CORONAVIRUS; MYCOBACTERIUM AVIUM; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SALMONELLA TYPHIMURIUM; SEQUENCE HOMOLOGY; STAPHYLOCOCCUS AUREUS; T CELL DEPLETION; T LYMPHOCYTE ACTIVATION; TH1 CELL; VIRUS REPLICATION; VIRUS VIRULENCE;

ANIMALS; AUTOANTIGENS; CENTRAL NERVOUS SYSTEM; CROSS REACTIONS; ENVIRONMENTAL EXPOSURE; HUMANS; MOLECULAR MIMICRY; MULTIPLE SCLEROSIS; MYELIN PROTEINS; VIRUS DISEASES;

EID: 83655191550     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2011.01076.x     Document Type: Review

References (63)

1. Steinman L. Multiple sclerosis: a coordinated immunological attack against myelin in the central nervous system. Cell 1996;85:299-302.
2. McFarland HF, Martin R. Multiple sclerosis: a complicated picture of autoimmunity. Nat Immunol 2007;8:913-919.
3. Wekerle H. Immunopathogenesis of multiple sclerosis. Acta Neurol 1991;13:197-204.
4. Sun JB, et al. Autoreactive T and B cells responding to myelin proteolipid protein in multiple sclerosis and controls. Eur J Immunol 1991;21:1461-1468.
5. 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;346:183-187.
6. Bernard CC, de Rosbo NK. Immunopathological recognition of autoantigens in multiple sclerosis. Acta Neurol 1991;13:171-178.
7. Whitaker JN, Mitchell GW, Raine CS, McFarland HF, Tourtellotte WW. Clinical features of multiple sclerosis. Multiple sclerosis: clinical and pathogenetic basis. London: Chapman and Hall, 1997:3-19.
8. Sospedra M, Martin R. Immunology of multiple sclerosis. Annu Rev Immunol 2005;23:683-747.
9. Hafler DA, et al. Risk alleles for multiple sclerosis identified by a genomewide study. N Engl J Med 2007;357:851-862.
10. Haines JL, et al. A complete genomic screen for multiple sclerosis underscores a role for the major histocompatability complex. The Multiple Sclerosis Genetics Group. Nat Genet 1996;13:469-471.
11. Kurtzke JF. Epidemiologic evidence for multiple sclerosis as an infection. Clin Microbiol Rev 1993;6:382-427.
12. Kurtzke JF, Hyllested K. Multiple sclerosis: an epidemic disease in the Faroes. Am Neurol Assoc 1975;100:213-215.
13. Kurtzke JF, Hyllested K. Multiple sclerosis in the Faroe Islands. I. Clinical and epidemiological features. Ann Neurol 1979;5:6-21.
14. Olson JK, Croxford JL, Miller SD. Virus-induced autoimmunity: Potential role of viruses in initiation, perpetuation, and progression of T cell-mediated autoimmune diseases. Viral Immunol 2001;14:227-250.
15. Fujinami RS. Can virus infections trigger autoimmune disease? J Autoimmun 2001;16:229-234.
16. Munz C, Lunemann JD, Getts MT, Miller SD. Antiviral immune responses: triggers of or triggered by autoimmunity? Nat Rev Immunol 2009;9:246-258.
17. Vanderlugt CL, Miller SD. Epitope spreading in immune-mediated diseases: implications for immunotherapy. Nat Rev Immunol 2002;2:85-95.
18. Miller SD, et al. Epitope spreading leads to myelin-specific autoimmune responses in SJL mice chronically infected with Theiler's virus. J Neurovirol 1997;3(Suppl. 1):S62-S65.
19. Fujinami RS, Oldstone MB. Amino acid homology between the encephalitogenic site of myelin basic protein and virus: mechanism for autoimmunity. Science 1985;230:1043-1045.
20. 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.
21. Basu D, Horvath S, Matsumoto I, Fremont DH, Allen PM. Molecular basis for recognition of an arthritic peptide and a foreign epitope on distinct MHC molecules by a single TCR. J Immunol 2000;164:5788-5796.
22. Basu D, Horvath S, O'Mara L, Donermeyer D, Allen PM. Two MHC surface amino acid differences distinguish foreign peptide recognition from autoantigen specificity. J Immunol 2001;166:4005-4011.
23. Kouskoff V, Korganow AS, Duchatelle V, Degott C, Benoist C, Mathis D. Organ-specific disease provoked by systemic autoimmunity. Cell 1996;87:811-822.
24. Kaufman DL, Erlander MG, Clare-Salzler M, Atkinson MA, Maclaren NK, Tobin AJ. Autoimmunity to two forms of glutamate decarboxylase in insulin- dependent diabetes mellitus. J Clin Invest 1992;89:283-292.
25. Lang HL, et al. A functional and structural basis for TCR cross-reactivity in multiple sclerosis. Nat Immunol 2002;3:940-943.
26. Ohashi PS, et al. Ablation of "tolerance" and induction of diabetes by virus infection in viral antigen transgenic mice. Cell 1991;65:305-317.
27. Oldstone MB, Nerenberg M, Southern P, Price J, Lewicki H. Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: role of anti-self (virus) immune response. Cell 1991;65:319-331.
28. Zhao ZS, Granucci F, Yeh L, Schaffer PA, Cantor H. Molecular mimicry by herpes simplex virus-type 1: Autoimmune disease after viral infection. Science 1998;279:1344-1347.
29. Olson JK, Croxford JL, Calenoff M, Dal Canto MC, Miller SD. A virus-induced molecular mimicry model of multiple sclerosis. J Clin Invest 2001;108:311-318.
30. Oleszak EL, Chang JR, Friedman H, Katsetos CD, Platsoucas CD. Theiler's virus infection: a model for multiple sclerosis. Clin Microbiol Rev 2004;17:174-207.
31. Miller SD, et al. Persistent infection with Theiler's virus leads to CNS autoimmunity via epitope spreading. Nat Med 1997;3:1133-1136.
32. Dal Canto MC, Kim BS, Miller SD, Melvold RW. Theiler's murine encephalomyelitis virus (TMEV)-induced demyelination: a model for human multiple sclerosis. Methods 1996;10:453-461.
33. Clatch RJ, Lipton HL, Miller SD. Characterization of Theiler's murine encephalomyelitis virus (TMEV)-specific delayed-type hypersensitivity responses in TMEV-induced demyelinating disease: correlation with clinical signs. J Immunol 1986;136:920-927.
34. Welsh CJ, Tonks P, Nash AA, Blakemore WF. The effect of L3T4 T cell depletion on the pathogenesis of Theiler's murine encephalomyelitis virus infection in CBA mice. J Gen Virol 1987;68:1659-1667.
35. Gerety SJ, et al. Class II-restricted T cell responses in Theiler's murine encephalomyelitis virus-induced demyelinating disease. V. Mapping of a dominant immunopathologic VP2 T cell epitope in susceptible SJL/J mice. J Immunol 1994;152:908-918.
36. Yauch RL, Kim BS. A predominant viral epitope recognized by T cells from the periphery and demyelinating lesions of SJL/J mice infected with Theiler's virus is located within VP1(233-244). J Immunol 1994;153:4508-4519.
37. Yauch RL, Kerekes K, Saujani K, Kim BS. Identification of a major T-cell epitope within VP3 amino acid residues 24 to 37 of Theiler's virus in demyelination-susceptible SJL/J mice. J Virol 1995;69:7315-7318.
38. Tompkins SM, Fuller KG, Miller SD. Theiler's virus-mediated autoimmunity: local presentation of CNS antigens and epitope spreading. Ann NY Acad Sci 2002;958:26-38.
39. McMahon EJ, Bailey SL, Castenada CV, Waldner H, Miller SD. Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis. Nat Med 2005;11:335-339.
40. Bailey SL, Schreiner B, McMahon EJ, Miller SD. CNS myeloid DCs presenting endogenous myelin peptides 'preferentially' polarize CD4(+) T(H)-17 cells in relapsing EAE. Nat Immunol 2007;8:172-180.
41. McRae BL, Miller SD. Fine specificity of CD4+ T cell responses to the dominant encephalitogenic PLP 139-151 peptide in SJL/J mice. Neurochem Res 1994;19:997-1004.
42. Carrizosa AM, et al. Expansion by self antigen is necessary for the induction of experimental autoimmune encephalomyelitis by T cells primed with a cross-reactive environmental antigen. J Immunol 1998;161:3307-3314.
43. McRae BL, Karandikar NJ, Miller SD. Degenerate antigen recognition by CD4+ effector T cells in experimental autoimmune encephalomyelitis. J Neuroimmunol 1997;75:156-162.
44. Olson JK, Eagar TN, Miller SD. Functional activation of myelin-specific T cells by virus-induced molecular mimicry. J Immunol 2002;169:2719-2726.
45. Smith CE, Miller SD. Multi-peptide coupled-cell tolerance ameliorates ongoing relapsing EAE associated with multiple pathogenic autoreactivities. J Autoimmun 2006;27:218-231.
46. Turley DM, Miller SD. Peripheral tolerance Induction using ethylenecarbodiimide-fixed APCs uses both direct and indirect mechanisms of antigen presentation for prevention of experimental autoimmune encephalomyelitis. J Immunol 2007;178:2212-2220.
47. Luo X, et al. ECDI-fixed allogeneic splenocytes induce donor-specific tolerance for long-term survival of islet transplants via two distinct mechanisms. Proc Natl Acad Sci USA 2008;105:14527-14532.
48. Karpus WJ, Pope JG, Peterson JD, Dal Canto MC, Miller SD. Inhibition of Theiler's virus-mediated demyelination by peripheral immune tolerance induction. J Immunol 1995;155:947-957.
49. Karpus WJ, Peterson JD, Miller SD. Anergy in vivo: down-regulation of antigen-specific CD4+Th1 but not Th2 cytokine responses. Int Immunol 1994;6:721-730.
50. Miller SD, et al. Class II-restricted T cell responses in Theiler's murine encephalomyelitis virus (TMEV)-induced demyelinating disease. III. Failure of neuroantigen-specific immune tolerance to affect the clinical course of demyelination. J Neuroimmunol 1990;26:9-23.
51. Croxford JL, Anger HA, Miller SD. Viral delivery of an epitope from Haemophilus influenzae induces central nervous system autoimmune disease by molecular mimicry. J Immunol 2005;174:907-917.
52. Croxford JL, Olson JK, Anger HA, Miller SD. Initiation and exacerbation of autoimmune demyelination of the central nervous system via virus-induced molecular mimicry: implications for the pathogenesis of multiple sclerosis. J Virol 2005;79:8581-8590.
53. Haring J, Perlman S. Mouse hepatitis virus. Curr Opin Microbiol 2001;4:462-466.
54. Murray RS, Brown B, Brian D, Cabirac GF. Detection of coronavirus RNA and antigen in multiple sclerosis brain. Ann Neurol 1992;31:525-533.
55. Stewart JN, Mounir S, Talbot PJ. Human coronavirus gene expression in the brains of multiple sclerosis patients. Virology 1992;191:502-505.
56. Croxford JL, Ercolini AM, Degutes M, Miller SD. Structural requirements for initiation of cross-reactivity and CNS autoimmunity with a PLP139-151 mimic peptide derived from murine hepatitis virus. Eur J Immunol 2006;36:2671-2680.
57. Schreiner B, Bailey SL, Miller SD. T-cell response dynamics in animal models of multiple sclerosis: implications for immunotherapies. Exp Rev Clin Immunol 2007;3:57-72.
58. Ercolini AM, Ludovic Croxford J, Degutes M, Miller SD. Cross-reactivity between peptide mimics of the immunodominant myelin proteolipid protein epitope PLP139-151: Comparison of peptide priming in CFA vs. viral delivery. J Neuroimmunol 2007;186:5-18.
59. Gregersen JW, Holmes S, Fugger L. Humanized animal models for autoimmune diseases. Tissue Antigens 2004;63:383-394.
60. Ellmerich S, et al. Disease-related epitope spread in a humanized T cell receptor transgenic model of multiple sclerosis. Eur J Immunol 2004;34:1839-1848.
61. Madsen LS, et al. A humanized model for multiple sclerosis using HLA-DR2 and a human T- cell receptor. Nat Genet 1999;23:343-347.
62. Greene MT, Ercolini AM, Degutes M, Miller SD. Differential induction of experimental autoimmune encephalomyelitis by myelin basic protein molecular mimics in mice humanized for HLA-DR2 and an MBP(85-99)-specific T cell receptor. J Autoimmun 2008;31:399-407.
63. Hausmann S, Martin M, Gauthier L, Wucherpfennig KW. Structural features of autoreactive TCR that determine the degree of degeneracy in peptide recognition. J Immunol 1999;162:338-344.