Death receptor signalling in central nervous system inflammation and demyelination

Trends in Neurosciences

Volumn 34, Issue 12, 2011, Pages 619-628

  McGuire, Conor ^a,b   Beyaert, Rudi ^a,b   van Loo, Geert ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

DEATH RECEPTOR; DEATH RECEPTOR 3; DEATH RECEPTOR 4; DEATH RECEPTOR 5; DEATH RECEPTOR 6; FAS ANTIGEN; FAS LIGAND; NEUROTROPHIN RECEPTOR P75; TUMOR NECROSIS FACTOR RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED DEATH DOMAIN PROTEIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

APOPTOSIS; CENTRAL NERVOUS SYSTEM; DEMYELINATION; HUMAN; INFLAMMATION; MULTIPLE SCLEROSIS; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TREATMENT PLANNING;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; CENTRAL NERVOUS SYSTEM; DEMYELINATING DISEASES; DISEASE MODELS, ANIMAL; FAS LIGAND PROTEIN; HUMANS; INFLAMMATION; MULTIPLE SCLEROSIS; RECEPTOR, NERVE GROWTH FACTOR; RECEPTORS, DEATH DOMAIN; RECEPTORS, TUMOR NECROSIS FACTOR; SIGNAL TRANSDUCTION; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR NECROSIS FACTOR-ALPHA;

EID: 82855165034     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2011.09.002     Document Type: Review

References (114)

1. Yuan J., Yankner B.A. Apoptosis in the nervous system. Nature 2000, 407:802-809.
2. Park S.M., et al. Nonapoptotic functions of FADD-binding death receptors and their signaling molecules. Curr. Opin. Cell Biol. 2005, 17:610-616.
3. Trapp B.D., Nave K.A. Multiple sclerosis: an immune or neurodegenerative disorder?. Annu. Rev. Neurosci. 2008, 31:247-269.
4. Baxter A.G. The origin and application of experimental autoimmune encephalomyelitis. Nat. Rev. Immunol. 2007, 7:904-912.
5. van Loo G., et al. Inhibition of transcription factor NF-kappaB in the central nervous system ameliorates autoimmune encephalomyelitis in mice. Nat. Immunol. 2006, 7:954-961.
6. Buss R.R., et al. Adaptive roles of programmed cell death during nervous system development. Annu. Rev. Neurosci. 2006, 29:1-35.
7. Blaschke A.J., et al. Widespread programmed cell death in proliferative and postmitotic regions of the fetal cerebral cortex. Development 1996, 122:1165-1174.
8. McConnell M.J., et al. Mathematical modeling supports substantial mouse neural progenitor cell death. Neural Dev. 2009, 4:28.
9. Wilkie A.L., et al. Widespread tangential dispersion and extensive cell death during early neurogenesis in the mouse neocortex. Dev. Biol. 2004, 267:109-118.
10. Hamburger V., Levi-Montalcini R. Proliferation, differentiation and degeneration in the spinal ganglia of the chick embryo under normal and experimental conditions. J. Exp. Zool. 1949, 111:457-501.
11. Schecterson L.C., Bothwell M. Neurotrophin receptors: old friends with new partners. Dev. Neurobiol. 2010, 70:332-338.
12. Underwood C.K., Coulson E.J. The p75 neurotrophin receptor. Int. J. Biochem. Cell Biol. 2008, 40:1664-1668.
13. de la Rosa E.J., de Pablo F. Cell death in early neural development: beyond the neurotrophic theory. Trends Neurosci. 2000, 23:454-458.
14. Vila M., Przedborski S. Targeting programmed cell death in neurodegenerative diseases. Nat. Rev. Neurosci. 2003, 4:365-375.
15. Cheema Z.F., et al. Fas/Apo [apoptosis]-1 and associated proteins in the differentiating cerebral cortex: induction of caspase-dependent cell death and activation of NF-kappaB. J. Neurosci 1999, 19:1754-1770.
16. McQuillen P.S., et al. A novel role for p75NTR in subplate growth cone complexity and visual thalamocortical innervation. J. Neurosci. 2002, 22:3580-3593.
17. Naumann T., et al. Complete deletion of the neurotrophin receptor p75NTR leads to long-lasting increases in the number of basal forebrain cholinergic neurons. J. Neurosci. 2002, 22:2409-2418.
18. Nikolaev A., et al. APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 2009, 457:981-989.
19. von Schack D., et al. Complete ablation of the neurotrophin receptor p75NTR causes defects both in the nervous and the vascular system. Nat. Neurosci. 2001, 4:977-978.
20. Iosif R.E., et al. Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J. Neurosci. 2006, 26:9703-9712.
21. Park K.J., et al. p75NTR-dependent, myelin-mediated axonal degeneration regulates neural connectivity in the adult brain. Nat. Neurosci. 2010, 13:559-566.
22. Twohig J.P., et al. Age-dependent maintenance of motor control and corticostriatal innervation by death receptor 3. J. Neurosci. 2010, 30:3782-3792.
23. Zuliani C., et al. Control of neuronal branching by the death receptor CD95 (Fas/Apo-1). Cell Death Differ. 2006, 13:31-40.
24. Locksley R.M., et al. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 2001, 104:487-501.
25. Wilson N.S., et al. Death receptor signal transducers: nodes of coordination in immune signaling networks. Nat. Immunol. 2009, 10:348-355.
26. Kucharczak J., et al. To be, or not to be: NF-kappaB is the answer - role of Rel/NF-kappaB in the regulation of apoptosis. Oncogene 2003, 22:8961-8982.
27. Vandenabeele P., et al. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 2010, 11:700-714.
28. Kaiser W.J., et al. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 2011, 471:368-372.
29. Oberst A., et al. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 2011, 471:363-367.
30. Zhang H., et al. Functional complementation between FADD and RIP1 in embryos and lymphocytes. Nature 2011, 471:373-376.
31. Welz P.-S., et al. FADD prevents RIP3-mediated epithelial cell necrosis and chronic intestinal inflammation. Nature 2011, 477:330-334.
32. Kreuz S., et al. NFkappaB activation by Fas is mediated through FADD, caspase-8, and RIP and is inhibited by FLIP. J. Cell Biol. 2004, 166:369-380.
33. Micera A., et al. Nerve growth factor and tissue repair remodeling: trkA(NGFR) and p75(NTR), two receptors one fate. Cytokine Growth Factor Rev. 2007, 18:245-256.
34. Nicol G.D., Vasko M.R. Unraveling the story of NGF-mediated sensitization of nociceptive sensory neurons: ON or OFF the Trks?. Mol. Interv. 2007, 7:26-41.
35. Caminero A., et al. Tumor necrosis factor alpha (TNF-alpha), anti-TNF-alpha and demyelination revisited: an ongoing story. J. Neuroimmunol. 2011, 234:1-6.
36. Patel J.R., Brewer G.J. Age-related changes to tumor necrosis factor receptors affect neuron survival in the presence of beta-amyloid. J. Neurosci. Res. 2008, 86:2303-2313.
37. Yan P., et al. Expression of the type 1 and type 2 receptors for tumor necrosis factor after traumatic spinal cord injury in adult rats. Exp. Neurol. 2003, 183:286-297.
38. Akassoglou K., et al. Astrocyte-specific but not neuron-specific transmembrane TNF triggers inflammation and degeneration in the central nervous system of transgenic mice. J. Immunol. 1997, 158:438-445.
39. Probert L., et al. Spontaneous inflammatory demyelinating disease in transgenic mice showing central nervous system-specific expression of tumor necrosis factor alpha. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:11294-11298.
40. Ruddle N.H., et al. An antibody to lymphotoxin and tumor necrosis factor prevents transfer of experimental allergic encephalomyelitis. J. Exp. Med. 1990, 172:1193-1200.
41. Eugster H.P., et al. Severity of symptoms and demyelination in MOG-induced EAE depends on TNFR1. Eur. J. Immunol. 1999, 29:626-632.
42. Frei K., et al. Tumor necrosis factor alpha and lymphotoxin alpha are not required for induction of acute experimental autoimmune encephalomyelitis. J. Exp. Med. 1997, 185:2177-2182.
43. Kassiotis G., et al. TNF accelerates the onset but does not alter the incidence and severity of myelin basic protein-induced experimental autoimmune encephalomyelitis. Eur. J. Immunol. 1999, 29:774-780.
44. Korner H., et al. Critical points of tumor necrosis factor action in central nervous system autoimmune inflammation defined by gene targeting. J. Exp. Med. 1997, 186:1585-1590.
45. Liu J., et al. TNF is a potent anti-inflammatory cytokine in autoimmune-mediated demyelination. Nat. Med. 1998, 4:78-83.
46. Anon 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 1999, 53:457-465.
47. van Oosten B.W., et al. Increased MRI activity and immune activation in two multiple sclerosis patients treated with the monoclonal anti-tumor necrosis factor antibody cA2. Neurology 1996, 47:1531-1534.
48. Arnett H.A., et al. TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat. Neurosci. 2001, 4:1116-1122.
49. Kassiotis G., Kollias G. Uncoupling the proinflammatory from the immunosuppressive properties of tumor necrosis factor (TNF) at the p55 TNF receptor level: implications for pathogenesis and therapy of autoimmune demyelination. J. Exp. Med. 2001, 193:427-434.
50. Suvannavejh G.C., et al. Divergent roles for p55 and p75 tumor necrosis factor receptors in the pathogenesis of MOG(35-55)-induced experimental autoimmune encephalomyelitis. Cell. Immunol. 2000, 205:24-33.
51. Alexopoulou L., et al. Transmembrane TNF protects mutant mice against intracellular bacterial infections, chronic inflammation and autoimmunity. Eur. J. Immunol. 2006, 36:2768-2780.
52. Pitt D., et al. Glutamate excitotoxicity in a model of multiple sclerosis. Nat. Med. 2000, 6:67-70.
53. Takeuchi H., et al. Tumor necrosis factor-alpha induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J. Biol. Chem. 2006, 281:21362-21368.
54. Taylor D.L., et al. Stimulation of microglial metabotropic glutamate receptor mGlu2 triggers tumor necrosis factor alpha-induced neurotoxicity in concert with microglial-derived Fas ligand. J. Neurosci. 2005, 25:2952-2964.
55. Akassoglou K., et al. Oligodendrocyte apoptosis and primary demyelination induced by local TNF/p55TNF receptor signaling in the central nervous system of transgenic mice: models for multiple sclerosis with primary oligodendrogliopathy. Am. J. Pathol. 1998, 153:801-813.
56. Hisahara S., et al. Targeted expression of baculovirus p35 caspase inhibitor in oligodendrocytes protects mice against autoimmune-mediated demyelination. EMBO J. 2000, 19:341-348.
57. Hisahara S., et al. ICE/CED-3 family executes oligodendrocyte apoptosis by tumor necrosis factor. J. Neurochem. 1997, 69:10-20.
58. Hovelmeyer N., et al. Apoptosis of oligodendrocytes via Fas and TNF-R1 is a key event in the induction of experimental autoimmune encephalomyelitis. J. Immunol. 2005, 175:5875-5884.
59. Mc Guire C., et al. Oligodendrocyte-specific FADD deletion protects mice from autoimmune-mediated demyelination. J. Immunol. 2010, 185:7646-7653.
60. Ciusani E., et al. Soluble Fas (Apo-1) levels in cerebrospinal fluid of multiple sclerosis patients. J. Neuroimmunol. 1998, 82:5-12.
61. Dowling P., et al. Involvement of the CD95 (APO-1/Fas) receptor/ligand system in multiple sclerosis brain. J. Exp. Med. 1996, 184:1513-1518.
62. D'Souza S.D., et al. Multiple sclerosis: Fas signaling in oligodendrocyte cell death. J. Exp. Med. 1996, 184:2361-2370.
63. Aktas O., et al. Death ligands and autoimmune demyelination. Neuroscientist 2006, 12:305-316.
64. Waldner H., et al. Fas- and FasL-deficient mice are resistant to induction of autoimmune encephalomyelitis. J. Immunol. 1997, 159:3100-3103.
65. Sabelko K.A., et al. Fas and Fas ligand enhance the pathogenesis of experimental allergic encephalomyelitis, but are not essential for immune privilege in the central nervous system. J. Immunol. 1997, 159:3096-3099.
66. Dittel B.N., et al. Evidence for Fas-dependent and Fas-independent mechanisms in the pathogenesis of experimental autoimmune encephalomyelitis. J. Immunol. 1999, 162:6392-6400.
67. Elliott E.A., et al. Treatment of experimental encephalomyelitis with a novel chimeric fusion protein of myelin basic protein and proteolipid protein. J. Clin. Invest. 1996, 98:1602-1612.
68. Suvannavejh G.C., et al. Fas-mediated apoptosis in clinical remissions of relapsing experimental autoimmune encephalomyelitis. J. Clin. Invest. 2000, 105:223-231.
69. Sabelko-Downes K.A., et al. Dual role for Fas ligand in the initiation of and recovery from experimental allergic encephalomyelitis. J. Exp. Med. 1999, 189:1195-1205.
70. Ethell D.W., Buhler L.A. Fas ligand-mediated apoptosis in degenerative disorders of the brain. J. Clin. Immunol. 2003, 23:363-370.
71. Bonetti B., et al. Cell death during autoimmune demyelination: effector but not target cells are eliminated by apoptosis. J. Immunol. 1997, 159:5733-5741.
72. Rensing-Ehl A., et al. Neurons induced to express major histocompatibility complex class I antigen are killed via the perforin and not the Fas (APO-1/CD95) pathway. Eur. J. Immunol. 1996, 26:2271-2274.
73. Zhu B., et al. Intrathecal Fas ligand infusion strengthens immunoprivilege of central nervous system and suppresses experimental autoimmune encephalomyelitis. J. Immunol. 2002, 169:1561-1569.
74. Wildbaum G., et al. A targeted DNA vaccine encoding Fas ligand defines its dual role in the regulation of experimental autoimmune encephalomyelitis. J. Clin. Invest. 2000, 106:671-679.
75. Flugel A., et al. Neuronal FasL induces cell death of encephalitogenic T lymphocytes. Brain Pathol. 2000, 10:353-364.
76. Sun D., et al. Cell death mediated by Fas-FasL interaction between glial cells and MBP-reactive T cells. J. Neurosci. Res. 1998, 52:458-467.
77. Ponomarev E.D., Dittel B.N. Gamma delta T cells regulate the extent and duration of inflammation in the central nervous system by a Fas ligand-dependent mechanism. J. Immunol. 2005, 174:4678-4687.
78. Hoffmann O., et al. Tumour necrosis factor-related apoptosis-inducing ligand (TRAIL) in central nervous system inflammation. J. Mol. Med. 2009, 87:753-763.
79. Matysiak M., et al. TRAIL induces death of human oligodendrocytes isolated from adult brain. Brain 2002, 125:2469-2480.
80. 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. 1999, 19:3809-3817.
81. Nitsch R., et al. Human brain-cell death induced by tumour-necrosis-factor-related apoptosis-inducing ligand (TRAIL). Lancet 2000, 356:827-828.
82. Kikuchi S., et al. TNF-related apoptosis inducing ligand (TRAIL) gene polymorphism in Japanese patients with multiple sclerosis. J. Neuroimmunol. 2005, 167:170-174.
83. Weber A., et al. Identification and functional characterization of a highly polymorphic region in the human TRAIL promoter in multiple sclerosis. J. Neuroimmunol. 2004, 149:195-201.
84. Cannella B., et al. Multiple sclerosis: death receptor expression and oligodendrocyte apoptosis in established lesions. J. Neuroimmunol. 2007, 188:128-137.
85. Dorr J., et al. Lack of tumor necrosis factor-related apoptosis-inducing ligand but presence of its receptors in the human brain. J. Neurosci. 2002, 22:RC209.
86. Huang W.X., et al. Apoptosis mediators fasL and TRAIL are upregulated in peripheral blood mononuclear cells in MS. Neurology 2000, 55:928-934.
87. Aktas O., et al. Neuronal damage in autoimmune neuroinflammation mediated by the death ligand TRAIL. Neuron 2005, 46:421-432.
88. Hilliard B., et al. Roles of TNF-related apoptosis-inducing ligand in experimental autoimmune encephalomyelitis. J. Immunol. 2001, 166:1314-1319.
89. Cretney E., et al. TNF-related apoptosis-inducing ligand (TRAIL)/Apo2L suppresses experimental autoimmune encephalomyelitis in mice. Immunol. Cell Biol. 2005, 83:511-519.
90. Lunemann J.D., et al. Death ligand TRAIL induces no apoptosis but inhibits activation of human (auto)antigen-specific T cells. J. Immunol. 2002, 168:4881-4888.
91. Hirata S., et al. Involvement of regulatory T cells in the experimental autoimmune encephalomyelitis-preventive effect of dendritic cells expressing myelin oligodendrocyte glycoprotein plus TRAIL. J. Immunol. 2007, 178:918-925.
92. Ikeda T., et al. Dual effects of TRAIL in suppression of autoimmunity: the inhibition of Th1 cells and the promotion of regulatory T cells. J. Immunol. 2010, 185:5259-5267.
93. Mi S., et al. Death receptor 6 negatively regulates oligodendrocyte survival, maturation and myelination. Nat. Med. 2011, 17:816-821.
94. Kuester M., et al. The crystal structure of death receptor 6 (DR6): a potential receptor of the amyloid precursor protein (APP). J. Mol. Biol. 2011, 409:189-201.
95. Schmidt C.S., et al. Resistance to myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis by death receptor 6-deficient mice. J. Immunol. 2005, 175:2286-2292.
96. Dechant G., Barde Y.A. The neurotrophin receptor p75(NTR): novel functions and implications for diseases of the nervous system. Nat. Neurosci. 2002, 5:1131-1136.
97. Gu C., et al. Oligodendrocyte apoptosis mediated by caspase activation. J. Neurosci. 1999, 19:3043-3049.
98. Dowling P., et al. Up-regulated p75NTR neurotrophin receptor on glial cells in MS plaques. Neurology 1999, 53:1676-1682.
99. Gold S.M., et al. Basal serum levels and reactivity of nerve growth factor and brain-derived neurotrophic factor to standardized acute exercise in multiple sclerosis and controls. J. Neuroimmunol. 2003, 138:99-105.
100. Laudiero L.B., et al. Multiple sclerosis patients express increased levels of beta-nerve growth factor in cerebrospinal fluid. Neurosci. Lett. 1992, 147:9-12.
101. De Simone R., et al. mRNA for NGF and p75 in the central nervous system of rats affected by experimental allergic encephalomyelitis. Neuropathol. Appl. Neurobiol. 1996, 22:54-59.
102. Soilu-Hanninen M., et al. Treatment of experimental autoimmune encephalomyelitis with antisense oligonucleotides against the low affinity neurotrophin receptor. J. Neurosci. Res. 2000, 59:712-721.
103. Copray S., et al. Deficient p75 low-affinity neurotrophin receptor expression exacerbates experimental allergic encephalomyelitis in C57/BL6 mice. J. Neuroimmunol. 2004, 148:41-53.
104. Kust B., et al. Deficient p75 low-affinity neurotrophin receptor expression does alter the composition of cellular infiltrate in experimental autoimmune encephalomyelitis in C57BL/6 mice. J. Neuroimmunol. 2006, 174:92-100.
105. Zhang J., et al. Bone marrow stromal cell therapy reduces proNGF and p75 expression in mice with experimental autoimmune encephalomyelitis. J. Neurol. Sci. 2009, 279:30-38.
106. Casaccia-Bonnefil P., et al. Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature 1996, 383:716-719.
107. Cohen R.I., et al. Nerve growth factor and neurotrophin-3 differentially regulate the proliferation and survival of developing rat brain oligodendrocytes. J. Neurosci. 1996, 16:6433-6442.
108. Ladiwala U., et al. p75 neurotrophin receptor expression on adult human oligodendrocytes: signaling without cell death in response to NGF. J. Neurosci. 1998, 18:1297-1304.
109. Yoon S.O., et al. Competitive signaling between TrkA and p75 nerve growth factor receptors determines cell survival. J. Neurosci. 1998, 18:3273-3281.
110. Copray J.C., et al. p75NTR independent oligodendrocyte death in cuprizone-induced demyelination in C57BL/6 mice. Neuropathol. Appl. Neurobiol. 2005, 31:600-609.
111. French L.E., Tschopp J. Protein-based therapeutic approaches targeting death receptors. Cell Death Differ. 2003, 10:117-123.
112. Hirata S., et al. Prevention of experimental autoimmune encephalomyelitis by transfer of embryonic stem cell-derived dendritic cells expressing myelin oligodendrocyte glycoprotein peptide along with TRAIL or programmed death-1 ligand. J. Immunol. 2005, 174:1888-1897.
113. VandenBerghe T., et al. Necroptosis, necrosis and secondary necrosis converge on similar cellular disintegration features. Cell Death Differ. 2010, 17:922-930.
114. Matsushima G.K., Morell P. The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol. 2001, 11:107-116.