Mechanisms Underlying Inflammation in Neurodegeneration

Cell

Volumn 140, Issue 6, 2010, Pages 918-934

  Glass, Christopher K ^a,b   Saijo, Kaoru ^a   Winner, Beate ^c   Marchetto, Maria Carolina ^c   Gage, Fred H ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALEMTUZUMAB; ALPHA SYNUCLEIN; ALPHA TOCOPHEROL; AMYLOID PRECURSOR PROTEIN; APOLIPOPROTEIN E; ARUNDIC ACID; BETA SECRETASE; CELASTROL; CELECOXIB; CEP 1347; GAMMA SECRETASE; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR; INTERLEUKIN 12; MINOCYCLINE; MYELIN BASIC PROTEIN; MYELOID DIFFERENTIATION FACTOR 88; NIMESULIDE; PARKIN; ROSIGLITAZONE; SELENIUM; TAR DNA BINDING PROTEIN; TARENFLURBIL; TAU PROTEIN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TRANSCRIPTION FACTOR AP 1; UBIQUINONE; UNINDEXED DRUG;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; ANTIINFLAMMATORY ACTIVITY; CLINICAL TRIAL; DEGENERATIVE DISEASE; DISEASE ASSOCIATION; DISEASE COURSE; DRUG SAFETY; ENVIRONMENTAL FACTOR; HUMAN; INFLAMMATION; MULTIPLE SCLEROSIS; NERVE CELL NECROSIS; NERVOUS SYSTEM INFLAMMATION; NEUROTOXICITY; PARKINSON DISEASE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SENILE PLAQUE; ANIMAL; BRAIN; IMMUNOLOGY; PATHOLOGY;

ANIMALS; BRAIN; HUMANS; INFLAMMATION; NEURODEGENERATIVE DISEASES;

EID: 77950363010     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2010.02.016     Document Type: Review

References (147)

1. ANZgene Genome-wide association study identifies new multiple sclerosis susceptibility loci on chromosomes 12 and 20. Nat. Genet. 2009, 41:824-828.
2. Aisen P.S., Schafer K.A., Grundman M., Pfeiffer E., Sano M., Davis K.L., Farlow M.R., Jin S., Thomas R.G., Thal L.J. Effects of rofecoxib or naproxen vs placebo on Alzheimer disease progression: a randomized controlled trial. JAMA 2003, 289:2819-2826.
3. Akiyama H. Inflammatory response in Alzheimer's disease. Tohoku J. Exp. Med. 1994, 174:295-303.
4. Akiyama H., Barger S., Barnum S., Bradt B., Bauer J., Cole G.M., Cooper N.R., Eikelenboom P., Emmerling M., Fiebich B.L., et al. Inflammation and Alzheimer's disease. Neurobiol. Aging 2000, 21:383-421.
5. Amit I., Garber M., Chevrier N., Leite A.P., Donner Y., Eisenhaure T., Guttman M., Grenier J.K., Li W., Zuk O., et al. Unbiased reconstruction of a mammalian transcriptional network mediating pathogen responses. Science 2009, 326:257-263.
6. Bailey S.L., Schreiner B., McMahon E.J., Miller S.D. CNS myeloid DCs presenting endogenous myelin peptides 'preferentially' polarize CD4+ T(H)-17 cells in relapsing EAE. Nat. Immunol. 2007, 8:172-180.
7. Balistreri C.R., Colonna-Romano G., Lio D., Candore G., Caruso C. TLR4 polymorphisms and ageing: implications for the pathophysiology of age-related diseases. J. Clin. Immunol. 2009, 29:406-415.
8. Ballatore C., Lee V.M., Trojanowski J.Q. Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nat. Rev. Neurosci. 2007, 8:663-672.
9. Banerjee R., Mosley R.L., Reynolds A.D., Dhar A., Jackson-Lewis V., Gordon P.H., Przedborski S., Gendelman H.E. Adaptive immune neuroprotection in G93A-SOD1 amyotrophic lateral sclerosis mice. PLoS ONE 2008, 3:e2740.
10. Barbeito L.H., Pehar M., Cassina P., Vargas M.R., Peluffo H., Viera L., Estevez A.G., Beckman J.S. A role for astrocytes in motor neuron loss in amyotrophic lateral sclerosis. Brain Res. Brain Res. Rev. 2004, 47:263-274.
11. Beers D.R., Henkel J.S., Zhao W., Wang J., Appel S.H. CD4+ T cells support glial neuroprotection, slow disease progression, and modify glial morphology in an animal model of inherited ALS. Proc. Natl. Acad. Sci. USA 2008, 105:15558-15563.
12. Benner E.J., Banerjee R., Reynolds A.D., Sherman S., Pisarev V.M., Tsiperson V., Nemachek C., Ciborowski P., Przedborski S., Mosley R.L., et al. Nitrated alpha-synuclein immunity accelerates degeneration of nigral dopaminergic neurons. PLoS ONE 2008, 3:e1376.
13. Bertram L., Tanzi R.E. Thirty years of Alzheimer's disease genetics: the implications of systematic meta-analyses. Nat. Rev. Neurosci. 2008, 9:768-778.
14. Block M.L., Hong J.S. Chronic microglial activation and progressive dopaminergic neurotoxicity. Biochem. Soc. Trans. 2007, 35:1127-1132.
15. Boillee S., Yamanaka K., Lobsiger C.S., Copeland N.G., Jenkins N.A., Kassiotis G., Kollias G., Cleveland D.W. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 2006, 312:1389-1392.
16. Boissonneault V., Filali M., Lessard M., Relton J., Wong G., Rivest S. Powerful beneficial effects of macrophage colony-stimulating factor on beta-amyloid deposition and cognitive impairment in Alzheimer's disease. Brain 2009, 132:1078-1092.
17. Braak H., Del Tredici K., Rub U., de Vos R.A., Jansen Steur E.N., Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 2003, 24:197-211.
18. Braak H., Sastre M., Del Tredici K. Development of alpha-synuclein immunoreactive astrocytes in the forebrain parallels stages of intraneuronal pathology in sporadic Parkinson's disease. Acta Neuropathol. 2007, 114:231-241.
19. Brochard V., Combadiere B., Prigent A., Laouar Y., Perrin A., Beray-Berthat V., Bonduelle O., Alvarez-Fischer D., Callebert J., Launay J.M., et al. Infiltration of CD4+ lymphocytes into the brain contributes to neurodegeneration in a mouse model of Parkinson disease. J. Clin. Invest. 2009, 119:182-192.
20. Bu G. Apolipoprotein E and its receptors in Alzheimer's disease: pathways, pathogenesis and therapy. Nat. Rev. Neurosci. 2009, 10:333-344.
21. Cardona A.E., Pioro E.P., Sasse M.E., Kostenko V., Cardona S.M., Dijkstra I.M., Huang D., Kidd G., Dombrowski S., Dutta R., et al. Control of microglial neurotoxicity by the fractalkine receptor. Nat. Neurosci. 2006, 9:917-924.
22. Cartier L., Hartley O., Dubois-Dauphin M., Krause K.H. Chemokine receptors in the central nervous system: role in brain inflammation and neurodegenerative diseases. Brain Res. Brain Res. Rev. 2005, 48:16-42.
23. Castano A., Herrera A.J., Cano J., Machado A. Lipopolysaccharide intranigral injection induces inflammatory reaction and damage in nigrostriatal dopaminergic system. J. Neurochem. 1998, 70:1584-1592.
24. Chiu I.M., Chen A., Zheng Y., Kosaras B., Tsiftsoglou S.A., Vartanian T.K., Brown R.H., Carroll M.C. T lymphocytes potentiate endogenous neuroprotective inflammation in a mouse model of ALS. Proc. Natl. Acad. Sci. USA 2008, 105:17913-17918.
25. Choi S.H., Aid S., Bosetti F. The distinct roles of cyclooxygenase-1 and -2 in neuroinflammation: implications for translational research. Trends Pharmacol. Sci. 2009, 30:174-181.
26. Clement A.M., Nguyen M.D., Roberts E.A., Garcia M.L., Boillee S., Rule M., McMahon A.P., Doucette W., Siwek D., Ferrante R.J., et al. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 2003, 302:113-117.
27. Cua D.J., Sherlock J., Chen Y., Murphy C.A., Joyce B., Seymour B., Lucian L., To W., Kwan S., Churakova T., et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003, 421:744-748.
28. Cudkowicz M.E., Shefner J.M., Schoenfeld D.A., Zhang H., Andreasson K.I., Rothstein J.D., Drachman D.B. Trial of celecoxib in amyotrophic lateral sclerosis. Ann. Neurol. 2006, 60:22-31.
29. Dalakas M.C. B cells as therapeutic targets in autoimmune neurological disorders. Nat. Clin. Pract. Neurol. 2008, 4:557-567.
30. Damier P., Hirsch E.C., Zhang P., Agid Y., Javoy-Agid F. Glutathione peroxidase, glial cells and Parkinson's disease. Neuroscience 1993, 52:1-6.
31. Danzer K.M., Haasen D., Karow A.R., Moussaud S., Habeck M., Giese A., Kretzschmar H., Hengerer B., Kostka M. Different species of alpha-synuclein oligomers induce calcium influx and seeding. J. Neurosci. 2007, 27:9220-9232.
32. Di Giorgio F.P., Boulting G.L., Bobrowicz S., Eggan K.C. Human embryonic stem cell-derived motor neurons are sensitive to the toxic effect of glial cells carrying an ALS-causing mutation. Cell Stem Cell 2008, 3:637-648.
33. Di Virgilio F., Ceruti S., Bramanti P., Abbracchio M.P. Purinergic signalling in inflammation of the central nervous system. Trends Neurosci. 2009, 32:79-87.
34. Dimos J.T., Rodolfa K.T., Niakan K.K., Weisenthal L.M., Mitsumoto H., Chung W., Croft G.F., Saphier G., Leibel R., Goland R., et al. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 2008, 321:1218-1221.
35. Doi Y., Mizuno T., Maki Y., Jin S., Mizoguchi H., Ikeyama M., Doi M., Michikawa M., Takeuchi H., Suzumura A. Microglia activated with the toll-like receptor 9 ligand CpG attenuate oligomeric amyloid {beta} neurotoxicity in in vitro and in vivo models of Alzheimer's disease. Am. J. Pathol. 2009, 175:2121-2132.
36. Ebert A.D., Yu J., Rose F.F., Mattis V.B., Lorson C.L., Thomson J.A., Svendsen C.N. Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 2009, 457:277-280.
37. Eisen A. Amyotrophic lateral sclerosis: A 40-year personal perspective. J. Clin. Neurosci. 2009, 16:505-512.
38. Frohman E.M., Racke M.K., Raine C.S. Multiple sclerosis-the plaque and its pathogenesis. N. Engl. J. Med. 2006, 354:942-955.
39. Fugger L., Friese M.A., Bell J.I. From genes to function: the next challenge to understanding multiple sclerosis. Nat. Rev. Immunol. 2009, 9:408-417.
40. Fujinami R.S., Oldstone M.B. Amino acid homology between the encephalitogenic site of myelin basic protein and virus: mechanism for autoimmunity. Science 1985, 230:1043-1045.
41. Gao H.M., Kotzbauer P.T., Uryu K., Leight S., Trojanowski J.Q., Lee V.M. Neuroinflammation and oxidation/nitration of alpha-synuclein linked to dopaminergic neurodegeneration. J. Neurosci. 2008, 28:7687-7698.
42. Gasser T. Molecular pathogenesis of Parkinson disease: insights from genetic studies. Expert Rev. Mol. Med. 2009, 11:e22.
43. Gerhard A., Pavese N., Hotton G., Turkheimer F., Es M., Hammers A., Eggert K., Oertel W., Banati R.B., Brooks D.J. In vivo imaging of microglial activation with [11C](R)-PK11195 PET in idiopathic Parkinson's disease. Neurobiol. Dis. 2006, 21:404-412.
44. Gordon P.H., Moore D.H., Miller R.G., Florence J.M., Verheijde J.L., Doorish C., Hilton J.F., Spitalny G.M., MacArthur R.B., Mitsumoto H., et al. Efficacy of minocycline in patients with amyotrophic lateral sclerosis: a phase III randomised trial. Lancet Neurol. 2007, 6:1045-1053.
45. Gordon P.H., Cheung Y.K., Levin B., Andrews H., Doorish C., Macarthur R.B., Montes J., Bednarz K., Florence J., Rowin J., et al. A novel, efficient, randomized selection trial comparing combinations of drug therapy for ALS. Amyotroph. Lateral Scler. 2008, 9:212-222.
46. Goverman J. Autoimmune T cell responses in the central nervous system. Nat. Rev. Immunol. 2009, 9:393-407.
47. Gowing G., Dequen F., Soucy G., Julien J.P. Absence of tumor necrosis factor-alpha does not affect motor neuron disease caused by superoxide dismutase 1 mutations. J. Neurosci. 2006, 26:11397-11402.
48. Granic I., Dolga A.M., Nijholt I.M., van Dijk G., Eisel U.L. Inflammation and NF-kappaB in Alzheimer's disease and diabetes. J. Alzheimers Dis. 2009, 16:809-821.
49. Grathwohl S.A., Kalin R.E., Bolmont T., Prokop S., Winkelmann G., Kaeser S.A., Odenthal J., Radde R., Eldh T., Gandy S., et al. Formation and maintenance of Alzheimer's disease beta-amyloid plaques in the absence of microglia. Nat. Neurosci. 2009, 12:1361-1363.
50. Haass C., Selkoe D.J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat. Rev. Mol. Cell Biol. 2007, 8:101-112.
51. Halle A., Hornung V., Petzold G.C., Stewart C.R., Monks B.G., Reinheckel T., Fitzgerald K.A., Latz E., Moore K.J., Golenbock D.T. The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat. Immunol. 2008, 9:857-865.
52. Hirsch E.C., Hunot S. Neuroinflammation in Parkinson's disease: a target for neuroprotection?. Lancet Neurol. 2009, 8:382-397.
53. Hunot S., Boissiere F., Faucheux B., Brugg B., Mouatt-Prigent A., Agid Y., Hirsch E.C. Nitric oxide synthase and neuronal vulnerability in Parkinson's disease. Neuroscience 1996, 72:355-363.
54. Hunter R.L., Dragicevic N., Seifert K., Choi D.Y., Liu M., Kim H.C., Cass W.A., Sullivan P.G., Bing G. Inflammation induces mitochondrial dysfunction and dopaminergic neurodegeneration in the nigrostriatal system. J. Neurochem. 2007, 100:1375-1386.
55. Hur E.M., Youssef S., Haws M.E., Zhang S.Y., Sobel R.A., Steinman L. Osteopontin-induced relapse and progression of autoimmune brain disease through enhanced survival of activated T cells. Nat. Immunol. 2007, 8:74-83.
56. Husemann J., Loike J.D., Anankov R., Febbraio M., Silverstein S.C. Scavenger receptors in neurobiology and neuropathology: their role on microglia and other cells of the nervous system. Glia 2002, 40:195-205.
57. Jaeger S., Pietrzik C.U. Functional role of lipoprotein receptors in Alzheimer's disease. Curr. Alzheimer Res. 2008, 5:15-25.
58. Jin J.J., Kim H.D., Maxwell J.A., Li L., Fukuchi K. Toll-like receptor 4-dependent upregulation of cytokines in a transgenic mouse model of Alzheimer's disease. J. Neuroinflammation 2008, 5:23.
59. Jones A., Kulozik P., Ostertag A., Herzig S. Common pathological processes and transcriptional pathways in Alzheimer's disease and type 2 diabetes. J. Alzheimers Dis. 2009, 16:787-808.
60. Kang J., Rivest S. MyD88-deficient bone marrow cells accelerate onset and reduce survival in a mouse model of amyotrophic lateral sclerosis. J. Cell Biol. 2007, 179:1219-1230.
61. Kastner A., Hirsch E.C., Lejeune O., Javoy-Agid F., Rascol O., Agid Y. Is the vulnerability of neurons in the substantia nigra of patients with Parkinson's disease related to their neuromelanin content?. J. Neurochem. 1992, 59:1080-1089.
62. Kim J., Basak J.M., Holtzman D.M. The role of apolipoprotein E in Alzheimer's disease. Neuron 2009, 63:287-303.
63. Kim W.G., Mohney R.P., Wilson B., Jeohn G.H., Liu B., Hong J.S. Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J. Neurosci. 2000, 20:6309-6316.
64. Kitazawa M., Yamasaki T.R., LaFerla F.M. Microglia as a potential bridge between the amyloid beta-peptide and tau. Ann. N Y Acad. Sci. 2004, 1035:85-103.
65. Korn T., Bettelli E., Oukka M., Kuchroo V.K. IL-17 and Th17 cells. Annu. Rev. Immunol. 2009, 27:485-517.
66. Kriz J., Nguyen M.D., Julien J.P. Minocycline slows disease progression in a mouse model of amyotrophic lateral sclerosis. Neurobiol. Dis. 2002, 10:268-278.
67. Kroner A., Vogel F., Kolb-Maurer A., Kruse N., Toyka K.V., Hemmer B., Rieckmann P., Maurer M. Impact of the Asp299Gly polymorphism in the toll-like receptor 4 (tlr-4) gene on disease course of multiple sclerosis. J. Neuroimmunol. 2005, 165:161-165.
68. Kuhn D.M., Francescutti-Verbeem D.M., Thomas D.M. Dopamine quinones activate microglia and induce a neurotoxic gene expression profile: relationship to methamphetamine-induced nerve ending damage. Ann. N Y Acad. Sci. 2006, 1074:31-41.
69. Kwiatkowski T.J., Bosco D.A., Leclerc A.L., Tamrazian E., Vanderburg C.R., Russ C., Davis A., Gilchrist J., Kasarskis E.J., Munsat T., et al. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 2009, 323:1205-1208.
70. Landreth G.E., Reed-Geaghan E.G. Toll-like receptors in Alzheimer's disease. Curr. Top. Microbiol. Immunol. 2009, 336:137-153.
71. Lang H.L., Jacobsen H., Ikemizu S., Andersson C., Harlos K., Madsen L., Hjorth P., Sondergaard L., Svejgaard A., Wucherpfennig K., et al. A functional and structural basis for TCR cross-reactivity in multiple sclerosis. Nat. Immunol. 2002, 3:940-943.
72. Lassmann H., Bruck W., Lucchinetti C. Heterogeneity of multiple sclerosis pathogenesis: implications for diagnosis and therapy. Trends Mol. Med. 2001, 7:115-121.
73. Lee S.J. Origins and effects of extracellular alpha-synuclein: implications in Parkinson's disease. J. Mol. Neurosci. 2008, 34:17-22.
74. Letiembre M., Liu Y., Walter S., Hao W., Pfander T., Wrede A., Schulz-Schaeffer W., Fassbender K. Screening of innate immune receptors in neurodegenerative diseases: a similar pattern. Neurobiol. Aging 2009, 30:759-768.
75. Licastro F., Porcellini E., Caruso C., Lio D., Corder E.H. Genetic risk profiles for Alzheimer's disease: integration of APOE genotype and variants that up-regulate inflammation. Neurobiol. Aging 2007, 28:1637-1643.
76. Liu Y., Hao W., Dawson A., Liu S., Fassbender K. Expression of amyotrophic lateral sclerosis-linked SOD1 mutant increases the neurotoxic potential of microglia via TLR2. J. Biol. Chem. 2009, 284:3691-3699.
77. Luchsinger J.A., Gustafson D.R. Adiposity, type 2 diabetes, and Alzheimer's disease. J. Alzheimers Dis. 2009, 16:693-704.
78. Lumeng C.N., Bodzin J.L., Saltiel A.R. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 2007, 117:175-184.
79. Mantovani S., Garbelli S., Pasini A., Alimonti D., Perotti C., Melazzini M., Bendotti C., Mora G. Immune system alterations in sporadic amyotrophic lateral sclerosis patients suggest an ongoing neuroinflammatory process. J. Neuroimmunol. 2009, 210:73-79.
80. Marchetto M.C., Muotri A.R., Mu Y., Smith A.M., Cezar G.G., Gage F.H. Non-cell-autonomous effect of human SOD1 G37R astrocytes on motor neurons derived from human embryonic stem cells. Cell Stem Cell 2008, 3:649-657.
81. Marta M., Meier U.C., Lobell A. Regulation of autoimmune encephalomyelitis by toll-like receptors. Autoimmun. Rev. 2009, 8:506-509.
82. Marzolo M.P., Bu G. Lipoprotein receptors and cholesterol in APP trafficking and proteolytic processing, implications for Alzheimer's disease. Semin. Cell Dev. Biol. 2009, 20:191-200.
83. McCoy M.K., Tansey M.G. TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. J. Neuroinflammation 2008, 5:45.
84. McGeer P.L., Itagaki S., Boyes B.E., McGeer E.G. Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 1988, 38:1285-1291.
85. McGeer P.L., McGeer E.G. Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve 2002, 26:459-470.
86. McGeer P.L., McGeer E.G. Glial reactions in Parkinson's disease. Mov. Disord. 2008, 23:474-483.
87. Migliore L., Coppede F. Genetics, environmental factors and the emerging role of epigenetics in neurodegenerative diseases. Mutat. Res. 2009, 667:82-97.
88. Minoretti P., Gazzaruso C., Vito C.D., Emanuele E., Bianchi M., Coen E., Reino M., Geroldi D. Effect of the functional toll-like receptor 4 Asp299Gly polymorphism on susceptibility to late-onset Alzheimer's disease. Neurosci. Lett. 2006, 391:147-149.
89. Nadeau S., Rivest S. Role of microglial-derived tumor necrosis factor in mediating CD14 transcription and nuclear factor kappa B activity in the brain during endotoxemia. J. Neurosci. 2000, 20:3456-3468.
90. Nagatsu T., Sawada M. Inflammatory process in Parkinson's disease: role for cytokines. Curr. Pharm. Des. 2005, 11:999-1016.
91. Neeper M., Schmidt A.M., Brett J., Yan S.D., Wang F., Pan Y.C., Elliston K., Stern D., Shaw A. Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J. Biol. Chem. 1992, 267:14998-15004.
92. Neumann M., Sampathu D.M., Kwong L.K., Truax A.C., Micsenyi M.C., Chou T.T., Bruce J., Schuck T., Grossman M., Clark C.M., et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006, 314:130-133.
93. Neymotin A., Petri S., Calingasan N.Y., Wille E., Schafer P., Stewart C., Hensley K., Beal M.F., Kiaei M. Lenalidomide (Revlimid) administration at symptom onset is neuroprotective in a mouse model of amyotrophic lateral sclerosis. Exp. Neurol. 2009, 220:191-197.
94. Nguyen M.D., Julien J.P., Rivest S. Induction of proinflammatory molecules in mice with amyotrophic lateral sclerosis: no requirement for proapoptotic interleukin-1beta in neurodegeneration. Ann. Neurol. 2001, 50:630-639.
95. Nguyen M.D., D'Aigle T., Gowing G., Julien J.P., Rivest S. Exacerbation of motor neuron disease by chronic stimulation of innate immunity in a mouse model of amyotrophic lateral sclerosis. J. Neurosci. 2004, 24:1340-1349.
96. Nikolaev A., McLaughlin T., O'Leary D.D., Tessier-Lavigne M. APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 2009, 457:981-989.
97. Ousman S.S., Tomooka B.H., van Noort J.M., Wawrousek E.F., O'Connor K.C., Hafler D.A., Sobel R.A., Robinson W.H., Steinman L. Protective and therapeutic role for alphaB-crystallin in autoimmune demyelination. Nature 2007, 448:474-479.
98. Park J.Y., Kim K.S., Lee S.B., Ryu J.S., Chung K.C., Choo Y.K., Jou I., Kim J., Park S.M. On the mechanism of internalization of alpha-synuclein into microglia: roles of ganglioside GM1 and lipid raft. J. Neurochem. 2009, 110:400-411.
99. Pehar M., Cassina P., Vargas M.R., Castellanos R., Viera L., Beckman J.S., Estevez A.G., Barbeito L. Astrocytic production of nerve growth factor in motor neuron apoptosis: implications for amyotrophic lateral sclerosis. J. Neurochem. 2004, 89:464-473.
100. Perry V.H., Cunningham C., Holmes C. Systemic infections and inflammation affect chronic neurodegeneration. Nat. Rev. Immunol. 2007, 7:161-167.
101. Pocivavsek A., Burns M.P., Rebeck G.W. Low-density lipoprotein receptors regulate microglial inflammation through c-Jun N-terminal kinase. Glia 2009, 57:444-453.
102. Pocivavsek A., Mikhailenko I., Strickland D.K., Rebeck G.W. Microglial low-density lipoprotein receptor-related protein 1 modulates c-Jun N-terminal kinase activation. J. Neuroimmunol. 2009, 214:25-32.
103. Ramasamy R., Yan S.F., Schmidt A.M. RAGE: therapeutic target and biomarker of the inflammatory response-the evidence mounts. J. Leukoc. Biol. 2009, 86:505-512.
104. Raoul C., Estevez A.G., Nishimune H., Cleveland D.W., deLapeyriere O., Henderson C.E., Haase G., Pettmann B. Motoneuron death triggered by a specific pathway downstream of Fas. potentiation by ALS-linked SOD1 mutations. Neuron 2002, 35:1067-1083.
105. Raoul C., Buhler E., Sadeghi C., Jacquier A., Aebischer P., Pettmann B., Henderson C.E., Haase G. Chronic activation in presymptomatic amyotrophic lateral sclerosis (ALS) mice of a feedback loop involving Fas, Daxx, and FasL. Proc. Natl. Acad. Sci. USA 2006, 103:6007-6012.
106. Reed-Geaghan E.G., Savage J.C., Hise A.G., Landreth G.E. CD14 and toll-like receptors 2 and 4 are required for fibrillar A{beta}-stimulated microglial activation. J. Neurosci. 2009, 29:11982-11992.
107. Reines S.A., Block G.A., Morris J.C., Liu G., Nessly M.L., Lines C.R., Norman B.A., Baranak C.C. Rofecoxib: no effect on Alzheimer's disease in a 1-year, randomized, blinded, controlled study. Neurology 2004, 62:66-71.
108. Reynolds A.D., Kadiu I., Garg S.K., Glanzer J.G., Nordgren T., Ciborowski P., Banerjee R., Gendelman H.E. Nitrated alpha-synuclein and microglial neuroregulatory activities. J. Neuroimmune Pharmacol. 2008, 3:59-74.
109. Richard K.L., Filali M., Prefontaine P., Rivest S. Toll-like receptor 2 acts as a natural innate immune receptor to clear amyloid beta 1-42 and delay the cognitive decline in a mouse model of Alzheimer's disease. J. Neurosci. 2008, 28:5784-5793.
110. Risner M.E., Saunders A.M., Altman J.F., Ormandy G.C., Craft S., Foley I.M., Zvartau-Hind M.E., Hosford D.A., Roses A.D. Efficacy of rosiglitazone in a genetically defined population with mild-to-moderate Alzheimer's disease. Pharmacogenomics J. 2006, 6:246-254.
111. Rissman R.A., De Blas A.L., Armstrong D.M. GABA(A) receptors in aging and Alzheimer's disease. J. Neurochem. 2007, 103:1285-1292.
112. Roodveldt C., Christodoulou J., Dobson C.M. Immunological features of alpha-synuclein in Parkinson's disease. J. Cell. Mol. Med. 2008, 12:1820-1829.
113. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.X., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62.
114. Saijo K., Winner B., Carson C.T., Collier J.G., Boyer L., Rosenfeld M.G., Gage F.H., Glass C.K. A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 2009, 137:47-59.
115. Sastre M., Walter J., Gentleman S.M. Interactions between APP secretases and inflammatory mediators. J. Neuroinflammation 2008, 5:25.
116. Schmidt A.M., Vianna M., Gerlach M., Brett J., Ryan J., Kao J., Esposito C., Hegarty H., Hurley W., Clauss M., et al. Isolation and characterization of two binding proteins for advanced glycosylation end products from bovine lung which are present on the endothelial cell surface. J. Biol. Chem. 1992, 267:14987-14997.
117. Schmidt A.M., Sahagan B., Nelson R.B., Selmer J., Rothlein R., Bell J.M. The role of RAGE in amyloid-beta peptide-mediated pathology in Alzheimer's disease. Curr. Opin. Investig. Drugs 2009, 10:672-680.
118. Simi A., Tsakiri N., Wang P., Rothwell N.J. Interleukin-1 and inflammatory neurodegeneration. Biochem. Soc. Trans. 2007, 35:1122-1126.
119. Sospedra M., Martin R. Immunology of multiple sclerosis. Annu. Rev. Immunol. 2005, 23:683-747.
120. Srikanth V., Maczurek A., Phan T., Steele M., Westcott B., Juskiw D., Munch G. Advanced glycation endproducts and their receptor RAGE in Alzheimer's disease. Neurobiol. Aging. 2009, Published online May 21, 2009. 10.1016/j.neurobiolaging.2009.04.016.
121. Stewart C.R., Stuart L.M., Wilkinson K., van Gils J.M., Deng J., Halle A., Rayner K.J., Boyer L., Zhong R., Frazier W.A., et al. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat. Immunol. 2009, 11:155-161.
122. Streit W.J. Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 2002, 40:133-139.
123. Tahara K., Kim H.D., Jin J.J., Maxwell J.A., Li L., Fukuchi K. Role of toll-like receptor signalling in Abeta uptake and clearance. Brain 2006, 129:3006-3019.
124. Tansey M.G., McCoy M.K., Frank-Cannon T.C. Neuroinflammatory mechanisms in Parkinson's disease: potential environmental triggers, pathways, and targets for early therapeutic intervention. Exp. Neurol. 2007, 208:1-25.
125. Tikka T.M., Vartiainen N.E., Goldsteins G., Oja S.S., Andersen P.M., Marklund S.L., Koistinaho J. Minocycline prevents neurotoxicity induced by cerebrospinal fluid from patients with motor neurone disease. Brain 2002, 125:722-731.
126. Tontonoz P., Spiegelman B.M. Fat and beyond: the diverse biology of PPARgamma. Annu. Rev. Biochem. 2008, 77:289-312.
127. Torchinsky M.B., Garaude J., Martin A.P., Blander J.M. Innate immune recognition of infected apoptotic cells directs T(H)17 cell differentiation. Nature 2009, 458:78-82.
128. Trapp B.D., Nave K.A. Multiple sclerosis: an immune or neurodegenerative disorder?. Annu. Rev. Neurosci. 2008, 31:247-269.
129. Turner B.J., Talbot K. Transgenics, toxicity and therapeutics in rodent models of mutant SOD1-mediated familial ALS. Prog. Neurobiol. 2008, 85:94-134.
130. Uranishi H., Tetsuka T., Yamashita M., Asamitsu K., Shimizu M., Itoh M., Okamoto T. Involvement of the pro-oncoprotein TLS (translocated in liposarcoma) in nuclear factor-kappa B p65-mediated transcription as a coactivator. J. Biol. Chem. 2001, 276:13395-13401.
131. Urushitani M., Sik A., Sakurai T., Nukina N., Takahashi R., Julien J.P. Chromogranin-mediated secretion of mutant superoxide dismutase proteins linked to amyotrophic lateral sclerosis. Nat. Neurosci. 2006, 9:108-118.
132. Van Den Heuvel C., Thornton E., Vink R. Traumatic brain injury and Alzheimer's disease: a review. Prog. Brain Res. 2007, 161:303-316.
133. Vance C., Rogelj B., Hortobagyi T., De Vos K.J., Nishimura A.L., Sreedharan J., Hu X., Smith B., Ruddy D., Wright P., et al. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 2009, 323:1208-1211.
134. Vargas M.R., Pehar M., Diaz-Amarilla P.J., Beckman J.S., Barbeito L. Transcriptional profile of primary astrocytes expressing ALS-linked mutant SOD1. J. Neurosci. Res. 2008, 86:3515-3525.
135. Vitek M.P., Brown C.M., Colton C.A. APOE genotype-specific differences in the innate immune response. Neurobiol. Aging 2009, 30:1350-1360.
136. Walter S., Letiembre M., Liu Y., Heine H., Penke B., Hao W., Bode B., Manietta N., Walter J., Schulz-Schuffer W., et al. Role of the toll-like receptor 4 in neuroinflammation in Alzheimer's disease. Cell. Physiol. Biochem. 2007, 20:947-956.
137. Wang X., Arai S., Song X., Reichart D., Du K., Pascual G., Tempst P., Rosenfeld M.G., Glass C.K., Kurokawa R. Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature 2008, 454:126-130.
138. Watson G.S., Cholerton B.A., Reger M.A., Baker L.D., Plymate S.R., Asthana S., Fishel M.A., Kulstad J.J., Green P.S., Cook D.G., et al. Preserved cognition in patients with early Alzheimer disease and amnestic mild cognitive impairment during treatment with rosiglitazone: a preliminary study. Am. J. Geriatr. Psychiatry 2005, 13:950-958.
139. Wilms H., Rosenstiel P., Sievers J., Deuschl G., Zecca L., Lucius R. Activation of microglia by human neuromelanin is NF-kappaB dependent and involves p38 mitogen-activated protein kinase: implications for Parkinson's disease. FASEB J. 2003, 17:500-502.
140. Wyss-Coray T., Loike J.D., Brionne T.C., Lu E., Anankov R., Yan F., Silverstein S.C., Husemann J. Adult mouse astrocytes degrade amyloid-beta in vitro and in situ. Nat. Med. 2003, 9:453-457.
141. Yamanaka K., Boillee S., Roberts E.A., Garcia M.L., McAlonis-Downes M., Mikse O.R., Cleveland D.W., Goldstein L.S. Mutant SOD1 in cell types other than motor neurons and oligodendrocytes accelerates onset of disease in ALS mice. Proc. Natl. Acad. Sci. USA 2008, 105:7594-7599.
142. Yamanaka K., Chun S.J., Boillee S., Fujimori-Tonou N., Yamashita H., Gutmann D.H., Takahashi R., Misawa H., Cleveland D.W. Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat. Neurosci. 2008, 11:251-253.
143. Yamin G. NMDA receptor-dependent signaling pathways that underlie amyloid beta-protein disruption of LTP in the hippocampus. J. Neurosci. Res. 2009, 87:1729-1736.
144. Yan S.D., Chen X., Fu J., Chen M., Zhu H., Roher A., Slattery T., Zhao L., Nagashima M., Morser J., et al. RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 1996, 382:685-691.
145. 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 1992, 356:63-66.
146. Yiangou Y., Facer P., Durrenberger P., Chessell I.P., Naylor A., Bountra C., Banati R.R., Anand P. COX-2, CB2 and P2X7-immunoreactivities are increased in activated microglial cells/macrophages of multiple sclerosis and amyotrophic lateral sclerosis spinal cord. BMC Neurol. 2006, 6:12.
147. Zhang W., Wang T., Pei Z., Miller D.S., Wu X., Block M.L., Wilson B., Zhang W., Zhou Y., Hong J.S., et al. Aggregated alpha-synuclein activates microglia: a process leading to disease progression in Parkinson's disease. FASEB J. 2005, 19:533-542.