Phagocytic clearance in neurodegeneration

American Journal of Pathology

Volumn 178, Issue 4, 2011, Pages 1416-1428

  Sokolowski, Jennifer D ^a   Mandell, James W ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 2 MACROGLOBULIN; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN ANTIBODY; AMYLOID BETA RECEPTOR; ANTIBODY; APOLIPOPROTEIN; APOLIPOPROTEIN E; CD36 ANTIGEN; CHAPERONE; CLUSTERIN; COMPLEMENT; CYTOKINE; GLYCOPROTEIN; IMMUNOGLOBULIN; INTERLEUKIN 10; INTERLEUKIN 4; LACTADHERIN; NONSTEROID ANTIINFLAMMATORY AGENT; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; APOPTOSIS; ASTROCYTE; ASTROCYTOSIS; CELL ACTIVATION; CELL DEATH; CELL INFILTRATION; CELL INTERACTION; CENTRAL NERVOUS SYSTEM DISEASE; CENTRAL NERVOUS SYSTEM INFLAMMATION; CLEARANCE; COMPLEMENT SYSTEM; DEGENERATIVE DISEASE; DISEASE SEVERITY; ENDOCYTOSIS; GENE EXPRESSION PROFILING; GENE MUTATION; GENETIC ASSOCIATION; GLIA CELL; GLIOSIS; HISTOPATHOLOGY; HUMAN; IMMUNIZATION; IMMUNOHISTOCHEMISTRY; IMMUNOTHERAPY; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MEDIATOR; MICROGLIA; MICROGLIOSIS; MOLECULAR RECOGNITION; NERVE CELL; NERVE CELL NECROSIS; NEURAL STEM CELL; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PHAGOCYTE; PHAGOCYTOSIS; PHENOTYPE; PHOTORECEPTOR; PIGMENT EPITHELIUM; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; RETINA DEGENERATION; RETINITIS PIGMENTOSA; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION; SYNAPSE; T LYMPHOCYTE;

EID: 79953657142     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2010.12.051     Document Type: Review

References (99)

1. Elliott MR, Ravichandran KS: Clearance of apoptotic cells: implications in health and disease. J Cell Biol 2010, 189:1059-1070
2. Lee CY, Landreth GE: The role of microglia in amyloid clearance from the AD brain. J Neural Transm 2010, 117:949-960
3. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA: A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 2008, 28:264-278
4. DeWitt DA, Perry G, Cohen M, Doller C, Silver J: Astrocytes regulate microglial phagocytosis of senile plaque cores of Alzheimer's disease. Exp Neurol 1998, 149:329-340 (Pubitemid 28115071)
5. Takuma K, Fang F, Zhang W, Yan S, Fukuzaki E, Du H, Sosunov A, McKhann G, Funatsu Y, Nakamichi N, Nagai T, Mizoguchi H, Ibi D, Hori O, Ogawa S, Stern DM, Yamada K, Yan SS: RAGE-mediated signaling contributes to intraneuronal transport of amyloid-beta and neuronal dysfunction. Proc Natl Acad Sci USA 2009, 106:20021-20026
6. Hu X, Crick SL, Bu G, Frieden C, Pappu RV, Lee JM: Amyloid seeds formed by cellular uptake, concentration, and aggregation of the amyloid-beta peptide. Proc Natl Acad Sci USA 2009, 106:20324-20329
7. Fuentealba RA, Liu Q, Zhang J, Kanekiyo T, Hu X, Lee JM, LaDu MJ, Bu G: Low-density lipoprotein receptor-related protein 1 (LRP1) mediates neuronal Abeta42 uptake and lysosomal trafficking. PLoS One 2010, 5:e11884
8. Siskova Z, Page A, O'Connor V, Perry VH: Degenerating synaptic boutons in prion disease: microglia activation without synaptic stripping. Am J Pathol 2009, 175:1610-1621
9. van Noort JM, Bsibsi M: Toll-like receptors in the CNS: implications for neurodegeneration and repair. Prog Brain Res 2009, 175:139-148
10. Simard AR, Soulet D, Gowing G, Julien JP, Rivest S: Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 2006, 49:489-502 (Pubitemid 43221886)
11. Tsuchiya T, Park KC, Toyonaga S, Yamada SM, Nakabayashi H, Nakai E, Ikawa N, Furuya M, Tominaga A, Shimizu K: Characterization of microglia induced from mouse embryonic stem cells and their migration into the brain parenchyma. J Neuroimmunol 2005, 160:210-218 (Pubitemid 40248611)
12. Mildner A, Schmidt H, Nitsche M, Merkler D, Hanisch UK, Mack M, Heikenwalder M, Bruck W, Priller J, Prinz M: Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat Neurosci 2007, 10:1544-1553 (Pubitemid 350175884)
13. Fraser DA, Pisalyaput K, Tenner AJ: C1q enhances microglial clearance of apoptotic neurons and neuronal blebs, and modulates subsequent inflammatory cytokine production. J Neurochem 2010, 112:733-743
14. Morgan D, Gordon MN, Tan J, Wilcock D, Rojiani AM: Dynamic complexity of the microglial activation response in transgenic models of amyloid deposition: implications for Alzheimer therapeutics. J Neuropathol Exp Neurol 2005, 64:743-753 (Pubitemid 41285806)
15. Michelucci A, Heurtaux T, Grandbarbe L, Morga E, Heuschling P: Characterization of the microglial phenotype under specific pro-inflammatory and anti-inflammatory conditions: effects of oligomeric and fibrillar amyloid-beta. J Neuroimmunol 2009, 210:3-12
16. Carson MJ, Sutcliffe JG: Balancing function vs. self defense: the CNS as an active regulator of immune responses. J Neurosci Res 1999, 55:1-8 (Pubitemid 29014405)
17. Colton CA, Mott RT, Sharpe H, Xu Q, Van Nostrand WE, Vitek MP: Expression profiles for macrophage alternative activation genes in AD and in mouse models of AD. J Neuroinflammation 2006, 3:27
18. Town T, Nikolic V, Tan J: The microglial "activation" continuum: from innate to adaptive responses. J Neuroinflammation 2005, 2:24
19. Calingasan NY, Erdely HA, Altar CA: Identification of CD40 ligand in Alzheimer's disease and in animal models of Alzheimer's disease and brain injury. Neurobiol Aging 2002, 23:31-39 (Pubitemid 34066533)
20. Biber K, Neumann H, Inoue K, Boddeke HW: Neuronal 'On' and 'Off' signals control microglia. Trends Neurosci 2007, 30:596-602
21. Reynolds AD, Banerjee R, Liu J, Gendelman HE, Mosley RL: Neuroprotective activities of CD4+CD25+ regulatory T cells in an animal model of Parkinson's disease. J Leukoc Biol 2007, 82:1083-1094 (Pubitemid 350133504)
22. Koenigsknecht-Talboo J, Landreth GE: Microglial phagocytosis induced by fibrillar beta-amyloid and IgGs are differentially regulated by proinflammatory cytokines. J Neurosci 2005, 25:8240-8249 (Pubitemid 41292118)
23. Yamamoto M, Kiyota T, Walsh SM, Liu J, Kipnis J, Ikezu T: Cytokine-mediated inhibition of fibrillar amyloid-beta peptide degradation by human mononuclear phagocytes. J Immunol 2008, 181:3877-3886
24. Kohli L, Roth KA: Autophagy: cerebral home cooking. Am J Pathol 2010, 176:1065-1071
25. Strauss O: The retinal pigment epithelium in visual function. Physiol Rev 2005, 85:845-881
26. Hall MO, Prieto AL, Obin MS, Abrams TA, Burgess BL, Heeb MJ, Agnew BJ: Outer segment phagocytosis by cultured retinal pigment epithelial cells requires Gas6. Exp Eye Res 2001, 73:509-520 (Pubitemid 33078226)
27. Nandrot EF, Anand M, Almeida D, Atabai K, Sheppard D, Finnemann SC: Essential role for MFG-E8 as ligand for alphavbeta5 integrin in diurnal retinal phagocytosis. Proc Natl Acad Sci USA 2007, 104:12005-12010 (Pubitemid 47185620)
28. Ryeom SW, Silverstein RL, Scotto A, Sparrow JR: Binding of anionic phospholipids to retinal pigment epithelium may be mediated by the scavenger receptor CD36. J Biol Chem 1996, 271:20536-20539 (Pubitemid 26281828)
29. Finnemann SC, Nandrot EF: MerTK activation during RPE phagocytosis in vivo requires alphaVbeta5 integrin. Adv Exp Med Biol 2006, 572:499-503 (Pubitemid 44249811)
30. Bok D, Hall MO: The role of the pigment epithelium in the etiology of inherited retinal dystrophy in the rat. J Cell Biol 1971, 49:664-682
31. Gal A, Li Y, Thompson DA, Weir J, Orth U, Jacobson SG, Apfelstedt-Sylla E, Vollrath D: Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nat Genet 2000, 26:270-271
32. Tschernutter M, Schlichtenbrede FC, Howe S, Balaggan KS, Munro PM, Bainbridge JW, Thrasher AJ, Smith AJ, Ali RR: Long-term preservation of retinal function in the RCS rat model of retinitis pigmentosa following lentivirus-mediated gene therapy. Gene Ther 2005, 12:694-701 (Pubitemid 40561508)
33. Selkoe DJ: Toward a comprehensive theory for Alzheimer's disease. Hypothesis: Alzheimer's disease is caused by the cerebral accumulation and cytotoxicity of amyloid beta-protein. Ann N Y Acad Sci 2000, 924:17-25
34. Nagele RG, D'Andrea MR, Lee H, Venkataraman V, Wang HY: Astrocytes accumulate A beta 42 and give rise to astrocytic amyloid plaques in Alzheimer disease brains. Brain Res 2003, 971:197-209 (Pubitemid 36423321)
35. D'Andrea MR, Cole GM, Ard MD: The microglial phagocytic role with specific plaque types in the Alzheimer disease brain. Neurobiol Aging 2004, 25:675-683 (Pubitemid 38686491)
36. Haass C, Hung AY, Selkoe DJ: Processing of beta-amyloid precursor protein in microglia and astrocytes favors an internal localization over constitutive secretion. J Neurosci 1991, 11:3783-3793
37. Itagaki S, McGeer PL, Akiyama H, Zhu S, Selkoe D: Relationship of microglia and astrocytes to amyloid deposits of Alzheimer disease. J Neuroimmunol 1989, 24:173-182 (Pubitemid 19271472)
38. Nicoll JA, Barton E, Boche D, Neal JW, Ferrer I, Thompson P, Vlachouli C, Wilkinson D, Bayer A, Games D, Seubert P, Schenk D, Holmes C: Abeta species removal after abeta42 immunization. J Neuropathol Exp Neurol 2006, 65:1040-1048 (Pubitemid 44684661)
39. Shie FS, Breyer RM, Montine TJ: Microglia lacking E prostanoid receptor subtype 2 have enhanced Abeta phagocytosis yet lack Abeta-activated neurotoxicity. Am J Pathol 2005, 166:1163-1172 (Pubitemid 40524440)
40. Wyss-Coray T, Loike JD, Brionne TC, Lu E, Anankov R, Yan F, Silverstein SC, Husemann J: Adult mouse astrocytes degrade amyloid- beta in vitro and in situ. Nat Med 2003, 9:453-457 (Pubitemid 36460080)
41. Mandrekar S, Jiang Q, Lee CY, Koenigsknecht-Talboo J, Holtzman DM, Landreth GE: Microglia mediate the clearance of soluble Abeta through fluid phase macropinocytosis. J Neurosci 2009, 29:4252-4262
42. Koenigsknecht J, Landreth G: Microglial phagocytosis of fibrillar beta-amyloid through a beta1 integrin-dependent mechanism. J Neurosci 2004, 24:9838-9846 (Pubitemid 39463564)
43. Sondag CM, Dhawan G, Combs CK: Beta amyloid oligomers and fibrils stimulate differential activation of primary microglia. J Neuroinflammation 2009, 6:1
44. Pereson S, Wils H, Kleinberger G, McGowan E, Vandewoestyne M, Van Broeck B, Joris G, Cuijt I, Deforce D, Hutton M, Van Broeckhoven C, Kumar-Singh S: Progranulin expression correlates with dense-core amyloid plaque burden in Alzheimer disease mouse models. J Pathol 2009, 219:173-181
45. Emmerling MR, Watson MD, Raby CA, Spiegel K: The role of complement in Alzheimer's disease pathology. Biochim Biophys Acta 2000, 1502:158-171 (Pubitemid 30433865)
46. Heneka MT, O'Banion MK: Inflammatory processes in Alzheimer's disease. J Neuroimmunol 2007, 184:69-91 (Pubitemid 46365992)
47. Walker DG, Link J, Lue LF, Dalsing-Hernandez JE, Boyes BE: Gene expression changes by amyloid beta peptide-stimulated human postmortem brain microglia identify activation of multiple inflammatory processes [Erratum appeared in J Leukoc Biol 2006, 80:448]. J Leukoc Biol 2006, 79:596-610 (Pubitemid 44831236)
48. Wyss-Coray T, Lin C, Yan F, Yu GQ, Rohde M, McConlogue L, Masliah E, Mucke L: TGF-beta1 promotes microglial amyloid-beta clearance and reduces plaque burden in transgenic mice. Nat Med 2001, 7:612-618 (Pubitemid 32448330)
49. Jellinger KA: Challenges in neuronal apoptosis. Curr Alzheimer Res 2006, 3:377-391
50. Johnstone M, Gearing AJ, Miller KM: A central role for astrocytes in the inflammatory response to beta-amyloid; chemokines, cytokines and reactive oxygen species are produced. J Neuroimmunol 1999, 93:182-193 (Pubitemid 29051564)
51. Desideri G, Cipollone F, Necozione S, Marini C, Lechiara MC, Taglieri G, Zuliani G, Fellin R, Mezzetti A, di Orio F, Ferri C: Enhanced soluble CD40 ligand and Alzheimer's disease: evidence of a possible pathogenetic role. Neurobiol Aging 2008, 29:348-356 (Pubitemid 351215586)
52. Nikolic WV, Hou H, Town T, Zhu Y, Giunta B, Sanberg CD, Zeng J, Luo D, Ehrhart J, Mori T, Sanberg PR, Tan J: Peripherally administered human umbilical cord blood cells reduce parenchymal and vascular beta-amyloid deposits in Alzheimer mice. Stem Cells Dev 2008, 17:423-439 (Pubitemid 351948205)
53. Harold D, Abraham R, Hollingworth P, Sims R, Gerrish A, Hamshere ML, et al: Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease [Erratum appeared in Nat Genet 2009, 41:1156]. Nat Genet 2009, 41:1088-1093
54. Lambert JC, Heath S, Even G, Campion D, Sleegers K, Hiltunen M, et al: Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease. Nat Genet 2009, 41:1094-1099
55. Barnum SR: Complement biosynthesis in the central nervous system. Crit Rev Oral Biol Med 1995, 6:132-146
56. Tenner AJ, Fonseca MI: The double-edged flower: roles of complement protein C1q in neurodegenerative diseases. Adv Exp Med Biol 2006, 586:153-176
57. Eikelenboom P, Hack CE, Rozemuller JM, Stam FC: Complement activation in amyloid plaques in Alzheimer's dementia. Virchows Arch B Cell Pathol Incl Mol Pathol 1989, 56:259-262 (Pubitemid 19049180)
58. Bradt BM, Kolb WP, Cooper NR: Complement-dependent proinflammatory properties of the Alzheimer's disease beta-peptide. J Exp Med 1998, 188:431-438 (Pubitemid 28369133)
59. Wyss-Coray T, Yan F, Lin AH, Lambris JD, Alexander JJ, Quigg RJ, Masliah E: Prominent neurodegeneration and increased plaque formation in complement-inhibited Alzheimer's mice. Proc Natl Acad Sci USA 2002, 99:10837-10842
60. Maier M, Peng Y, Jiang L, Seabrook TJ, Carroll MC, Lemere CA: Complement C3 deficiency leads to accelerated amyloid beta plaque deposition and neurodegeneration and modulation of the microglia/macrophage phenotype in amyloid precursor protein transgenic mice. J Neurosci 2008, 28:6333-6341
61. Singhrao SK, Neal JW, Rushmere NK, Morgan BP, Gasque P: Differential expression of individual complement regulators in the brain and choroid plexus. Lab Invest 1999, 79:1247-1259 (Pubitemid 29489449)
62. Szabo P, Relkin N, Weksler ME: Natural human antibodies to amyloid beta peptide. Autoimmun Rev 2008, 7:415-420
63. Schenk D, Barbour R, Dunn W, Gordon G, Grajeda H, Guido T, Hu K, Huang J, Johnson-Wood K, Khan K, Kholodenko D, Lee M, Liao Z, Lieberburg I, Motter R, Mutter L, Soriano F, Shopp G, Vasquez N, Vandevert C, Walker S, Wogulis M, Yednock T, Games D, Seubert P: Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 1999, 400:173-177 (Pubitemid 29327547)
64. Wilcock DM, Rojiani A, Rosenthal A, Levkowitz G, Subbarao S, Alamed J, Wilson D, Wilson N, Freeman MJ, Gordon MN, Morgan D: Passive amyloid immunotherapy clears amyloid and transiently activates microglia in a transgenic mouse model of amyloid deposition. J Neurosci 2004, 24:6144-6151 (Pubitemid 38891105)
65. Relkin NR, Szabo P, Adamiak B, Burgut T, Monthe C, Lent RW, Younkin S, Younkin L, Schiff R, Weksler ME: 18-Month study of intravenous immunoglobulin for treatment of mild Alzheimer disease. Neurobiol Aging 2009, 30:1728-1736
66. Bacskai BJ, Kajdasz ST, McLellan ME, Games D, Seubert P, Schenk D, Hyman BT: Non-Fc-mediated mechanisms are involved in clearance of amyloid-beta in vivo by immunotherapy. J Neurosci 2002, 22:7873-7878 (Pubitemid 35379092)
67. Das P, Howard V, Loosbrock N, Dickson D, Murphy MP, Golde TE: Amyloid-beta immunization effectively reduces amyloid deposition in FcRgamma-/- knock-out mice. J Neurosci 2003, 23:8532-8538 (Pubitemid 37158753)
68. Kotilinek LA, Bacskai B, Westerman M, Kawarabayashi T, Younkin L, Hyman BT, Younkin S, Ashe KH: Reversible memory loss in a mouse transgenic model of Alzheimer's disease. J Neurosci 2002, 22:6331-6335 (Pubitemid 35386387)
69. Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J, Salvesen GS, Roses AD: Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc Natl Acad Sci USA 1993, 90:1977-1981 (Pubitemid 23069980)
70. Koistinaho M, Lin S, Wu X, Esterman M, Koger D, Hanson J, Higgs R, Liu F, Malkani S, Bales KR, Paul SM: Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloid-beta peptides. Nat Med 2004, 10:719-726 (Pubitemid 38937637)
71. Kim J, Castellano JM, Jiang H, Basak JM, Parsadanian M, Pham V, Mason SM, Paul SM, Holtzman DM: Overexpression of low-density lipoprotein receptor in the brain markedly inhibits amyloid deposition and increases extracellular A beta clearance. Neuron 2009, 64:632-644
72. Tamboli IY, Prager K, Thal DR, Thelen KM, Dewachter I, Pietrzik CU, St George-Hyslop P, Sisodia SS, De Strooper B, Heneka MT, Filippov MA, Müller U, van Leuven F, Lutjohann D, Walter J: Loss of gammasecretase function impairs endocytosis of lipoprotein particles and membrane cholesterol homeostasis. J Neurosci 2008, 28:12097-12106
73. Colton CA, Needham LK, Brown C, Cook D, Rasheed K, Burke JR, Strittmatter WJ, Schmechel DE, Vitek MP: APOE genotype-specific differences in human and mouse macrophage nitric oxide production. J Neuroimmunol 2004, 147:62-67 (Pubitemid 38114948)
74. Koldamova R, Fitz NF, Lefterov I: The role of ATP-binding cassette transporter A1 in Alzheimer's disease and neurodegeneration. Biochim Biophys Acta 2010, 1801:824-830
75. Nuutinen T, Suuronen T, Kauppinen A, Salminen A: Clusterin: a forgotten player in Alzheimer's disease. Brain Res Rev 2009, 61:89-104
76. Zlokovic BV, Martel CL, Matsubara E, McComb JG, Zheng G, McCluskey RT, Frangione B, Ghiso J: Glycoprotein 330/megalin: probable role in receptor-mediated transport of apolipoprotein J alone and in a complex with Alzheimer disease amyloid beta at the blood-brain and blood-cerebrospinal fluid barriers. Proc Natl Acad Sci USA 1996, 93:4229-4234
77. Fabrizi C, Businaro R, Lauro GM, Fumagalli L: Role of alpha2-macroglobulin in regulating amyloid beta-protein neurotoxicity: protective or detrimental factor? J Neurochem 2001, 78:406-412
78. Broe M, Shepherd CE, Milward EA, Halliday GM: Relationship between DNA fragmentation, morphological changes and neuronal loss in Alzheimer's disease and dementia with Lewy bodies. Acta Neuropathol 2001, 101:616-624 (Pubitemid 32684761)
79. Boddaert J, Kinugawa K, Lambert JC, Boukhtouche F, Zoll J, Merval R, Blanc-Brude O, Mann D, Berr C, Vilar J, Garabedian B, Journiac N, Charue D, Silvestre JS, Duyckaerts C, Amouyel P, Mariani J, Tedgui A, Mallat Z: Evidence of a role for lactadherin in Alzheimer's disease. Am J Pathol 2007, 170:921-929
80. Scheff SW, Price DA, Schmitt FA, Mufson EJ: Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment. Neurobiol Aging 2006, 27:1372-1384 (Pubitemid 44279897)
81. Avagyan H, Goldenson B, Tse E, Masoumi A, Porter V, Wiedau-Pazos M, Sayre J, Ong R, Mahanian M, Koo P, Bae S, Micic M, Liu PT, Rosenthal MJ, Fiala M: Immune blood biomarkers of Alzheimer disease patients. J Neuroimmunol 2009, 210:67-72
82. McGeer PL, McGeer EG: Glial reactions in Parkinson's disease. Mov Disord 2008, 23:474-483
83. 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
84. Brown DR, Schmidt B, Kretzschmar HA: Role of microglia and host prion protein in neurotoxicity of a prion protein fragment. Nature 1996, 380:345-347 (Pubitemid 26097115)
85. Nagl M, Kacani L, Müllauer B, Lemberger EM, Stoiber H, Sprinzl GM, Schennach H, Dierich MP: Phagocytosis and killing of bacteria by professional phagocytes and dendritic cells. Clin Diagn Lab Immunol 2002, 9:1165-1168 (Pubitemid 35283276)
86. Lee HJ, Suk JE, Patrick C, Bae EJ, Cho JH, Rho S, Hwang D, Masliah E, Lee SJ: Direct transfer of alpha-synuclein from neuron to astroglia causes inflammatory responses in synucleinopathies. J Biol Chem 2010, 285:9262-9272
87. Rogers J, Kirby LC, Hempelman SR, Berry DL, McGeer PL, Kaszniak AW, Zalinski J, Cofield M, Mansukhani L, Willson P: Clinical trial of indomethacin in Alzheimer's disease. Neurology 1993, 43:1609-1611 (Pubitemid 23230557)
88. Gagne JJ, Power MC: Anti-inflammatory drugs and risk of Parkinson disease: a meta-analysis. Neurology 2010, 74:995-1002
89. Kinchen JM, Ravichandran KS: Journey to the grave: signaling events regulating removal of apoptotic cells. J Cell Sci 2007, 120:2143-2149 (Pubitemid 47074120)
90. Okun E, Mattson MP, Arumugam TV: Involvement of Fc receptors in disorders of the central nervous system. Neuromolecular Med 2009, 12:164-178
91. Landreth GE, Reed-Geaghan EG: Toll-like receptors in Alzheimer's disease. Curr Top Microbiol Immunol 2009, 336:137-153
92. Reed-Geaghan EG, Savage JC, Hise AG, Landreth GE: CD14 and Toll-like receptors 2 and 4 are required for fibrillar A{beta}-stimulated microglial activation. J Neurosci 2009, 29:11982-11992
93. Kielian T: Overview of Toll-like receptors in the CNS. Curr Top Microbiol Immunol 2009, 336:1-14
94. Iribarren P, Zhou Y, Hu J, Le Y, Wang JM: Role of formyl peptide receptor-like 1 (FPRL1/FPR2) in mononuclear phagocyte responses in Alzheimer disease. Immunol Res 2005, 31:165-176 (Pubitemid 40628955)
95. Wilhelmus MM, Otte-Höller I, van Triel JJ, Veerhuis R, Maat-Schieman ML, Bu G, de Waal RM, Verbeek MM: Lipoprotein receptorrelated protein-1 mediates amyloid-beta-mediated cell death of cerebrovascular cells. Am J Pathol 2007, 171:1989-1999
96. Donahue JE, Flaherty SL, Johanson CE, Duncan JA 3rd, Silverberg GD, Miller MC, Tavares R, Yang W, Wu Q, Sabo E, Hovanesian V, Stopa EG: RAGE, LRP-1, and amyloid-beta protein in Alzheimer's disease. Acta Neuropathol 2006, 112:405-415
97. Deane R, Du Yan S, Submamaryan RK, LaRue B, Jovanovic S, Hogg E, Welch D, Manness L, Lin C, Yu J, Zhu H, Ghiso J, Frangione B, Stern A, Schmidt AM, Armstrong DL, Arnold B, Liliensiek B, Nawroth P, Hofman F, Kindy M, Stern D, Zlokovic B: RAGE mediates amyloid-beta peptide transport across the bloodbrain barrier and accumulation in brain. Nat Med 2003, 9:907-913 (Pubitemid 36889934)
98. Alarcón R, Fuenzalida C, Santibáñez M, von Bernhardi R: Expression of scavenger receptors in glial cells. Comparing the adhesion of astrocytes and microglia from neonatal rats to surface-bound betaamyloid. J Biol Chem 2005, 280:30406-30415 (Pubitemid 41216224)
99. Paresce DM, Ghosh RN, Maxfield FR: Microglial cells internalize aggregates of the Alzheimer's disease amyloid beta-protein via a scavenger receptor. Neuron 1996, 17:553-565 (Pubitemid 26322226)