Brain microglia and blood-derived macrophages: Molecular profiles and functional roles in multiple sclerosis and animal models of autoimmune demyelinating disease

Brain Research Reviews

Volumn 46, Issue 3, 2004, Pages 261-281

  Raivich, Gennadij ^a   Banati, Richard ^b  

^a Perinatal Brain Repair Group   (United Kingdom)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Bone marrow chimaera; Cellular and molecular biology; Lymphocyte; Major histocompatibility complex; Neuroglia and myelin

Indexed keywords

CELL ADHESION MOLECULE; CHEMOKINE; CYTOKINE; GLYCOLIPID; GROWTH FACTOR; IMMUNOGLOBULIN; LIPID; MYELIN; NEUROTROPHIN; PROTEINASE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR; TRIACYLGLYCEROL LIPASE;

APOPTOSIS; AUTOIMMUNE DISEASE; CELL FUNCTION; CELL INTERACTION; CELL MIGRATION; CELL POPULATION; CELL SUBPOPULATION; CELLULAR IMMUNITY; CENTRAL NERVOUS SYSTEM; CHIMERA; DEMYELINATING DISEASE; ENZYME ACTIVITY; GENETICS; IMMUNE RESPONSE; INFLAMMATION; LYMPHOCYTE ACTIVATION; MACROPHAGE; MAJOR HISTOCOMPATIBILITY COMPLEX; MICROGLIA; MOLECULAR BIOLOGY; MONOCYTE; MULTIPLE SCLEROSIS; NERVE FIBER; NEUROPATHOLOGY; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REMISSION; REVIEW; T LYMPHOCYTE; WHITE MATTER;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; IMMUNE TOLERANCE; INFLAMMATION MEDIATORS; MACROPHAGES; MICROGLIA; MULTIPLE SCLEROSIS; T-LYMPHOCYTES;

EID: 9644310402     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2004.06.006     Document Type: Review

References (270)

1. Abdul-Majid K.B., Stefferl A., Bourquin C., Lassmann H., Linington C., Olsson T., Kleinau S., Harris R.A. Fc receptors are critical for autoimmune inflammatory damage to the central nervous system in experimental autoimmune encephalomyelitis. Scand. J. Immunol. 55:2002;70-81
2. Ahn M., Min D.S., Kang J., Jung K., Shin T. Increased expression of phospholipase D1 in the spinal cords of rats with experimental autoimmune encephalomyelitis. Neurosci. Lett. 316(2):2001;95-98
3. Alliot F., Godin I., Pessac B. Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain. Dev. Brain Res. 117:1999;145-152
4. Angelov D.N., Neiss W.F., Streppel M., Walther M., Guntinas-Lichius O., Stennert E. ED2-positive perivascular cells act as neuronophages during delayed neuronal loss in the facial nucleus of the rat. Glia. 16:1996;129-139
5. Anthony D.C., Ferguson B., Matyzak M.K., Miller K.M., Esiri M.M., Perry V.H. Differential matrix metalloproteinase expression in cases of multiple sclerosis and stroke. Neuropathol. Appl. Neurobiol. 23:1997;406-415
6. Bagasra O., Michaels F.H., Zheng Y.M., Bobroski L.E., Spitsin S.V., Fu Z.F., Tawadros R., Koprowski H. Activation of the inducible form of nitric oxide synthase in the brains of patients with multiple sclerosis. Proc. Natl. Acad. Sci. U. S. A. 92:1995;12041-12045
7. Balashov K.E., Rottman J.B., Weiner H.L., Hancock W.W. CCR5(+) and CXCR3(+) T cells are increased in multiple sclerosis and their ligands MIP-1alpha and IP-10 are expressed in demyelinating brain lesions. Proc. Natl. Acad. Sci. U. S. A. 96:1999;6873-6878
8. Banati R.B., Gehrmann J., Lannes-Vieira J., Wekerle H., Kreutzberg G.W. Inflammatory reaction in experimental autoimmune encephalomyelitis (EAE) is accompanied by a microglial expression of the beta A4-amyloid precursor protein (APP). Glia. 14:1995;209-215
9. 3H]PK11195 binding to activated microglia. J. Neurocytol. 26:1997;77-82
10. 11C](R)-PK11195 positron emission tomography imaging of activated microglia in vivo in Rasmussen's encephalitis. Neurology. 53:1999;2199-2203
11. Banati R.B., Newcombe J., Gunn R.N., Cagnin A., Turkheimer F., Heppner F., Price G., Wegner F., Giovannoni G., Miller D.H., Perkin G.D., Smith T., Hewson A.K., Bydder G., Kreutzberg G.W., Jones T., Cuzner M.L., Myers R. The peripheral benzodiazepine binding site in the brain in multiple sclerosis: quantitative in vivo imaging of microglia as a measure of disease activity. Brain. 123:2000;2321-2337
12. Barnum S.R. Complement biosynthesis in the central nervous system. Crit. Rev. Oral Biol. Med. 6:1995;132-146
13. Barnum S.R. Complement in central nervous system inflammation. Immunol. Res. 26:2002;7-13
14. Bartnik B.L., Juurlink B.H., Devon R.M. Macrophages: their myelinotrophic or neurotoxic actions depend upon tissue oxidative stress. Mult. Scler. Feb. 6(1):2000;37-42
15. Battistini L., Fischer F.R., Raine C.S., Brosnan C.F. CD1b is expressed in multiple sclerosis lesions. J. Neuroimmunol. 67:1996;145-151
16. Bauer J., Berkenbosch F., Van Dam A.M., Dijkstra C.D. Demonstration of interleukin-1 beta in Lewis rat brain during experimental allergic encephalomyelitis by immunocytochemistry at the light and ultrastructural level. J. Neuroimmunol. 48:1993;13-21
17. Bauer J., Sminia T., Wouterlood F.G., Dijkstra C.D. Phagocytic activity of macrophages and microglial cells during the course of acute and chronic relapsing experimental autoimmune encephalomyelitis. J. Neurosci. Res. 38:1994;365-375
18. Bauer J., Huitinga I., Zhao W., Lassmann H., Hickey W.F., Dijkstra C.D. The role of macrophages, perivascular cells, and microglial cells in the pathogenesis of experimental autoimmune encephalomyelitis. Glia. 15:1995;437-446
19. Bauer J., Bradl M., Hickley W.F., Forss-Petter S., Breitschopf H., Linington C., Wekerle H., Lassmann H. T-cell apoptosis in inflammatory brain lesions: destruction of T cells does not depend on antigen recognition. Am. J. Pathol. 153:1998;715-724
20. Becher B., Durell B.G., Miga A.V., Hickey W.F., Noelle R.J. The clinical course of experimental autoimmune encephalomyelitis and inflammation is controlled by the expression of CD40 within the central nervous system. J. Exp. Med. 193:2001;967-974
21. Bitsch A., da Costa C., Bunkowski S., Weber F., Rieckmann P., Bruck W. Identification of macrophage populations expressing tumor necrosis factor-alpha mRNA in acute multiple sclerosis. Acta Neuropathol. (Berl.). 95:1998;373-377
22. Bitsch A., Kuhlmann T., Da Costa C., Bunkowski S., Polak T., Bruck W. Tumour necrosis factor alpha mRNA expression in early multiple sclerosis lesions: correlation with demyelinating activity and oligodendrocyte pathology. Glia. 29:2000;366-375
23. Bo L., Peterson J.W., Mork S., Hoffman P.A., Gallatin W.M., Ransohoff R.M., Trapp B.D. Distribution of immunoglobulin superfamily members ICAM-1, -2, -3, and the beta 2 integrin LFA-1 in multiple sclerosis lesions. J. Neuropathol. Exp. Neurol. 55:1996;1060-1072
24. Bohatschek M., Gschwendtner A., von Maltzan X., Kloss C.U.A., Pfeffer K., Labow M., Bluthmann H., Raivich G. Cytokine-mediated regulation of MHC1, MHC2 and B7-2, in the axotomized mouse facial motor nucleus. Soc. Neurosci. Abs. 25:1999;1535
25. Bohatschek M., Kloss C.U., Kalla R., Raivich G. In vitro model of microglial deramification: ramified microglia transform into amoeboid phagocytes following addition of brain cell membranes to microglia-astrocyte cocultures. J. Neurosci. Res. 64:2001;508-522
26. Bonetti B., Pohl J., Gao Y.L., Raine C.S. Cell death during autoimmune demyelination: effector but not target cells are eliminated by apoptosis. J. Immunol. 159:1997;5733-5741
27. Botto M., Walport M.J. C1q, autoimmunity and apoptosis. Immunobiology. 205:2002;395-406
28. Boyle E.A., McGeer P.L. Cellular immune response in multiple sclerosis plaques. Am. J. Pathol. 137:1990;575-584
29. Brenner T., Brocke S., Szafer F., Sobel R.A., Parkinson J.F., Perez D.H., Steinman L. Inhibition of nitric oxide synthase for treatment of experimental autoimmune encephalomyelitis. J. Immunol. 158:1997;2940-2946
30. Brocker T., Riedinger M., Karjalainen K. Targeted expression of major histocompatibility complex (MHC) class II molecules demonstrates that dendritic cells can induce negative but not positive selection of thymocytes in vivo. J. Exp. Med. 185:1997;541-550
31. Brockhaus J., Moller T., Kettenmann H. Phagocytozing ameboid microglial cells studied in a mouse corpus callosum slice preparation. Glia. 16:1996;81-90
32. Bruck W., Porada P., Poser S., Rieckmann P., Hanefeld F., Kretzschmar H.A., Lassmann H. Monocyte/macrophage differentiation in early multiple sclerosis lesions. Ann. Neurol. 38:1995;788-796
33. Brune B., Ullrich V. Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Mol. Pharmacol. 32:1987;497-504
34. Bushong E.A., Martone M.E., Jones Y.Z., Ellisman M.H. Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J. Neurosci. 22:2002;183-192
35. Cagnin A., Brooks D.J., Kennedy A.M., Gunn R.N., Myers R., Turkheimer F.E., Jones T., Banati R.B. In-vivo measurement of activated microglia in dementia. Lancet. 358:2001;461-467
36. Calida D.M., Constantinescu C., Purev E., Zhang G.X., Ventura E.S., Lavi E., Rostami A. Cutting edge: C3, a key component of complement activation, is not required for the development of myelin oligodendrocyte glycoprotein peptide-induced experimental autoimmune encephalomyelitis in mice. J. Immunol. 166:2001;723
37. Cannella B., Cross A.H., Raine C.S. Adhesion-related molecules in the central nervous system. Upregulation correlates with inflammatory cell influx during relapsing experimental autoimmune encephalomyelitis. Lab. Invest. 65:1991;23-31
38. Cannella B., Pitt D., Marchionni M., Raine C.S. Neuregulin and erbB receptor expression in normal and diseased human white matter. J. Neuroimmunol. 100:1999;233-242
39. Carlin J.M., Borden E.C., Sondel P.M., Byrne G.I. Interferon-induced indoleamine 2,3-dioxygenase activity in human mononuclear phagocytes. J. Leukoc. Biol. 45:1989;29-34
40. Cautain B., Damoiseaux J., Bernard I., van Straaten H., van Breda Vriesman P., Boneu B., Druet P., Saoudi A. Essential role of TGF-beta in the natural resistance to experimental allergic encephalomyelitis in rats. Eur. J. Immunol. 31:2001;1132-1140
41. Chang T.T., Jabs C., Sobel R.A., Kuchroo V.K., Sharpe A.H. Studies in B7-deficient mice reveal a critical role for B7 costimulation in both induction and effector phases of experimental autoimmune encephalomyelitis. J. Exp. Med. 190:1999;733-740
42. Cipriani B., Chen L., Hiromatsu K., Knowles H., Raine C.S., Battistini L., Porcelli S.A., Brosnan C.F. Upregulation of group 1 CD1 antigen presenting molecules in guinea pigs with experimental autoimmune encephalomyelitis: an immunohistochemical study. Brain Pathol. 13:2003;1-9
43. Columba-Cabezas S., Serafini B., Ambrosini E., Sanchez M., Penna G., Adorini L., Aloisi F. Induction of macrophage-derived chemokine/CCL22 expression in experimental autoimmune encephalomyelitis and cultured microglia: implications for disease regulation. J. Neuroimmunol. 130:2002;10-21
44. Columba-Cabezas S., Serafini B., Ambrosini E., Aloisi F. Lymphoid chemokines CCL19 and CCL21 are expressed in the central nervous system during experimental autoimmune encephalomyelitis: implications for the maintenance of chronic neuroinflammation. Brain Pathol. 13:2003;38-51
45. Cossins J.A., Clements J.M., Ford J., Miller K.M., Pigott R., Vos W., Van der Valk P., De Groot C.J. Enhanced expression of MMP-7 and MMP-9 in demyelinating multiple sclerosis lesions. Acta Neuropathol. (Berl.). 94:1997;590-598
46. Cossmann P.H., Eggli P.S., Christ B., Kurz H. Mesoderm-derived cells proliferate in the embryonic central nervous system: confocal microscopy and three-dimensional visualization. Histochem. Cell Biol. 107:1997;205-213
47. Cross A.H., Misko T.P., Lin R.F., Hickey W.F., Trotter J.L., Tilton R.G. Aminoguanidine, an inhibitor of inducible nitric oxide synthase, ameliorates experimental autoimmune encephalomyelitis in SJL mice. J. Clin. Invest. 93:1994;2684-2690
48. Cua D.J., Sherlock J., Chen Y., Murphy C.A., Joyce B., Seymour B., Lucian L., To W., Kwan S., Churakova T., Zurawski S., Wiekowski M., Lira S.A., Gorman D., Kastelein R.A., Sedgwick J.D. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature. 421:2003;744-748
49. Cuzner M.L., Gveric D., Strand C., Loughlin A.J., Paemen L., Opdenakker G., Newcombe J. The expression of tissue-type plasminogen activator, matrix metalloproteases and endogenous inhibitors in the central nervous system in multiple sclerosis: comparison of stages in lesion evolution. J. Neuropathol. Exp. Neurol. 55:1996;1194-1204
50. Dangond F., Windhagen A., Groves C.J., Hafler D.A. Constitutive expression of costimulatory molecules by human microglia and its relevance to CNS autoimmunity. J. Neuroimmunol. 76:1997;132-138
51. Davoust N., Nataf S., Reiman R., Holers M.V., Campbell I.L., Barnum S.R. Central nervous system-targeted expression of the complement inhibitor sCrry prevents experimental allergic encephalomyelitis. J. Immunol. 163:1999;6551-6556
52. De Groot C.J., Ruuls S.R., Theeuwes J.W., Dijkstra C.D., Van der Valk P. Immunocytochemical characterization of the expression of inducible and constitutive isoforms of nitric oxide synthase in demyelinating multiple sclerosis lesions. J. Neuropathol. Exp. Neurol. 56:1997;10-20
53. Deininger M.H., Schluesener H.J. Cyclooxygenases-1 and -2 are differentially localized to microglia and endothelium in rat EAE and glioma. J. Neuroimmunol. 95:1999;202-208
54. Deininger M.H., Zhao Y., Schluesener H.J. CP-10, a chemotactic peptide, is expressed in lesions of experimental autoimmune encephalomyelitis, neuritis, uveitis and in C6 gliomas. J. Neuroimmunol. 93:1999;156-163
55. De Simone R., Giampaolo A., Giometto B., Gallo P., Levi G., Peschle C., Aloisi F. The costimulatory molecule B7 is expressed on human microglia in culture and in multiple sclerosis acute lesions. J. Neuropathol. Exp. Neurol. 54:1995;175-187
56. Dietzschold B., Schwaeble W., Schafer M.K., Hooper D.C., Zehng Y.M., Petry F., Sheng H., Fink T., Loos M., Koprowski H., et al. Expression of C1q, a subcomponent of the rat complement system, is dramatically enhanced in brains of rats with either Borna disease or experimental allergic encephalomyelitis. J. Neurol. Sci. 130:1995;11-16
57. Dowling P., Ming X., Raval S., Husar W., Casaccia- Bonnefil P., Chao M., Cook S., Blumberg B. Up-regulated p75NTR neurotrophin receptor on glial cells in MS plaques. Neurology. 53:1999;1676-1682
58. Dubois B., Masure S., Hurtenbach U., Paemen L., Heremans H., van den Oord J., Sciot R., Meinhardt T., Hammerling G., Opdenakker G., Arnold B. Resistance of young gelatinase B-deficient mice to experimental autoimmune encephalomyelitis and necrotizing tail lesions. Clin. Invest. 104:1999;1507-1515
59. Emerson M.R., LeVine S.M. Heme oxygenase-1 and NADPH cytochrome P450 reductase expression in experimental allergic encephalomyelitis: an expanded view of the stress response. J. Neurochem. 75:2000;2555-2562
60. Engelhardt B., Laschinger M., Schulz M., Samulowitz U., Vestweber D., Hoch G. The development of experimental autoimmune encephalomyelitis in the mouse requires alpha4-integrin but not alpha4beta7-integrin. J. Clin. Invest. 102:1998;2096-2105
61. Espejo C., Carrasco J., Hidalgo J., Penkowa M., Garcia A., Saez-Torres I., Martinez-Caceres E.M. Differential expression of metallothioneins in the CNS of mice with experimental autoimmune encephalomyelitis. Neuroscience. 105:2001;1055-1065
62. Ferguson B., Matyszak M.K., Esiri M.M., Perry V.H. Axonal damage in acute multiple sclerosis lesions. Brain. 120:1997;393-399
63. Fischer H.G., Reichmann G. Brain dendritic cells and macrophages/ microglia in central nervous system inflammation. J. Immunol. 166:2001;2717-2726
64. Fleury S.G., Croteau G., Sekaly R.P. CD4 and CD8 recognition of class II and class I molecules of the major histocompatibility complex. Semin. Immunol. 3:1991;177-185
65. Flugel A., Bradl M., Kreutzberg G.W., Graeber M.B. Transformation of donor-derived bone marrow precursors into host microglia during autoimmune CNS inflammation and during the retrograde response to axotomy. J. Neurosci. Res. 66:2001;74-82
66. Flugel A., Matsumuro K., Neumann H., Klinkert W.E., Birnbacher R., Lassmann H., Otten U., Wekerle H. Anti-inflammatory activity of nerve growth factor in experimental autoimmune encephalomyelitis: inhibition of monocyte transendothelial migration. Eur. J. Immunol. 31:2001;11-22
67. Ford A.L., Goodsall A.L., Hickey W.F., Sedgwick J.D. Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex vivo antigen presentation to myelin basic protein-reactive CD4+ T cells compared. J. Immunol. 154:1995;4309-4321
68. Ford A.L., Foulcher E., Lemckert F.A., Sedgwick J.D. Microglia induce CD4 T lymphocyte final effector function and death. J. Exp. Med. 184:1996;1737-1745
69. Garthwaite G., Goodwin D.A., Batchelor A.M., Leeming K., Garthwaite J. Nitric oxide toxicity in CNS white matter: an in vitro study using rat optic nerve. Neuroscience. 109:2002;145-155
70. Gasque P., Fontaine M., Morgan B.P. Complement expression in human brain. Biosynthesis of terminal pathway components and regulators in human glial cells and cell lines. J. Immunol. 154:1995;4726-4733
71. Gasque P., Singhrao S.K., Neal J.W., Wang P., Sayah S., Fontaine M., Morgan B.P. The receptor for complement anaphylatoxin C3a is expressed by myeloid cells and nonmyeloid cells in inflamed human central nervous system: analysis in multiple sclerosis and bacterial meningitis. J. Immunol. 160:1998;3543-3554
72. Gerritse K., Laman J.D., Noelle R.J., Aruffo A., Ledbetter J.A., Boersma W.J., Claassen E. CD40-CD40 ligand interactions in experimental allergic encephalomyelitis and multiple sclerosis. Proc. Natl. Acad. Sci. U. S. A. 93:1996;2499-2504
73. Geurts J.J., Wolswijk G., Bo L., Van Der Valk P., Polman C.H., Troost D., Aronica E. Altered expression patterns of group I and II metabotropic glutamate receptors in multiple sclerosis. Brain. 126:2003;1755-1766
74. Giovannoni G., Heales S.J., Land J.M., Thompson E.J. The potential role of nitric oxide in multiple sclerosis. Mult. Scler. 4:1998;212-216
75. Girvin A.M., Dal Canto M.C., Miller S.D. CD40/CD40L interaction is essential for the induction of EAE in the absence of CD28-mediated co-stimulation. J. Autoimmun. 18:2002;83-94
76. Gobin S.J., Montagne L., Van Zutphen M., Van Der Valk P., Van Den Elsen P.J., De Groot C.J. Upregulation of transcription factors controlling MHC expression in multiple sclerosis lesions. Glia. 36:2001;68-77
77. Goldenberg P.Z., Kwon E.E., Benjamins J.A., Whitaker J.N., Quarles R.H., Prineas J.W. Opsonization of normal myelin by anti-myelin antibodies and normal serum. J. Neuroimmunol. 23:1989;157-166
78. Gordon E.J., Myers K.J., Dougherty J.P., Rosen H., Ron Y. Both anti-CD11a (LFA-1) and anti-CD11b (MAC-1) therapy delay the onset and diminish the severity of experimental autoimmune encephalomyelitis. J. Neuroimmunol. 62:1995;153-160
79. Gran B., Zhang G.X., Yu S., Li J., Chen X.H., Ventura E.S., Kamoun M., Rostami A. IL-12p35-deficient mice are susceptible to experimental autoimmune encephalomyelitis: evidence for redundancy in the IL-12 system in the induction of central nervous system autoimmune demyelination. J. Immunol. 169:2002;7104-7110
80. Grewal I.S., Foellmer H.G., Grewal K.D., Wang H., Lee W.P., Tumas D., Janeway C.A. Jr., Flavell R.A. CD62L is required on effector cells for local interactions in the CNS to cause myelin damage in experimental allergic encephalomyelitis. Immunity. 14:2001;291-302
81. Guillemin G.J., Kerr S.J., Pemberton L.A., Smith D.G., Smythe G.A., Armati P.J., Brew B.J. IFN-beta1b induces kynurenine pathway metabolism in human macrophages: potential implications for multiple sclerosis treatment. J. Interferon. Cytokine. Res. 21:2001;1097-1101
82. Gutowski N.J., Newcombe J., Cuzner M.L. Tenascin-R and C in multiple sclerosis lesions: relevance to extracellular matrix remodelling. Neuropathol. Appl. Neurobiol. 25:1999;207-214
83. Gveric D., Kaltschmidt C., Cuzner M.L., Newcombe J. Transcription factor NF-kappaB and inhibitor I kappaBalpha are localized in macrophages in active multiple sclerosis lesions. J. Neuropathol. Exp. Neurol. 57:1998;168-178
84. Gveric D., Cuzner M.L., Newcombe J. Insulin-like growth factors and binding proteins in multiple sclerosis plaques. Neuropathol. Appl. Neurobiol. 25:1999;215-225
85. Hayes G.M., Woodroofe M.N., Cuzner M.L. Microglia are the major cell type expressing MHC class II in human white matter. J. Neurol. Sci. 80:1987;25-37
86. Hickey W.F., Kimura H. Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science. 239:1988;290-292
87. Hoek R.M., Ruuls S.R., Murphy C.A., Wright G.J., Goddard R., Zurawski S.M., Blom B., Homola M.E., Streit W.J., Brown M.H., Barclay A.N., Sedgwick J.D. Down-regulation of the macrophage lineage through interaction with OX2 (CD200). Science. 290:2000;1768-1771
88. Hosokawa M., Klegeris A., Maguire J., McGeer P.L. Expression of complement messenger RNAs and proteins by human oligodendroglial cells. Glia. 42:2003;417-423
89. Huang D.R., Wang J., Kivisakk P., Rollins B.J., Ransohoff R.M. 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. 193:2001;713-726
90. Huitinga I., Damoiseaux J.G., Dopp E.A., Dijkstra C.D. Treatment with anti-CR3 antibodies ED7 and ED8 suppresses experimental allergic encephalomyelitis in Lewis rats. Eur. J. Immunol. 23:1993;709-715
91. Huitinga I., Ruuls S.R., Jung S., Van Rooijen N., Hartung H.P., Dijkstra C.D. Macrophages in T cell line-mediated, demyelinating, and chronic relapsing experimental autoimmune encephalomyelitis in Lewis rats. Clin. Exp. Immunol. 100:1995;344-351
92. Huitinga I., Bauer J., Strijbos P.J., Rothwell N.J., Dijkstra C.D., Tilders F.J. Effect of annexin-1 on experimental autoimmune encephalomyelitis (EAE) in the rat. Clin. Exp. Immunol. Jan. 111(1):1998;198-204
93. Hulkower K., Brosnan C.F., Aquino D.A., Cammer W., Kulshrestha S., Guida M.P., Rapoport D.A., Berman J.W. Expression of CSF-1, c-fms, and MCP-1 in the central nervous system of rats with experimental allergic encephalomyelitis. J. Immunol. 150:1993;2525-2533
94. Huseby E.S., 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. 194:2001;669-676
95. Jacobs C.A., Baker P.E., Roux E.R., Picha K.S., Toivola B., Waugh S., Kennedy M.K. Experimental autoimmune encephalomyelitis is exacerbated by IL-1 alpha and suppressed by soluble IL-1 receptor. J. Immunol. 146:1991;2983-2989
96. Jahng A.W., Maricic I., Pedersen B., Burdin N., Naidenko O., Kronenberg M., Koezuka Y., Kumar V. Activation of natural killer T cells potentiates or prevents experimental autoimmune encephalomyelitis. J. Exp. Med. 194:2001;1789-1799
97. Jander S., Stoll G. Strain-specific expression of microglial keratan sulfate proteoglycans in the normal rat central nervous system: inverse correlation with constitutive expression of major histocompatibility complex class II antigens. Glia Nov. 18(3):1996;255-260
98. Jander S., Pohl J., D'Urso D., Gillen C., Stoll G. Time course and cellular localization of interleukin-10 mRNA and protein expression in autoimmune inflammation of the rat central nervous system. Am. J. Pathol. 152:1998;975-982
99. Jee Y., Kim G., Tanuma N., Matsumoto Y. STAT expression and localization in the central nervous system during autoimmune encephalomyelitis in Lewis rats. J. Neuroimmunol. 114:2001;40-47
100. Jee Y., Yoon W.K., Okura Y., Tanuma N., Matsumoto Y. Upregulation of monocyte chemotactic protein-1 and CC chemokine receptor 2 in the central nervous system is closely associated with relapse of autoimmune encephalomyelitis in Lewis rats. J. Neuroimmunol. 128:2002;49-57
101. Jiang Y., Salafranca M.N., Adhikari S., Xia Y., Feng L., Sonntag M.K., de Fiebre C.M., Pennell N.A., Streit W.J., Harrison J.K. Chemokine receptor expression in cultured glia and rat experimental allergic encephalomyelitis. J. Neuroimmunol. 86:1998;1-12
102. Johns T.G., Bernard C.C. Binding of complement component Clq to myelin oligodendrocyte glycoprotein: a novel mechanism for regulating CNS inflammation. Mol. Immunol. 34:1997;33-38
103. Jones R.E., Mass M., Bourdette D.N. Myelin basic protein-specific T lymphocytes induce chronic relapsing experimental autoimmune encephalomyelitis in lymphocyte-deficient (SCID) mice. J. Neuroimmunol. 93:1999;92-101
104. Juedes A.E., Ruddle N.H. Resident and infiltrating central nervous system APCs regulate the emergence and resolution of experimental autoimmune encephalomyelitis. J. Immunol. 166(8):2001 (Apr. 15);5168-5175
105. Juedes A.E., Hjelmstrom P., Bergman C.M., Neild A.L., Ruddle N.H. Kinetics and cellular origin of cytokines in the central nervous system: insight into mechanisms of myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis. J. Immunol. 164:2000;419-426
106. Karpus W.J., Lukacs N.W., McRae B.L., Strieter R.M., Kunkel S.L., Miller S.D. An important role for the chemokine macrophage inflammatory protein-1 alpha in the pathogenesis of the T cell-mediated autoimmune disease, experimental autoimmune encephalomyelitis. J. Immunol. 155:1995;5003-5010
107. Kawai K., Kobayashi Y., Shiratori M., Sobue G., Tamatani T., Miyasaka M., Yoshikai Y. Intrathecal administration of antibodies against LFA-1 and against ICAM-1 suppresses experimental allergic encephalomyelitis in rats. Cell Immunol. 171:1996;262-268
108. Kean R.B., Spitsin S.V., Mikheeva T., Scott G.S., Hooper D.C. The peroxynitrite scavenger uric acid prevents inflammatory cell invasion into the central nervous system in experimental allergic encephalomyelitis through maintenance of blood-central nervous system barrier integrity. J. Immunol. 165:2000;6511-6518
109. Kent S.J., Karlik S.J., Cannon C., Hines D.K., Yednock T.A., Fritz L.C., Horner H.C. A monoclonal antibody to alpha 4 integrin suppresses and reverses active experimental allergic encephalomyelitis. J. Neuroimmunol. 58:1995;1-10
110. Kerschensteiner M., Stadelmann C., Buddeberg B.S., Merkler D., Bareyre F.M., Anthony D.C., Linington C., Bruck W., Schwab M.E. Targeting experimental autoimmune encephalomyelitis lesions to a predetermined axonal tract system allows for refined behavioral testing in an animal model of multiple sclerosis. Am. J. Pathol. 164:2004;1455-1469
111. Kiefer R., Schweitzer T., Jung S., Toyka K.V., Hartung H.P. Sequential expression of transforming growth factor-beta1 by T-cells, macrophages, and microglia in rat spinal cord during autoimmune inflammation. J. Neuropathol. Exp. Neurol. 57:1998;385-395
112. Kloss C.U., Werner A., Klein M.A., Shen J., Menuz K., Probst J.C., Kreutzberg G.W., Raivich G. Integrin family of cell adhesion molecules in the injured brain: regulation and cellular localization in the normal and regenerating mouse facial motor nucleus. J. Comp. Neurol. 411:1999;162-178
113. Klyushnenkova E.N., Vanguri P. Ia expression and antigen presentation by glia: strain and cell type-specific differences among rat astrocytes and microglia. J. Neuroimmunol. 79(2):1997;190-201
114. Koeberle P.D., Ball A.K. Nitric oxide synthase inhibition delays axonal degeneration and promotes the survival of axotomized retinal ganglion cells. Exp. Neurol. 158:1999;366-381
115. Konno H., Yamamoto T., Iwasaki Y., Saitoh T., Suzuki H., Terunuma H. Ia-expressing microglial cells in experimental allergic encephalomyelitis in rats. Acta Neuropathol. (Berl.). 77:1989;472-479
116. Korner H., Lemckert F.A., Chaudhri G., Etteldorf S., Sedgwick J.D. Tumor necrosis factor blockade in actively induced experimental autoimmune encephalomyelitis prevents clinical disease despite activated T cell infiltration to the central nervous system. Eur. J. Immunol. 27:1997;1973-1981
117. Kosel S., Egensperger R., Bise K., Arbogast S., Mehraein P., Graeber M.B. Long-lasting perivascular accumulation of major histocompatibility complex class II-positive lipophages in the spinal cord of stroke patients: possible relevance for the immune privilege of the brain. Acta Neuropathol. (Berl.). 94:1997;532-538
118. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19:1996;312-318
119. Kuchroo V.K., Das M.P., Brown J.A., Ranger A.M., Zamvil S.S., Sobel R.A., Weiner H.L., Nabavi N., Glimcher L.H. B7-1 and B7-2 costimulatory molecules activate differentially the Th1/Th2 developmental pathways: application to autoimmune disease therapy. Cell. 80:1995;707-718
120. Kuhlmann T., Lingfeld G., Bitsch A., Schuchardt J., Bruck W. Acute axonal damage in multiple sclerosis is most extensive in early disease stages and decreases over time. Brain. 125:2002;2202-2212
121. Kurz H., Christ B. Embryonic CNS macrophages and microglia do not stem from circulating, but from extravascular precursors. Glia. 22:1998;98-102
122. Laman J.D., van Meurs M., Schellekens M.M., de Boer M., Melchers B., Massacesi L., Lassmann H., Claassen E., Hart B.A. Expression of accessory molecules and cytokines in acute EAE in marmoset monkeys (Callithrix jacchus). J. Neuroimmunol. 86:1998;30-45
123. Larsson M., Fonteneau J.F., Bhardwaj N. Dendritic cells resurrect antigens from dead cells. Trends Immunol. 22:2001;141-148
124. Lenercept Multiple Sclerosis Study Group University of British Columbia MS/MRI Analysis Group TNF neutralization in MS: results of a randomized, placebo-controlled multicenter study. The Lenercept Multiple Sclerosis Study Group and The University of British Columbia MS/MRI Analysis Group. Neurology. 53:1999;457-465
125. Leonard J.P., Waldburger K.E., Goldman S.J. Prevention of experimental autoimmune encephalomyelitis by antibodies against interleukin 12. J. Exp. Med. 181:1995;381-386
126. Leong S.K., Ling E.A. Amoeboid and ramified microglia: their interrelationship and response to brain injury. Glia. 6:1992;39-47
127. LeVine S.M. Iron deposits in multiple sclerosis and Alzheimer's disease brains. Brain Res. 760(1-2):1997 (Jun. 20);298-303
128. Li H., Cuzner M.L., Newcombe J. Microglia-derived macrophages in early multiple sclerosis plaques. Neuropathol. Appl. Neurobiol. 22:1996;207-215
129. Li J., Gran B., Zhang G.X., Ventura E.S., Siglienti I., Rostami A., Kamoun M. Differential expression and regulation of IL-23 and IL-12 subunits and receptors in adult mouse microglia. J. Neurol. Sci. 215:2003;95-103
130. Lider O., Miller A., Miron S., Hershkoviz R., Weiner H.L., Zhang X.M., Heber-Katz E. Nonencephalitogenic CD4-CD8- V alpha 2V beta 8.2+ anti-myelin basic protein rat T lymphocytes inhibit disease induction. J. Immunol. 147(4):1991 (Aug. 15);1208-1213
131. Liedtke W., Cannella B., Mazzaccaro R.J., Clements J.M., Miller K.M., Wucherpfennig K.W., Gearing A.J., Raine C.S. Effective treatment of models of multiple sclerosis by matrix metalloproteinase inhibitors. Ann. Neurol. 44:1998;35-46
132. Linehan S.A., Martinez-Pomares L., Stahl P.D., Gordon S. Mannose receptor and its putative ligands in normal murine lymphoid and nonlymphoid organs: in situ expression of mannose receptor by selected macrophages, endothelial cells, perivascular microglia, and mesangial cells, but not dendritic cells. J. Exp. Med. 189:1999;1961-1972
133. Linnington C., Webb M., Woodhams P.L. A novel myelin-associated glycoprotein defined by a mouse monoclonal antibody. J. Neuroimmunol. 6:1984;387-396
134. Liszewski M.K., Atkinson J.P. The role of complement in autoimmunity. Immunol. Ser. 54:1991;13-37
135. Liu J., Marino M.W., Wong G., Grail D., Dunn A., Bettadapura J., Slavin A.J., Old L., Bernard C.C. TNF is a potent anti-inflammatory cytokine in autoimmune-mediated demyelination. Nat. Med. 4:1998;78-83
136. Liu X., Mashour G.A., Webster H.F., Kurtz A. Basic FGF and FGF receptor 1 are expressed in microglia during experimental autoimmune encephalomyelitis: temporally distinct expression of midkine and pleiotrophin. Glia. 24:1998;390-397
137. Liu J.S., Zhao M.L., Brosnan C.F., Lee S.C. Expression of inducible nitric oxide synthase and nitrotyrosine in multiple sclerosis lesions. Am. J. Pathol. 158:2001;2057-2066
138. Liu Y., Zhu B., Luo L., Li P., Paty D.W., Cynader M.S. Heme oxygenase-1 plays an important protective role in experimental autoimmune encephalomyelitis. Neuroreport. 12:2001;1841-1845
139. Lu W., Bhasin M., Tsirka S.E. Involvement of tissue plasminogen activator in onset and effector phases of experimental allergic encephalomyelitis. J. Neurosci. 22:2002;10781-10789
140. Lucchinetti C., Bruck W., Parisi J., Scheithauer B., Rodriguez M., Lassmann H. Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann. Neurol. 47:2000;707-717
141. Madri J.A., Graesser D., Haas T. The roles of adhesion molecules and proteinases in lymphocyte transendothelial migration. Biochem. Cell Biol. 74:1996;749-757
142. Maeda A., Sobel R.A. Matrix metalloproteinases in the normal human central nervous system, microglial nodules, and multiple sclerosis lesions. J. Neuropathol. Exp. Neurol. 55:1996;300-309
143. Maier J., Kincaid C., Pagenstecher A., Campbell I.L. Regulation of signal transducer and activator of transcription and suppressor of cytokine-signaling gene expression in the brain of mice with astrocyte-targeted production of interleukin-12 or experimental autoimmune encephalomyelitis. Am. J. Pathol. 160:2002;271-288
144. Marotta C.A., Majocha R.E., Tate B. Molecular and cellular biology of Alzheimer amyloid. J. Mol. Neurosci. 3:1992;111-125
145. Marusic S., Miyashiro J.S., Douhan J. III, Konz R.F., Xuan D., Pelker J.W., Ling V., Leonard J.P., Jacobs K.A. Local delivery of granulocyte macrophage colony-stimulating factor by retrovirally transduced antigen-specific T cells leads to severe, chronic experimental autoimmune encephalomyelitis in mice. Neurosci. Lett. 332:2002;185-189
146. Matejuk A., Dwyer J., Ito A., Bruender Z., Vandenbark A.A., Offner H. Effects of cytokine deficiency on chemokine expression in CNS of mice with EAE. J. Neurosci. Res. 67:2002;680-688
147. Matsumoto Y., Ohmori K., Fujiwara M. Microglial and astroglial reactions to inflammatory lesions of experimental autoimmune encephalomyelitis in the rat central nervous system. J. Neuroimmunol. 37:1992;23-33
148. McCombe P.A., Fordyce B.W., de Jersey J., Yoong G., Pender M.P. Expression of CD45RC and Ia antigen in the spinal cord in acute experimental allergic encephalomyelitis: an immunocytochemical and flow cytometric study. J. Neurol. Sci. 113:1992;177-186
149. McCombe P.A., de Jersey J., Pender M.P. Inflammatory cells, microglia and MHC class II antigen-positive cells in the spinal cord of Lewis rats with acute and chronic relapsing experimental autoimmune encephalomyelitis. J. Neuroimmunol. 51:1994;153-167
150. McGeer P.L., Itagaki S., McGeer E.G. Expression of the histocompatibility glycoprotein HLA-DR in neurological disease. Acta Neuropathol. (Berl.). 76(6):1988;550-557
151. McQualter J.L., Darwiche R., Ewing C., Onuki M., Kay T.W., Hamilton J.A., Reid H.H., Bernard C.C. Granulocyte macrophage colony-stimulating factor: a new putative therapeutic target in multiple sclerosis. J. Exp. Med. 194:2001;873-882
152. Mead R.J., Singhrao S.K., Neal J.W., Lassmann H., Morgan B.P. The membrane attack complex of complement causes severe demyelination associated with acute axonal injury. J. Immunol. 168:2002;458-465
153. Mead R.J., Neal J.W., Griffiths M.R., Linington C., Botto M., Lassmann H., Morgan B.P. Deficiency of the complement regulator CD59a enhances disease severity, demyelination and axonal injury in murine acute experimental allergic encephalomyelitis. Lab. Invest. 84:2004;21-28
154. Miceli M.C., Parnes J.R. The roles of CD4 and CD8 in T cell activation. Semin. Immunol. 3:1991;133-141
155. Ming X., Li W., Maeda Y., Blumberg B., Raval S., Cook S.D., Dowling P.C. Caspase-1 expression in multiple sclerosis plaques and cultured glial cells. J. Neurol. Sci. 197:2002;9-18
156. Mitrovic B., Parkinson J., Merrill J.E. An in vitro model of oligodendrocyte destruction by nitric oxide and its relevance to multiple sclerosis. Methods. 10:1996;501-513
157. Miyagishi R., Kikuchi S., Takayama C., Inoue Y., Tashiro K. Identification of cell types producing RANTES, MIP-1 alpha and MIP-1 beta in rat experimental autoimmune encephalomyelitis by in situ hybridization. J. Neuroimmunol. 77:1997;17-26
158. Miyamoto K., Miyake S., Yamamura T. A synthetic glycolipid prevents autoimmune encephalomyelitis by inducing TH2 bias of natural killer T cells. Nature. 413:2001;531-534
159. Muller-Ladner U., Jones J.L., Wetsel R.A., Gay S., Raine C.S., Barnum S.R. Enhanced expression of chemotactic receptors in multiple sclerosis lesions. J. Neurol. Sci. 144:1996;135-141
160. Murphy C.A., Hoek R.M., Wiekowski M.T., Lira S.A., Sedgwick J.D. Interactions between hemopoietically derived TNF and central nervous system - resident glial chemokines underlie initiation of autoimmune inflammation in the brain. J. Immunol. 169:2002;7054-7062
161. Nagra R.M., Becher B., Tourtellotte W.W., Antel J.P., Gold D., Paladino T., Smith R.A., Nelson J.R., Reynolds W.F. Immunohistochemical and genetic evidence of myeloperoxidase involvement in multiple sclerosis. J. Neuroimmunol. 78:1997;97-107
162. Nataf S., Davoust N., Barnum S.R. Kinetics of anaphylatoxin C5a receptor expression during experimental allergic encephalomyelitis. J. Neuroimmunol. 91:1998;147-155
163. Nataf S., Carroll S.L., Wetsel R.A., Szalai A.J., Barnum S.R. Attenuation of experimental autoimmune demyelination in complement-deficient mice. J. Immunol. 165:2000;5867-5873
164. Navascues J., Moujahid A., Almendros A., Marin-Teva J.L., Cuadros M.A. Origin of microglia in the quail retina: central-to-peripheral and vitreal-to-scleral migration of microglial precursors during development. J. Comp. Neurol. 354:1995;209-228
165. Nedergaard M. Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science. 263:1994;1768-1771
166. Nguyen K.B., McCombe P.A., Pender M.P. Macrophage apoptosis in the central nervous system in experimental autoimmune encephalomyelitis. J. Autoimmun. 7:1994;145-152
167. O'Brien N.C., Charlton B., Cowden W.B., Willenborg D.O. Inhibition of nitric oxide synthase initiates relapsing remitting experimental autoimmune encephalomyelitis in rats, yet nitric oxide appears to be essential for clinical expression of disease. J. Immunol. 167:2001;5904-5912
168. Ohmori K., Hong Y., Fujiwara M., Matsumoto Y. In situ demonstration of proliferating cells in the rat central nervous system during experimental autoimmune encephalomyelitis. Evidence suggesting that most infiltrating T cells do not proliferate in the target organ. Lab. Invest. 66:1992;54-62
169. Okuda Y., Sakoda S., Fujimura H., Yanagihara T. Aminoguanidine, a selective inhibitor of the inducible nitric oxide synthase, has different effects on experimental allergic encephalomyelitis in the induction and progression phase. J. Neuroimmunol. 81:1998;201-210
170. Oleszak E.L., Katsetos C.D., Kuzmak J., Varadhachary A. Inducible nitric oxide synthase in Theiler's murine encephalomyelitis virus infection. J. Virol. 71:1997;3228-3235
171. Owens T., Tran E., Hassan-Zahraee M., Krakowski M. Immune cell entry to the CNS - a focus for immunoregulation of EAE. Res. Immunol. 149:1998;781-789
172. Pagenstecher A., Stalder A.K., Kincaid C.L., Shapiro S.D., Campbell I.L. Differential expression of matrix metalloproteinase and tissue inhibitor of matrix metalloproteinase genes in the mouse central nervous system in normal and inflammatory states. Am. J. Pathol. 152:1998;729-741
173. Pagenstecher A., Lassmann S., Carson M.J., Kincaid C.L., Stalder A.K., Campbell I.L. Astrocyte-targeted expression of IL-12 induces active cellular immune responses in the central nervous system and modulates experimental allergic encephalomyelitis. J. Immunol. 164:2000;4481-4492
174. Pan Y., Lloyd C., Zhou H., Dolich S., Deeds J., Gonzalo J.A., Vath J., Gosselin M., Ma J., Dussault B., Woolf E., Alperin G., Culpepper J., Gutierrez-Ramos J.C., Gearing D. Neurotactin, a membrane-anchored chemokine upregulated in brain inflammation. Nature. 387:1997;611-617
175. Penkowa M., Espejo C., Martinez-Caceres E.M., Poulsen C.B., Montalban X., Hidalgo J. Altered inflammatory response and increased neurodegeneration in metallothionein I+II deficient mice during experimental autoimmune encephalomyelitis. J. Neuroimmunol. 119:2001;248-260
176. Peterson J.W., Bo L., Mork S., Chang A., Ransohoff R.M., Trapp B.D. VCAM-1-positive microglia target oligodendrocytes at the border of multiple sclerosis lesions. J. Neuropathol. Exp. Neurol. 61:2002;539-546
177. Piddlesden S.J., Lassmann H., Zimprich F., Morgan B.P., Linington C. The demyelinating potential of antibodies to myelin oligodendrocyte glycoprotein is related to their ability to fix complement. Am. J. Pathol. 143:1993;555-564
178. Piddlesden S.J., Storch M.K., Hibbs M., Freeman A.M., Lassmann H., Morgan B.P. Soluble recombinant complement receptor 1 inhibits inflammation and demyelination in antibody-mediated demyelinating experimental allergic encephalomyelitis. J. Immunol. 152:1994;5477-5484
179. Polfliet M.M., van de Veerdonk F., Dopp E.A., van Kesteren-Hendrikx E.M., van Rooijen N., Dijkstra C.D., van den Berg T.K. The role of perivascular and meningeal macrophages in experimental allergic encephalomyelitis. J. Neuroimmunol. 122:2002;1-8
180. Prat A., Biernacki K., Lavoie J.F., Poirier J., Duquette P., Antel J.P. Migration of multiple sclerosis lymphocytes through brain endothelium. Arch Neurol. 59:2002;391-397
181. Priller J., Flugel A., Wehner T., Boentert M., Haas C.A., Prinz M., Fernandez-Klett F., Prass K., Bechmann I., de Boer B.A., Frotscher M., Kreutzberg G.W., Persons D.A., Dirnagl U. Targeting gene-modified hematopoietic cells to the central nervous system: use of green fluorescent protein uncovers microglial engraftment. Nat. Med. 7:2001;1356-1361
182. Prineas J.W., Graham J.S. Multiple sclerosis: capping of surface immunoglobulin G on macrophages engaged in myelin breakdown. Ann. Neurol. 10:1981;149-158
183. Prosiegel M., Neu I., Mallinger J., Wildfeuer A., Mehlber L., Vogl S., Hoffmann G., Ruhenstroth-Bauer G. Suppression of experimental autoimmune encephalomyelitis by dual cyclo-oxygenase and 5-lipoxygenase inhibition. Acta Neurol. Scand. 79:1989;223-226
184. Qi X., Guy J., Nick H., Valentine J., Rao N. Increase of manganese superoxide dismutase, but not of Cu/Zn-SOD, in experimental optic neuritis. Invest. Ophthalmol. Vis. Sci. 38:1997;1203-1212
185. Raivich G., Bohatschek M., Kloss C.U., Werner A., Jones L.L., Kreutzberg G.W. Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain. Res. Rev. 30:1999;77-105
186. Reichert F., Rotshenker S. Galectin-3/MAC-2 in experimental allergic encephalomyelitis. Exp. Neurol. 160:1999;508-514
187. Reimann J., Bohm W., Schirmbeck R. Alternative processing pathways for MHC class I-restricted epitope presentation to CD8+ cytotoxic T lymphocytes. Biol. Chem. Hoppe Seyler. 375:1994;731-736
188. Reiman R., Gerard C., Campbell I.L., Barnum S.R. Disruption of the C5a receptor gene fails to protect against experimental allergic encephalomyelitis. Eur. J. Immunol. 32:2002;1157-1163
189. Renno T., Krakowski M., Piccirillo C., Lin J.Y., Owens T. TNF-alpha expression by resident microglia and infiltrating leukocytes in the central nervous system of mice with experimental allergic encephalomyelitis. Regulation by Th1 cytokines. J. Immunol. 154:1995;944-953
190. Rinner W.A., Bauer J., Schmidts M., Lassmann H., Hickey W.F. Resident microglia and hematogenous macrophages as phagocytes in adoptively transferred experimental autoimmune encephalomyelitis: an investigation using rat radiation bone marrow chimeras. Glia. 14:1995;257-266
191. Rott O., Fleischer B., Cash E. Interleukin-10 prevents experimental allergic encephalomyelitis in rats. Eur. J. Immunol. 24:1994;1434-1440
192. Rottman J.B., Slavin A.J., Silva R., Weiner H.L., Gerard C.G., Hancock W.W. Leukocyte recruitment during onset of experimental allergic encephalomyelitis is CCR1 dependent. Eur. J. Immunol. 30:2000;2372-2377
193. Ruffini F., Furlan R., Poliani P.L., Brambilla E., Marconi P.C., Bergami A., Desina G., Glorioso J.C., Comi G., Martino G. Fibroblast growth factor-II gene therapy reverts the clinical course and the pathological signs of chronic experimental autoimmune encephalomyelitis in C57BL/6 mice. Gene Ther. 8:2001;1207-1213
194. Ruuls S.R., Bauer J., Sontrop K., Huitinga I., 't Hart B.A., Dijkstra C.D. Reactive oxygen species are involved in the pathogenesis of experimental allergic encephalomyelitis in Lewis rats. J. Neuroimmunol. 56:1995;207-217
195. Ruuls S.R., Van Der Linden S., Sontrop K., Huitinga I., Dijkstra C.D. Aggravation of experimental allergic encephalomyelitis (EAE) by administration of nitric oxide (NO) synthase inhibitors. Clin. Exp. Immunol. 103:1996;467-474
196. Saeki T., Naya A. CCR1 chemokine receptor antagonist. Curr. Pharm. Des. 9:2003;1201-1208
197. Sakurai K., Zou J.P., Tschetter J.R., Ward J.M., Shearer G.M. Effect of indoleamine 2,3-dioxygenase on induction of experimental autoimmune encephalomyelitis. J. Neuroimmunol. 129:2002;186-196
198. Schiffenbauer J., Streit W.J., Butfiloski E., LaBow M., Edwards C. III, Moldawer L.L. The induction of EAE is only partially dependent on TNF receptor signaling but requires the IL-1 type I receptor. Clin. Immunol. 95:2000;117-123
199. Schluesener H.J., Seid K. Heme oxygenase-1 in lesions of rat experimental autoimmune encephalomyelitis and neuritis. J. Neuroimmunol. 110:2000;114-120
200. Schluesener H.J., Seid K., Kretzschmar J., Meyermann R. Leukocyte chemotactic factor, a natural ligand to CD4, is expressed by lymphocytes and microglial cells of the MS plaque. J. Neurosci. Res. 44:1996;606-611
201. Schluesener H.J., Seid K., Zhao Y., Meyermann R. Localization of endothelial-monocyte-activating polypeptide II (EMAP II), a novel proinflammatory cytokine, to lesions of experimental autoimmune encephalomyelitis, neuritis and uveitis: expression by monocytes and activated microglial cells. Glia. 20:1997;365-372
202. Schonrock L.M., Kuhlmann T., Adler S., Bitsch A., Bruck W. Identification of glial cell proliferation in early multiple sclerosis lesions. Neuropathol. Appl. Neurobiol. 24:1998;320-330
203. Scolding N.J., Morgan B.P., Houston W.A., Linington C., Campbell A.K., Compston D.A. Vesicular removal by oligodendrocytes of membrane attack complexes formed by activated complement. Nature. 339:1989;620-622
204. Sedgwick J.D., Schwender S., Gregersen R., Dorries R., ter Meulen V. Resident macrophages (ramified microglia) of the adult brown Norway rat central nervous system are constitutively major histocompatibility complex class II positive. J. Exp. Med. 177:1993;1145-1152
205. Selmaj K., Raine C.S., Cross A.H. Anti-tumor necrosis factor therapy abrogates autoimmune demyelination. Ann. Neurol. 30:1991;694-700
206. Shields D.C., Tyor W.R., Deibler G.E., Banik N.L. Increased calpain expression in experimental demyelinating optic neuritis: an immunocytochemical study. Brain Res. 784:1998;299-304
207. Shin T., Kojima T., Tanuma N., Ishihara Y., Matsumoto Y. The subarachnoid space as a site for precursor T cell proliferation and effector T cell selection in experimental autoimmune encephalomyelitis. J. Neuroimmunol. 56:1995;171-178
208. Sievers J., Parwaresch R., Wottge H.U. Blood monocytes and spleen macrophages differentiate into microglia-like cells on monolayers of astrocytes: morphology. Glia. 12:1994;245-258
209. Simpson J., Rezaie P., Newcombe J., Cuzner M.L., Male D., Woodroofe M.N. Expression of the beta-chemokine receptors CCR2, CCR3 and CCR5 in multiple sclerosis central nervous system tissue. J. Neuroimmunol. 108:2000;192-200
210. Singhrao S.K., Neal J.W., Morgan B.P., Gasque P. Increased complement biosynthesis by microglia and complement activation on neurons in Huntington's disease. Exp. Neurol. 159:1999;362-376
211. Smith M.E. Phagocytic properties of microglia in vitro: implications for a role in multiple sclerosis and EAE. Microsc. Res. Tech. 54:2001;81-94
212. Smith T., Schmied M., Hewson A.K., Lassmann H., Cuzner M.L. Apoptosis of T cells and macrophages in the central nervous system of intact and adrenalectomized Lewis rats during experimental allergic encephalomyelitis. J. Autoimmun. 9:1996;167-174
213. Soane L., Rus H., Niculescu F., Shin M.L. Inhibition of oligodendrocyte apoptosis by sublytic C5b-9 is associated with enhanced synthesis of bcl-2 and mediated by inhibition of caspase-3 activation. J. Immunol. 163:1999;6132-6138
214. Sorensen T.L., Tani M., Jensen J., Pierce V., Lucchinetti C., Folcik V.A., Qin S., Rottman J., Sellebjerg F., Strieter R.M., Frederiksen J.L., Ransohoff R.M. Expression of specific chemokines and chemokine receptors in the central nervous system of multiple sclerosis patients. J. Clin. Invest. 103:1999;807-815
215. Stadelmann C., Kerschensteiner M., Misgeld T., Bruck W., Hohlfeld R., Lassmann H. BDNF and gp145trkB in multiple sclerosis brain lesions: neuroprotective interactions between immune and neuronal cells? Brain. 125:2002;75-85
216. Stalder A.K., Carson M.J., Pagenstecher A., Asensio V.C., Kincaid C., Benedict M., Powell H.C., Masliah E., Campbell I.L. Late-onset chronic inflammatory encephalopathy in immune-competent and severe combined immune-deficient (SCID) mice with astrocyte-targeted expression of tumor necrosis factor. Am. J. Pathol. 153:1998;767-783
217. Stefferl A., Brehm U., Storch M., Lambracht-Washington D., Bourquin C., Wonigeit K., Lassmann H., Linington C. Myelin oligodendrocyte glycoprotein induces experimental autoimmune encephalomyelitis in the "resistant" Brown Norway rat: disease susceptibility is determined by MHC and MHC-linked effects on the B cell response. J. Immunol. 163:1999;40-49
218. Stephenson D.T., Schober D.A., Smalstig E.B., Mincy R.E., Gehlert D.R., Clemens J.A. Peripheral benzodiazepine receptors are colocalized with activated microglia following transient global forebrain ischemia in the rat. J. Neurosci. 15:1995;5263-5274
219. Stevens D.B., Gould K.E., Swanborg R.H. Transforming growth factor-beta 1 inhibits tumor necrosis factor-alpha/lymphotoxin production and adoptive transfer of disease by effector cells of autoimmune encephalomyelitis. J. Neuroimmunol. 51:1994;77-83
220. Stoll G., Jander S. The role of microglia and macrophages in the pathophysiology of the CNS. Prog. Neurobiol. 58:1999;233-247
221. Storch M.K., Fischer-Colbrie R., Smith T., Rinner W.A., Hickey W.F., Cuzner M.L., Winkler H., Lassmann H. Co-localization of secretoneurin immunoreactivity and macrophage infiltration in the lesions of experimental autoimmune encephalomyelitis. Neuroscience. 71:1996;885-893
222. Streit W.J., Kreutzberg G.W. Response of endogenous glial cells to motor neuron degeneration induced by toxic ricin. J. Comp. Neurol. 268:1988;248-263
223. Streit W.J., Graeber M.B., Kreutzberg G.W. Expression of Ia antigen on perivascular and microglial cells after sublethal and lethal motor neuron injury. Exp. Neurol. 105:1989;115-126
224. Subramanian S., Bourdette D.N., Corless C., Vandenbark A.A., Offner H., Jones R.E. T lymphocytes promote the development of bone marrow-derived APC in the central nervous system. J. Immunol. 166:2001;370-376
225. Sugita M., Moody D.B., Jackman R.M., Grant E.P., Rosat J.P., Behar S.M., Peters P.J., Porcelli S.A., Brenner M.B. CD1 - a new paradigm for antigen presentation and T cell activation. Clin. Immunol. Immunopathol. 87:1998;8-14
226. Sun D., Whitaker J.N., Huang Z., Liu D., Coleclough C., Wekerle H., Raine C.S. Myelin antigen-specific CD8+ T cells are encephalitogenic and produce severe disease in C57BL/6 mice. J. Immunol. 166:2001;7579-7587
227. Suter T., Malipiero U., Otten L., Ludewig B., Muelethaler-Mottet A., Mach B., Reith W., Fontana A. Dendritic cells and differential usage of the MHC class II transactivator promoters in the central nervous system in experimental autoimmune encephalitis. Eur. J. Immunol. 30:2000;794-802
228. Suzuki M., Raisman G. The glial framework of central white matter tracts: segmented rows of contiguous interfascicular oligodendrocytes and solitary astrocytes give rise to a continuous meshwork of transverse and longitudinal processes in the adult rat fimbria. Glia. 6:1992;222-235
229. Takahashi J.L., Giuliani F., Power C., Imai Y., Yong V.W. Interleukin-1beta promotes oligodendrocyte death through glutamate excitotoxicity. Ann. Neurol. 53:2003;588-595
230. Taupin V., Renno T., Bourbonniere L., Peterson A.C., Rodriguez M., Owens T. Increased severity of experimental autoimmune encephalomyelitis, chronic macrophage/microglial reactivity, and demyelination in transgenic mice producing tumor necrosis factor-alpha in the central nervous system. Eur. J. Immunol. 27:1997;905-913
231. Teige I., Treschow A., Teige A., Mattsson R., Navikas V., Leanderson T., Holmdahl R., Issazadeh-Navikas S. IFN-beta gene deletion leads to augmented and chronic demyelinating experimental autoimmune encephalomyelitis. J. Immunol. 170:2003;4776-4784
232. Teige A., Teige I., Lavasani S., Bockermann R., Mondoc E., Holmdahl R., Issazadeh-Navikas S. CD1-dependent regulation of chronic central nervous system inflammation in experimental autoimmune encephalomyelitis. J. Immunol. 172:2004;186-194
233. Tomlinson S. Complement defense mechanisms. Curr. Opin. Immunol. 5:1995;83-89
234. Tran E.H., Hardin-Pouzet H., Verge G., Owens T. Astrocytes and microglia express inducible nitric oxide synthase in mice with experimental allergic encephalomyelitis. J. Neuroimmunol. 74:1997;121-129
235. Tran E.H., Hoekstra K., van Rooijen N., Dijkstra C.D., Owens T. 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. 161:1998;3767-3775
236. Tran G.T., Hodgkinson S.J., Carter N., Killingsworth M., Spicer S.T., Hall B.M. Attenuation of experimental allergic encephalomyelitis in complement component 6-deficient rats is associated with reduced complement C9 deposition, P-selectin expression, and cellular infiltrate in spinal cords. J. Immunol. 168:2002;4293-4300
237. Trapp B.D., Peterson J., Ransohoff R.M., Rudick R., Mork S., Bo L. Axonal transection in the lesions of multiple sclerosis. N. Engl. J. Med. 338:1998;278-285
238. Trebst C., Sorensen T.L., Kivisakk P., Cathcart M.K., Hesselgesser J., Horuk R., Sellebjerg F., Lassmann H., Ransohoff R.M. CCR1+/CCR5+ mononuclear phagocytes accumulate in the central nervous system of patients with multiple sclerosis. Am. J. Pathol. 159:2001;1701-1710
239. Trebst C., Staugaitis S.M., Kivisakk P., Mahad D., Cathcart M.K., Tucky B., Wei T., Rani M.R., Horuk R., Aldape K.D., Pardo C.A., Lucchinetti C.F., Lassmann H., Ransohoff R.M. CC chemokine receptor 8 in the central nervous system is associated with phagocytic macrophages. Am. J. Pathol. 162:2003;427-438
240. Ulvestad E., Williams K., Mork S., Antel J., Nyland H. Phenotypic differences between human monocytes/macrophages and microglial cells studied in situ and in vitro. J. Neuropathol. Exp. Neurol. 53:1994;492-501
241. Valdo P., Stegagno C., Mazzucco S., Zuliani E., Zanusso G., Moretto G., Raine C.S., Bonetti B. Enhanced expression of NGF receptors in multiple sclerosis lesions. J. Neuropathol. Exp. Neurol. 61:2002;91-98
242. Van Dam A.M., Bauer J., Man-A-Hing W.K., Marquette C., Tilders F.J., Berkenbosch F. Appearance of inducible nitric oxide synthase in the rat central nervous system after rabies virus infection and during experimental allergic encephalomyelitis but not after peripheral administration of endotoxin. J. Neurosci. Res. 40:1995;251-260
243. van der Laan L.J., Ruuls S.R., Weber K.S., Lodder I.J., Dopp E.A., Dijkstra C.D. Macrophage phagocytosis of myelin in vitro determined by flow cytometry: phagocytosis is mediated by CR3 and induces production of tumor necrosis factor-alpha and nitric oxide. J. Neuroimmunol. 70:1996;145-152
244. van Oosten B.W., Barkhof F., Truyen L., Boringa J.B., Bertelsmann F.W., von Blomberg B.M., Woody J.N., Hartung H.P., Polman C.H. Increased MRI activity and immune activation in two multiple sclerosis patients treated with the monoclonal anti-tumor necrosis factor antibody cA2. Neurology. 47:1996;1531-1534
245. Villiers C.L., Villiers M.B., Marche P.N. Role of the complement C3 protein in the control of the specific immune response. Ann. Biol. Clin. 57:1999;127-135
246. Villoslada P., Hauser S.L., Bartke I., Unger J., Heald N., Rosenberg D., Cheung S.W., Mobley W.C., Fisher S., Genain C.P. Human nerve growth factor protects common marmosets against autoimmune encephalomyelitis by switching the balance of T helper cell type 1 and 2 cytokines within the central nervous system. J. Exp. Med. 191:2000;1799-1806
247. Vos C.M., van Haastert E.S., de Groot C.J., van der Valk P., de Vries H.E. Matrix metalloproteinase-12 is expressed in phagocytotic macrophages in active multiple sclerosis lesions. J. Neuroimmunol. 138:2003;106-114
248. Waldburger K.E., Hastings R.C., Schaub R.G., Goldman S.J., Leonard J.P. Adoptive transfer of experimental allergic encephalomyelitis after in vitro treatment with recombinant murine interleukin-12. Preferential expansion of interferon-gamma-producing cells and increased expression of macrophage-associated inducible nitric oxide synthase as immunomodulatory mechanisms. Am. J. Pathol. 148:1996;375-382
249. Walport M.J., Davies K.A., Morley B.J., Botto M. Complement deficiency and autoimmunity. Ann. N. Y. Acad. Sci. 815:1997;267-281
250. Walther M., Popratiloff A., Lachnit N., Hofmann N., Streppel M., Guntinas-Lichius O., Neiss W.F., Angelov D.N. Exogenous antigen containing perivascular phagocytes induce a non-encephalitogenic extravasation of primed lymphocytes. J. Neuroimmunol. 117:2001;30-42
251. Washington R.A., Becher B., Balabanov R., Antel J., Dore-Duffy P. Expression of the activation marker urokinase plasminogen-activator receptor in cultured human central nervous system microglia. J. Neurosci. Res. 45:1996;392-399
252. Weerth S.H., Rus H., Shin M.L., Raine C.S. Complement C5 in experimental autoimmune encephalomyelitis (EAE) facilitates remyelination and prevents gliosis. Am. J. Pathol. 163:2003;1069-1080
253. Weinberg A.D., Wegmann K.W., Funatake C., Whitham R.H. Blocking OX-40/OX-40 ligand interaction in vitro and in vivo leads to decreased T cell function and amelioration of experimental allergic encephalomyelitis. J. Immunol. 162:1999;1818-1826
254. Welsh C.T., Rose J.W., Hill K.E., Townsend J.J. Augmentation of adoptively transferred experimental allergic encephalomyelitis by administration of a monoclonal antibody specific for LFA-1 alpha. J. Neuroimmunol. 43:1993;161-167
255. Werner A., Martin S., Gutierrez-Ramos J.C., Raivich G. Leukocyte recruitment and neuroglial activation during facial nerve regeneration in ICAM-1-deficient mice: effects of breeding strategy. Cell Tissue Res. 305:2001;25-41
256. Werner K., Bitsch A., Bunkowski S., Hemmerlein B., Bruck W. The relative number of macrophages/microglia expressing macrophage colony-stimulating factor and its receptor decreases in multiple sclerosis lesions. Glia. 40:2002;121-129
257. Wesemann D.R., Dong Y., O'Keefe G.M., Nguyen V.T., Benveniste E.N. Suppressor of cytokine signaling 1 inhibits cytokine induction of CD40 expression in macrophages. J. Immunol. 169:2002;2354-2360
258. Whitney L.W., Ludwin S.K., McFarland H.F., Biddison W.E. Microarray analysis of gene expression in multiple sclerosis and EAE identifies 5-lipoxygenase as a component of inflammatory lesions. J. Neuroimmunol. 121:2001;40-48
259. Wildfeuer A., Neu I.S., Safayhi H., Metzger G., Wehrmann M., Vogel U., Ammon H.P. Effects of boswellic acids extracted from a herbal medicine on the biosynthesis of leukotrienes and the course of experimental autoimmune encephalomyelitis. Arzneimittelforschung. 48:1998;668-674
260. Willenborg D.O., Staykova M.A., Miyasaka M. Short term treatment with soluble neuroantigen and anti-CD11a (LFA-1) protects rats against autoimmune encephalomyelitis: treatment abrogates autoimmune disease but not autoimmunity. J. Immunol. 157:1996;1973-1980
261. Willenborg D.O., Fordham S.A., Staykova M.A., Ramshaw I.A., Cowden W.B. IFN-gamma is critical to the control of murine autoimmune encephalomyelitis and regulates both in the periphery and in the target tissue: a possible role for nitric oxide. J. Immunol. 163:1999;5278-5286
262. Williams K., Ulvestad E., Antel J.P. B7/BB-1 antigen expression on adult human microglia studied in vitro and in situ. Eur. J. Immunol. 24:1994;3031-3037
263. Wren D.R., 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. Sci. U. S. A. 86:1989;9025-9029
264. Wright G.J., Puklavec M.J., Willis A.C., Hoek R.M., Sedgwick J.D., Brown M.H., Barclay A.N. Lymphoid/neuronal cell surface OX2 glycoprotein recognizes a novel receptor on macrophages implicated in the control of their function. Immunity. 13:2000;233-242
265. Wyss-Coray T., Borrow P., Brooker M.J., Mucke L. Astroglial overproduction of TGF-beta 1 enhances inflammatory central nervous system disease in transgenic mice. J. Neuroimmunol. 77:1997;45-50
266. Yednock T.A., Cannon C., Fritz L.C., Sanchez-Madrid F., Steinman L., Karin N. Prevention of experimental autoimmune encephalomyelitis by antibodies against alpha 4 beta 1 integrin. Nature. 356:1992;63-66
267. Zhang G.X., Yu S., Gran B., Li J., Siglienti I., Chen X., Calida D., Ventura E., Kamoun M., Rostami A. Role of IL-12 receptor beta 1 in regulation of T cell response by APC in experimental autoimmune encephalomyelitis. J. Immunol. 171:2003;4485-4492
268. Zhang G.X., Gran B., Yu S., Li J., Siglienti I., Chen X., Kamoun M., Rostami A. Induction of experimental autoimmune encephalomyelitis in IL-12 receptor-beta 2-deficient mice: IL-12 responsiveness is not required in the pathogenesis of inflammatory demyelination in the central nervous system. J. Immunol. 170:2003;2153-2160
269. Ziaber J., Baj Z., Pasnik J., Chmielewski H., Tchorzewski H. Expression of aminopeptidase N (APN) on peripheral blood mononuclear cells' surface as a marker of these cells' transendothelial migration properties in the course of multiple sclerosis. Mediators Inflamm. 9:2000;45-48
270. Zinkernagel R.M., Doherty P.C. The discovery of MHC restriction. Immunol. Today. 18:1997;14-17