The Activation Status of Neuroantigen-specific T Cells in the Target Organ Determines the Clinical Outcome of Autoimmune Encephalomyelitis

Journal of Experimental Medicine

Volumn 199, Issue 2, 2004, Pages 185-197

  Kawakami, Naoto ^a   Lassmann, Silke ^a   Li, Zhaoxia ^a   Odoardi, Francesca ^a   Ritter, Thomas ^b   Ziemssen, Tjalf ^a   Klinkert, Wolfgang E F ^a   Ellwart, Joachim W ^c   Bradl, Monika ^d   Krivacic, Kimberly ^e   Lassmann, Hans ^d,f   Ransohoff, Richard M ^e   Volk, Hans Dieter ^b   Wekerle, Hartmut ^a   Linington, Christopher ^a,g   Flügel, Alexander ^a  

^a MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d UNIVERSITY OF VIENNA   (Austria)

^e LERNER RESEARCH INSTITUTE   (United States)

^f UNIVERSITY OF FREIBURG   (Germany)

^g UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Autoimmunity of the CNS; Disease model; Multiple sclerosis; Reactivation in the CNS; Retroviral gene transfer

Indexed keywords

AUTOANTIGEN; GREEN FLUORESCENT PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN; MYELIN BASIC PROTEIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; PROTEIN S100B; RETROVIRUS VECTOR;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE COURSE; GENE TRANSFER; INFLAMMATION; LYMPHOCYTE ACTIVATION; LYMPHOCYTE MIGRATION; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; RAT; RAT STRAIN; T LYMPHOCYTE;

ADOPTIVE TRANSFER; ANIMALS; AUTOANTIGENS; CELL LINE; CENTRAL NERVOUS SYSTEM; CYTOKINES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GREEN FLUORESCENT PROTEINS; INFLAMMATION MEDIATORS; LUMINESCENT PROTEINS; LYMPHOCYTE ACTIVATION; ORGAN SPECIFICITY; PHENOTYPE; RATS; RATS, INBRED LEW; RECOMBINANT PROTEINS; T-LYMPHOCYTES;

EID: 1642458745     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20031064     Document Type: Article

References (61)

1. Wekerle, H., K. Kojima, J. Lannes-Vieira, H. Lassmann, and C. Linington. 1994. Animal models. Ann. Neurol. 36:S47-S53.
2. Ben-Nun, A., H. Wekerle, and I.R. Cohen. 1981. The rapid isolation of clonable antigen-specific T lymphocyte lines capable of mediating autoimmune encephalomyelitis. Eur. J. Immunol. 11:195-199.
3. Benveniste, E.N. 1997. Role of macrophages/microglia in multiple sclerosis and experimental allergic encephalomyelitis. J. Mol. Med. 75:165-173.
4. + T cells specific for an astrocyte protein, S100β. J. Neural Transm. 49(Suppl.):43-51.
5. Linington, C., T. Berger, L. Perry, S. Weerth, D. Hinze-Selch, Y. Zhang, H.-C. Lu, H. Lassmann, and H. Wekerle. 1993. T cells specific for the myelin oligodendrocyte glycoprotein (MOG) mediate an unusual autoimmune inflammatory response in the central nervous system. Eur. J. Immunol. 23:1364-1372.
6. Storch, M.K., A. Stefferl, U. Brehm, R. Weissert, E. Wallström, M. Kerschensteiner, T. Olsson, C. Linington, and H. Lassmann. 1998. Autoimmunity to myelin oligodendrocyte glycoprotein in rats mimics the spectrum of multiple sclerosis pathology. Brain Pathol. 8:681-694.
7. Eylar, E.H., P.J. Kniskern, and J.J. Jackson. 1974. Myelin basic protein. Methods Enzymol. 32:323-341.
8. Adelmann, M., J. Wood, I. Benzel, P. Fiori, H. Lassmann, J.-M. Matthieu, M.V. Gardinier, K. Dommair, and C. Linington. 1995. The N-terminal domain of the myelin oligodendrocyte glycoprotein (MOG) induces acute demyelinating experimental autoimmune encephalomyelitis in the Lewis rat. J. Neuroimmunol. 63:17-27.
9. + T lymphocytes: Green fluorescent protein engineered, encephalitogenic T cells used to illuminate immune responses in the brain. Nature Med. 5:843-847.
10. Markowitz, D., S. Goff, and A. Bank. 1988. A safe packaging line for gene transfer: Separating viral genes on two different plasmids. J. Virol. 62:1120-1124.
11. Miller, A.D., and G. Rosman. 1989. Improved retroviral vectors for gene transfer and expression. Biotechniques. 7:980-990.
12. Flügel, A., T. Berkowicz, T. Ritter, M. Labeur, D. Jenne, Z. Li, J. Ellwart, M. Willem, H. Lassmann, and H. Wekerle. 2001. Migratory activity and functional changes of green fluorescent effector T cells before and during experimental autoimmune encephalomyelitis. Immunity. 14:547-560.
13. Vass, K., H. Lassmann, H. Wekerle, and H.M. Wisniewski. 1986. The distribution of Ia antigen in the lesions of rat acute experimental allergic encephalomyelitis. Acta. Neuropathol. 70:149-160.
14. Cohen, J.A., D.M. Essayan, B. Zweiman, and R.P. Lisak. 1987. Limiting dilution analysis of the frequency of antigen-reactive lymphocytes isolated from the central nervous system of Lewis rats with experimental allergic encephalomyelitis. Cell. Immunol. 108:203-213.
15. Glabinski, A.R., M. Tani, R.M. Strieter, V.K. Tuohy, and R.M. Ransohoff. 1997. Synchronous synthesis of α- and β-chemokines by cells of diverse lineage in the central nervous system of mice with relapses of chronic autoimmune encephalomyelitis. Am. J. Pathol. 150:617-30.
16. Glabinski, A.R., V. Balasingam, M. Tani, S.L. Kunkel, R.M. Strieter, V.W. Yong, and R.M. Ransohoff. 1996. Chemokine monocyte chemoattractant protein-1 is expressed by astrocytes after mechanical injury to the brain. J. Immunol. 156:4363-4368.
17. Tani, M., A.R. Glabinski, V.K. Tuohy, M.H. Stoler, M.L. Estes, and R.M. Ransohoff. 1996. In situ hybridization analysis of glial fibrillary acidic protein mRNA reveals evidence of biphasic astrocyte activation during acute experimental autoimmune encephalomyelitis. Am. J. Pathol. 148:889-896.
18. McTigue, D.M., M. Tani, K. Krivacic, A. Chernovsky, G.S. Kelner, D. Maciejewski, R., Maki, R.M. Ransohoff, and B.T. Stokes. 1998. Selective chemokine mRNA accumulation in the rat spinal cord after contusion injury. J. Neurosci. Res. 53:368-376.
19. Brosnan, C.F., M.B. Bornstein, and B.R. Bloom. 1981. The effects of macrophage depletion on the clinical and pathologic expression of experimental allergic encephalomyelitis. J. Immunol. 126:614-620.
20. Huitinga, I., N. Van Rooijen, C.J.A. De Groot, B.M.J. Uitdehaag, and C.D. Dijkstra. 1990. Suppression of experimental allergic encephalomyelitis in Lewis rats after elimination of macrophages. J. Exp. Med. 172:1025-1033.
21. Ransohoff, R.M. 1999. Mechanisms of inflammation in MS tissue: adhesion molecules and chemokines. J. Neuroimmunol. 98:57-68.
22. Kojima, K., T. Berger, H. Lassmann, D. Hinze-Selch, Y. Zhang, J. Gehrmann, H. Wekerle, and C. Linington. 1994. Experimental autoimmune panencephalitis and uveoretinitis in the Lewis rat transferred by T lymphocytes specific for the S100β molecule, a calcium-binding protein of astroglia. J. Exp. Med. 180:817-829.
23. Stefferl, A., A. Schubart, M. Storch, A. Amini, I.H. Mather, H. Lassmann, and C. Linington. 2000. Butyrophilin, a milk protein, modulates the encephalitogenic T cell response to myelin oligodendrocyte glycoprotein in experimental autoimmune encephalomyelitis. J. Immunol. 165:2859-2865.
24. 14C-labelled cells during acute, chronic, and relapsing experimental allergic encephalomyelitis. Lab. Invest. 63:162-170.
25. Wekerle, H., C. Linington, H. Lassmann, and R. Meyermann. 1986. Cellular immune reactivity within the CNS. Trends Neurosci. 9:271-277.
26. Hickey, W.F., B.L. Hsu, and H. Kimura. 1991. T lymphocyte entry into the central nervous system. J. Neurosci. Res. 28:254-260.
27. Liu, H., M. Rhodes, D.L. Wiest, and D.A.A. Vignali. 2000. On the dynamics of the TCR:CD3 complex cell surface expression and downmodulation. Immunity 13:665-675.
28. Grakoui, A., S.K. Bromley, C. Sumen, M.M. Davis, A.S. Shaw, P.M. Allen, and M.L. Dustin. 1999. The immunological synapse: a molecular machine controlling T cell activation. Science. 285:221-227.
29. + T cells. J. Exp. Med. 186:757-766.
30. Neumann, H., and H. Wekerle. 1998. Neuronal control of the immune response in the central nervous system: linking brain immunity to neurodegeneration. J. Neuropathol. Exp. Neurol. 58:1-9.
31. Neumann, H., T. Misgeld, K. Matsumuro, and H. Wekerle. 1998. Neurotrophins inhibit major histocompatibility class II inducibility of microglia: involvement of the p75 neurotrophin receptor. Proc. Natl. Acad. Sci. USA. 95:5779-5784.
32. Meinl, E., F. Aloisi, B. Ertl, F. Weber, R. De Waal Malefijt, H. Wekerle, and R. Hohlfeld. 1994. Multiple sclerosis: immunomodulatory effects of human astrocytes on T cells. Brain. 117:1323-1332.
33. Xiao, B.-G., A. Diab, J. Zhu, P. Van der Meide, and H. Link. 1998. Astrocytes induce hyporesponsiveness of myelin basic protein-reactive T and B cell function. J. Neuroimmunol. 89:113-121.
34. Aloisi, F., F. Ria, and L. Adorini. 2000. Regulation of T cell responses by CNS antigen presenting cells: different roles for microglia and astrocytes. Immunol. Today. 21:141-147.
35. Brabb, T., P. Von Dassow, N. Ordonez, B. Schnabel, B. Duke, and J. Goverman. 2000. In situ tolerance within the central nervous system as a mechanism for preventing autoimmunity. J. Exp. Med. 192:871-880.
36. Critchfield, J.M., M.K. Racke, J.C. Zuñiga-Pflücker, B. Cannella, C.S. Raine, J. Goverman, and M.J. Lenardo. 1994. T cell deletion in high antigen dose therapy of autoimmune encephalomyelitis. Science. 263:1139-1143.
37. Hayashi, N., D. Liu, B. Min, S. Ben-Sasson, and W.E. Paul. 2002. Antigen challenge leads to in vivo activation and elimination of highly polarized TH1 memory T cells. Proc. Natl. Acad. Sci. USA. 99:6187-6191.
38. Pender, M.P., K.B. Nguyen, P.A. McCombe, and J.F.R. Kerr. 1991. Apoptosis in the nervous system in experimental allergic encephalomyelitis. J. Neurol. Sci. 104:81-87.
39. Schmied, M., H. Breitschopf, R. Gold, H. Zischler, G. Rothe, H. Wekerle, and H. Lassmann. 1993. Apoptosis of T lymphocytes-a mechanism to control inflammation in the brain. Am. J. Pathol. 143:446-452.
40. Flügel, A., F.-W. Schwaiger, H. Neumann, I. Medana, M. Willem, H. Wekerle, G.W. Kreutzberg, and M.B. Graeber. 2000. Neuronal FasL induces cell death of encephalitogenic T lymphocytes. Brain Pathol. 10:353-364.
41. Fritz, R.B., and I. Kalvakolanu. 1995. Thymic expression of the golli-myelin basic protein gene in the SJL/J mouse. J. Neuroimmunol. 57:93-99.
42. Fritz, R.B., and M.-L. Zhao. 1996. Thymic expression of myelin basic protein (MBP). Activation of MBP-specific T cells by thymic cells in the absence of exogenous MBP. J. Immunol. 157:5249-5253.
43. Kalwy, S.A., M.-C. Marty, P. Bausero, and B. Pessac. 1998. Myelin basic protein-related proteins in mouse brain and immune tissues. J. Neurochem. 70:435-438.
44. Mor, F., G.L. Boccaccio, and T. Unger. 1998. Expression of autoimmune disease-related antigens by cells of the immune system. J. Neurosci. Res. 54:254-262.
45. Kojima, K., H. Lassmann, H. Wekerle, and C. Linington. 1997. The thymus and self tolerance: co-existence of encephalitogenic S-100β specific T cells and their nominal autoantigen, S-100β, in the normal rat thymus. Int. Immunol. 9:897-904.
46. Lauriola, L., F. Michetti, V.M. Stolfi, G. Tallini, and D. Cocchia. 1984. Detection by S-100 immunolabelling of interdigitating reticulum cells in human thymuses. Virchows Arch. 45:187-195.
47. Kondo, H., T. Iwanaga, and T. Nakajima. 1983. An immunocytochemical study on the localization of S-100 protein in the retina of rats. Cell Tiss. Res. 231:527-532.
48. Kondo, K., K. Mukai, Y. Sato, Y. Matsuno, Y. Shimosato, and Y. Monden. 1990. An immunohistochemical study of thymic epithelial tumors. III. The distribution of interdigitating reticulum cells and S-100β-positive small lymphocytes. Am. J. Surg. Pathol. 14:1139-1147.
49. Iglesias, A., J. Bauer, T. Litzenburger, A. Schubart, and C. Linington. 2001. T- and B-cell responses to myelin oligodendrocyte glycoprotein in experimental autoimmune encephalomyelitis and multiple sclerosis. Glia. 36:220-234.
50. Berger, T., S. Weerth, K. Kojima, C. Linington, H. Wekerle, and H. Lassmann. 1997. Experimental autoimmune encephalomyelitis: the antigen specificity of T-lymphocytes determines the topography of lesions in the central and peripheral nervous system. Lab. Invest. 76:355-364.
51. Tran, E.H., K. Hoekstra, N. Van Rooijen, C.D. Dijkstra, and T. Owens. 1998. Immune invasion of the central nervous system parenchyma and experimental allergic encephalomyelitis, but not leukocyte extravasation from blood, are prevented in macrophage depleted mice. J. Immunol. 161:3767-3775.
52. Martiney, J.A., A.J. Rajan, P.C. Charles, A. Cerami, P.C. Ulrich, S. Macphail, K.J. Tracey, and C.F. Brosnan. 1998. Prevention and treatment of experimental autoimmune encephalomyelitis by CNI-1493, a macrophage deactivating agent. J. Immunol. 160:5588-5595.
53. Izikson, L., R.S. Klein, A.D. Luster, and H.L. Weiner. 2002. Targeting monocyte recruitment in CNS autoimmune disease. Clinical Immunology. 103:125-131.
54. Karpus, WJ., N.W. Lukacs, B.L. McRae, R.M. Strieter, S.L. Kunkel, and S.D. Miller. 1995. An important role for the chemokine macrophage inflammatory protein-1α in the pathogenesis of the T cell-mediated autoimmune disease, experimental autoimmune encephalomyelitis. J. Immunol. 155: 5003-5010.
55. Youssef, S., G. Wildbaum, and N. Karin. 1999. Prevention of experimental autoimmune encephalomyelitis by MIP-1α and MCP-1 naked DNA. J. Autoimmun. 13:21-29.
56. Huang, D.R., J. Wang, P. Kivisäkk, B.J. Rollins, and R.M. Ransohoff. 2001. Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J. Exp. Med. 193:713-726.
57. Glabinski, A.R., B. Bielicki, and R.M. Ransohoff. 2003. Chemokine upregulation follows cytokine expression in chronic relapsing experimental autoimmune encephalomyelitis. Scand. J. Immunol. 58:81-88.
58. McManus, C.M., C.F. Brosnan, and J.W. Berman. 2000. Cytokine induction of MIP-1 alpha and MIP-1 beta in human fetal microglia. J. Immunol. 160:1449-1455.
59. Oh, J.-W., L.M. Schwiebert, and E.N. Benveniste. 1999. Cytokine regulation of CC and CXC chemokine expression by human astrocytes. J. Neurovirol. 5:82-94.
60. André, I., A. Gonzalez, B. Wang, J. Katz, C. Benoist, and D. Mathis. 1996. Checkpoints in the progression of autoimmune disease: lessons from diabetes mellitus. Proc. Natl. Acad. Sci. USA. 93:2260-2263.
61. Schwartz, M., G. Moalem, R. Leibowitz-Amit, and I.R. Cohen. 1999. Innate and adaptive immune responses can be beneficial for CNS repair. Trends Neurosci. 22:295-299.