New Roles for Fc receptors in neurodegeneration-The impact on Immunotherapy for Alzheimer's Disease

Frontiers in Neuroscience

Volumn , Issue 8 JUL, 2014, Pages

  Fuller, James ^a   Stavenhagen, Jeff ^b   Teeling, Jessica L ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b H LUNDBECK A S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; AUTOANTIBODY; FC RECEPTOR; IMMUNOGLOBULIN G; AMYLOID BETA PROTEIN;

ALZHEIMER DISEASE; ARTICLE; CLINICAL TRIAL (TOPIC); GENE EXPRESSION; HUMAN; HUMORAL IMMUNITY; IMMUNOTHERAPY; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; ACTIVE IMMUNIZATION; AGING; AMNESIA; ANTIGEN ANTIBODY COMPLEX; ASTROCYTE; BRAIN BLOOD VESSEL; BRAIN NERVE CELL; CENTRAL NERVOUS SYSTEM; CEREBROVASCULAR DISEASE; CLEARANCE; COGNITIVE DEFECT; DEGENERATIVE DISEASE; DISEASE EXACERBATION; EFFECTOR CELL; ENDOTHELIUM CELL; EPISODIC MEMORY; INFLAMMATION; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; OLIGODENDROGLIA; PASSIVE IMMUNIZATION; PATHOGENESIS; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; RECEPTOR BINDING; TISSUE INJURY; TRANSGENIC MOUSE;

EID: 84905898497     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2014.00235     Document Type: Article

References (87)

1. Adolfsson, O., Pihlgren, M., Toni, N., Varisco, Y., Buccarello, A. L., Antoniello, K., Lohmann, S., Piorkowska, K., Gafner, V., Atwal, J. K. et al. (2012). An Effector-Reduced Anti-ß-Amyloid (Aß) Antibody with Unique Aß Binding Properties Promotes Neuroprotection and Glial Engulfment of Aß. The Journal of Neuroscience 32, 9677-9689.
2. Allsop, D., Wong, C. W., Ikeda, S., Landon, M., Kidd, M. and Glenner, G. G. (1988). Evidence for the origin of cerebral amyloid in Alzheimer's disease drom A Beta protein precursor. Neuropathol Appl Neurobiol 14, 254-255.
3. Andoh, T. and Kuraishi, Y. (2004). Primary sensory neurons express the high affinity IgG Fc gamma RI receptor and responds to IgG-antigen complex. Journal of Pharmacological Sciences 94, 74P-74P.
4. Bacskai, B. J., Kajdasz, S. T., McLellan, M. E., Games, D., Seubert, P., Schenk, D. and Hyman, B. T. (2002). Non-Fc-mediated mechanisms are involved in clearance of amyloid-beta in vivo by immunotherapy. Journal of Neuroscience 22, 7873-7878
5. Bard, F., Cannon, C., Barbour, R., Burke, R. L., Games, D., Grajeda, H., Guido, T., Hu, K., Huang, J. P., Johnson-Wood, K. et al. (2000). Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nature Medicine 6, 916-919.
6. Bellinger, F. P., Madamba, S. and Siggins, G. R. (1993). Interleukin 1 Beta inhibits synaptic strength and lon-term potentiation in the rat CA1 hippocampus. Brain Res 628, 227-234.
7. Bie, B. W., Jiang; Yang, Hui; Xu, Jijun J; Brown, David L Naguib, Mohamed. (2014). Epigentic suppresion of neuroligin 1 underlies amyloid induced memory deficiency. Nat Neuroscience 17, 223-231.
8. Bouras, C., Riederer, B. M., Kovari, E., Hof, P. R. and Giannakopoulos, P. (2005). Humoral immunity in brain aging and Alzheimer's disease. Brain Research Reviews 48, 477-487.
9. Brody, D. L. and Holtzman, D. M. (2008). Active and passive immunotherapy for Neurodegenerative disorders. In Annual Review of Neuroscience, vol. 31, pp. 175-193.
10. Bruhns, P., Iannascoli, B., England, P., Mancardi, D. A., Fernandez, N., Jorieux, S. and Daeron, M. (2009). Specificity and affinity of human Fc gamma receptors and their polymorphic variants for human IgG subclasses. Blood 113, 3716-3725.
11. Cao, S., Standaert, D. G. and Harms, A. S. (2012). The gamma chain subunit of Fc receptors is required for alpha-synuclein-induced pro-inflammatory signaling in microglia. J Neuroinflammation 9.
12. Cao, S., Theodore, S. and Standaert, D. G. (2010). Fc gamma receptors are required for NF468 kappa B signaling, microglial activation and dopaminergic neurodegeneration in an AAV-synuclein mouse model of Parkinson's disease. Mol Neurodegener 5.
13. Carbone, F., Nencioni, A., Mach, F., Vuilleumier, N. and Montecucco, F. (2013). Evidence on the pathogenic role of auto-antibodies in acute cardiovascular diseases. Thromb Haemost 109, 854-868.
14. Clynes, R., Maizes, J. S., Guinamard, R., Ono, M., Takai, T. and Ravetch, J. V. (1999). Modulation of immune complex-induced inflammation in vivo by the coordinate expression of activation and inhibitory Fc receptors. Journal of Experimental Medicine 189, 179-185.
15. Congdon, E. E., Gu, J. P., Sait, H. B. R. and Sigurdsson, E. M. (2013). Antibody Uptake into Neurons Occurs Primarily via Clathrin-dependent Fc gamma Receptor Endocytosis and Is a Prerequisite for Acute Tau Protein Clearance. Journal of Biological Chemistry 288, 35452-35465.
16. Cribbs, D. H., Berchtold, N. C., Perreau, V., Coleman, P. D., Rogers, J., Tenner, A. J. and Cotman, C. W. (2012). Extensive innate immune gene activation accompanies brain aging, increasing vulnerability to cognitive decline and neurodegeneration: a microarray study. J Neuroinflammation 9.
17. D'Andrea, M. R. (2003). Evidence linking neuronal cell death to autoimmunity in Alzheimer's disease. Brain Res 982, 19-30.
18. Das, P., Howard, V., Loosbrock, N., Dickson, D., Murphy, M. P. and Golde, T. E. (2003). Amyloid-beta immunization effectively reduces amyloid deposition in FcR gamma(-/-) knock-out mice. Journal of Neuroscience 23, 8532-8538.
19. Deane, R., Sagare, A., Hamm, K., Parisi, M., LaRue, B., Guo, H., Wu, Z., Holtzman, D. M. and Zlokovic, B. V. (2005). IgG-assisted age-dependent clearance of Alzheimer's amyloid beta peptide by the blood-brain barrier neonatal Fc receptor. J Neurosci 25, 11495-503.
20. DeMattos, R. B., Bales, K. R., Cummins, D. J., Dodart, J. C., Paul, S. M. and Holtzman, D. M. (2001). Peripheral anti-A beta antibody alters CNS and plasma A beta clearance and decreases brain A beta burden in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 98, 8850-5.
21. Diamond, B., Kowal, C., Huerta, P. T., Aranow, C., Mackay, M., DeGiorgio, L. A., Lee, J., Triantaylopoulou, A., Cohen-Solal, J. and Volpe, B. T. (2006). Immunity and acquired alterations in cognition and emotion: Lessons from SLE. In Advances in Immunology, Vol 494 89, vol. 89 (ed. F. W. Alt), pp. 289-320.
22. Doody, R. S., Thomas, R. G., Farlow, M., Iwatsubo, T., Vellas, B., Joffe, S., Kieburtz, K., Raman, R., Sun, X., Aisen, P. S. et al. (2014). Phase 3 Trials of Solanezumab for Mild-to-Moderate Alzheimer's Disease. New England Journal of Medicine 370, 311-321.
23. Engelhardt, J. I., Le, W. D., Siklos, L., Obal, I., Boda, K. and Appel, S. H. (2000). Stereotaxic injection of IgG from patients with Alzheimer disease initiates injury of cholinergic neurons of the basal forebrain. Archives of Neurology 57, 681-686.
24. Fernandez-Vizarra, P., Lopez-Franco, O., Mallavia, B., Higuera-Matas, A., Lopez-Parra, V., Ortiz-Munoz, G., Ambrosio, E., Egido, J., Almeida, O. F. X. and Gomez-Guerrero, C. (2012). Immunoglobulin G Fc receptor deficiency prevents Alzheimer-like pathology and cognitive impairment in mice. Brain 135, 2826-2837.
25. Freeman, G. B., Brown, T. P., Wallace, K. and Bales, K. R. (2012). Chronic Administration of an Aglycosylated Murine Antibody of Ponezumab Does Not Worsen Microhemorrhages in Aged Tg2576 Mice. Current Alzheimer Research 9, 1059-1068.
26. Geijtenbeek, T. B. H. and Gringhuis, S. I. (2009). Signalling through C-type lectin receptors: shaping immune responses. Nature Reviews Immunology 9, 465-479.
27. Goate, A., Chartier-Harlin, M.-C., Mullan, M., Brown, J., Crawford, F., Fidani, L., Giuffra, L., Haynes, A., Irving, N., James, L. et al. (1991). Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349, 704-706.
28. Guerreiro, R., Wojtas, A., Bras, J., Carrasquillo, M., Rogaeva, E., Majounie, E., Cruchaga, C., Sassi, C., Kauwe, J. S. K., Younkin, S. et al. (2013). TREM2 Variants in Alzheimer's Disease. New England Journal of Medicine 368, 117-127.
29. Hardy, J. and Selkoe, D. J. (2002). Medicine-The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353-356.
30. Hart, A. D., Wyttenbach, A., Perry, V. H. and Teeling, J. L. (2012). Age related changes in microglial phenotype vary between CNS regions: Grey versus white matter differences. Brain Behavior and Immunity 26, 754-765.
31. He, Y., Le, W.-D. and Appel, S. H. (2002). Role of Fc? Receptors in Nigral Cell Injury Induced by Parkinson Disease Immunoglobulin Injection into Mouse Substantia Nigra. Exp Neurol 176, 322-327.
32. Hoarau, J. J., Krejbich-Trotot, P., Jaffar-Bandjee, M. C., Das, T., Thon-Hon, G. V., Kumar, S., Neal, J. W. and Gasque, P. (2011). Activation and Control of CNS Innate Immune Responses in Health and Diseases: A Balancing Act Finely Tuned by Neuroimmune Regulators (NIReg). Cns & Neurological Disorders-Drug Targets 10, 25-43.
33. Hollingworth, P. Harold, D. Sims, R. Gerrish, A. Lambert, J.-C. Carrasquillo, M. M. Abraham, R. Hamshere, M. L. Pahwa, J. S. Moskvina, V. et al. (2011). Common variants at ABCA7, MS4A6A/MS4A4E, EPHA1, CD33 and CD2AP are associated with Alzheimer's disease. Nature Genetics 43, 429-+.
34. Holmes, C., Cunningham, C., Zotova, E., Culliford, D. and Perry, V. H. (2011). Proinflammatory cytokines, sickness behavior, and Alzheimer disease. Neurology 77, 212-218.
35. Hulse, R. E., Swenson, W. G., Kunkler, P. E., White, D. M. and Kraig, R. P. (2008). Monomeric IgG Is Neuroprotective via Enhancing Microglial Recycling Endocytosis and TNF-alpha. Journal of Neuroscience 28, 12199-12211.
36. Kam, T.-I., Song, S., Gwon, Y., Park, H., Yan, J.-J., Im, I., Choi, J.-W., Choi, T.-Y., Kim, J., Song, D.-K. et al. (2013). Fc?RIIb mediates amyloid-ß neurotoxicity and memory impairment in Alzheimer's disease. The Journal of Clinical Investigation 123, 2791-2802.
37. Katsuki, H., Nakai, S., Hirai, Y., Akaji, K., Kiso, Y. and Satoh, M. (1990). Interleukin-1-Beta inhibits long-term potentiation in the CA3 region of mouse hippocampal slices. Eur J Pharmacol 181, 323-326.
38. Komine-Kobayashi, M., Chou, N., Mochizuki, H., Nakao, A., Mizuno, Y. and Urabe, T. (2004). Dual Role of Fc? Receptor in Transient Focal Cerebral Ischemia in Mice. Stroke 35, 958-963.
39. Lambert, J.-C. Ibrahim-Verbaas, C. A. Harold, D. Naj, A. C. Sims, R. Bellenguez, C. Jun, G. DeStefano, A. L. Bis, J. C. Beecham, G. W. et al. (2013). Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer's disease. Nature Genetics 45, 1452-U206.
40. Lambert, J. C., Heath, S., Even, G., Campion, D., Sleegers, K., Hiltunen, M., Combarros, O., Zelenika, D., Bullido, M. J., Tavernier, B. et al. (2009). Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease. Nat Genet 41, 1094-9.
41. Le, W. D., Rowe, D., Xie, W. J., Ortiz, I., He, Y. and Appel, S. H. (2001). Microglial activation and dopaminergic cell injury: An in vitro model relevant to Parkinson's disease. Journal of Neuroscience 21, 8447-8455.
42. Lemere, C. A. and Masliah, E. (2010). Can Alzheimer disease be prevented by amyloid-beta immunotherapy? (vol 6, pg 108, 2010). Nature Reviews Neurology 6.
43. Li, Y. N., Qin, X. J., Kuang, F., Wu, R., Duan, M. L., Ju, G. and Wang, B. R. (2008). Alterations of Fc Gamma Receptor I and Toll-Like Receptor 4 Mediate the Antiinflammatory Actions of Microglia and Astrocytes After Adrenaline-Induced Blood-Brain Barrier Opening in Rats. J Neurosci Res 86, 3556-3565.
44. Lu, J., Moochhala, S., Kaur, C. and Ling, E. A. (2001). Cellular inflammatory response associated with breakdown of the blood-brain barrier after closed head injury in rats. J Neurotrauma 18, 399-408.
45. Lunnon, K., Teeling, J. L., Tutt, A. L., Cragg, M. S., Glennie, M. J. and Perry, V. H. (2011). Systemic inflammation modulates Fc receptor expression on microglia during chronic neurodegeneration. J Immunol 186, 7215-24.
46. Mantovani, A., Sica, A., Sozzani, S., Allavena, P., Vecchi, A. and Locati, M. (2004). The chemokine system in diverse forms of macrophage activation and polarization. Trends in Immunology 25, 677-686.
47. Masters, C. L., Simms, G., Weinman, N. A., Multhaup, G., McDonald, B. L. and Beyreuther, K. (1985). Amyloid plaque core protein in alzheimer-disease and down syndrome. Proceedings of the National Academy of Sciences of the United States of America 82, 4245-4249.
48. Mohamed, H. A., Mosier, D. R., Zou, L. L., Siklos, L., Alexianu, M. E., Engelhardt, J. I., Beers, D.R., Le, W. D. and Appel, S. H. (2002). Immunoglobulin Fc gamma receptor promotes immunoglobulin uptake, immunoglobulin-mediated calcium increase, and neurotransmitter release in motor neurons. J Neurosci Res 69, 110-116.
49. Morgan, D. (2009). The Role of Microglia in Antibody-Mediated Clearance of Amyloid-Beta from the Brain. Cns & Neurological Disorders-Drug Targets 8, 7-15.
50. Mosser, D. M. (2003). The many faces of macrophage activation. Journal of Leukocyte Biology 73, 209-212.
51. Mosser, D. M. and Edwards, J. P. (2008). Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8, 958-969.
52. Mullan, M., Crawford, F., Axelman, K., Houlden, H., Lilius, L., Winblad, B. and Lannfelt, L. (1992). A Pathogenic mutation for probable Alzheimer's Disease in the APP gene at the N terminus of beta amyloid. Nature Genetics 1, 345-347.
53. Murinello, S., Mullins, R. F., Lotery, A. J., Perry, V. H. and Teeling, J. L. (2014). Fc gamma Receptor Upregulation Is Associated With Immune Complex Inflammation in the Mouse Retina and Early Age-Related Macular Degeneration. Invest Ophthalmol Vis Sci 55, 247-258.
54. Nakahara, J., Tan-Takeuchi, K., Seiwa, C., Gotoh, M., Kaifu, T., Ujike, A., Inui, M., Yagi, T., Ogawa, M., Aiso, S. et al. (2003). Signaling via immunoglobulin Fc receptors induces oligodendrocyte precursor cell differentiation. Dev Cell 4, 841-852.
55. Nakamura, K., Hirai, H., Torashima, T., Miyazaki, T., Tsurui, H., Xiu, Y., Ohtsuji, M., Lin, Q. S., Tsukamoto, K., Nishimura, H. et al. (2007). CD3 and immunoglobulin G Fc receptor regulate cerebellar functions. Mol Cell Biol 27, 5128-5134.
56. Nimmerjahn, F. and Ravetch, J. V. (2008). Fcgamma receptors as regulators of immune responses. Nat Rev Immunol 8, 34-47.
57. Nitsch, R. M. and Hock, C. (2008). Targeting beta-amyloid pathology in Alzheimer's disease with A beta immunotherapy. Neurotherapeutics 5, 415-420.
58. Nyland, H., Mork, S. and Matre, R. (1984). Fc gamma receptors in multiple sclerosis brains. Ann N Y Acad Sci 436, 476-479.
59. Olson, M. I. and Shaw, C.-M. (1969). Presenile dementia and Alzheimer Disease in mongolism. Brain 92, 147-156.
60. Orr, C. F., Rowe, D. B., Mizuno, Y., Mori, H. and Halliday, G. M. (2005). A possible role for humoral immunity in the pathogenesis of Parkinson's disease. Brain 128, 2665-2674.
61. Peress, N. S., Fleit, H. B., Perillo, E., Kuljis, R. and Pezzullo, C. (1993). Identifcation of Fc gamma RI, II and III on normal human brain ramified microglia in senile plaques in Alzheimer's Disease. Journal of Neuroimmunology 48, 71-80.
62. Poduslo, J. F., Curran, G. L. and Berg, C. T. (1994). MACROMOLECULAR PERMEABILITY ACROSS THE BLOOD-NERVE AND BLOOD-BRAIN BARRIERS. Proceedings of the National Academy of Sciences of the United States of America 91, 5705-5709.
63. Puentener, U., Booth, S. G., Perry, V. H. and Teeling, J. L. (2012). Long-term impact of systemic bacterial infection on the cerebral vasculature and microglia. J Neuroinflammation 9.
64. Reisberg, B., Doody, R., Stoffler, A., Schmitt, F., Ferris, S., Mobius, H. J. and Memantine Study, G. (2003). Memantine in moderate-to-severe Alzheimer's disease. New England Journal of Medicine 348, 1333-1341.
65. Rinne, J. O., Brooks, D. J., Rossor, M. N., Fox, N. C., Bullock, R., Klunk, W. E., Mathis, C. A., Blennow, K., Barakos, J., Okello, A. A. et al. (2010). (11)C-PiB PET assessment of change in fibrillar amyloid-beta load in patients with Alzheimer's disease treated with bapineuzumab: a phase 2, double616 blind, placebo-controlled, ascending-dose study. Lancet Neurology 9, 363-372.
66. Ross, F. M., Allan, S. M., Rothwell, N. J. and Verkhratsky, A. (2003). A dual role for interleukin-1 in LTP in mouse hippocampal slices. Journal of Neuroimmunology 144, 61-67.
67. Salloway, S., Sperling, R., Fox, N. C., Blennow, K., Klunk, W., Raskind, M., Sabbagh, M., Honig, L. S., Porsteinsson, A. P., Ferris, S. et al. (2014). Two Phase 3 Trials of Bapineuzumab in Mild-to-Moderate Alzheimer's Disease. New England Journal of Medicine 370, 322-333.
68. Salloway, S. P., Black, R., Sperling, R., Fox, N., Gilman, S., Schenk, D. and Grundman, M. (2010). A phase 2 multiple ascending dose trial of bapineuzumab in mild to moderate Alzheimer Disease Reply. Neurology 74, 2026-2027.
69. Schenk, D. (2002). Amyloid-beta immunotherapy for Alzheimer's disease: the end of the beginning. Nature Reviews Neuroscience 3, 824-828.
70. Schlachetzki, F., Zhu, C. N. and Pardridge, W. M. (2002). Expression of the neonatal Fc receptor (FcRn) at the blood-brain barrier. J Neurochem 81, 203-206.
71. Stellwagen, D. and Malenka, R. C. (2006). Synaptic scaling mediated by glial TNF-alpha. Nature 440, 1054-1059.
72. Strittmatter, W. J. and Roses, A. D. (1995). Apolipoprotein E and Alzheimer's disease. Proceedings of the National Academy of Sciences of the United States of America 92, 4725-4727.
73. Takai, T., Li, M., Sylvestre, D., Clynes, R. and Ravetch, J. V. (1994). FCR GAMMA-CHAIN DELETION RESULTS IN PLEIOTROPIC EFFECTOR CELL DEFECTS. Cell 76, 519-529.
74. Tariot Pn, F. M. R. G. G. T. (2004). Memantine treatment in patients with moderate to severe alzheimer disease already receiving donepezil: A randomized controlled trial. JAMA 291, 317-324.
75. Teeling, J. L., Carare, R. O., Glennie, M. J. and Perry, V. H. (2012). Intracerebral immune complex formation induces inflammation in the brain that depends on Fc receptor interaction. Acta Neuropathol 124, 479-490.
76. Ulvestad, E., Williams, K., Vedeler, C., Antel, J., Nyland, H., Mork, S. and Matre, R. (1994). Reactive microglia in multiple sclerosis lesions have an increased expression of receptors for the Fc part of IgG. J Neurol Sci 121, 125-131.
77. Wilcock, D. M., Alamed, J., Gottschall, P. E., Grimm, J., Rosenthal, A., Pons, J., Ronan, V., Symmonds, K., Gordon, M. N. and Morgan, D. (2006). Deglycosylated anti-amyloid-beta antibodies eliminate cognitive deficits and reduce parenchymal amyloid with minimal vascular consequences in aged amyloid precursor protein transgenic mice. J Neurosci 26, 5340-6.
78. Wilcock, D. M., Munireddy, S. K., Rosenthal, A., Ugen, K. E., Gordon, M. N. and Morgan, D. (2004a). Microglial activation facilitates Abeta plaque removal following intracranial anti-Abeta antibody administration. Neurobiol Dis 15, 11-20.
79. Wilcock, D. M., Rojiani, A., Rosenthal, A., Levkowitz, G., Subbarao, S., Alamed, J., Wilson, D., Wilson, N., Freeman, M. J., Gordon, M. N. et al. (2004b). Passive amyloid immunotherapy clears amyloid and transiently activates microglia in a transgenic mouse model of amyloid deposition. J Neurosci 24, 6144-51.
80. Wilcock, D. M., Rojiani, A., Rosenthal, A., Subbarao, S., Freeman, M. J., Gordon, M. N. and Morgan, D. (2004c). Passive immunotherapy against Abeta in aged APP-transgenic mice reverses cognitive deficits and depletes parenchymal amyloid deposits in spite of increased vascular amyloid and microhemorrhage. J Neuroinflammation 1, 24.
81. Wilcock, D. M., Zhao, Q., Morgan, D., Gordon, M. N., Everhart, A., Wilson, J. G., Lee, J. E. and Colton, C. A. (2011a). Diverse inflammatory responses in transgenic mouse models of AD and the effect of immunotherapy on these responses. ASN Neuro.
82. Wilcock, D. M., Zhao, Q., Morgan, D., Gordon, M. N., Everhart, A., Wilson, J. G., Lee, J. E. and Colton, C. A. (2011b). Diverse inflammatory responses in transgenic mouse models of Alzheimer's disease and the effect of immunotherapy on these responses. ASN Neuro 3, 249-58.
83. Wyss-Coray, T., Lin, C., Yan, F. R., Yu, G. Q., Rohde, M., McConlogue, L., Masliah, E. and Mucke, L. (2001). TGF-beta 1 promotes microglial amyloid-beta clearance and reduces plaque burden in transgenic mice. Nature Medicine 7, 612-618.
84. Yang, L., Lindholm, K., Konishi, Y., Li, R. and Shen, Y. (2002). Target Depletion of Distinct Tumor Necrosis Factor Receptor Subtypes Reveals Hippocampal Neuron Death and Survival through Different Signal Transduction Pathways. The Journal of Neuroscience 22, 3025-3032.
85. Yuasa, T., Kubo, S., Yoshino, T., Ujike, A., Matsumura, K., Ono, M., Ravetch, J. V. and Takai, T. (1999). Deletion of Fc gamma receptor IIB renders H-2(b) mice susceptible to collagen-induced arthritis. Journal of Experimental Medicine 189, 187-194.
86. Zhang, Y. and Pardridge, W. M. (2001). Mediated efflux of IgG molecules from brain to blood across the blood-brain barrier. Journal of Neuroimmunology 114, 168-172.
87. Zotova, E., Bharambe, V., Cheaveau, M., Morgan, W., Holmes, C., Harris, S., Neal, J. W., Love, S., Nicoll, J. A. R. and Boche, D. (2013). Inflammatory components in human Alzheimer's disease and after active amyloid-beta(42) immunization. Brain 136, 2677-2696.