Anti-human TREM2 induces microglia proliferation and reduces pathology in an Alzheimer's disease model.

Wang S, Mustafa M, Yuede CM, Salazar SV, Kong P, Long H, Ward M, Siddiqui O, Paul R, Gilfillan S, Ibrahim A, Rhinn H, Tassi I, Rosenthal A, Schwabe T, Colonna M
The Journal of experimental medicine 2020
Open on PubMed

TREM2 is a receptor for lipids expressed in microglia. The R47H variant of human TREM2 impairs ligand binding and increases Alzheimer's disease (AD) risk. In mouse models of amyloid β (Aβ) accumulation, defective TREM2 function affects microglial response to Aβ plaques, exacerbating tissue damage, whereas TREM2 overexpression attenuates pathology. Thus, AD may benefit from TREM2 activation. Here, we examined the impact of an anti-human TREM2 agonistic mAb, AL002c, in a mouse AD model expressing either the common variant (CV) or the R47H variant of TREM2. Single-cell RNA-seq of microglia after acute systemic administration of AL002c showed induction of proliferation in both CV- and R47H-transgenic mice. Prolonged administration of AL002c reduced filamentous plaques and neurite dystrophy, impacted behavior, and tempered microglial inflammatory response. We further showed that a variant of AL002c is safe and well tolerated in a first-in-human phase I clinical trial and engages TREM2 based on cerebrospinal fluid biomarkers. We conclude that AL002 is a promising candidate for AD therapy.

14 Figures Extracted
Figure 1
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Figure 1.
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AL002c is a TREM2 agonist. (A) CV- and R47H-derived BMM were cultured for 7 d, harvested, and stained with AL002c (black solid line histograms) or ...
Figure S1.
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AL002c activates hTREM2 signaling and function in vitro. (A) Parental, hTREM2-CV, and -R47H 2B4 reporter cell lines were stimulated with plate-bound ...
Figure S2.
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AL002 pharmacokinetics. (A) Timeline of pharmacokinetics (PK) study of AL002 in TREM2-Bac-Tg mice. A single dose of AL002 was administered on day 0 a...
Figure 2.
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scRNA-seq analysis of microglia in treated mice. (A) Schematic of the scRNA-seq experiment. (B) UMAP of microglia subclustered from all Cd45 + c...
Figure S3.
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scRNA-seq of Cd45 + cells from brains of AL002c- and IgG-treated mice. (A) UMAP of all Cd45 + cells. Clusters were annotated using previously ident...
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Impact of antibody treatment and TREM2 variants on microglia clusters. (A) Comparison of genes’ mean cluster z-scores from microglial clusters (x a...
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AL002c expands metabolically active and proliferating microglia. (A and B) Bar plot of the percentage of cells in cluster 7 (**, P = 6.4 × 10 −3 ; ...
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AL002c reduces soluble Aβ load and modifies the conformation of Aβ plaques. (A) Timeline of AL002c treatment in CV-KO-5XFAD or R47H-KO-5XFAD mi...
Figure S4.
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Impact of AL002c treatment on total Aβ load. (A) Quantification of methoxy-X04 + area coverage in the cortex (Ctx) and hippocampus (HC) of treated m...
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AL002c ameliorates neuronal damage and impacts anxiety-like traits. (A) Representative confocal images from the cortex of indicated groups of mice,...
Figure S5.
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Impact of AL002c treatment on microglia clustering around plaques and Spp1 production (A) Representative confocal images from the hippocampus of indi...
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Impact of AL002c on microglial responses to Aβ . (A) Morphology of microglia associated with plaques (blue) highlighting the shape of cell bodies (r...
Figure 8.
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Biomarkers in first-in-human phase I clinical trial. (A and B) Administration of a single dose of AL002 caused a dose-dependent decrease in cerebro...