The controversy surrounding the pathogenesis of the multiple sclerosis lesion

Mayo Clinic Proceedings

Volumn 72, Issue 7, 1997, Pages 665-678

  Claudia, F ^a   Lucchinett, I ^a   Rodriguez, Moses ^a  

^a MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CYTOKINE; T LYMPHOCYTE RECEPTOR;

AUTOIMMUNITY; CONFERENCE PAPER; DEMYELINATION; INFLAMMATION; LYMPHOCYTE COUNT; MULTIPLE SCLEROSIS; OLIGODENDROGLIA; REMYELINIZATION; T LYMPHOCYTE;

EID: 0030748022     PISSN: 00256196     EISSN: None     Source Type: Journal    
DOI: 10.4065/72.7.665     Document Type: Conference Paper

References (137)

1. Prineas JW, Graham JS. Multiple sclerosis: capping of surface immunoglobulin G on macrophages engaged in myelin breakdown. AnnNeurol 1981;10:149-158
2. Wucherpfennig KW, Strominger JL. Molecular mimicry in T cellmediated autoimmunity: viral peptides activate human T cell clones specific for myelin basic protein. Cell 1995;80:695-705
3. Marrack P, Kappler J. Subversion of the immune system by pathogens. Cell 1994;76:323-332
4. Oldstone MBA. Virus-induced autoimmunity: molecular mimicry as a route to autoimmune disease. J Autoimmun 1989;2(Suppl): 187-194
5. Zamvil SS, Steinman L. The T lymphocyte in experimental allergic encephalomyelitis. Annu Rev Immunol 1990;8:579-621
6. Fierz W. MS as autoimmune disease: myelin antigens. Res Immunol 1989; 140:181-187
7. Johnson D, Hafler DA, Fallis RJ, Lees MB, Brady RO, Quarles RH, et al. Cell-mediated immunity to myelin-associated glycoprotein, proteolipid protein, and myelin basic protein in multiple sclerosis. J Neuroimmunol 1986; 13:99-108
8. Matsiota-Bernard P, Roullet E, Ragimbeau J, Avrameas S. T cell activation by autoantigens in multiple sclerosis. Autoimmunity 1993; 16:237-243
9. 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
10. AllegrettaM, Nicklas JA, Sriram S, Albertini RJ. T cells responsive to myelin basic protein in patients with multiple sclerosis. Science 1990:247:718-721
11. Lodge PA, Johnson C, Sriram S. Frequency of MBP and MBP peptide-reactive T cells in the HPRT mutant T-cell population of MS patients. Neurology 1996;46:1410-1415
12. Acha-Orbea H, Mitchell DJ, Timmermann L, Wraith DC, Tausch GS, Waldor MK, et al. Limited heterogeneity of T cell receptors from lymphocytes mediating autoimmune encephalomyelitis allows specific immune intervention. Cell 1988;54:263-273
13. Owhashi M, Heber-Katz E. Protection from experimental allergic encephalomyelitis conferred by a monoclonal antibody directed against a shared idiotype on rat T cell receptors specific for myelin basic protein. J Exp Med 1988;168:2153-2164
14. Utz U, Biddison WE, McFarland HF, McFarlin DE, Flerlage M, Martin R. Skewed T-cell receptor repertoire in genetically identical twins correlates with multiple sclerosis. Nature 1993;364:243-247
15. Kotzin BL, Karuturi S, Chou YK, Lafferty J, Forrester JM, Better M, et al. Preferential T-cell receptor β-chain variable gene use in myelin basic protein-reactive T-cell clones from patients with multiple sclerosis. Proc Natl Acad Sei U S A 1991;88:9161-9165
16. Oksenberg JR, Stuart S, Begovich AB, Bell RB, Erlich HA, Steinman L, et al. Limited heterogeneity of rearranged T-cell receptor V alpha transcripts in brains of multiple sclerosis patients [published erratum appears in Nature 1991;353:94]. Nature 1990;345:344-346
17. Vandenbark AA, Chou YK, Bourdette DN, Whitham R, Hashim GA, Offner H. T cell receptor peptide therapy for autoimmune disease. J Autoimmun 1992;5(Suppl A):83-92
18. Wucherpfennig KW, Newcombe J, Li H, Keddy C, Cuzner ML, Hafler DA. T cell receptor Va-V repertoire and cytokine gene expression in active multiple sclerosis lesions. J Exp Med 1992; 175:993-1002
19. Meinl E, Weber F, Drexler K, Morelle C, Ott M, SaruhanDireskeneli G, et al. Myelin basic protein-specific T lymphocyte repertoire in multiple sclerosis: complexity of the response and dominance of nested epitopes due to recruitment of multiple T cell clones. J Clin Invest 1993:92:2633-2643
20. Altmann DM, Sansom D, March SGE. What is the basis for HLADQ associations with autoimmune disease? Immunol Today 1991:12:267-270
21. Goodkin DE, Ransohoff RM, Rudick RA. Experimental therapies for multiple sclerosis: current status. Cleve Clin J Med 1992:59:63-74
22. Lindsey JW, Hodgkinson S, Mehta R, Mitchell D, Enzmann D, Steinman L. Repeated treatment with chimeric anti-CD4 antibody in multiple sclerosis. Ann Neurol 1994;36:183-189
23. Barkhof F, Thompson AJ, Hodgkinson S, van Oosten B, Lai M, Polman CH, et al. Double-blind placebo-controlled, MR monitored exploratory trial of chimeric anti-CD4 antibodies in MS [abstract]. J Neuroimmunol Suppl 1995;1:15
24. Sriram S, Carroll L, Fortin S, Cooper S, Ranges G. In vivo immunomodulation by monoclonal anti-CD4 antibody. II. Effect on T cell response to myelin basic protein and experimental allergic encephalomyelitis. J Immunol 1988; 141:464-468
25. Wynn DR. Rodriguez M. O'Fallon WM, Kurland LT. A reappraisal of the epidemiology of multiple sclerosis in Olmsted County. Minnesota. Neurology 1990;40:780-786
26. Kennedy PGE, Steiner l. On the possible viral aetiology of multiple sclerosis. Q J Med 1994:87:523-528
27. Rodriguez M. Multiple sclerosis: basic concepts and hypothesis. Mayo Clin Proc 1989;64:570-576
28. Reddy EP. Sandberg-Wollheim M, Mettus RV. Ray PE, DeFreitas E, Koprowski H. Amplification and molecular cloning of HTLV-I sequences from DNA of multiple sclerosis patients [published erratum appears in Science 1989;246:246]. Science 1989;243:529533
29. Richardson JH, Wucherpfennig KW, Endo N, Rudge P, Dalgleish AG, Hafler DA. PCR analysis of DNA from multiple sclerosis patients for the presence of HTLV-I. Science 1989;246:821-823
30. Challoner PB, Smith KT, Parker JD, MacLeod DL, Coulter SN, Rose TM, et al. Plaque-associated expression of human herpesvirus 6 in multiple sclerosis. Proc Natl Acad Sei U S A 1995;92:74407444
31. 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
32. Zhang Y, Burger D, Saruhan G, Jeannet M, Steck AJ. The Tlymphocyte response against myelin-associated glycoprotein and myelin basic protein in patients with multiple sclerosis. Neurology 1993;43:403-407
33. Sun J, Link H, Olsson T, Xiao BG, Andersson G, Ekre HP, et al. T and B cell responses to myelin-oligodendrocyte glycoprotein in multiple sclerosis. J Immunol 1991;146:1490-1495
34. Jonker M, van Lambalgen R, Mitchell DJ, Durham SK, Steinman L. Successful treatment of EAE in rhesus monkeys with MHC class II specific monoclonal antibodies. J Autoimmun 1988; 1:399414
35. Bo L, Mork S, Kong PA, Nyland H, Pardo CA, Trapp BD. Detection of MHC class H-antigens on macrophages and microglia, but not on astrocytes and endothelia in active multiple sclerosis lesions. J Neuroimmunol 1994;51:135-146
36. McGeer PL, Itagaki S, Tago H, McGeer EG. Reactive microglia in patients with senile dementia of the Alzheimer type are positive for the histocompatibility glycoprotein HLA-DR. Neurosci Lett 1987;79:195-200
37. Raine CS. Multiple sclerosis: immune system molecule expression in the central nervous system. J Neuropathol Exp Neurol 1994;53:328-337
38. Sobel RA. The pathology of multiple sclerosis. Neurol Clin 1995 Feb;13:l-21
39. McCallum K, Esiri MM, Tourtellotte WW, Booss J. T cell subsets in multiple sclerosis: gradients at plaque borders and differences in nonplaque regions. Brain 1987;! 10:1297-1308
40. Tsuchida T, Parker KC, Turner RV, McFarland HF, Coligan JE, Biddison WE. Autoreactive CD8+ T-cell responses to human myelin protein-derived peptides [published erratum appears in Proc Natl Acad Sei U S A 1995;92:9432]. Proc Natl Acad Sei U S A 1994;91:10859-10863
41. Grenier Y, Ruijs TC, Robitaille Y, Olivier A, Antel JP. Immunohistochemical studies of adult human glial cells. J Neuroimmunol 1989:21:103-115
42. Koh D-R, Fung-Leung W-P, Ho A, Gray D, Acha-Orbea H, Mak TW. Less mortality but more relapses in experimental allergic encephalomyelitis in CDS ' mice. Science 1992;256:1210-1213
43. Jiang H, Zhang SI, Pernis B. Role of CD8+ T cells in murine experimental allergic encephalomyelitis. Science 1992;256:12131215
44. Sethna MP, Lampson LA. Immune modulation within the brain: recruitment of inflammatory cells and increased major histocompatibility antigen expression following intracerebral injection of interferon-gamma. J Neuroimmunol 1991;34:121-132
45. Lipton HL, Dal Canto MC. Theiler's virus-induced demyelination: prevention by immunosuppression. Science 1976; 192:62-64
46. Rodriguez M, Quddus J. Effect of cyclosporin A, silica quartz dust, and protease inhibitors on virus-induced demyelination. J Neuroimmunol 1986; 13:159-174
47. Rodriguez M, Sriram S. Successful therapy of Theiler's virusinduced demyelination (DA strain) with monoclonal anti-Lyt-2 antibody. J Immunol 1988:140:2950-2955
48. Fiette L, Aubert C, Brahic M, Rossi CP. Theiler's virus infection of β2-microglobulin-deficient mice. J Virol 1993;67:589-592
49. Rodriguez M, Dunkel AJ, Thiemann RL, Leibowitz J, Zijlstra M, Jaenisch R. Abrogation of resistance to Theiler's virus-induced demyelination in H-2b mice deficient in β2-microglobulin. J Immunol 1993; 151:266-276
50. Esiri MM, Reading MC. Macrophage populations associated with multiple sclerosis plaques. Neuropathol Appl Neurobiol 1987; 13:451-465
51. Rodriguez M, Scheithauer B. Ultrastructure of multiple sclerosis. Ultrastruct Pathol 1994;18:3-13
52. Brück W, Schmied M, Suchanek G, Brück Y, Breitschopf H, Poser S, et al. Oligodendrocytes in the early course of multiple sclerosis. AnnNeurol 1994;35:65-73
53. Lassmann H, Suchanek G, Ozawa K. Histopathology and thé blood-cerebrospinal fluid barrier in multiple sclerosis. Ann Neurol 1994;36(Suppl 1):S42-S46
54. Lassmann H, Schmied M, Vass K, Hickey WF. Bone marrow derived elements and resident microglia in brain inflammation. Glia 1993;7:19-24
55. Brosnan CF, Bornstein MB, Bloom BR. The effects of macrophage depletion on the clinical and pathologic expression of experimental allergic encephalomyelitis. J Immunol 1981 ; 126:614-620
56. Matsumoto Y, Ohmori K, Fujiwara M. Microglial and astroglial reactions to inflammatory lesions of experimental allergic encephalomyelitis in the rat central nervous system. J Neuroimmunol 1992;37:23-33
57. Lee SC, Liu W, Dickson DW, Brosnan CF, Berman JW. Cytokine production by human fetal microglia and astrocytes: differential induction by lipopolysaccharide and IL-Iβ. J Immunol 1993; 150:2659-2667
58. Sebire G, Emilie D, Wallon C, Hery C, Devergne O, Delfraissy JF, et al. In vitro production of IL-6, IL-1 β, and tumor necrosis factoroc by human embryonic microglial and neural cells. J Immunol 1993;150:1517-1523
59. Gehrmann J, Banati RB, Kreutzberg GW. Microglia in the immune surveillance of the brain: human microglia constitutively express HLA-DR molecules. J Neuroimmunol 1993;48:189-198
60. Williams K Jr, Ulvestad E, Cragg L, Blain M, Antel JP. Induction of primary T cell responses by human glial cells. J Neurosci Res 1993;36:382-390
61. Gonzalez-Scarano F, Grossman RI, Galetta S, Atlas SW, Silberberg DH. Multiple sclerosis disease activity correlates with gadoliniumenhanced magnetic resonance imaging. AnnNeurol 1987;21:300306
62. Wu E, Raine CS. Multiple sclerosis: interactions between oligodendrocytes and hypertrophie astrocytes and their occurrence in other, nondemyelinating conditions. Lab Invest 1992;67:88-99
63. McKeown SR, Alien IV. The fragility of cerebral lysosomes in multiple sclerosis. Neuropathol Appl Neurobiol 1979;5:405-415
64. Raine CS. Multiple sclerosis and chronic relapsing EAE: comparative ultrastructural neuropathology. In: Hallpike JF, Adams CWM, Tourtellotte WW, editors. Multiple Sclerosis: Pathology, Diagnosis and Management. Baltimore: Williams & Wilkins; 1983. pp 413-460
65. Ghatak NR. Occurrence of oligodendrocytes within astrocytes in demyelinating lesions. J Neuropathol Exp Neurol 1992;51:40-46
66. Prineas JW, Kwon EE, Goldenberg PZ, Cho ES, Sharer LR. Interaction of astrocytes and newly formed oligodendrocytes in resolving multiple sclerosis lesions. Lab Invest 1990;63:624-636
67. Aloisi F, Care A, Borsellino G, Gallo P, Rosa S, Bassani A, et al. Production of hemolymphopoietic cytokines (IL-6, IL-8, colonystimulating factors) by normal human astrocytes in response to ILlβ and tumor necrosis factor-cc. J Immunol 1992; 149:2358-2366
68. Hohlfeld R. Neurological autoimmune disease and the trimolecular complex of T-lymphocytes. AnnNeurol 1989;25:531-538
69. Hickey WF, Kimura H. Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 1988;239:290-292
70. Matsumoto Y, Ohmori K, Fujiwara M. Immune regulation by brain cells in the central nervous system: microglia but not astrocytes present myelin basic protein to encephalitogenic T cells under in vivo-mimicking conditions. Immunology 1992:76:209-216
71. Weber F, Meinl E, Aloisi F, Nevinny-Stickel C, Albert E, Wekerle H, et al. Human astrocytes are only partially competent antigen presenting cells: possible implications for lesion development in multiple sclerosis. Brain 1994:117:59-69
72. Meinl E, Aloisi F, Ertl B, Weber F, de Waal Malefyt R, Wekerle H, et al. Multiple sclerosis: immunomodulatory effects of human astrocytes on T cells. Brain 1994; 117:1323-1332
73. Wilkin GP, Marriott DR, Cholewinski AJ. Astrocyte heterogeneity. Trends Neurosci 1990;13:43-46
74. Khoury SJ, Hancock WW, Weiner HL. Oral tolerance to myelin basic protein and natural recovery from experimental autoimmune encephalomyelitis are associated with downregulation of inflammatory cytokines and differential upregulation of transforming growth factor β, interleukin 4, and prostaglandin E expression in the brain. J Exp Med 1992; 176:1355-1364
75. Selmaj K, Raine CS, Cross AH. Anti-tumor necrosis factor therapy abrogates autoimmune demyelination. Ann Neurol 1991;30:694700
76. Tokuchi F, Nishizawa M, Nihei J, Motoyama K, Nagashima K, Tabira T. Lymphokine production by encephalitogenic and nonencephalitogenic T-cell clones reactive to the same antigenic determinant. J Neuroimmunol 1990;30:71-79
77. Renno T, Krakowski M, Piccirillo C, Lin JY. Owens T. TNF-oc expression by resident microglia and infiltrating leukocytes in the central nervous system of mice with experimental allergic encephalomyelitis: regulation by TH1 cytokines. J Immunol 1995:154:944-953
78. Jenkins HG, Ikeda H. Tumour necrosis factor causes an increase in axonal transport of protein and demyelination in the mouse optic nerve. J Neurol Sei 1992:108:99-104
79. Butt AM, Jenkins HG. Morphological changes in oligodendrocytes in the intact mouse optic nerve following intravitreal injection of tumour necrosis factor. J Neuroimmunol 1994;51:27-33
80. Probert L, Akassoglou K, Pasparakis M, Kontogeorgos G, Kollias G. Spontaneous inflammatory demyelinating disease in transgenic mice showing central nervous system-specific expression of tumor necrosis factor a. Proc Natl Acad Sei U S A 1995;92:11294-11298
81. Sharief MK, Thompson EJ. In vivo relationship of tumor necrosis factor-alpha to blood-brain barrier damage in patients with active multiple sclerosis. J Neuroimmunol 1992;38:27-33
82. Selmaj KW, Raine CS. Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann Neurol 1988:23:339-346
83. Merrill JE. Effects of interleukin-1 and tumor necrosis factor-a on astrocytes, microglia, oligodendrocytes, and glial precursors in vitro. Dev Neurosci 1991:13:130-137
84. Zajicek JP, Wing M, Scolding NJ, Compston DA. Interactions between oligodendrocytes and microglia: a major role for complement and tumor necrosis factor in oligodendrocyte adherence and killing. Brain 1992;! 15:1611-1631
85. Paya CV, Leibson PJ, Patick AK, Rodriguez M. Inhibition of Theiler's virus-induced demyelination in vivo by tumor necrosis factor alpha. Int Immunol 1990;2:909-913
86. Maimone D, Gregory S, Arnason BGW, Reder AT. Cytokine levels in the cerebrospinal fluid and serum of patients with multiple sclerosis. J Neuroimmunol 1991;32:67-74
87. Peter JB, Boctor FN, Tourtellotte WW. Serum and CSF levels of IL-2, sIL-2R, TNF-a, and IL-Iβ in chronic progressive multiple sclerosis: expected lack of clinical utility. Neurology 1991; 41:121-123
88. Merrill JE, Strom SR, Ellison GW, Myers LW. In vitro study of mediators of inflammation in multiple sclerosis. J Clin Immunol 1989:9:84-96
89. Rudick RA, Ransohoff RM. Cytokine secretion by multiple sclerosis monocytes: relationship to disease activity. Arch Neurol 1992:49:265-270
90. CannellaB, Raine CS. The adhesion molecule and cytokine profile of multiple sclerosis lesions. Ann Neurol 1995:37:424-435
91. Brosnan CF. Cannella B, Battistini L, Raine CS. Cytokine localization in multiple sclerosis lesions: correlation with adhesion molecule expression and reactive nitrogen species. Neurology 1995;45(Suppl6):S16-S21
92. Cannella B, Raine CS. Cytokines up-regulate la expression in organotypic cultures of central nervous system tissue. J Neuroimmunol 1989:24:239-248
93. Traugott U. Lebon P. Multiple sclerosis: involvement of interferons in lesion pathogenesis. Ann Neurol 1988;24:243-251
94. Beck J, Rondot P, Catinot L, Falcoff E, Kirchner H, Wietzerbin J. Increased production of interferon gamma and tumor necrosis factor precedes clinical manifestation in multiple sclerosis: do cytokines trigger off exacerbations? Acta Neurol Scand 1988; 78:318-323
95. Panitch HS, Hirsch RL, Schindler J, Johnson KP. Treatment of multiple sclerosis with gamma interferon: exacerbations associated with activation of the immune system. Neurology 1987:37:10971102
96. Olsson T, Zhi WW, Hojeberg B, Kostulas V. Jiang YP, Anderson G, et al. Autoreactive T lymphocytes in multiple sclerosis determined by antigen-induced secretion of interferon-gamma. J Clin Invest 1990:86:981-985
97. Taupin V, Renno T. Bourbonnière L, Peterson AC, Rodriguez M, Owens T. Increased severity of experimental autoimmune encephalomyelitis, chronic macrophage/microglial reactivity, and demyelination in transgenic mice producing tumor necrosis factorex in the central nervous system. Eur J Immunol 1997:27:905-913
98. Becher B, Dodelet V, Fedorowicz V, Antel JP. Soluble tumor necrosis factor receptor inhibits interleukin 12 production by stimulated human adult microglial cells in vitro. J Clin Invest 1996:98:1539-1543
99. Windhagen A, Newcombe J. Dangond F, Strand C. Woodroofe MN, Cuzner ML, et al. Expression of costimulatory molecules B7-1 (CD80), B7-2 (CD86), and interleukin 12 cytokine in multiple sclerosis lesions. J Exp Med 1995:182:1985-1996
100. Lassmann H, Brunner C, Bradl M, Linington C. Experimental allergic encephalomyelitis: the balance between encephalitogenic T lymphocytes and demyelinating antibodies determines size and structure of demyelinated lesions. Acta Neuropathol 1988;75:566576
101. Mehta PD, Miller JA, Tourtellotte WW. Oligoclonal IgG bands in plaques from multiple sclerosis brains. Neurology 1982:32:372376
102. Linington C, Bradl M, Lassmann H, Brunner C, Vass K. Augmentation of demyelination in rat acute allergic encephalomyelitis by circulating mouse monoclonal antibodies directed against a myelin/oligodendrocyte glycoprotein. Am J Pathol 1988; 130:443454
103. Scolding N, Linington C, Compston A. Immune mechanisms in the pathogenesis of demyelinating diseases. Autoimmunity 1989; 4:131-142
104. Scolding NJ, Houston WAJ, Morgan BP, Campbell AK, Compston DAS. Reversible injury of cultured rat oligodendrocytes by complement. Immunology 1989:67:441-446
105. Scolding NJ, Morgan BP, Houston A, Campbell AK, Linington C, Compston DAS. Normal rat serum cytotoxicity against syngeneic oligodendrocytes: complement activation and attack in the absence of anti-myelin antibodies. J Neurol Sei 1989:89:289-300
106. Zajicek J, Wing MG, Lachmann PJ, Compston DAS. Mechanisms of oligodendrocyte interaction with normal human serum-defining the role of complement. J Neurol Sei 1992; 108:65-72
107. Zajicek JP, Wing MG, Compston DAS. Normal human oligodendrocyte susceptibility to complement and the expression of complement regulatory proteins on their surface [abstract]. J Neurol 1992;239(Suppl2):S97
108. Wren DR, Noble M. Oligodendrocytes and oligodendrocyte/type-2 astrocyte progenitor cells of adult rats are specifically susceptible to the lytic effects of complement in absence of antibody. Proc Natl Acad Sei USA 1989;86:9025-9029
109. Lumsden CE. The immunogenesis of the multiple sclerosis plaque. Brain Res 1971;28:365-390
110. Morgan BP, Campbell AK, Compston DAS. Terminal component of complement (C9) in cerebrospinal fluid of patients with multiple sclerosis. Lancet 1984;2:251-254
111. Compston DAS, Morgan BP, Campbell AK. Cerebrospinal fluid complement components in multiple sclerosis. In: Lowenthal A, Raus J, editors. Cellular and Humoral Components of Cerebrospinal Fluid in Multiple Sclerosis. New York: Plenum Press; 1987. pp 201-209
112. Gay D, Esiri M. Blood-brain barrier damage in acute multiple sclerosis plaques: an immunocytological study. Brain 1991; 114:557-572
113. Rodriguez M, Wynn DR, Kimlinger TK, Katzmann JA. Terminal component of complement (C9) in the cerebrospinal fluid of patients with multiple sclerosis and neurologic controls. Neurology 1990;40:855-857
114. Piddlesden SJ, Lassmann H, Zimprich F, Morgan BP, Linington C. The demyelinating potential of antibodies to myelin oligodendrocyte glycoprotein is related to their ability to fix complement. Am J Pathol 1993; 143:555-564
115. Rodriguez M, Lucchinetti CF, Clark RJ, Yaksh TL, Markowitz H, Lennon VA. Immunoglobulins and complement in demyelination induced in mice by Theiler's virus. J Immunol 1988; 140:800806
116. Prineas JW, Raine CS. Electron microscopy and immunoperoxidase studies of early multiple sclerosis lesions. Neurology 1976;26:29-32
117. Raine CS. The Dale E. McFarlin memorial lecture: the immunology of the multiple sclerosis lesion. Ann Neurol 1994;36(Suppl 1):S61-S72
118. McDonald WI. Rachelle Fishman-Matthew Moore Lecture: the pathological and clinical dynamics of multiple sclerosis. J Neuropathol Exp Neurol 1994;53:338-343
119. Nesbit GM, Forbes GS, Scheithauer BW, Okazaki H, Rodriguez M. Multiple sclerosis: histopathologic and MR and/or CT correlation in 37 cases at biopsy and 3 cases at autopsy. Radiology 1991; 180:467-474
120. Raine CS,WuE. Multiple sclerosis: remyelination in acute lesions. J Neuropathol Exp Neurol 1993;52:199-204
121. Rodriguez M, Scheithauer BW, Forbes G, Kelly PJ. Oligodendrocyte injury is an early event in lesions of multiple sclerosis. Mayo ClinProc 1993;68:627-636
122. DawsonJW. The histology of disseminated sclerosis. Trans R Soc Edinburgh 1916;50:517-740
123. Rodriguez M, Prayoonwiwat N, Howe C, Sanborn K. Proteolipid protein gene expression in demyelination and remyelination of the central nervous system: a model for multiple sclerosis. J Neuropathol Exp Neurol 1994;53:136-143
124. Périer O, Grégoire A. Electron microscopic features of multiple sclerosis lesions. Brain 1965;88:937-952
125. Prineas JW, Barnard RO, Kwon EE, Sharer LR, Cho ES. Multiple sclerosis: remyelination of nascent lesions. Ann Neurol 1993;33:137-151
126. Selmaj K, Brosnan CE, Raine CS. Colocalization of lymphocytes bearing yo T-cell receptor and heat shock protein hsp65+ oligodendrocytes in multiple sclerosis. Proc Natl Acad Sei USA 1991;88:6452-6456
127. Ozawa K, Suchanek G, Breitschopf H, Brack W, Budka H, Jellinger K, et al. Patterns of oligodendroglia pathology in multiple sclerosis. Brain 1994;! 17:1311-1322
128. Lucchinetti CF, Brack W, Rodriguez M, Lassmann H. Distinct patterns of multiple sclerosis pathology indicates heterogeneity on pathogenesis. Brain Pathol 1996;6:259-274
129. Marburg O. Die sogenannte "akute multiple Sklerose" (Encephalomyelitis periaxialis scleroticans). Jahrb Psychiatrie Neurol 1906; 27:213-312
130. Richardson EP Jr. Pathology of multiple sclerosis: some new developments. Clin Neurosci 1994;2:253-257
131. Rodriguez M, Miller DJ. Immune promotion of central nervous system remyelination. Prog Brain Res 1994; 103:343-355
132. Rodriguez M, Lindsley MD. Immunosuppression promotes CNS remyelination in chronic virus-induced demyelinating disease. Neurology 1992;42:348-357
133. Lassmann H. Comparative Neuropathology of Chronic Experimental Allergic Encephalomyelitis and Multiple Sclerosis. Berlin: Springer-Verlag; 1983
134. Raine CS, Traugott U. Chronic relapsing experimental autoimmune encephalomyelitis: ultrastructure of the central nervous system of animals treated with combinations of myelin components. Lab Invest 1983;48:275-284
135. Rodriguez M, Lennon VA. Immunoglobulins promote remyelination in the central nervous system. Ann Neurol 1990;27:1217
136. Miller DJ, Sanborn KS, Katzmann JA, Rodriguez M. Monoclonal autoantibodies promote central nervous system repair in an animal model of multiple sclerosis. J Neurosci 1994; 14:6230-6238
137. Asakura K, Miller DJ, Murray K, Bansal R, Pfeiffer SE, Rodriguez M. Monoclonal autoantibody SCH94.03, which promotes central nervous system remyelination, recognizes an antigen on the surface of oliogodendrocytes. J Neurosci Res 1996;43:273-281