Th17 and Th1 responses directed against the immunizing epitope, as opposed to secondary epitopes, dominate the autoimmune repertoire during relapses of experimental autoimmune encephalomyelitis

Journal of Neuroscience Research

Volumn 85, Issue 8, 2007, Pages 1685-1693

  Kroenke, Mark A ^a   Segal, Benjamin M ^a,b  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b Box 605 ^*  (United States)

Author keywords

Animal model; Autoimmunity; Epitope spreading; Multiple sclerosis; T lymphocyte

Indexed keywords

EPITOPE; GAMMA INTERFERON; INTERLEUKIN 17;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; HELPER CELL; IMMUNIZATION; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; RELAPSE; T LYMPHOCYTE; TH1 CELL; TH17 CELL;

ANIMALS; BRAIN; CD4-POSITIVE T-LYMPHOCYTES; CELL LINEAGE; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; EPITOPES; IMMUNE TOLERANCE; INTERFERON TYPE II; INTERLEUKIN-17; LYMPH NODES; MICE; RECURRENCE; SPLEEN; T-LYMPHOCYTES, HELPER-INDUCER; TH1 CELLS;

EID: 34249805698     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21291     Document Type: Article

References (39)

1. Anderson AC, Nicholson JB, Legge KL, Turchin V, Zaghouani H, Kuchroo VK. 2000. High frequency of auto reactive myelin proteolipid protein-specific T cells in the periphery of naive mice: mechanisms of selection of the self-reactive repertoire. J Exp Med 191:761-770.
2. Billiau A, Heremans H, Vermeire K, Matthys P. 1998. Immunomodulatory properties of interferon-gamma. An update. Ann NY Acad Sci 856:22-32.
3. Chen Y, Langrish CL, McKenzie B, Joyce-Shaikh B, Stumhofer JS, McClanahan T, Blumenschein W, Churakovsa T, Low J, Presta L, Hunter CA, Kastelein RA, Cua DJ. 2006. Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis. J Clin Invest 116:1317-1326.
4. Ferber IA, Brocke S, Taylor-Edwards C, Ridgway W, Dinisco C, Steinman L, Dalton D, Fathman CG. 1996. Mice with a disrupted IFN-gamma gene are susceptible to the induction of experimental autoimmune encephalomyelitis. J Immunol 156:5-7.
5. Fontoura P, Garren H, Steinman L. 2005. Antigen-specific therapies in multiple sclerosis: going beyond proteins and peptides. Int Rev Immunol 24:415-416.
6. Gaur A, Wiers B, Liu A, Rothbard J, Fathman CG. 1992. Amelioration of autoimmune encephalomyelitis by myelin basic protein synthetic peptide-induced anergy. Science 258:1491-1494.
7. Goebels N, Hofstetter H, Schmidt S, Brunner C, Wekerle H, Hohlfeld R. 2000. Repertoire dynamics of auto reactive T cells in multiple sclerosis patients and healthy subjects: epitope spreading versus clonal persistence. Brain 123:508-518.
8. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, Weaver CT. 2005. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 6:1123-1132.
9. Ichikawa HT, Williams LP, Segal BM. 2002. Activation of APCs through CD40 or Toll-like receptor 9 overcomes tolerance and precipitates autoimmune disease. J Immunol 169:2781-2787.
10. Jones RE, Bourdette D, Moes N, Vandenbark A, Zamora A, Offner J. 2003. Epitope spreading is not required for relapses in experimental autoimmune encephalomyelitis. J Immunol 170:1690-1698.
11. Klein L, Klugmann M, Nave K, Tuohy VK, Kyewski B. 2000. Shaping of the auto reactive T-cell repertoire by a splice variant of self protein expressed in thymic epithelial cells. Nat Med 6:56-61.
12. Kleinschmidt-DeMasters BK, Tyler KL. 2005. Progressive multifocal leukoencephalopathy complicating treatment with natalizumab and interferon beta-1a for multiple sclerosis. N Engl J Med 353:369-374.
13. Kumar V. 1998. Determinant spreading during experimental autoimmune encephalomyelitis: is it potentiating, protecting or participating in the disease? Immunol Rev 164:73-80.
14. Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgewick JD, McClanahan T, Kastelein RA, Cua DJ. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 201:233-240.
15. Lindsey WJ. 1998. Use of reinduced experimental autoimmune encephalomyelitis to evaluate the importance of epitope spread. Int Immunol 10:743-748.
16. Martin R, McFarland HF. 1995. Immunological aspects of experimental allergic encephalomyelitis and multiple sclerosis. Crit Rev Clin Lab Sci 32:121-182.
17. Marusic S, Tonegawa S. 1997. Tolerance induction and autoimmune encephalomyelitis amelioration after administration of myelin basic protein-derived peptide. J Exp Med 186:507-515.
18. McMahon EJ, Bailey SL, Castenada CV, Waldner H, Miller SD. 2005. Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis. Nat Med 11:335-339.
19. McRae BL, Kennedy MK, Tan L, Dal Canto MC, Picha KS, Miller SD. 1992. Induction of active and adoptive relapsing experimental autoimmune encephalomyelitis (EAE) using an encephalitogenic epitope of proteolipid protein. J Neuroimmunol 38:229-240.
20. McRae BL, Vanderlugt CL, Dal Canto MC, Miller SD. 1995. Functional evidence for epitope spreading in the relapsing pathology of experimental autoimmune encephalomyelitis. J Exp Med 182:75-85.
21. Moreau T, Thorpe J, Miller D, Moseley I, Hale G, Waldmann H, Clayton D, Wing M, Scolding N, Compston A. 1994. Preliminary evidence from magnetic resonance imaging for reduction in disease activity after lymphocyte depletion in multiple sclerosis. Lancet 344:298-301.
22. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 6:1133-1141.
23. Polman CH, O'Connor PW, Havrdova E, Hutchinson M, Kappos L, Miller DH, Phillips JT, Lublin FD, Giovannoni G, Wajgt A, Toal M, Lynn F, Panzara MA, Sandrock AW,AFFIRM Investigators. 2006. A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis. N Engl J Med 354:899-910.
24. + regulatory cells mediate genetic resistance to experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 101:15434-15439.
25. Ristori G, Giubilei F, Giunti D, Perna A, Gasperini C, Buttinelli C, Salvetti M, Uccelli A. 2000. Myelin basic protein intramolecular spreading without disease progression in a patient with multiple sclerosis. J Neuroimmunol 110:240-243.
26. Segal BM, Shevach EM. 1996. IL-12 unmasks latent autoimmune disease in resistant mice. J Exp Med 184:771-775.
27. Segal BM, Dwyer BK, Shevach EM. 1998. An interleukin 10/12 immunoregulatory circuit controls susceptibility to autoimmune disease. J Exp Med 187:537-546.
28. Takacs K, Chandler P, Altmann DM. 1997. Relapsing and remitting experimental allergic encephalomyelitis: a focused response to the encephalitogenic peptide rather than epitope spread. Eur J Immunol 27:2927-2934.
29. Takacs K, Altmann DM. 1998. The case against epitope spreading in experimental allergic encephalomyelitis. Immunol Rev 164:101-110.
30. Targoni OS, Baus J, Hofstetter HH, Hesse MD, Karulin AY, Boehm BO, Forsthuber TG, Lehmann PV. 2001. Frequencies of neuroantigen-specific T cells in the central nervous system versus the immune periphery during the course of experimental autoimmune encephalomyelitis. J Immunol 166:4757-4764.
31. Tuohy VK, Yu M, Weinstock-Guttman B, Kinkel RP. 1997. Diversity and plasticity of self recognition during the development of multiple sclerosis. J Clin Invest 99:1682-1690.
32. Tuohy VK, Yu M, Yin L, Kawczak JA, Kinkel RP. 1999. Regression and spreading of self-recognition during the development of autoimmune demyelinating disease. J Autoimmun 13:11-20.
33. Vanderlugt CL, Neville KL, Nikcevich KM, Eagar TN, Bluestone JA, Miller SD. 2000. Pathologic role and temporal appearance of newly emerging auto epitopes in relapsing experimental autoimmune encephalomyelitis. J Immunol 164:670-678.
34. Vergelli M, Mazzanti B, Traggiai E, Biagioli T, Ballerini C, Pariqi A, Konse A, Pellicano G, Massacesi L. 2001. Short-term evolution of auto reactive T cell repertoire in multiple sclerosis. J Neurosci Res 66:517-524.
35. Voskuhl RR, Farris RW 2nd, Naqasato K, McFarland HF, Dalcq MD. 1996. Epitope spreading occurs in active but not passive EAE induced by myelin basic protein. J Neuroimmunol 70:103-111.
36. Whitman RH, Bourdette DN, Hashim GA, Herndon RM, Ilg RC, Vandenbark AA, Offner H. 1991. Lymphocytes from SJL/J mice immunized with spinal cord respond selectively to a peptide of proteolipid protein and transfer relapsing demyelinating experimental autoimmune encephalomyelitis. J Immunol 146:101-107.
37. Wildbaum G, Netzer N, Karin N. 2002. Tr1 cell-dependent active tolerance blunts the pathogenic effects of determinant spreading. J Clin Invest 110:701-710.
38. Willenborg DO, Fordham S, Bernard CC, Cowden WB, Ramshaw IA. 1996. IFN-gamma plays a critical down-regulatory role in the induction and effector phase of myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis. J Immunol 157:3223-3227.
39. Yin L, Yu M, Edling AE, Kawczak JA, Mathisen PM, Nanavati T, Johnson JM, Tuohy VK. 2001. Pre-emptive targeting of the epitope spreading cascade with genetically modified regulatory T cells during autoimmune demyelinating disease. J Immunol 167:6105-6112.