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Published in: Molecular Neurodegeneration 1/2017

Open Access 01-12-2017 | Research article

Amelioration of amyloid-β-induced deficits by DcR3 in an Alzheimer’s disease model

Authors: Yi-Ling Liu, Wei-Ting Chen, Yu-Yi Lin, Po-Hung Lu, Shie-Liang Hsieh, Irene Han-Juo Cheng

Published in: Molecular Neurodegeneration | Issue 1/2017

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Abstract

Background

Microglia mediate amyloid-beta peptide (Aβ)-induced neuroinflammation, which is one of the key events in the pathogenesis of Alzheimer’s disease (AD). Decoy receptor 3 (DcR3)/TNFRSF6B is a pleiotropic immunomodulator that promotes macrophage differentiation toward the M2 anti-inflammatory phenotype. Based on its role as an immunosupressor, we examined whether DcR3 could alleviate neuroinflammation and AD-like deficits in the central nervous system.

Method

We crossed human APP transgenic mice (line J20) with human DcR3 transgenic mice to generate wild-type, APP, DcR3, and APP/DcR3 mice for pathological analysis. The Morris water maze, fear conditioning test, open-field, and elevated-plus maze were used to access their cognitive behavioral changes. Furthermore, the pathological and immune profiles were examined by immunostaining, ELISA, Q-PCR, and IP. In vitro assays were designed to examine DcR3-mediated innate cytokine profile alteration and the potential protective mechanism.

Results

We reported that DcR3 ameliorates hippocampus-dependent memory deficits and reduces amyloid plaque deposition in APP transgenic mouse. The protective mechanism of DcR3 mediates through interacting with heparan sulfate proteoglycans and activating IL-4+YM1+ M2a-like microglia that reduces Aβ-induced proinflammatory cytokines and promotes phagocytosis ability of microglia.

Conclusion

The neuroprotective effect of DcR3 is mediated via modulating microglia activation into anti-inflammatory M2a phenotype, and upregulating DcR3 expression in the brain may be a potential therapeutic approach for AD.
Appendix
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Literature
3.
go back to reference Wright AL, Zinn R, Hohensinn B, Konen LM, Beynon SB, Tan RP, Clark IA, Abdipranoto A, Vissel B. Neuroinflammation and neuronal loss precede Abeta plaque deposition in the hAPP-J20 mouse model of Alzheimer’s disease. PLoS One. 2013;8:e59586.CrossRefPubMedPubMedCentral Wright AL, Zinn R, Hohensinn B, Konen LM, Beynon SB, Tan RP, Clark IA, Abdipranoto A, Vissel B. Neuroinflammation and neuronal loss precede Abeta plaque deposition in the hAPP-J20 mouse model of Alzheimer’s disease. PLoS One. 2013;8:e59586.CrossRefPubMedPubMedCentral
4.
go back to reference ADAPT-FS Research Group. Follow-up evaluation of cognitive function in the randomized Alzheimer’s disease anti-inflammatory prevention trial and its follow-up study. Alzheimers Dement. 2015;11:216–25. e211.CrossRef ADAPT-FS Research Group. Follow-up evaluation of cognitive function in the randomized Alzheimer’s disease anti-inflammatory prevention trial and its follow-up study. Alzheimers Dement. 2015;11:216–25. e211.CrossRef
5.
go back to reference Wang WY, Tan MS, Yu JT, Tan L. Role of pro-inflammatory cytokines released from microglia in Alzheimer’s disease. Ann Transl Med. 2015;3:136.PubMedPubMedCentral Wang WY, Tan MS, Yu JT, Tan L. Role of pro-inflammatory cytokines released from microglia in Alzheimer’s disease. Ann Transl Med. 2015;3:136.PubMedPubMedCentral
6.
go back to reference Koenigsknecht J, Landreth G. Microglial phagocytosis of fibrillar beta-amyloid through a beta1 integrin-dependent mechanism. J Neurosci. 2004;24:9838–46.CrossRefPubMed Koenigsknecht J, Landreth G. Microglial phagocytosis of fibrillar beta-amyloid through a beta1 integrin-dependent mechanism. J Neurosci. 2004;24:9838–46.CrossRefPubMed
7.
go back to reference Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci. 2009;29:13435–44.CrossRefPubMedPubMedCentral Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci. 2009;29:13435–44.CrossRefPubMedPubMedCentral
8.
go back to reference Jang E, Lee S, Kim JH, Seo JW, Lee WH, Mori K, Nakao K, Suk K. Secreted protein lipocalin-2 promotes microglial M1 polarization. FASEB J. 2013;27:1176–90.CrossRefPubMed Jang E, Lee S, Kim JH, Seo JW, Lee WH, Mori K, Nakao K, Suk K. Secreted protein lipocalin-2 promotes microglial M1 polarization. FASEB J. 2013;27:1176–90.CrossRefPubMed
9.
go back to reference David S, Kroner A. Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci. 2011;12:388–99.CrossRefPubMed David S, Kroner A. Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci. 2011;12:388–99.CrossRefPubMed
10.
go back to reference Hu X, Li P, Guo Y, Wang H, Leak RK, Chen S, Gao Y, Chen J. Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia. Stroke. 2012;43:3063–70.CrossRefPubMed Hu X, Li P, Guo Y, Wang H, Leak RK, Chen S, Gao Y, Chen J. Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia. Stroke. 2012;43:3063–70.CrossRefPubMed
11.
go back to reference Heneka MT, Kummer MP, Stutz A, Delekate A, Schwartz S, Vieira-Saecker A, Griep A, Axt D, Remus A, Tzeng TC, et al. NLRP3 is activated in Alzheimer’s disease and contributes to pathology in APP/PS1 mice. Nature. 2013;493:674–8.CrossRefPubMed Heneka MT, Kummer MP, Stutz A, Delekate A, Schwartz S, Vieira-Saecker A, Griep A, Axt D, Remus A, Tzeng TC, et al. NLRP3 is activated in Alzheimer’s disease and contributes to pathology in APP/PS1 mice. Nature. 2013;493:674–8.CrossRefPubMed
12.
go back to reference Tang Y, Le W. Differential roles of M1 and M2 microglia in neurodegenerative diseases. Mol Neurobiol. 2016;53:1181–94.CrossRefPubMed Tang Y, Le W. Differential roles of M1 and M2 microglia in neurodegenerative diseases. Mol Neurobiol. 2016;53:1181–94.CrossRefPubMed
13.
14.
go back to reference Orme J, Mohan C. Macrophage subpopulations in systemic lupus erythematosus. Discov Med. 2012;13:151–8.PubMed Orme J, Mohan C. Macrophage subpopulations in systemic lupus erythematosus. Discov Med. 2012;13:151–8.PubMed
15.
go back to reference Pepe G, Calderazzi G, De Maglie M, Villa AM, Vegeto E. Heterogeneous induction of microglia M2a phenotype by central administration of interleukin-4. J Neuroinflammation. 2014;11:211.CrossRefPubMedPubMedCentral Pepe G, Calderazzi G, De Maglie M, Villa AM, Vegeto E. Heterogeneous induction of microglia M2a phenotype by central administration of interleukin-4. J Neuroinflammation. 2014;11:211.CrossRefPubMedPubMedCentral
16.
go back to reference Chhor V, Le Charpentier T, Lebon S, Ore MV, Celador IL, Josserand J, Degos V, Jacotot E, Hagberg H, Savman K, et al. Characterization of phenotype markers and neuronotoxic potential of polarised primary microglia in vitro. Brain Behav Immun. 2013;32:70–85.CrossRefPubMedPubMedCentral Chhor V, Le Charpentier T, Lebon S, Ore MV, Celador IL, Josserand J, Degos V, Jacotot E, Hagberg H, Savman K, et al. Characterization of phenotype markers and neuronotoxic potential of polarised primary microglia in vitro. Brain Behav Immun. 2013;32:70–85.CrossRefPubMedPubMedCentral
17.
go back to reference Hickman SE, Kingery ND, Ohsumi TK, Borowsky ML, Wang LC, Means TK, El Khoury J. The microglial sensome revealed by direct RNA sequencing. Nat Neurosci. 2013;16:1896–905.CrossRefPubMedPubMedCentral Hickman SE, Kingery ND, Ohsumi TK, Borowsky ML, Wang LC, Means TK, El Khoury J. The microglial sensome revealed by direct RNA sequencing. Nat Neurosci. 2013;16:1896–905.CrossRefPubMedPubMedCentral
18.
go back to reference Cherry JD, Olschowka JA, O’Banion MK. Arginase 1+ microglia reduce Abeta plaque deposition during IL-1beta-dependent neuroinflammation. J Neuroinflammation. 2015;12:203.CrossRefPubMedPubMedCentral Cherry JD, Olschowka JA, O’Banion MK. Arginase 1+ microglia reduce Abeta plaque deposition during IL-1beta-dependent neuroinflammation. J Neuroinflammation. 2015;12:203.CrossRefPubMedPubMedCentral
19.
go back to reference Hsu TL, Chang YC, Chen SJ, Liu YJ, Chiu AW, Chio CC, Chen L, Hsieh SL. Modulation of dendritic cell differentiation and maturation by decoy receptor 3. J Immunol. 2002;168:4846–53.CrossRefPubMed Hsu TL, Chang YC, Chen SJ, Liu YJ, Chiu AW, Chio CC, Chen L, Hsieh SL. Modulation of dendritic cell differentiation and maturation by decoy receptor 3. J Immunol. 2002;168:4846–53.CrossRefPubMed
20.
go back to reference Zhang J, Salcedo TW, Wan X, Ullrich S, Hu B, Gregorio T, Feng P, Qi S, Chen H, Cho YH, et al. Modulation of T-cell responses to alloantigens by TR6/DcR3. J Clin Invest. 2001;107:1459–68.CrossRefPubMedPubMedCentral Zhang J, Salcedo TW, Wan X, Ullrich S, Hu B, Gregorio T, Feng P, Qi S, Chen H, Cho YH, et al. Modulation of T-cell responses to alloantigens by TR6/DcR3. J Clin Invest. 2001;107:1459–68.CrossRefPubMedPubMedCentral
21.
go back to reference Yang CR, Hsieh SL, Teng CM, Ho FM, Su WL, Lin WW. Soluble decoy receptor 3 induces angiogenesis by neutralization of TL1A, a cytokine belonging to tumor necrosis factor superfamily and exhibiting angiostatic action. Cancer Res. 2004;64:1122–9.CrossRefPubMed Yang CR, Hsieh SL, Teng CM, Ho FM, Su WL, Lin WW. Soluble decoy receptor 3 induces angiogenesis by neutralization of TL1A, a cytokine belonging to tumor necrosis factor superfamily and exhibiting angiostatic action. Cancer Res. 2004;64:1122–9.CrossRefPubMed
22.
go back to reference Chang YC, Chan YH, Jackson DG, Hsieh SL. The glycosaminoglycan-binding domain of decoy receptor 3 is essential for induction of monocyte adhesion. J Immunol. 2006;176:173–80.CrossRefPubMed Chang YC, Chan YH, Jackson DG, Hsieh SL. The glycosaminoglycan-binding domain of decoy receptor 3 is essential for induction of monocyte adhesion. J Immunol. 2006;176:173–80.CrossRefPubMed
23.
go back to reference Lin WW, Hsieh SL. Decoy receptor 3: a pleiotropic immunomodulator and biomarker for inflammatory diseases, autoimmune diseases and cancer. Biochem Pharmacol. 2011;81:838–47.CrossRefPubMed Lin WW, Hsieh SL. Decoy receptor 3: a pleiotropic immunomodulator and biomarker for inflammatory diseases, autoimmune diseases and cancer. Biochem Pharmacol. 2011;81:838–47.CrossRefPubMed
24.
go back to reference Chang YC, Chen TC, Lee CT, Yang CY, Wang HW, Wang CC, Hsieh SL. Epigenetic control of MHC class II expression in tumor-associated macrophages by decoy receptor 3. Blood. 2008;111:5054–63.CrossRefPubMed Chang YC, Chen TC, Lee CT, Yang CY, Wang HW, Wang CC, Hsieh SL. Epigenetic control of MHC class II expression in tumor-associated macrophages by decoy receptor 3. Blood. 2008;111:5054–63.CrossRefPubMed
25.
go back to reference Tai SK, Chang HC, Lan KL, Lee CT, Yang CY, Chen NJ, Chou TY, Tarng DC, Hsieh SL. Decoy receptor 3 enhances tumor progression via induction of tumor-associated macrophages. J Immunol. 2012;188:2464–71.CrossRefPubMed Tai SK, Chang HC, Lan KL, Lee CT, Yang CY, Chen NJ, Chou TY, Tarng DC, Hsieh SL. Decoy receptor 3 enhances tumor progression via induction of tumor-associated macrophages. J Immunol. 2012;188:2464–71.CrossRefPubMed
26.
go back to reference Mucke L, Masliah E, Yu GQ, Mallory M, Rockenstein EM, Tatsuno G, Hu K, Kholodenko D, Johnson-Wood K, McConlogue L. High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J Neurosci. 2000;20:4050–8.PubMed Mucke L, Masliah E, Yu GQ, Mallory M, Rockenstein EM, Tatsuno G, Hu K, Kholodenko D, Johnson-Wood K, McConlogue L. High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J Neurosci. 2000;20:4050–8.PubMed
27.
go back to reference Cheng IH, Scearce-Levie K, Legleiter J, Palop JJ, Gerstein H, Bien-Ly N, Puolivali J, Lesne S, Ashe KH, Muchowski PJ, Mucke L. Accelerating amyloid-beta fibrillization reduces oligomer levels and functional deficits in Alzheimer disease mouse models. J Biol Chem. 2007;282:23818–28.CrossRefPubMed Cheng IH, Scearce-Levie K, Legleiter J, Palop JJ, Gerstein H, Bien-Ly N, Puolivali J, Lesne S, Ashe KH, Muchowski PJ, Mucke L. Accelerating amyloid-beta fibrillization reduces oligomer levels and functional deficits in Alzheimer disease mouse models. J Biol Chem. 2007;282:23818–28.CrossRefPubMed
29.
go back to reference Shao CY, Mirra SS, Sait HB, Sacktor TC, Sigurdsson EM. Postsynaptic degeneration as revealed by PSD-95 reduction occurs after advanced Abeta and tau pathology in transgenic mouse models of Alzheimer’s disease. Acta Neuropathol. 2011;122:285–92.CrossRefPubMedPubMedCentral Shao CY, Mirra SS, Sait HB, Sacktor TC, Sigurdsson EM. Postsynaptic degeneration as revealed by PSD-95 reduction occurs after advanced Abeta and tau pathology in transgenic mouse models of Alzheimer’s disease. Acta Neuropathol. 2011;122:285–92.CrossRefPubMedPubMedCentral
30.
go back to reference Ramirez-Amaya V, Balderas I, Sandoval J, Escobar ML, Bermudez-Rattoni F. Spatial long-term memory is related to mossy fiber synaptogenesis. J Neurosci. 2001;21:7340–8.PubMed Ramirez-Amaya V, Balderas I, Sandoval J, Escobar ML, Bermudez-Rattoni F. Spatial long-term memory is related to mossy fiber synaptogenesis. J Neurosci. 2001;21:7340–8.PubMed
31.
go back to reference Gilbert PE, Brushfield AM. The role of the CA3 hippocampal subregion in spatial memory: a process oriented behavioral assessment. Prog Neuropsychopharmacol Biol Psychiatry. 2009;33:774–81.CrossRefPubMedPubMedCentral Gilbert PE, Brushfield AM. The role of the CA3 hippocampal subregion in spatial memory: a process oriented behavioral assessment. Prog Neuropsychopharmacol Biol Psychiatry. 2009;33:774–81.CrossRefPubMedPubMedCentral
32.
go back to reference Bolmont T, Haiss F, Eicke D, Radde R, Mathis CA, Klunk WE, Kohsaka S, Jucker M, Calhoun ME. Dynamics of the microglial/amyloid interaction indicate a role in plaque maintenance. J Neurosci. 2008;28:4283–92.CrossRefPubMedPubMedCentral Bolmont T, Haiss F, Eicke D, Radde R, Mathis CA, Klunk WE, Kohsaka S, Jucker M, Calhoun ME. Dynamics of the microglial/amyloid interaction indicate a role in plaque maintenance. J Neurosci. 2008;28:4283–92.CrossRefPubMedPubMedCentral
33.
go back to reference Yan P, Hu X, Song H, Yin K, Bateman RJ, Cirrito JR, Xiao Q, Hsu FF, Turk JW, Xu J, et al. Matrix metalloproteinase-9 degrades amyloid-beta fibrils in vitro and compact plaques in situ. J Biol Chem. 2006;281:24566–74.CrossRefPubMed Yan P, Hu X, Song H, Yin K, Bateman RJ, Cirrito JR, Xiao Q, Hsu FF, Turk JW, Xu J, et al. Matrix metalloproteinase-9 degrades amyloid-beta fibrils in vitro and compact plaques in situ. J Biol Chem. 2006;281:24566–74.CrossRefPubMed
34.
go back to reference Watanabe N, Araki W, Chui DH, Makifuchi T, Ihara Y, Tabira T. Glypican-1 as an Abeta binding HSPG in the human brain: its localization in DIG domains and possible roles in the pathogenesis of Alzheimer’s disease. FASEB J. 2004;18:1013–5.PubMed Watanabe N, Araki W, Chui DH, Makifuchi T, Ihara Y, Tabira T. Glypican-1 as an Abeta binding HSPG in the human brain: its localization in DIG domains and possible roles in the pathogenesis of Alzheimer’s disease. FASEB J. 2004;18:1013–5.PubMed
35.
go back to reference Kaur C, Sivakumar V, Yip GW, Ling EA. Expression of syndecan-2 in the amoeboid microglial cells and its involvement in inflammation in the hypoxic developing brain. Glia. 2009;57:336–49.CrossRefPubMed Kaur C, Sivakumar V, Yip GW, Ling EA. Expression of syndecan-2 in the amoeboid microglial cells and its involvement in inflammation in the hypoxic developing brain. Glia. 2009;57:336–49.CrossRefPubMed
36.
go back to reference Pitti RM, Marsters SA, Lawrence DA, Roy M, Kischkel FC, Dowd P, Huang A, Donahue CJ, Sherwood SW, Baldwin DT, et al. Genomic amplification of a decoy receptor for Fas ligand in lung and colon cancer. Nature. 1998;396:699–703.CrossRefPubMed Pitti RM, Marsters SA, Lawrence DA, Roy M, Kischkel FC, Dowd P, Huang A, Donahue CJ, Sherwood SW, Baldwin DT, et al. Genomic amplification of a decoy receptor for Fas ligand in lung and colon cancer. Nature. 1998;396:699–703.CrossRefPubMed
37.
go back to reference Sandwall E, O’Callaghan P, Zhang X, Lindahl U, Lannfelt L, Li JP. Heparan sulfate mediates amyloid-beta internalization and cytotoxicity. Glycobiology. 2010;20:533–41.CrossRefPubMed Sandwall E, O’Callaghan P, Zhang X, Lindahl U, Lannfelt L, Li JP. Heparan sulfate mediates amyloid-beta internalization and cytotoxicity. Glycobiology. 2010;20:533–41.CrossRefPubMed
38.
go back to reference O’Callaghan P, Li JP, Lannfelt L, Lindahl U, Zhang X. Microglial heparan sulfate proteoglycans facilitate the cluster-of-differentiation 14 (CD14)/toll-like receptor 4 (TLR4)-dependent inflammatory response. J Biol Chem. 2015;290:14904–14.CrossRefPubMedPubMedCentral O’Callaghan P, Li JP, Lannfelt L, Lindahl U, Zhang X. Microglial heparan sulfate proteoglycans facilitate the cluster-of-differentiation 14 (CD14)/toll-like receptor 4 (TLR4)-dependent inflammatory response. J Biol Chem. 2015;290:14904–14.CrossRefPubMedPubMedCentral
39.
go back to reference Zhan Y, Paolicelli RC, Sforazzini F, Weinhard L, Bolasco G, Pagani F, Vyssotski AL, Bifone A, Gozzi A, Ragozzino D, Gross CT. Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat Neurosci. 2014;17:400–6.CrossRefPubMed Zhan Y, Paolicelli RC, Sforazzini F, Weinhard L, Bolasco G, Pagani F, Vyssotski AL, Bifone A, Gozzi A, Ragozzino D, Gross CT. Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat Neurosci. 2014;17:400–6.CrossRefPubMed
40.
go back to reference Hong S, Beja-Glasser VF, Nfonoyim BM, Frouin A, Li S, Ramakrishnan S, Merry KM, Shi Q, Rosenthal A, Barres BA, et al. Complement and microglia mediate early synapse loss in Alzheimer mouse models. Science. 2016;352:712–6.CrossRefPubMedPubMedCentral Hong S, Beja-Glasser VF, Nfonoyim BM, Frouin A, Li S, Ramakrishnan S, Merry KM, Shi Q, Rosenthal A, Barres BA, et al. Complement and microglia mediate early synapse loss in Alzheimer mouse models. Science. 2016;352:712–6.CrossRefPubMedPubMedCentral
41.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
42.
go back to reference Fu AK, Hung KW, Yuen MY, Zhou X, Mak DS, Chan IC, Cheung TH, Zhang B, Fu WY, Liew FY, Ip NY. IL-33 ameliorates Alzheimer’s disease-like pathology and cognitive decline. Proc Natl Acad Sci U S A. 2016;113:2705-2713. Fu AK, Hung KW, Yuen MY, Zhou X, Mak DS, Chan IC, Cheung TH, Zhang B, Fu WY, Liew FY, Ip NY. IL-33 ameliorates Alzheimer’s disease-like pathology and cognitive decline. Proc Natl Acad Sci U S A. 2016;113:2705-2713.
43.
go back to reference Perego C, Fumagalli S, De Simoni MG. Temporal pattern of expression and colocalization of microglia/macrophage phenotype markers following brain ischemic injury in mice. J Neuroinflammation. 2011;8:174.CrossRefPubMedPubMedCentral Perego C, Fumagalli S, De Simoni MG. Temporal pattern of expression and colocalization of microglia/macrophage phenotype markers following brain ischemic injury in mice. J Neuroinflammation. 2011;8:174.CrossRefPubMedPubMedCentral
44.
go back to reference Ohtaki H, Ylostalo JH, Foraker JE, Robinson AP, Reger RL, Shioda S, Prockop DJ. Stem/progenitor cells from bone marrow decrease neuronal death in global ischemia by modulation of inflammatory/immune responses. Proc Natl Acad Sci U S A. 2008;105:14638–43.CrossRefPubMedPubMedCentral Ohtaki H, Ylostalo JH, Foraker JE, Robinson AP, Reger RL, Shioda S, Prockop DJ. Stem/progenitor cells from bone marrow decrease neuronal death in global ischemia by modulation of inflammatory/immune responses. Proc Natl Acad Sci U S A. 2008;105:14638–43.CrossRefPubMedPubMedCentral
45.
go back to reference Ye L, Huang Y, Zhao L, Li Y, Sun L, Zhou Y, Qian G, Zheng JC. IL-1beta and TNF-alpha induce neurotoxicity through glutamate production: a potential role for neuronal glutaminase. J Neurochem. 2013;125:897–908.CrossRefPubMedPubMedCentral Ye L, Huang Y, Zhao L, Li Y, Sun L, Zhou Y, Qian G, Zheng JC. IL-1beta and TNF-alpha induce neurotoxicity through glutamate production: a potential role for neuronal glutaminase. J Neurochem. 2013;125:897–908.CrossRefPubMedPubMedCentral
47.
go back to reference Dong W, Embury CM, Lu Y, Whitmire SM, Dyavarshetty B, Gelbard HA, Gendelman HE, Kiyota T. The mixed-lineage kinase 3 inhibitor URMC-099 facilitates microglial amyloid-beta degradation. J Neuroinflammation. 2016;13:184.CrossRefPubMedPubMedCentral Dong W, Embury CM, Lu Y, Whitmire SM, Dyavarshetty B, Gelbard HA, Gendelman HE, Kiyota T. The mixed-lineage kinase 3 inhibitor URMC-099 facilitates microglial amyloid-beta degradation. J Neuroinflammation. 2016;13:184.CrossRefPubMedPubMedCentral
48.
49.
go back to reference Fujisaka S, Usui I, Bukhari A, Ikutani M, Oya T, Kanatani Y, Tsuneyama K, Nagai Y, Takatsu K, Urakaze M, et al. Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes. 2009;58:2574–82.CrossRefPubMedPubMedCentral Fujisaka S, Usui I, Bukhari A, Ikutani M, Oya T, Kanatani Y, Tsuneyama K, Nagai Y, Takatsu K, Urakaze M, et al. Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes. 2009;58:2574–82.CrossRefPubMedPubMedCentral
50.
go back to reference Jablonski KA, Amici SA, Webb LM, Ruiz-Rosado Jde D, Popovich PG, Partida-Sanchez S, Guerau-de-Arellano M. Novel markers to delineate murine M1 and M2 macrophages. PLoS One. 2015;10:e0145342.CrossRefPubMedPubMedCentral Jablonski KA, Amici SA, Webb LM, Ruiz-Rosado Jde D, Popovich PG, Partida-Sanchez S, Guerau-de-Arellano M. Novel markers to delineate murine M1 and M2 macrophages. PLoS One. 2015;10:e0145342.CrossRefPubMedPubMedCentral
51.
go back to reference Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron. 2012;74:691–705.CrossRefPubMedPubMedCentral Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron. 2012;74:691–705.CrossRefPubMedPubMedCentral
52.
go back to reference Parkhurst CN, Yang G, Ninan I, Savas JN, Yates 3rd JR, Lafaille JJ, Hempstead BL, Littman DR, Gan WB. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell. 2013;155:1596–609.CrossRefPubMedPubMedCentral Parkhurst CN, Yang G, Ninan I, Savas JN, Yates 3rd JR, Lafaille JJ, Hempstead BL, Littman DR, Gan WB. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell. 2013;155:1596–609.CrossRefPubMedPubMedCentral
53.
go back to reference Wisniewski HM, Wegiel J, Wang KC, Lach B. Ultrastructural studies of the cells forming amyloid in the cortical vessel wall in Alzheimer’s disease. Acta Neuropathol. 1992;84:117–27.CrossRefPubMed Wisniewski HM, Wegiel J, Wang KC, Lach B. Ultrastructural studies of the cells forming amyloid in the cortical vessel wall in Alzheimer’s disease. Acta Neuropathol. 1992;84:117–27.CrossRefPubMed
54.
go back to reference Ma Y, Bao J, Zhao X, Shen H, Lv J, Ma S, Zhang X, Li Z, Wang S, Wang Q, Ji J. Activated cyclin-dependent kinase 5 promotes microglial phagocytosis of fibrillar beta-amyloid by up-regulating lipoprotein lipase expression. Mol Cell Proteomics. 2013;12:2833–44.CrossRefPubMedPubMedCentral Ma Y, Bao J, Zhao X, Shen H, Lv J, Ma S, Zhang X, Li Z, Wang S, Wang Q, Ji J. Activated cyclin-dependent kinase 5 promotes microglial phagocytosis of fibrillar beta-amyloid by up-regulating lipoprotein lipase expression. Mol Cell Proteomics. 2013;12:2833–44.CrossRefPubMedPubMedCentral
55.
go back to reference Condello C, Yuan P, Schain A, Grutzendler J. Microglia constitute a barrier that prevents neurotoxic protofibrillar Abeta42 hotspots around plaques. Nat Commun. 2015;6:6176.CrossRefPubMedPubMedCentral Condello C, Yuan P, Schain A, Grutzendler J. Microglia constitute a barrier that prevents neurotoxic protofibrillar Abeta42 hotspots around plaques. Nat Commun. 2015;6:6176.CrossRefPubMedPubMedCentral
56.
go back to reference Marsh SE, Abud EM, Lakatos A, Karimzadeh A, Yeung ST, Davtyan H, Fote GM, Lau L, Weinger JG, Lane TE, et al. The adaptive immune system restrains Alzheimer’s disease pathogenesis by modulating microglial function. Proc Natl Acad Sci U S A. 2016;113:E1316–1325.CrossRefPubMedPubMedCentral Marsh SE, Abud EM, Lakatos A, Karimzadeh A, Yeung ST, Davtyan H, Fote GM, Lau L, Weinger JG, Lane TE, et al. The adaptive immune system restrains Alzheimer’s disease pathogenesis by modulating microglial function. Proc Natl Acad Sci U S A. 2016;113:E1316–1325.CrossRefPubMedPubMedCentral
57.
go back to reference Zhang B, Gaiteri C, Bodea LG, Wang Z, McElwee J, Podtelezhnikov AA, Zhang C, Xie T, Tran L, Dobrin R, et al. Integrated systems approach identifies genetic nodes and networks in late-onset Alzheimer’s disease. Cell. 2013;153:707–20.CrossRefPubMedPubMedCentral Zhang B, Gaiteri C, Bodea LG, Wang Z, McElwee J, Podtelezhnikov AA, Zhang C, Xie T, Tran L, Dobrin R, et al. Integrated systems approach identifies genetic nodes and networks in late-onset Alzheimer’s disease. Cell. 2013;153:707–20.CrossRefPubMedPubMedCentral
58.
go back to reference Ritzel RM, Patel AR, Pan S, Crapser J, Hammond M, Jellison E, McCullough LD. Age- and location-related changes in microglial function. Neurobiol Aging. 2015;36:2153–63.CrossRefPubMed Ritzel RM, Patel AR, Pan S, Crapser J, Hammond M, Jellison E, McCullough LD. Age- and location-related changes in microglial function. Neurobiol Aging. 2015;36:2153–63.CrossRefPubMed
59.
go back to reference Pan XD, Zhu YG, Lin N, Zhang J, Ye QY, Huang HP, Chen XC. Microglial phagocytosis induced by fibrillar beta-amyloid is attenuated by oligomeric beta-amyloid: implications for Alzheimer’s disease. Mol Neurodegener. 2011;6:45.CrossRefPubMedPubMedCentral Pan XD, Zhu YG, Lin N, Zhang J, Ye QY, Huang HP, Chen XC. Microglial phagocytosis induced by fibrillar beta-amyloid is attenuated by oligomeric beta-amyloid: implications for Alzheimer’s disease. Mol Neurodegener. 2011;6:45.CrossRefPubMedPubMedCentral
60.
go back to reference Wang Y, Cella M, Mallinson K, Ulrich JD, Young KL, Robinette ML, Gilfillan S, Krishnan GM, Sudhakar S, Zinselmeyer BH, et al. TREM2 lipid sensing sustains the microglial response in an Alzheimer’s disease model. Cell. 2015;160:1061–71.CrossRefPubMedPubMedCentral Wang Y, Cella M, Mallinson K, Ulrich JD, Young KL, Robinette ML, Gilfillan S, Krishnan GM, Sudhakar S, Zinselmeyer BH, et al. TREM2 lipid sensing sustains the microglial response in an Alzheimer’s disease model. Cell. 2015;160:1061–71.CrossRefPubMedPubMedCentral
61.
go back to reference Bhattacharjee S, Zhao Y, Lukiw WJ. Deficits in the miRNA-34a-regulated endogenous TREM2 phagocytosis sensor-receptor in Alzheimer’s disease (AD); an update. Front Aging Neurosci. 2014;6:116.PubMedPubMedCentral Bhattacharjee S, Zhao Y, Lukiw WJ. Deficits in the miRNA-34a-regulated endogenous TREM2 phagocytosis sensor-receptor in Alzheimer’s disease (AD); an update. Front Aging Neurosci. 2014;6:116.PubMedPubMedCentral
62.
go back to reference Kiyota T, Gendelman HE, Weir RA, Higgins EE, Zhang G, Jain M. CCL2 affects beta-amyloidosis and progressive neurocognitive dysfunction in a mouse model of Alzheimer’s disease. Neurobiol Aging. 2013;34:1060–8.CrossRefPubMed Kiyota T, Gendelman HE, Weir RA, Higgins EE, Zhang G, Jain M. CCL2 affects beta-amyloidosis and progressive neurocognitive dysfunction in a mouse model of Alzheimer’s disease. Neurobiol Aging. 2013;34:1060–8.CrossRefPubMed
63.
go back to reference van Horssen J, Otte-Holler I, David G, Maat-Schieman ML, van den Heuvel LP, Wesseling P, de Waal RM, Verbeek MM. Heparan sulfate proteoglycan expression in cerebrovascular amyloid beta deposits in Alzheimer’s disease and hereditary cerebral hemorrhage with amyloidosis (Dutch) brains. Acta Neuropathol. 2001;102:604–14.CrossRefPubMed van Horssen J, Otte-Holler I, David G, Maat-Schieman ML, van den Heuvel LP, Wesseling P, de Waal RM, Verbeek MM. Heparan sulfate proteoglycan expression in cerebrovascular amyloid beta deposits in Alzheimer’s disease and hereditary cerebral hemorrhage with amyloidosis (Dutch) brains. Acta Neuropathol. 2001;102:604–14.CrossRefPubMed
64.
go back to reference Liu CC, Zhao N, Yamaguchi Y, Cirrito JR, Kanekiyo T, Holtzman DM, Bu G. Neuronal heparan sulfates promote amyloid pathology by modulating brain amyloid-beta clearance and aggregation in Alzheimer’s disease. Sci Transl Med. 2016;8:332ra344. Liu CC, Zhao N, Yamaguchi Y, Cirrito JR, Kanekiyo T, Holtzman DM, Bu G. Neuronal heparan sulfates promote amyloid pathology by modulating brain amyloid-beta clearance and aggregation in Alzheimer’s disease. Sci Transl Med. 2016;8:332ra344.
65.
go back to reference O’Callaghan P, Sandwall E, Li JP, Yu H, Ravid R, Guan ZZ, van Kuppevelt TH, Nilsson LN, Ingelsson M, Hyman BT, et al. Heparan sulfate accumulation with Abeta deposits in Alzheimer’s disease and Tg2576 mice is contributed by glial cells. Brain Pathol. 2008;18:548–61.PubMedPubMedCentral O’Callaghan P, Sandwall E, Li JP, Yu H, Ravid R, Guan ZZ, van Kuppevelt TH, Nilsson LN, Ingelsson M, Hyman BT, et al. Heparan sulfate accumulation with Abeta deposits in Alzheimer’s disease and Tg2576 mice is contributed by glial cells. Brain Pathol. 2008;18:548–61.PubMedPubMedCentral
66.
go back to reference Schulz JG, Annaert W, Vandekerckhove J, Zimmermann P, De Strooper B, David G. Syndecan 3 intramembrane proteolysis is presenilin/gamma-secretase-dependent and modulates cytosolic signaling. J Biol Chem. 2003;278:48651–7.CrossRefPubMed Schulz JG, Annaert W, Vandekerckhove J, Zimmermann P, De Strooper B, David G. Syndecan 3 intramembrane proteolysis is presenilin/gamma-secretase-dependent and modulates cytosolic signaling. J Biol Chem. 2003;278:48651–7.CrossRefPubMed
67.
go back to reference Zhang X, Wu C, Song J, Gotte M, Sorokin L. Syndecan-1, a cell surface proteoglycan, negatively regulates initial leukocyte recruitment to the brain across the choroid plexus in murine experimental autoimmune encephalomyelitis. J Immunol. 2013;191:4551–61.CrossRefPubMed Zhang X, Wu C, Song J, Gotte M, Sorokin L. Syndecan-1, a cell surface proteoglycan, negatively regulates initial leukocyte recruitment to the brain across the choroid plexus in murine experimental autoimmune encephalomyelitis. J Immunol. 2013;191:4551–61.CrossRefPubMed
68.
go back to reference Zhang X, Li JP. Heparan sulfate proteoglycans in amyloidosis. Prog Mol Biol Transl Sci. 2010;93:309–34.CrossRefPubMed Zhang X, Li JP. Heparan sulfate proteoglycans in amyloidosis. Prog Mol Biol Transl Sci. 2010;93:309–34.CrossRefPubMed
69.
go back to reference Simard JM, Tosun C, Ivanova S, Kurland DB, Hong C, Radecki L, Gisriel C, Mehta R, Schreibman D, Gerzanich V. Heparin reduces neuroinflammation and transsynaptic neuronal apoptosis in a model of subarachnoid hemorrhage. Transl Stroke Res. 2012;3:155–65.CrossRefPubMedPubMedCentral Simard JM, Tosun C, Ivanova S, Kurland DB, Hong C, Radecki L, Gisriel C, Mehta R, Schreibman D, Gerzanich V. Heparin reduces neuroinflammation and transsynaptic neuronal apoptosis in a model of subarachnoid hemorrhage. Transl Stroke Res. 2012;3:155–65.CrossRefPubMedPubMedCentral
70.
go back to reference Imbimbo BP, Solfrizzi V, Panza F. Are NSAIDs useful to treat Alzheimer’s disease or mild cognitive impairment? Front Aging Neurosci. 2010;2:19. Imbimbo BP, Solfrizzi V, Panza F. Are NSAIDs useful to treat Alzheimer’s disease or mild cognitive impairment? Front Aging Neurosci. 2010;2:19.
71.
go back to reference Solomon SD, Wittes J, Finn PV, Fowler R, Viner J, Bertagnolli MM, Arber N, Levin B, Meinert CL, Martin B, et al. Cardiovascular risk of celecoxib in 6 randomized placebo-controlled trials: the cross trial safety analysis. Circulation. 2008;117:2104–13.CrossRefPubMedPubMedCentral Solomon SD, Wittes J, Finn PV, Fowler R, Viner J, Bertagnolli MM, Arber N, Levin B, Meinert CL, Martin B, et al. Cardiovascular risk of celecoxib in 6 randomized placebo-controlled trials: the cross trial safety analysis. Circulation. 2008;117:2104–13.CrossRefPubMedPubMedCentral
72.
go back to reference Rogers J, Kirby LC, Hempelman SR, Berry DL, McGeer PL, Kaszniak AW, Zalinski J, Cofield M, Mansukhani L, Willson P, et al. Clinical trial of indomethacin in Alzheimer’s disease. Neurology. 1993;43:1609–11.CrossRefPubMed Rogers J, Kirby LC, Hempelman SR, Berry DL, McGeer PL, Kaszniak AW, Zalinski J, Cofield M, Mansukhani L, Willson P, et al. Clinical trial of indomethacin in Alzheimer’s disease. Neurology. 1993;43:1609–11.CrossRefPubMed
73.
go back to reference de Jong D, Jansen R, Hoefnagels W, Jellesma-Eggenkamp M, Verbeek M, Borm G, Kremer B. No effect of one-year treatment with indomethacin on Alzheimer’s disease progression: a randomized controlled trial. PLoS One. 2008;3:e1475.CrossRefPubMedPubMedCentral de Jong D, Jansen R, Hoefnagels W, Jellesma-Eggenkamp M, Verbeek M, Borm G, Kremer B. No effect of one-year treatment with indomethacin on Alzheimer’s disease progression: a randomized controlled trial. PLoS One. 2008;3:e1475.CrossRefPubMedPubMedCentral
74.
go back to reference Morihara T, Teter B, Yang F, Lim GP, Boudinot S, Boudinot FD, Frautschy SA, Cole GM. Ibuprofen suppresses interleukin-1beta induction of pro-amyloidogenic alpha1-antichymotrypsin to ameliorate beta-amyloid (Abeta) pathology in Alzheimer’s models. Neuropsychopharmacology. 2005;30:1111–20.CrossRefPubMed Morihara T, Teter B, Yang F, Lim GP, Boudinot S, Boudinot FD, Frautschy SA, Cole GM. Ibuprofen suppresses interleukin-1beta induction of pro-amyloidogenic alpha1-antichymotrypsin to ameliorate beta-amyloid (Abeta) pathology in Alzheimer’s models. Neuropsychopharmacology. 2005;30:1111–20.CrossRefPubMed
75.
go back to reference Pasqualetti P, Bonomini C, Dal Forno G, Paulon L, Sinforiani E, Marra C, Zanetti O, Rossini PM. A randomized controlled study on effects of ibuprofen on cognitive progression of Alzheimer’s disease. Aging Clin Exp Res. 2009;21:102–10.CrossRefPubMed Pasqualetti P, Bonomini C, Dal Forno G, Paulon L, Sinforiani E, Marra C, Zanetti O, Rossini PM. A randomized controlled study on effects of ibuprofen on cognitive progression of Alzheimer’s disease. Aging Clin Exp Res. 2009;21:102–10.CrossRefPubMed
76.
go back to reference Group AR, Martin BK, Szekely C, Brandt J, Piantadosi S, Breitner JC, Craft S, Evans D, Green R, Mullan M. Cognitive function over time in the Alzheimer’s Disease Anti-inflammatory Prevention Trial (ADAPT): results of a randomized, controlled trial of naproxen and celecoxib. Arch Neurol. 2008;65:896–905.CrossRef Group AR, Martin BK, Szekely C, Brandt J, Piantadosi S, Breitner JC, Craft S, Evans D, Green R, Mullan M. Cognitive function over time in the Alzheimer’s Disease Anti-inflammatory Prevention Trial (ADAPT): results of a randomized, controlled trial of naproxen and celecoxib. Arch Neurol. 2008;65:896–905.CrossRef
77.
go back to reference Reines SA, Block GA, Morris JC, Liu G, Nessly ML, Lines CR, Norman BA, Baranak CC, Rofecoxib Protocol 091 Study G. Rofecoxib: no effect on Alzheimer’s disease in a 1-year, randomized, blinded, controlled study. Neurology. 2004;62:66–71.CrossRefPubMed Reines SA, Block GA, Morris JC, Liu G, Nessly ML, Lines CR, Norman BA, Baranak CC, Rofecoxib Protocol 091 Study G. Rofecoxib: no effect on Alzheimer’s disease in a 1-year, randomized, blinded, controlled study. Neurology. 2004;62:66–71.CrossRefPubMed
78.
go back to reference Thal LJ, Ferris SH, Kirby L, Block GA, Lines CR, Yuen E, Assaid C, Nessly ML, Norman BA, Baranak CC, et al. A randomized, double-blind, study of rofecoxib in patients with mild cognitive impairment. Neuropsychopharmacology. 2005;30:1204–15.CrossRefPubMed Thal LJ, Ferris SH, Kirby L, Block GA, Lines CR, Yuen E, Assaid C, Nessly ML, Norman BA, Baranak CC, et al. A randomized, double-blind, study of rofecoxib in patients with mild cognitive impairment. Neuropsychopharmacology. 2005;30:1204–15.CrossRefPubMed
79.
go back to reference Chakrabarty P, Li A, Ceballos-Diaz C, Eddy JA, Funk CC, Moore B, DiNunno N, Rosario AM, Cruz PE, Verbeeck C, et al. IL-10 alters immunoproteostasis in APP mice, increasing plaque burden and worsening cognitive behavior. Neuron. 2015;85:519–33.CrossRefPubMedPubMedCentral Chakrabarty P, Li A, Ceballos-Diaz C, Eddy JA, Funk CC, Moore B, DiNunno N, Rosario AM, Cruz PE, Verbeeck C, et al. IL-10 alters immunoproteostasis in APP mice, increasing plaque burden and worsening cognitive behavior. Neuron. 2015;85:519–33.CrossRefPubMedPubMedCentral
80.
go back to reference Guillot-Sestier MV, Doty KR, Gate D, Rodriguez Jr J, Leung BP, Rezai-Zadeh K, Town T. Il10 deficiency rebalances innate immunity to mitigate Alzheimer-like pathology. Neuron. 2015;85:534–48.CrossRefPubMedPubMedCentral Guillot-Sestier MV, Doty KR, Gate D, Rodriguez Jr J, Leung BP, Rezai-Zadeh K, Town T. Il10 deficiency rebalances innate immunity to mitigate Alzheimer-like pathology. Neuron. 2015;85:534–48.CrossRefPubMedPubMedCentral
81.
go back to reference Latta CH, Sudduth TL, Weekman EM, Brothers HM, Abner EL, Popa GJ, Mendenhall MD, Gonzalez-Oregon F, Braun K, Wilcock DM. Determining the role of IL-4 induced neuroinflammation in microglial activity and amyloid-beta using BV2 microglial cells and APP/PS1 transgenic mice. J Neuroinflammation. 2015;12:41.CrossRefPubMedPubMedCentral Latta CH, Sudduth TL, Weekman EM, Brothers HM, Abner EL, Popa GJ, Mendenhall MD, Gonzalez-Oregon F, Braun K, Wilcock DM. Determining the role of IL-4 induced neuroinflammation in microglial activity and amyloid-beta using BV2 microglial cells and APP/PS1 transgenic mice. J Neuroinflammation. 2015;12:41.CrossRefPubMedPubMedCentral
82.
go back to reference Wang Y, Shen D, Wang VM, Yu CR, Wang RX, Tuo J, Chan CC. Enhanced apoptosis in retinal pigment epithelium under inflammatory stimuli and oxidative stress. Apoptosis. 2012;17:1144–55.CrossRefPubMedPubMedCentral Wang Y, Shen D, Wang VM, Yu CR, Wang RX, Tuo J, Chan CC. Enhanced apoptosis in retinal pigment epithelium under inflammatory stimuli and oxidative stress. Apoptosis. 2012;17:1144–55.CrossRefPubMedPubMedCentral
83.
go back to reference Chen MH, Kan HT, Liu CY, Yu WK, Lee SS, Wang JH, Hsieh SL. Serum decoy receptor 3 is a biomarker for disease severity in nonatopic asthma patients. J Formos Med Assoc. 2016;116:49–56. Chen MH, Kan HT, Liu CY, Yu WK, Lee SS, Wang JH, Hsieh SL. Serum decoy receptor 3 is a biomarker for disease severity in nonatopic asthma patients. J Formos Med Assoc. 2016;116:49–56.
84.
go back to reference Chen HF, Chen JS, Shun CT, Tsai YF, Ho HN. Decoy receptor 3 expression during the menstrual cycle and pregnancy, and regulation by sex steroids in endometrial cells in vitro. Hum Reprod. 2009;24:1350–8.CrossRefPubMed Chen HF, Chen JS, Shun CT, Tsai YF, Ho HN. Decoy receptor 3 expression during the menstrual cycle and pregnancy, and regulation by sex steroids in endometrial cells in vitro. Hum Reprod. 2009;24:1350–8.CrossRefPubMed
Metadata
Title
Amelioration of amyloid-β-induced deficits by DcR3 in an Alzheimer’s disease model
Authors
Yi-Ling Liu
Wei-Ting Chen
Yu-Yi Lin
Po-Hung Lu
Shie-Liang Hsieh
Irene Han-Juo Cheng
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Molecular Neurodegeneration / Issue 1/2017
Electronic ISSN: 1750-1326
DOI
https://doi.org/10.1186/s13024-017-0173-0

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