Role of macrophages/microglia in multiple sclerosis and experimental allergic encephalomyelitis

Journal of Molecular Medicine

Volumn 75, Issue 3, 1997, Pages 165-173

  Benveniste, Etty N ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Cytokines; Demyelination; Glial cells; Neuroimmunology

Indexed keywords

CYTOKINE;

ALLERGY; AUTOIMMUNITY; CENTRAL NERVOUS SYSTEM; ENCEPHALOMYELITIS; HUMAN; IMMUNOREACTIVITY; MACROPHAGE; MICROGLIA; MULTIPLE SCLEROSIS; REVIEW;

ANIMALS; CENTRAL NERVOUS SYSTEM; CHEMOKINES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; MACROPHAGES; METALLOENDOPEPTIDASES; MICROGLIA; MODELS, IMMUNOLOGICAL; MULTIPLE SCLEROSIS; PROTEASE INHIBITORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0030970058     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s001090050101     Document Type: Review

References (107)

1. del Rio-Hortega P (1932) Microglia. In: Penfield W (ed) Cytology and cellular pathology of the nervous system. Hoeber, New York, pp 481-584
2. Hickey WF, Kimura H (1988) Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 239:290-292
3. Perry VH, Gordon S (1988) Macrophages and microglia in the nervous system. Trends Neurosci 11:273-277
4. Banati RB, Gehrmann J, Schubert P, Kreutzberg GW (1993) Cytotoxicity of microglia. Glia 7:111-118
5. Gordon S (1995) The macrophage. Bioessays 17:977-986
6. Gehrmann J, Matsumoto Y, Kreutzberg GW (1995) Microglia: intrinsic immuneffector cell of the brain. Brain Res Rev 20:269-287
7. Moore S, Thanos S (1996) The concept of microglia in relation to central nervous system disease and regeneration. Prog Neurobiol 48:441-460
8. Streit WJ (1995) Microglial cells. In: Ransom BR, Kettenmann H (eds) Neuroglia. Oxford University Press, pp 85-96
9. Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312-318
10. Graeber MB, Streit WJ, Kreutzberg GW (1989) Identity of ED2-positive perivascular cells in rat brain. J Neurosci Res 22:103-106
11. Walker DG, Kim SU, McGeer PL (1995) Complement and cytokine gene expression in cultured microglia derived from postmortem human brains. J Neurosci Res 40:478-493
12. Shrikant P, Weber E, Jilling T, Benveniste EN (1995) ICAM-1 gene expression by glial cells: differential mechanisms of inhibition by interleukin-10 and interleukin-6. J Immunol 155:1489-1501
13. Panek RB, Benveniste EN (1995) Class II MHC gene expression in microglia: regulation by the cytokines IFN-γ, TNF-α and TGF-β. J Immunol 154:2846-2854
14. Frei K, Siepl C, Groscurth P, Bodmer S, Schwerdel C, Fontana A (1987) Antigen presentation and tumor cytotoxicity by interferon-γ-treated microglial cells. Eur J Immunol 17: 1271-1278
15. Suzumura A, Mezitis SGE, Gonatas NK, Silberberg DH (1987) MHC antigen expression on bulk isolated macrophage-microglia from newborn mouse brain: induction of Ia antigen expression by γ-interferon. J Neuroimmunol 15:263-278
16. Williams K, Ulvestad E, Antel JP (1994) B7/BB-1 antigen expression on adult human microglia studied in vitro and in situ. Eur J Immunol 24:3031-3037
17. De Simone R, Giampaolo A, Giometto B, Gallo P, Levi G, Peschle C, Aloisi F (1995) The costimulatory molecule B7 is expressed on human microglia in culture and in multiple sclerosis acute lesions. J Neuropath. Exp Neurol 54:175-187
18. Ulvestad E, Williams K, Bjerkvig R, Tiekotter K, Antel J, Matre R (1994) Human microglial cells have phenotypic and functional characteristics in common with both macrophages and dendritic antigen-presenting cells. J Leukoc Biol 56: 732-740
19. Korotzer AR, Watt J, Cribbs D, Tenner AJ, Burdick D, Glabe C, Cotman CW (1995) Cultured rat microglia express C1q and receptor for C1q: implications for amyloid effects on microglia. Exp Neurology 134:214-221
20. Williams K, Bar-Or A, Ulvestad E, Olivier A, Antel JP, Yong VW (1992) Biology of adult human microglia in culture: comparisons with peripheral blood monocytes and astrocytes. J Neuropathol Exp Neurol 51:538-549
21. Martin R, McFarland HF, McFarlin DE (1992) Immunological aspects of demyelinating diseases. Annu Rev Immunol 10:153-187
22. Hauser SL, Bhan AK, Gilles FH, Hoban CJ, Reinherz EL, Schlossman SF, Weiner HL (1983) Immunohistochemical staining of human brain with monoclonal antibodies that identify lymphocytes, monocytes and the Ia antigen. J Neuroimmunol 5:197-205
23. Prineas JW (1975) Pathology of the early lesion in multiple sclerosis. Human Pathol 6:531-554
24. Prineas JW, Wright RG (1978) Macrophages, lymphocytes and plasma cells in the perivascular compartment in chronic multiple sclerosis. Lab Invest 38:409-421
25. Bauer J, Sminia T, Wouterlood FG, Dijkstra CD (1994) Phagocytic activity of macrophages and microglial cells during the course of acute and chronic relapsing experimental autoimmune encephalomyelitis. J Neurosci Res 38:365-375
26. Hofman FM, VonHanwher R, Dinarello C, Mizel S, Hinton D, Merrill JE (1986) Immunoregulatory molecules and IL-2 receptors identified in multiple sclerosis brain. J Immunol 136:3239-3245
27. Winghagen A, Newcombe J, Dangond F, Strand C, Woodroofe MN, Cuzner ML, Hafler DA (1995) Expression of costimulatory molecules B7-1 (CD80), B7-2 (CD86), and interleukin 12 cytokine in multiple sclerosis lesions. J Exp Med 182:1985-1996
28. Gerritse K, Laman JD, Noelle RJ, Aruffo A, Ledbetter JA, Boersma WJA, Claassen E (1996) CD40-CD40 ligand interactions in experimental allergic encephalomyelitis and multiple sclerosis. Proc Natl Acad Sci USA 93:2499-2504
29. Alderson MR, Armitage RJ, Tough TW, Strockbine L, Fanslow WC, Spriggs MK (1993) CD40 expression by human monocytes: regulation by cytokines and activation of monocytes by the ligand for CD40. J Exp Med 178:669-674
30. Bignami A, Eng LF, Dahl D, Uyeda CT (1972) Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res 43:429-135
31. Thompson AJ, Miller D, Youl B, MacManus D, Moore S, Kingsley D, Kendall B, Feinstein A, McDonald WI (1992) Serial gadolinium-enhanced MRI in relapsing/remitting multiple sclerosis of varying disease duration. Neurology 42:60-63
32. Gay D, Esiri M (1991) Blood-brain barrier damage in acute multiple sclerosis plaques: an immunocytological study. Brain 114:557-572
33. Benveniste EN (1995) Role of cytokines in multiple sclerosis, autoimmune encephalitis, and other neurological disorders. In: Aggarawal B, Puri R (eds) Human cytokines: Their role in research and therapy. Blackwell, Boston, pp 195-216
34. Merrill JE, Benveniste EN (1996) Cytokines in inflammatory brain lesions: Helpful and harmful. Trends Neurosci 19: 331-338
35. Selmaj KW, Raine CS (1988) Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann Neurol 23: 339-346
36. Robbins DS, Shirazi Y, Drysdale BE, Lieberman A, Shin HS, Shin ML (1987) Production of cytotoxic factor for oligodendrocytes by stimulated astrocytes. J Immunol 139:2593-2597
37. Selmaj K, Raine CS, Cross AH (1991) Anti-tumor necrosis factor therapy abrogates autoimmune demyelination. Ann Neurol 30:694-700
38. Selmaj KW, Farooq M, Norton WT, Raine CS, Brosnan CF (1990) Proliferation of astrocytes in vitro in response to cytokines. A primary role for tumor necrosis factor. J Immunol 144:129-135
39. Giulian D, Lachman LB (1985) Interleukin-1 stimulation of astroglial proliferation after brain injury. Science 228:497-499
40. Swanborg RH (1995) Experimental autoimmune encephalomyelitis in rodents as a model for human demyelinating disease. Clin Immunol Immunopathol 77:4-13
41. Gehrmann J, Gold R, Linington C, Lannes-Vieira J, Wekerle H, Kreutzberg GW (1993) Microglial involvement in autoimmune inflammation of the central and peripheral nervous system. Glia 7:50-59
42. McCombe PA, de Jersey J, Pender MP (1994) 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 51:153-167
43. Ando DG, Clayton J, Kono D, Urban JL, Sercarz EE (1989) Encephalitogenic T cells in the B10.PL model of experimental allergic encephalomyelitis (EAE) are of the Th-1 lymphokine subtype. Cell Immunol 124:132-143
44. Mustafa M, Vingsbo C, Olsson T, Ljungdahl A, Hšjeberg B, Holmdahl R (1993) The major histocompatibility complex influences myelin basic protein 63-88-induced T cell cytokine profile and experimental autoimmune encephalomyelitis. Eur J Immunol 23:3089-3095
45. Karpus WJ, Gould KE, Swanborg RH (1992) CD4+ suppressor cells of autoimmune encephalomyelitis respond to T cell receptor-associated determinants on effector cells by interleukin-4 secretion. Eur J Immunol 22:1757-1763
46. Racke MK, Burnett D, Pak S-H, Albert PS, Cannella B, Raine CS, McFarlin DE, Scott DE (1995) Retinoid treatment of experimental allergic encephalomyelitis. J Immunol 154: 450-458
47. Stevens DB, Gould KE, Swanborg RH (1994) Transforming growth faclor-β1 inhibits tumor necrosis factor-α/lymphotoxin production and adoptive transfer of disease by effector cells of autoimmune encephalomyelitis. J Neuroimmunol 51: 77-83
48. Lee SC, Liu W, Roth P, Dickson DW, Berman JW, Brosnan CF (1993) Macrophage colony-stimulating factor in human fetal astrocytes and microglia: Differential regulation by cytokines and lipopolysaccharide, and modulation of class II MHC on microglia. J Immunol 150:594-604
49. Lee SC, Liu W, Dickson DW, Brosnan CF, Berman JW (1993) Cytokine production by human fetal microglia and astrocytes: Differential induction by lipopolysaccharide and IL-1β. J Immunol 150:2659-2667
50. Appel K, Honegger P, Gebicke-Haerter PJ (1995) Expression of interleukin-3 and tumor necrosis factor-β mRNAs in cultured microglia. J Neuroimmunol 60:83-91
51. Briers TW, Desmaretz C, Vanmechelen E (1994) Generation and characterization of mouse microglial cell lines. J Neuroimmunol 52:153-164
52. Murphy GM Jr, Jia X-C, Song Y, Ong E, Shrivastava R, Bocchini V, Lee YL, Eng LF (1995) Macrophage inflammatory protein 1-α mRNA expression in an immortalized microglial cell line and cortical astrocyte cultures. J Neurosci Res 40: 755-763
53. Giulian D, Baker TJ, Shih LC, Lachman LB (1986) Interleukin-1 of the central nervous system is produced by ameboid microglia. J Exp Med 164:594-604
54. Giulian D, Baker TJ (1986) Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci 6:2163-2178
55. Righi M, Mori L, De Libero G, Sironi M, Biondi A, Mantovani A, Donini SD, Ricciardi-Castagnoli P (1989) Monokine production by microglial cell clones. Eur J Immunol 19: 1443-1448
56. Gottschall PE, Yu X, Bing B (1995) Increased production of gelatinase B (matrix metalloproteinase-9) and interleukin-6 by activated rat microglia in culture. J Neurosci Res 42: 335-342
57. Chao CC, Hu S, Sheng WS, Peterson PK (1995) Tumor necrosis factor-alpha production by human fetal microglial cells: regulation by other cytokines. Dev Neurosci 17:97-105
58. Chao CC, Hu S, Sheng WS, Tsang M, Peterson PK (1995) Tumor necrosis factor-α mediates the release of bioactive transforming growth factor-β in murine microglial cell cultures. Clin Immunol Immunopathol 77:358-365
59. Norris JG, Benveniste EN (1993) Interleukin-6 production by astrocytes: induction by the neurotransmitter norepinephrine. J Neuroimmunol 45:137-146
60. Zajicek JP, Wing M, Scolding NJ, Compston DAS (1992) Interactions between oligodendrocytes and microglia. Brain 115:1611-1631
61. Merrill JE, Ignarro LJ, Sherman MP, Melinek J, Lane TE (1993) Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J Immunol 151:2132-2141
62. Colton CA, Keri JE, Chen W-T, Monsky WL (1993) Protease production by cultured microglia: substrate gel analysis and immobilized matrix degradation. J Neurosci Res 35:297-304
63. Cammer W, Bloom BR, Norton WT, Gordon S (1978) Degradation of basic protein in myelin by neutral proteases secreted by stimulated macrophages: a possible mechanism of inflammatory demyelination. Proc Natl Acad Sci USA 75: 1554-1558
64. Shrikant P, Benveniste EN (1996) The central nervous system as an immunocompetent organ: role of glial cells in antigen presentation. J Immunol 157:1819-1822
65. June CH, Bluestone JA, Nadler LM, Thompson CB (1994) The B7 and CD28 receptor families. Immunol Today 15: 321-331
66. Satoh J-I, Lee YB, Kim SU (1995) T-cell costimulatory molecules B7-1 (CD80) and B7-2 (CD86) are expressed in human microglia but not in astrocytes in culture. Brain Res 704:92-96
67. Woodroofe MN, Hayes GM, Cuzner ML (1989) Fc receptor density. MHC antigen expression and Superoxide production are increased in interferon-gamma-treated microglia isolated from adult rat brain. Immunol 68:421-426
68. Suzumura A, Sawada M, Itoh Y, Marunouchi T (1994) Interleukin-4 induces proliferation and activation of microglia but suppresses their induction of class II major histocompatibility complex antigen expression. J Neuroimmunol 53:209-218
69. Racke MK, Bonomo A, Scott DE, Cannella B, Levine A, Raine CS, Shevach EM, Röcken M (1994) Cytokine-induced immune deviation as a therapy for inflammatory autoimmune disease. J Exp Med 180:1961-1966
70. Brosnan CF, Bornstein MB, Bloom BR (1981) The effects of macrophage depletion on the clinical and pathologic expression of experimental allergic encephalomyelitis. J Immunol 126:614-620
71. Huitinga I, van Rooijen N, de Groot CJA, Uitdehaag BMJ, Dijkstra CD (1990) Suppression of experimental allergic encephalomyelitis in lewis rats after elimination of macrophages. J Exp Med 172:1025-1033
72. Bauer J, Huitinga I, Zhao W, Lassmann H, Hiekey WF, Dijkstra CD (1995) The role of macrophages, perivascular cells, amd microglial cells in the pathogenesis of experimental autoimmune encephalomyelitis. Glia 15:437-446
73. Springer TA (1994) Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76:301-314
74. Huitinga I, Damoiseaux JGMC, Döpp EA, Dijkstra CD (1993) Treatment with anti-CR3 antibodies ED7 and ED8 suppresses experimental allergic encephalomyelitis in lewis rats. Eur J Immunol 23:709-715
75. Gordon EJ, Myers KJ, Dougherty JP, Rosen H, Ron Y (1995) Both anti-CD11a (LFA-1) and anti-CD11b (MAC-1) therapy delay the onset and diminish the severity of experimental autoimmune encephalomyelitis. J Neuroimmunol 62:153-160
76. Baggiolini M, Dewald B, Moser B (1994) Interleukin-8 and related chemotactic cytokines - CXC and CC chemokines. Adv Immunol 55:97-178
77. Strieter RM, Standiford TJ, Huffnagle GB, Colletti LM, Lukacs NW, Kunkel SL (1996) "The good, the bad, and the ugly" the role of chemokines in models of human disease. J Immunol 156:3583-3586
78. Hulkower K, Brosnan CF, Aquino DA, Cammer W, Kulshrestha S, Guida MP, Rapoport DA, Berman JW (1993) Expression of CSF-1, c-fms, and MCP-1 in the central nervous system of rats with experimental allergic encephalomyelitis. J Immunol 150:2525-2533
79. Berman JW, Guida MP, Warren J, Amat J, Brosnan CF (1996) Localization of monocyte chemoattractant peptide-1 expression in the central nervous system in experimental autoimmune encephalomyelitis and trauma in the rat. J Immunol 156:3017-3023
80. Ransohoff RM, Hamilton TA, Tani M, Stoler MH, Shick HE, Major JA, Estes ML, Thomas DM, Tuohy VK (1993) Astrocyte expression of mRNA encoding cytokines IP-10 and JE/MCP-1 in experimental autoimmune encephalomyelitis. FASEB J 7:592-600
81. Fuentes ME, Durham SK, Swerdel MR, Lewin AC, Barton DS, Megill JR, Bravo R, Lira SA (1995) Controlled recruitment of monocytes and macrophages to specific organs through transgenic expression of monocyte chemoattractant protein-1. J Immunol 155:5769-5776
82. Godiska R, Chantry D, Dietsch GN, Gray PW (1995) Chemokine expression in murine experimental allergic encephalomyelitis. J Neuroimmunol 58:167-176
83. Karpus WJ, Lukacs NW, McRae BL, Strieter RM, Kunkel SL, Miller SD (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
84. Gijbels K, Masure S, Carton H, Opdenakker G (1992) Gelatinase in the cerebrospinal fluid of patients with multiple sclerosis and other inflammatory neurological disorders. J Neuroimmunol 41:29-34
85. Gijbels K, Proost P, Masure S, Carton H, Billiau A, Opdenakker G (1993) Gelatinase B is present in the cerebrospinal fluid during experimental autoimmune encephalomyelitis and cleaves myelin basic protein. J Neurosci Res 36:432-440
86. Maeda A, Sobel RA (1996) Matrix metalloproteinases in the normal human central nervous system, microglial nodules, and multiple sclerosis lesions. J Neuropath. Exp Neurol 55: 300-309
87. Welgus HG, Campbell EJ, Cury JD, Eisen AZ, Senior RM, Wilhelm SM, Goldberg GI (1990) Neutral metalloproteinases produced by human mononuclear phagocytes: enzyme profile, regulation, and expression during cellular development. J Clin Invest 86:1496-1502
88. Beezhold DH, Personius C (1992) Fibronectin fragments stimulate tumor necrosis factor secretion by human monocytes. J Leukoc. Biol 51:59-64
89. Gijbels K, Galardy RE, Steinman L (1994) Reversal of experimental autoimmune encephalomyelitis with a hydroxamate inhibitor of matrix metalloproteases. J Clin Invest 94: 2177-2182
90. Malik N, Greenfield BW, Wahl AF, Kiener PA (1996) Activation of human monocytes through CD40 induces matrix metalloproteinases. J Immunol 156:3952-3960
91. Wagner DH Jr, Stout RD, Suttles J (1994) Role of the CD40-CD40 ligand interaction in CD4+ T cell contact-dependent activation of monocyte interleukin-1 synthesis. Eur J Immunol 24:3148-1354
92. Shu U, Kiniwa M, Wu CY, Muliszewski C, Vezzio N, Hakimi J, Gately M, Delespesse G (1995) Activated T cells induce interleukin-12 production by monocytes via CD40-CD40 ligand interaction. Eur J Immunol 25:1125-1128
93. Tian L, Noelle RJ, Lawrence DA (1995) Activated T cells enhance nitric oxide production by murine splenic macrophages through gp39 and LFA-1. Eur J Immunol 25:306-309
94. Beck J, Rondot P, Catinot L, Falcoff E, Kirchner H, Wietzerbin J (1988) Increased production of interferon gamma and tumor necrosis factor precedes clinical manifestation in multiple sclerosis: do cytokines trigger off exacerbations? Acta Neurol Scand 78:318-323
95. Merrill JE, Strom SR, Ellison GW, Myers LW (1989) In vitro study of mediators of inflammation in multiple sclerosis. J Clin Immunol 9:84-96
96. Rieckmann P, Albrecht M, Kitze B, Weber T, Tumani H, Broocks A, Lüer W, Helwig A, Poser S (1995) Tumor necrosis factor-α messenger RNA expression in patients with relapsing-remitting multiple sclerosis is associated with disease activity. Ann Neurol 37:82-88
97. Correale J, Gilmore W, McMillan M, Li S, McCarthy K, Le T, Weiner LP (1995) Patterns of cytokine secretion by autoreactive proteolipid protein-specific T cell clones during the course of multiple sclerosis. J Immunol 154:2959-2968
98. Khoury SJ, Hancock WW, Weiner HL (1992) 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 prostaslandin E expression in the brain. J Exp Med 176: 1355-1364
99. Renno T, Krakowski M, Piccirillo C, Lin J-Y, Owens T (1995) TNF-α expression by resident microglia and infiltrating leukocytes in the central nervous system of mice with experimental allergic encephalomyelitis. J Immunol 154:944-953
100. Ruddle NH, Bergman CM, McGrath KM, Lingenheld EG, Grunnet ML, Padula SJ, Clark RB (1990) An antibody to lymphotoxin and tumor necrosis factor prevents transfer of experimental allergic encephalomyelitis. J Exp Med 172:1193-1200
101. Selmaj K, Papierz W, Glabinski A, Kohno T (1995) Prevention of chronic relapsing experimental autoimmune encephalomyelitis by soluble tumor necrosis factor receptor I. J Neuroimmunol 56:135-141
102. Baker D, Butler D, Scallon BJ, O'Neill JK, Turk JL, Feldmann M (1994) Control of established experimental allergic encephalomyelitis by inhibition of tumor necrosis factor (TNF) activity within the central nervous system using monoclonal antibodies and TNF receptor-immunoglobulin fusion proteins. Eur J Immunol 24:2040-2048
103. Probert L, Akassoglou K, Pasparakis M, Kontogeorgos G, Kollias G (1995) Spontaneous inflammatory demyelinating disease in transgenic mice showing central nervous system-specific expression of tumor necrosis factor α. Proc Natl Acad Sci USA 92:11294-11298
104. Gebicke-Haerter PJ, Appel K, Taylor GD, Schobert A, Rich IN, Northoff H, Berger M (1994) Rat microglial interleukin-3. J Neuroimmunol 50:203-214
105. Appel K, Buttini M, Sauter A, Gebicke-Haerter PJ (1995) Cloning of rat interleukin-3 receptor β-subunit from cultured microglia and its mRNA expression in vivo. J Neurosci 15: 5800-5809
106. Lee TT, Martin FC, Merrill JE (1993) Lymphokine induction of rat microglia multinucleated giant cell formation. Glia 8: 51-61
107. Chiang C-S, Powell HC, Gold LH, Samimi A, Campbell IL (1996) Macrophage/microglial-mediated primary demyelination and motor disease induced by the central nervous system production of interleukin-3 in transgenic mice. J Clin Invest 97:1512-1524