The brain as a target of inflammation: common pathways link inflammatory and neurodegenerative diseases

Trends in Neurosciences

Volumn 29, Issue 9, 2006, Pages 518-527

  Zipp, Frauke ^a   Aktas, Orhan ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER DISEASE VACCINE; CORTICOSTEROID; CYCLOOXYGENASE 1 INHIBITOR; CYCLOOXYGENASE 2 INHIBITOR; FLAVONOID; GLATIRAMER; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; IMMUNOGLOBULIN; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; MINOCYCLINE; NONSTEROID ANTIINFLAMMATORY AGENT; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ADRENOLEUKODYSTROPHY; ALLERGIC ENCEPHALOMYELITIS; ALZHEIMER DISEASE; AUTOIMMUNITY; BACTERIAL MENINGITIS; BONE MARROW TRANSPLANTATION; CLINICAL TRIAL; DEGENERATIVE DISEASE; DEMYELINATION; EXCITOTOXICITY; HUMAN; HUNTINGTON CHOREA; IMMUNE SYSTEM; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; INFLAMMATION; MACROPHAGE; MICROGLIA; MULTIPLE SCLEROSIS; NERVE CELL LESION; NERVE DEGENERATION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; STROKE; VACCINATION;

ANIMALS; BRAIN; HUMANS; IMMUNOTHERAPY; INFLAMMATION; MULTIPLE SCLEROSIS; NERVE DEGENERATION; NEURODEGENERATIVE DISEASES;

EID: 33747890559     PISSN: 01662236     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tins.2006.07.006     Document Type: Review

References (143)

1. Wekerle H., et al. Cellular immune reactivity within the CNS. Trends Neurosci. 9 (1986) 271-277
2. Heppner F.L., et al. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat. Med. 11 (2005) 146-152
3. Greter M., et al. Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis. Nat. Med. 11 (2005) 328-334
4. Ferguson B., et al. Axonal damage in acute multiple sclerosis lesions. Brain 120 (1997) 393-399
5. Trapp B.D., et al. Axonal transection in the lesions of multiple sclerosis. N. Engl. J. Med. 338 (1998) 278-285
6. Kornek B., et al. Multiple sclerosis and chronic autoimmune encephalomyelitis: a comparative quantitative study of axonal injury in active, inactive, and remyelinated lesions. Am. J. Pathol. 157 (2000) 267-276
7. Peterson J.W., et al. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann. Neurol. 50 (2001) 389-400
8. Kidd D., et al. Cortical lesions in multiple sclerosis. Brain 122 (1999) 17-26
9. Sailer M., et al. Focal thinning of the cerebral cortex in multiple sclerosis. Brain 126 (2003) 1734-1744
10. Inglese M., et al. Indirect evidence for early widespread gray matter involvement in relapsing-remitting multiple sclerosis. NeuroImage 21 (2004) 1825-1829
11. Schulz D., et al. Cognition in the early stage of multiple sclerosis. J. Neurol (2006) 10.1007/s00415-006-0145-8
12. Iragui-Madoz V.J. Electrophysiology of multiple sclerosis. In: Daly D.D., and Pedley T.A. (Eds). Current Practice Of Clinical Electroencephalography (1990), Raven 708-738
13. Eriksson M., et al. Epileptic seizures, cranial neuralgias and paroxysmal symptoms in remitting and progressive multiple sclerosis. Mult. Scler. 8 (2002) 495-499
14. Evangelou N., et al. Regional axonal loss in the corpus callosum correlates with cerebral white matter lesion volume and distribution in multiple sclerosis. Brain 123 (2000) 1845-1849
15. De Stefano N., et al. Evidence of axonal damage in the early stages of multiple sclerosis and its relevance to disability. Arch. Neurol. 58 (2001) 65-70
16. Nau R., and Bruck W. Neuronal injury in bacterial meningitis: mechanisms and implications for therapy. Trends Neurosci. 25 (2002) 38-45
17. Kaul M., et al. Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410 (2001) 988-994
18. Newman T.A., et al. T-cell- and macrophage-mediated axon damage in the absence of a CNS-specific immune response: involvement of metalloproteinases. Brain 124 (2001) 2203-2214
19. Giuliani F., et al. Vulnerability of human neurons to T cell-mediated cytotoxicity. J. Immunol. 171 (2003) 368-379
20. Steinman L., and Zamvil S.S. Virtues and pitfalls of EAE for the development of therapies for multiple sclerosis. Trends Immunol. 26 (2005) 565-571
21. Nitsch R., et al. Direct impact of T cells on neurons revealed by two-photon microscopy in living brain tissue. J. Neurosci. 24 (2004) 2458-2464
22. Aktas O., et al. Neuronal damage in autoimmune neuroinflammation mediated by the death ligand TRAIL. Neuron 46 (2005) 421-432
23. Traugott U., et al. Multiple sclerosis: distribution of T cell subsets within active chronic lesions. Science 219 (1983) 308-310
24. Medana I., et al. Transection of major histocompatibility complex class I-induced neurites by cytotoxic T lymphocytes. Am. J. Pathol. 159 (2001) 809-815
25. Linker R.A., et al. EAE in β-2 microglobulin-deficient mice: axonal damage is not dependent on MHC-I restricted immune responses. Neurobiol. Dis. 19 (2005) 218-228
26. Sun D., et al. Suppression of experimentally induced autoimmune encephalomyelitis by cytolytic T-T cell interactions. Nature 332 (1988) 843-845
27. + T cells in murine experimental allergic encephalomyelitis. Science 256 (1992) 1213-1215
28. Khanna K.M., et al. Immunity to latent viral infection: many skirmishes but few fatalities. Trends Immunol. 25 (2004) 230-234
29. Farber K., and Kettenmann H. Physiology of microglial cells. Brain Res. Rev. 48 (2005) 133-143
30. Bechmann I., et al. Circulating monocytic cells infiltrate layers of anterograde axonal degeneration where they transform into microglia. FASEB J. 19 (2005) 647-649
31. Diestel A., et al. Activation of microglial poly(ADP-ribose)-polymerase-1 by cholesterol breakdown products during neuroinflammation: a link between demyelination and neuronal damage. J. Exp. Med. 198 (2003) 1729-1740
32. Mitchell L., et al. Dual phases of apoptosis in pneumococcal meningitis. J. Infect. Dis. 190 (2004) 2039-2046
33. Iliev A.I., et al. Neuronal injury mediated via stimulation of microglial toll-like receptor-9 (TLR9). FASEB J. 18 (2004) 412-414
34. Bechmann I. Failed central nervous system regeneration: a downside of immune privilege?. Neuromolecular Med. 7 (2005) 217-228
35. Takeuchi H., et al. Neuritic beading induced by activated microglia is an early feature of neuronal dysfunction toward neuronal death by inhibition of mitochondrial respiration and axonal transport. J. Biol. Chem. 280 (2005) 10444-10454
36. Barnett M.H., and Prineas J.W. Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann. Neurol. 55 (2004) 458-468
37. Coles A.J., et al. Monoclonal antibody treatment exposes three mechanisms underlying the clinical course of multiple sclerosis. Ann. Neurol. 46 (1999) 296-304
38. Lappe-Siefke C., et al. Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat. Genet. 33 (2003) 366-374
39. Linker R.A., et al. CNTF is a major protective factor in demyelinating CNS disease: a neurotrophic cytokine as modulator in neuroinflammation. Nat. Med. 8 (2002) 620-624
40. Tsunoda I., et al. Axonal injury heralds virus-induced demyelination. Am. J. Pathol. 162 (2003) 1259-1269
41. Raivich G., et al. Immune surveillance in the injured nervous system: T-lymphocytes invade the axotomized mouse facial motor nucleus and aggregate around sites of neuronal degeneration. J. Neurosci. 18 (1998) 5804-5816
42. Bechmann I., et al. Presence of B7-2 (CD86) and lack of B7-1 (CD80) on myelin phagocytosing MHC-II-positive rat microglia is associated with nondestructive immunity in vivo. FASEB J. 15 (2001) 1086-1088
43. Babcock A.A., et al. Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS. J. Neurosci. 23 (2003) 7922-7930
44. McMahon E.J., et al. Absence of macrophage-inflammatory protein-1α delays central nervous system demyelination in the presence of an intact blood-brain barrier. J. Immunol. 167 (2001) 2964-2971
45. Rovaris M., et al. Axonal injury in early multiple sclerosis is irreversible and independent of the short-term disease evolution. Neurology 65 (2005) 1626-1630
46. Lucchinetti C.F., et al. Distinct patterns of multiple sclerosis pathology indicates heterogeneity in pathogenesis. Brain Pathol. 6 (1996) 259-274
47. Sofroniew M.V., and Isacson O. Distribution of degeneration of cholinergic neurons in the septum following axotomy in different portions of the fimbria-fornix: a correlation between degree of cell loss and proximity of neuronal somata to the lesion. J. Chem. Neuroanat. 1 (1988) 327-337
48. Dalton C.M., et al. Early development of multiple sclerosis is associated with progressive grey matter atrophy in patients presenting with clinically isolated syndromes. Brain 127 (2004) 1101-1107
49. Schwartz M., et al. Protective autoimmunity against the enemy within: fighting glutamate toxicity. Trends Neurosci. 26 (2003) 297-302
50. Kerschensteiner M., et al. Neurotrophic cross-talk between the nervous and immune systems: implications for neurological diseases. Ann. Neurol. 53 (2003) 292-304
51. Moser H.W., et al. Adrenoleukodystrophy: new approaches to a neurodegenerative disease. JAMA. 294 (2005) 3131-3134
52. Dirnagl U., et al. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 22 (1999) 391-397
53. Danton G.H., and Dietrich W.D. Inflammatory mechanisms after ischemia and stroke. J. Neuropathol. Exp. Neurol. 62 (2003) 127-136
54. Saleh A., et al. In vivo MRI of brain inflammation in human ischaemic stroke. Brain 127 (2004) 1670-1677
55. Allan S.M., et al. Interleukin-1 and neuronal injury. Nat. Rev. Immunol. 5 (2005) 629-640
56. Akiyama H., et al. Inflammation and Alzheimer's disease. Neurobiol. Aging 21 (2000) 383-421
57. Floden A.M., et al. Beta-amyloid-stimulated microglia induce neuron death via synergistic stimulation of tumor necrosis factor alpha and NMDA receptors. J. Neurosci. 25 (2005) 2566-2575
58. Bellucci A., et al. Induction of inflammatory mediators and microglial activation in mice transgenic for mutant human P301S tau protein. Am. J. Pathol. 165 (2004) 1643-1652
59. Heneka M.T., et al. Locus ceruleus degeneration promotes Alzheimer pathogenesis in amyloid precursor protein 23 transgenic mice. J. Neurosci. 26 (2006) 1343-1354
60. McGeer P.L., et al. Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 38 (1988) 1285-1291
61. Langston J.W., et al. Evidence of active nerve cell degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine exposure. Ann. Neurol. 46 (1999) 598-605
62. Sapp E., et al. Early and progressive accumulation of reactive microglia in the Huntington disease brain. J. Neuropathol. Exp. Neurol. 60 (2001) 161-172
63. Gelinas D.S., et al. Immunotherapy for Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 101 Suppl. 2 (2004) 14657-14662
64. Zhang W., et al. Aggregated α-synuclein activates microglia: a process leading to disease progression in Parkinson's disease. FASEB J. 19 (2005) 533-542
65. Cannella B., and Raine C.S. The adhesion molecule and cytokine profile of multiple sclerosis lesions. Ann. Neurol. 37 (1995) 424-435
66. Emsley H.C., et al. A randomised phase II study of interleukin-1 receptor antagonist in acute stroke patients. J. Neurol. Neurosurg. Psychiatry 76 (2005) 1366-1372
67. Dörr J., et al. Lack of tumor necrosis factor-related apoptosis-inducing ligand but presence of its receptors in the human brain. J. Neurosci. 22 (2002) RC209
68. Nitsch R., et al. Human brain-cell death induced by tumour-necrosis-factor-related apoptosis-inducing ligand (TRAIL). Lancet 356 (2000) 827-828
69. Ehrlich S., et al. Regulation of soluble and surface-bound TRAIL in human T cells, B cells, and monocytes. Cytokine 24 (2003) 244-253
70. Fulda S., et al. Smac agonists sensitize for Apo2L/TRAIL- or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat. Med. 8 (2002) 808-815
71. Miura Y., et al. Tumor necrosis factor-related apoptosis-inducing ligand induces neuronal death in a murine model of HIV central nervous system infection. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 2777-2782
72. Ryan L.A., et al. TNF-related apoptosis-inducing ligand mediates human neuronal apoptosis: links to HIV-1-associated dementia. J. Neuroimmunol. 148 (2004) 127-139
73. Martin-Villalba A., et al. CD95 ligand (Fas-L/APO-1L) and tumor necrosis factor-related apoptosis-inducing ligand mediate ischemia-induced apoptosis in neurons. J. Neurosci. 19 (1999) 3809-3817
74. Cantarella G., et al. Neutralization of TRAIL death pathway protects human neuronal cell line from β-amyloid toxicity. Cell Death Differ. 10 (2003) 134-141
75. Guix F.X., et al. The physiology and pathophysiology of nitric oxide in the brain. Prog. Neurobiol. 76 (2005) 126-152
76. Waxman S.G. Nitric oxide and the axonal death cascade. Ann. Neurol. 53 (2003) 150-153
77. Beal M.F. Mitochondria take center stage in aging and neurodegeneration. Ann. Neurol. 58 (2005) 495-505
78. Dutta R., et al. Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann. Neurol. 59 (2006) 478-489
79. Burt R.K., et al. Hematopoietic stem cell transplantation for multiple sclerosis. Arch. Neurol. 62 (2005) 860-864
80. Peters C., et al. Cerebral X-linked adrenoleukodystrophy: the international hematopoietic cell transplantation experience from 1982 to 1999. Blood 104 (2004) 881-888
81. Beck R.W., et al. The effect of corticosteroids for acute optic neuritis on the subsequent development of multiple sclerosis. The Optic Neuritis Study Group. N. Engl. J. Med. 329 (1993) 1764-1769
82. de Gans J., and van de Beek D. Dexamethasone in adults with bacterial meningitis. N. Engl. J. Med. 347 (2002) 1549-1556
83. McGeer P.L., et al. Arthritis and anti-inflammatory agents as possible protective factors for Alzheimer's disease: a review of 17 epidemiologic studies. Neurology 47 (1996) 425-432
84. Lim G.P., et al. Ibuprofen suppresses plaque pathology and inflammation in a mouse model for Alzheimer's disease. J. Neurosci. 20 (2000) 5709-5714
85. Heneka M.T., et al. Acute treatment with the PPARγ agonist pioglitazone and ibuprofen reduces glial inflammation and Aβ1-42 levels in APPV717I transgenic mice. Brain 128 (2005) 1442-1453
86. Chen H., et al. Nonsteroidal anti-inflammatory drugs and the risk of Parkinson disease. Arch. Neurol. 60 (2003) 1059-1064
87. Teismann P., and Ferger B. Inhibition of the cyclooxygenase isoenzymes COX-1 and COX-2 provide neuroprotection in the MPTP-mouse model of Parkinson's disease. Synapse 39 (2001) 167-174
88. Scali C., et al. The selective cyclooxygenase-2 inhibitor rofecoxib suppresses brain inflammation and protects cholinergic neurons from excitotoxic degeneration in vivo. Neuroscience 117 (2003) 909-919
89. Hohlfeld R., and Wekerle H. Autoimmune concepts of multiple sclerosis as a basis for selective immunotherapy: From pipe dreams to (therapeutic) pipelines. Proc. Natl. Acad. Sci. U. S. A (2004)
90. Frenkel D., et al. Nasal vaccination with a proteosome-based adjuvant and glatiramer acetate clears beta-amyloid in a mouse model of Alzheimer disease. J. Clin. Invest. 115 (2005) 2423-2433
91. Benner E.J., et al. Therapeutic immunization protects dopaminergic neurons in a mouse model of Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 9435-9440
92. Aktas O., et al. Green tea epigallocatechin-3-gallate mediates T cellular NF-κB inhibition and exerts neuroprotection in autoimmune encephalomyelitis. J. Immunol. 173 (2004) 5794-5800
93. Hendriks J.J., et al. Flavonoids influence monocytic GTPase activity and are protective in experimental allergic encephalitis. J. Exp. Med. 200 (2004) 1667-1672
94. Rezai-Zadeh K., et al. Green tea epigallocatechin-3-gallate (EGCG) modulates amyloid precursor protein cleavage and reduces cerebral amyloidosis in Alzheimer transgenic mice. J. Neurosci. 25 (2005) 8807-8814
95. Levites Y., et al. Green tea polyphenol (-)-epigallocatechin-3-gallate prevents N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced dopaminergic neurodegeneration. J. Neurochem. 78 (2001) 1073-1082
96. Fazekas F., et al. Randomised placebo-controlled trial of monthly intravenous immunoglobulin therapy in relapsing-remitting multiple sclerosis. Lancet 349 (1997) 589-593
97. Achiron A., et al. Intravenous immunoglobulin treatment of experimental T cell-mediated autoimmune disease. Upregulation of T cell proliferation and downregulation of tumor necrosis factor α secretion. J. Clin. Invest. 93 (1994) 600-605
98. Dodel R.C., et al. Intravenous immunoglobulins containing antibodies against β-amyloid for the treatment of Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 75 (2004) 1472-1474
99. Youssef S., et al. The HMG-CoA reductase inhibitor, atorvastatin, promotes a Th2 bias and reverses paralysis in central nervous system autoimmune disease. Nature 420 (2002) 78-84
100. Aktas O., et al. Treatment of relapsing paralysis in experimental encephalomyelitis by targeting Th1 cells through atorvastatin. J. Exp. Med. 197 (2003) 725-733
101. Vollmer T., et al. Oral simvastatin treatment in relapsing-remitting multiple sclerosis. Lancet 363 (2004) 1607-1608
102. Wolozin B., et al. Decreased prevalence of Alzheimer disease associated with 3-hydroxy-3-methyglutaryl coenzyme A reductase inhibitors. Arch. Neurol. 57 (2000) 1439-1443
103. Selley M.L. Simvastatin prevents 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced striatal dopamine depletion and protein tyrosine nitration in mice. Brain Res. 1037 (2005) 1-6
104. Singh I., et al. Lovastatin for X-linked adrenoleukodystrophy. N. Engl. J. Med. 339 (1998) 702-703
105. Feinstein D.L., et al. Peroxisome proliferator-activated receptor-γ agonists prevent experimental autoimmune encephalomyelitis. Ann. Neurol. 51 (2002) 694-702
106. Dehmer T., et al. Protection by pioglitazone in the MPTP model of Parkinson's disease correlates with IκBα induction and block of NFκB and iNOS activation. J. Neurochem. 88 (2004) 494-501
107. Masliah E., et al. Effects of α-synuclein immunization in a mouse model of Parkinson's disease. Neuron 46 (2005) 857-868
108. + T cells. J. Immunol. 171 (2003) 6549-6555
109. Fox R.J., and Ransohoff R.M. New directions in MS therapeutics: vehicles of hope. Trends Immunol. 25 (2004) 632-636
110. Connolly Jr. E.S., et al. Cerebral protection in homozygous null ICAM-1 mice after middle cerebral artery occlusion. Role of neutrophil adhesion in the pathogenesis of stroke. J. Clin. Invest. 97 (1996) 209-216
111. Braun J.S., et al. Neuroprotection by a caspase inhibitor in acute bacterial meningitis. Nat. Med. 5 (1999) 298-302
112. Brundula V., et al. Targeting leukocyte MMPs and transmigration. Minocycline as a potential therapy for multiple sclerosis. Brain 125 (2002) 1297-1308
113. Metz L.M., et al. Minocycline reduces gadolinium-enhancing magnetic resonance imaging lesions in multiple sclerosis. Ann. Neurol. 55 (2004) 756
114. Chen M., et al. Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat. Med. 6 (2000) 797-801
115. Yrjanheikki J., et al. Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 15769-15774
116. Benveniste E.N., et al. Immunological aspects of microglia: relevance to Alzheimer's disease. Neurochem. Int. 39 (2001) 381-391
117. Cagnin A., et al. In-vivo measurement of activated microglia in dementia. Lancet 358 (2001) 461-467
118. Griffin D.E., et al. Identification of the inflammatory cells in the central nervous system of patients with adrenoleukodystrophy. Ann. Neurol. 18 (1985) 660-664
119. Itagaki S., et al. Presence of T-cytotoxic suppressor and leucocyte common antigen positive cells in Alzheimer's disease brain tissue. Neurosci. Lett. 91 (1988) 259-264
120. Furlan R., et al. Vaccination with amyloid-β peptide induces autoimmune encephalomyelitis in C57/BL6 mice. Brain 126 (2003) 285-291
121. + T cells dominate the T cell infiltrate in active multiple sclerosis lesions as shown by micromanipulation and single cell polymerase chain reaction. J. Exp. Med. 192 (2000) 393-404
122. Medana I.M., et al. MHC class I-restricted killing of neurons by virus-specific CD8+ T lymphocytes is effected through the Fas/FasL, but not the perforin pathway. Eur. J. Immunol. 30 (2000) 3623-3633
123. + T cells in the brain correlate with early central nervous system dysfunction in simian immunodeficiency virus infection. J. Immunol. 167 (2001) 5429-5438
124. Cepok S., et al. Short-lived plasma blasts are the main B cell effector subset during the course of multiple sclerosis. Brain 128 (2005) 1667-1676
125. Becher B., et al. 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
126. Tan J., et al. Role of CD40 ligand in amyloidosis in transgenic Alzheimer's mice. Nat. Neurosci. 5 (2002) 1288-1293
127. Okuno T., et al. Loss of dopaminergic neurons by the induction of inducible nitric oxide synthase and cyclooxygenase-2 via CD 40: relevance to Parkinson's disease. J. Neurosci. Res. 81 (2005) 874-882
128. Zipp F., et al. Immune (dys)regulation in multiple sclerosis: Role of the CD95/CD95 ligand system. Immunol. Today 20 (1999) 550-554
129. Walsh M.J., and Murray J.M. Dual implication of 2′,3′-cyclic nucleotide 3′ phosphodiesterase as major autoantigen and C3 complement-binding protein in the pathogenesis of multiple sclerosis. J. Clin. Invest. 101 (1998) 1923-1931
130. De Simoni M.G., et al. The powerful neuroprotective action of C1-inhibitor on brain ischemia-reperfusion injury does not require C1q. Am. J. Pathol. 164 (2004) 1857-1863
131. Wyss-Coray T., et al. Prominent neurodegeneration and increased plaque formation in complement-inhibited Alzheimer's mice. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 10837-10842
132. Muthian G., et al. COX-2 inhibitors modulate IL-12 signaling through JAK-STAT pathway leading to Th1 response in experimental allergic encephalomyelitis. J. Clin. Immunol. 26 (2006) 73-85
133. Hoozemans J.J., et al. Maximal COX-2 and ppRb expression in neurons occurs during early Braak stages prior to the maximal activation of astrocytes and microglia in Alzheimer's disease. J. Neuroinflamm. 2 (2005) 27
134. Pitt D., et al. Glutamate excitotoxicity in a model of multiple sclerosis. Nat. Med. 6 (2000) 67-70
135. Smith T., et al. Autoimmune encephalomyelitis ameliorated by AMPA antagonists. Nat. Med. 6 (2000) 62-66
136. Taylor D.L., et al. Stimulation of microglial metabotropic glutamate receptor mGlu2 triggers tumor necrosis factor α-induced neurotoxicity in concert with microglial-derived Fas ligand. J. Neurosci. 25 (2005) 2952-2964
137. Zeron M.M., et al. Increased sensitivity to N-methyl-d-aspartate receptor-mediated excitotoxicity in a mouse model of Huntington's disease. Neuron 33 (2002) 849-860
138. Koedel U., et al. Role of Caspase-1 in experimental pneumococcal meningitis: evidence from pharmacologic Caspase inhibition and Caspase-1-deficient mice. Ann. Neurol. 51 (2002) 319-329
139. Jurewicz A., et al. Tumour necrosis factor-induced death of adult human oligodendrocytes is mediated by apoptosis inducing factor. Brain 128 (2005) 2675-2688
140. Bruce A.J., et al. Altered neuronal and microglial responses to excitotoxic and ischemic brain injury in mice lacking TNF receptors. Nat. Med. 2 (1996) 788-794
141. Liu J., et al. TNF is a potent anti-inflammatory cytokine in autoimmune-mediated demyelination. Nat. Med. 4 (1998) 78-83
142. Diem R., et al. Reduction of potassium currents and phosphatidylinositol 3-kinase-dependent AKT phosphorylation by tumor necrosis factor-α rescues axotomized retinal ganglion cells from retrograde cell death in vivo. J. Neurosci. 21 (2001) 2058-2066
143. Sato K., et al. TRAIL-expressing T cells induce apoptosis of vascular smooth muscle cells in the atherosclerotic plaque. J. Exp. Med. 203 (2006) 239-250