Cited by 32Alzheimer's disease research and treatmentsNeuroinflammation and Neurodegeneration MechanismsDementia and Cognitive Impairment Research

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APOE from astrocytes restores Alzheimer’s Aβ-pathology and DAM-like responses in APOE deficient microglia

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Abstract

The major genetic risk factor for Alzheimer’s disease (AD), APOE4 , accelerates beta-amyloid (Aβ) plaque formation, but whether this is caused by APOE expressed in microglia or astrocytes is debated. We express here the human APOE isoforms in astrocytes in an Apoe -deficient AD mouse model. This is not only sufficient to restore the amyloid plaque pathology but also induces the characteristic transcriptional pathological responses in Apoe- deficient microglia surrounding the plaques. We find that both APOE4 and the protective APOE2 from astrocytes increase fibrillar plaque deposition, but differentially affect soluble Aβ aggregates. Microglia and astrocytes show specific alterations in function of APOE genotype expressed in astrocytes. Our experiments indicate a central role of the astrocytes in APOE mediated amyloid plaque pathology and in the induction of associated microglia responses.

Overview

AI snapshot

Written from the paper’s full text.

TL;DR

Astrocyte-derived human APOE is sufficient to restore fibrillar Aβ plaque pathology and induce DAM-like microglial responses in Apoe-deficient AppNL-G-F mice. Unexpectedly, APOE2 increased fibrillar plaque deposition similarly to APOE4 relative to APOE3, while APOE4 showed a dose-dependent association with guanidine-soluble Aβ42.

Key findings

  • Astrocyte APOE restored fibrillar plaques in AAV-transduced cortex; APOE2 and APOE4 both significantly increased X-34+ plaque load versus APOE3, while APOE3 plaques were smaller and more compact (e.g., APOEKO vs APOE2 p < 0.0001; APOE2 vs APOE3 p = 0.375 for plaque number; APOE2 vs APOE4 p = 0.0061).
  • APOE4 showed a strong dose-dependent relationship with guanidine-soluble Aβ42 (R² = 0.61, slope = 0.23, p = 0.007); APOE2 followed a similar trend (R² = 0.43, slope = 0.11, p = 0.077), while APOE3 showed no association (R² = 0.006, p = 0.843).
  • Soluble Aβ aggregates were highest in APOEKO brains; APOE4 and APOE3 showed low levels, and APOE2 was intermediate (APOEKO vs APOE2 p = 0.0016; APOEKO vs APOE3 p < 0.0001; APOEKO vs APOE4 p < 0.0001).
  • Apoe-deficient microglia clustered around astrocyte-induced plaques and expressed DAM markers Cd68 and Ctsd; scRNAseq of 18,569 microglia showed APOE4 upregulation of DAM markers (Cd74, Cst7, Cd63, Cd9, Ccl6), complement genes (C1qa, C1qb, C1qc), and Nfkbia versus APOE2.
  • Astrocyte scRNAseq retained 18,667 astrocytes; APOEKO had the most DEGs versus APOE3 (375 UP, 321 DOWN), and APOE4 astrocytes downregulated autophagy-related genes (Actg1, Tax1bp1, Sqstm1, Lamp1, Lamp2).
  • Microglia depletion with PLX3397 reduced microglia by 83% (APOE2), 77% (APOE3), and 87% (APOE4); fibrillar plaques remained substantial, with only APOE4 showing a statistically significant decrease in plaque load, while APOE2 and APOE4 showed significant decreases in Aβ42 after accounting for APOE levels.

Methods

  • Human APOE2, APOE3, or APOE4 plus mCherry was expressed in astrocytes of AppNL-G-F x Apoe−/− mice using AAV2/8 under the ALDH1L1 promoter, injected ICV at postnatal day 2/3; mCherry-only AAV served as APOEKO control. Mice were analyzed at 6 months.
  • Amyloid pathology was assessed by X-34 staining and immunofluorescence; APOE and Aβ42 were quantified by MSD-ELISA; soluble Aβ aggregates were quantified by SiMPull/TIRF; microglia depletion used PLX3397 (600 mg/kg chow) from 2 to 6 months.
  • Droplet-based scRNAseq was performed on FACS-isolated mCherry+/ACSA2+ astrocytes and CD11b+/CD45-low microglia; differential expression used MAST with Bonferroni correction, and GO enrichment used g:Profiler.

Limitations

  • The paper states AAV-mediated transgene expression causes overexpression of APOE under a non-native promoter; lipidation status of APOE isoforms was not explored; gender- and ethnicity-specific effects were not investigated; and microglia could not be isolated only from AAV-transduced regions, likely diluting transcriptomic effect sizes.
  • The paper also notes that because microglia depletion began at 2 months, initial amyloid seeding may already have occurred, so a role for microglia in APOE-induced initial seeding cannot be ruled out.
  • The text makes evident that APOE expression and Aβ pathology are closely associated in this model, making it difficult to determine direct versus indirect contributors to the DEG changes in microglia and astrocytes.

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Integrity signals

Registry

Crossref · 10.1038/s44321-024-00162-7

Cites

207 of 207 references verified0 citation errors · 0 not checkable

Statistics

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Figures

Image 1
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Image 2
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Figure 1 Expression of APOE in astrocytes is sufficient to restore fibrillar Aβ plaque pathology. (A) AAV2/8 vector was used to express human APOE under the ALDH1L1 promoter. AAV particles were injected via ICV in AppNL-G-Fx Apoe−/− neonatal mice on postnatal days two or three (P2/P3). Samples were collected for analysis at 6 months of age. (B) IF images of AAV-transduced cortical regions (see Appendix Fig. S2A) at 6 months of age. mCherry (red) shows the transduced astrocytes. X-34 (white) shows the fibrillar plaque deposits. Scale bar: 100 µm. (C) Bar plots showing (i) number of X-34+ plaques per field of view (FOV, 20× magnification) and (ii) area of X-34+ plaques (as fraction of total area in FOV, 20× magnification), in the AAV-transduced cortical region. Data points show mean value of 3 fields of view per mouse (n = 6–10 mice per group). In C(i), for APOEKO vs APOE2 ****p < 0.0001; APOEKO vs APOE3 **p = 0.0036; APOEKO vs APOE4 ****p < 0.0001; APOE2 vs APOE3 p = 0.375; APOE2 vs APOE4 **p = 0.0061; APOE3 vs APOE4 ****p < 0.0001. In C(ii), for for APOEKO vs APOE2 ****p < 0.0001; APOEKO vs APOE3 p = 0.2237; APOEKO vs APOE4 ****p < 0.0001; APOE2 vs APOE3 **p = 0.0078; APOE2 vs APOE4 **p = 0.0071; APOE3 vs APOE4 ****p < 0.0001. (D) Bar plot showing total APOE levels in brain homogenates measured by MSD-ELISA. Data points show mean value for 2 technical replicates per mouse (n = 8–10 mice per group). ns = non-significant. For APOEKO vs APOE2 ****p < 0.0001; APOEKO vs APOE3 ****p < 0.0001; APOEKO vs APOE4 ****p < 0.0001; APOE2 vs APOE3 p = 0.9731; APOE2 vs APOE4 p = 0.6311; APOE3 vs APOE4 p = 0.8603. (E) Scatter plot showing linear regression between total APOE levels (x-axis) and corresponding guanidine-soluble Aβ42 levels (y-axis), measured by MSD-ELISA. Data points show mean value of 2 technical replicates per mouse (n = 8–10 mice per group). (F) TIRF images of mab 6E10-positive Aβ aggregates (white) captured from soaked brain fraction using SimPull technique. Scale bar: 10 µm. (G) Quantification of mAb 6E10-positive Aβ aggregates. Data points show mean value for 3 technical replicates per mouse (n = 4 mice per group, 9 field of views per technical replicate). For APOEKO vs APOE2 **p = 0.0016; APOEKO vs APOE3 ****p < 0.0001; APOEKO vs APOE4 ****p < 0.0001; APOE2 vs APOE3 *p = 0.0223; APOE2 vs APOE4 *p = 0.0296; APOE3 vs APOE4 p = 0.9984. Colour legend for experimental groups in (D), (E) and (G) are indicated in (C). Statistical tests: Data presented as mean ± SEM (C), (D), and (G). One-way ANOVA and Tukey’s multiple comparison test (C), (D), and (G). Source data are available online for this figure.
Figure 1 Expression of APOE in astrocytes is sufficient to restore fibrillar Aβ plaque pathology. (A) AAV2/8 vector was used to express human APOE under the ALDH1L1 promoter. AAV particles were injected via ICV in AppNL-G-Fx Apoe−/− neonatal mice on postnatal days two or three (P2/P3). Samples were collected for analysis at 6 months of age. (B) IF images of AAV-transduced cortical regions (see Appendix Fig. S2A) at 6 months of age. mCherry (red) shows the transduced astrocytes. X-34 (white) shows the fibrillar plaque deposits. Scale bar: 100 µm. (C) Bar plots showing (i) number of X-34+ plaques per field of view (FOV, 20× magnification) and (ii) area of X-34+ plaques (as fraction of total area in FOV, 20× magnification), in the AAV-transduced cortical region. Data points show mean value of 3 fields of view per mouse (n = 6–10 mice per group). In C(i), for APOEKO vs APOE2 ****p < 0.0001; APOEKO vs APOE3 **p = 0.0036; APOEKO vs APOE4 ****p < 0.0001; APOE2 vs APOE3 p = 0.375; APOE2 vs APOE4 **p = 0.0061; APOE3 vs APOE4 ****p < 0.0001. In C(ii), for for APOEKO vs APOE2 ****p < 0.0001; APOEKO vs APOE3 p = 0.2237; APOEKO vs APOE4 ****p < 0.0001; APOE2 vs APOE3 **p = 0.0078; APOE2 vs APOE4 **p = 0.0071; APOE3 vs APOE4 ****p < 0.0001. (D) Bar plot showing total APOE levels in brain homogenates measured by MSD-ELISA. Data points show mean value for 2 technical replicates per mouse (n = 8–10 mice per group). ns = non-significant. For APOEKO vs APOE2 ****p < 0.0001; APOEKO vs APOE3 ****p < 0.0001; APOEKO vs APOE4 ****p < 0.0001; APOE2 vs APOE3 p = 0.9731; APOE2 vs APOE4 p = 0.6311; APOE3 vs APOE4 p = 0.8603. (E) Scatter plot showing linear regression between total APOE levels (x-axis) and corresponding guanidine-soluble Aβ42 levels (y-axis), measured by MSD-ELISA. Data points show mean value of 2 technical replicates per mouse (n = 8–10 mice per group). (F) TIRF images of mab 6E10-positive Aβ aggregates (white) captured from soaked brain fraction using SimPull technique. Scale bar: 10 µm. (G) Quantification of mAb 6E10-positive Aβ aggregates. Data points show mean value for 3 technical replicates per mouse (n = 4 mice per group, 9 field of views per technical replicate). For APOEKO vs APOE2 **p = 0.0016; APOEKO vs APOE3 ****p < 0.0001; APOEKO vs APOE4 ****p < 0.0001; APOE2 vs APOE3 *p = 0.0223; APOE2 vs APOE4 *p = 0.0296; APOE3 vs APOE4 p = 0.9984. Colour legend for experimental groups in (D), (E) and (G) are indicated in (C). Statistical tests: Data presented as mean ± SEM (C), (D), and (G). One-way ANOVA and Tukey’s multiple comparison test (C), (D), and (G). Source data are available online for this figure.CC BY · PubMed Central
Figure EV1 Astrocyte-derived APOE modulates the size and compactness of fibrillar Aβ plaques. (A) Composite tile showing individual X-34+ fibrillar plaques, with increasing plaque size (measured in diameter) along the x-axis and increasing compactness (measured in Angular Second Moment (ASM) value) along the y-axis. Higher ASM values correlate with higher compactness. Scale bar: 10 µm. (B) Stacked bar plot showing proportion of X-34+ fibrillar plaques from APOE2, APOE3 and APOE4 groups in different size categories (diameter in µm) along the x-axis. Lower limit for plaque size set to 5 µm in diameter. Size categories used: small (5–20 µm diameter), medium (20–40 µm diameter) and large (above 40 µm diameter). (C) Box plot showing ASM values as an estimate of plaque compactness in APOE2, APOE3 and APOE4 groups. Size categories used: (i) small (5–20 µm diameter), (ii) medium (20–40 µm diameter) and (iii) large (above 40 µm diameter). Data points show value for individual plaques (n = 6–10 mice per group. 3 FOV per mouse). In C(i), APOE2 vs APOE3 **p = 0.0093; APOE2 vs APOE4 p = 0.547; APOE3 vs APOE4 ***p = 0.0003. In C(ii), APOE2 vs APOE3 ***p = 0.0001; APOE2 vs APOE4 p = 0.9818; APOE3 vs APOE4 ****p < 0.0001. In C(iii), APOE2 vs APOE3 ****p < 0.0001; APOE2 vs APOE4 p = 0.471; APOE3 vs APOE4 ****p < 0.0001. Statistical tests: Data presented as median and interquartile range ± values within 1.5 times the interquartile range (C). Minima and maxima for box plots in C(i) APOE2 (0.001, 0.0457), APOE3 (0.0011, 0.0501), APOE4 (0.0007, 0.0565); in C(ii) APOE2 (0.0011, 0.0106), APOE3 (0.0015, 0.0184), APOE4 (0.0008, 0.0111); in C(iii) APOE2 (0.0012, 0.0106), APOE3 (0.0024, 0.0097), APOE4 (0.0009, 0.0095). Linear mixed effects model with Tukey’s HSD test in (C) done at mouse sample level.
Figure EV1 Astrocyte-derived APOE modulates the size and compactness of fibrillar Aβ plaques. (A) Composite tile showing individual X-34+ fibrillar plaques, with increasing plaque size (measured in diameter) along the x-axis and increasing compactness (measured in Angular Second Moment (ASM) value) along the y-axis. Higher ASM values correlate with higher compactness. Scale bar: 10 µm. (B) Stacked bar plot showing proportion of X-34+ fibrillar plaques from APOE2, APOE3 and APOE4 groups in different size categories (diameter in µm) along the x-axis. Lower limit for plaque size set to 5 µm in diameter. Size categories used: small (5–20 µm diameter), medium (20–40 µm diameter) and large (above 40 µm diameter). (C) Box plot showing ASM values as an estimate of plaque compactness in APOE2, APOE3 and APOE4 groups. Size categories used: (i) small (5–20 µm diameter), (ii) medium (20–40 µm diameter) and (iii) large (above 40 µm diameter). Data points show value for individual plaques (n = 6–10 mice per group. 3 FOV per mouse). In C(i), APOE2 vs APOE3 **p = 0.0093; APOE2 vs APOE4 p = 0.547; APOE3 vs APOE4 ***p = 0.0003. In C(ii), APOE2 vs APOE3 ***p = 0.0001; APOE2 vs APOE4 p = 0.9818; APOE3 vs APOE4 ****p < 0.0001. In C(iii), APOE2 vs APOE3 ****p < 0.0001; APOE2 vs APOE4 p = 0.471; APOE3 vs APOE4 ****p < 0.0001. Statistical tests: Data presented as median and interquartile range ± values within 1.5 times the interquartile range (C). Minima and maxima for box plots in C(i) APOE2 (0.001, 0.0457), APOE3 (0.0011, 0.0501), APOE4 (0.0007, 0.0565); in C(ii) APOE2 (0.0011, 0.0106), APOE3 (0.0015, 0.0184), APOE4 (0.0008, 0.0111); in C(iii) APOE2 (0.0012, 0.0106), APOE3 (0.0024, 0.0097), APOE4 (0.0009, 0.0095). Linear mixed effects model with Tukey’s HSD test in (C) done at mouse sample level.CC BY · PubMed Central
Figure 2 APOE expression and astrocyte cell-states in AppNL-G-F mouse brain. (A) UMAP plot showing 18,667 astrocytes (mCherry+/Acsa2+) sorted from 6 months old mouse brains from the four experimental groups (n = 2–3 mice per group). Different sub-populations identified have been assigned Cluster numbers. Dotted lines separate the clusters with telencephalon astrocyte signatures. (B) Dot plot showing the top 10 differentially expressed genes in each cluster. Colour scale indicates normalized expression level, scaled per gene (z-score). Dot size indicates percentage of cells, in each cluster, expressing the gene. (C) Bar plot showing the proportion of astrocytes from each experimental group present in the different clusters. (D) Bar plot showing top 10 significantly enriched GO Biological process terms for Clusters a0 and a6, ordered according to −log10(adjusted p-value). Statistical tests: g:SCS multiple testing correction method (Kolberg et al, 2023) in (D) applying significance threshold of 0.05.
Figure 2 APOE expression and astrocyte cell-states in AppNL-G-F mouse brain. (A) UMAP plot showing 18,667 astrocytes (mCherry+/Acsa2+) sorted from 6 months old mouse brains from the four experimental groups (n = 2–3 mice per group). Different sub-populations identified have been assigned Cluster numbers. Dotted lines separate the clusters with telencephalon astrocyte signatures. (B) Dot plot showing the top 10 differentially expressed genes in each cluster. Colour scale indicates normalized expression level, scaled per gene (z-score). Dot size indicates percentage of cells, in each cluster, expressing the gene. (C) Bar plot showing the proportion of astrocytes from each experimental group present in the different clusters. (D) Bar plot showing top 10 significantly enriched GO Biological process terms for Clusters a0 and a6, ordered according to −log10(adjusted p-value). Statistical tests: g:SCS multiple testing correction method (Kolberg et al, 2023) in (D) applying significance threshold of 0.05.CC BY · PubMed Central
Figure 3 APOE isoforms modulate astrocyte transcriptome in AppNL-G-F mouse brain. (A) Upset plot showing number of differentially expressed genes (UP or DOWN) in telencephalon astrocytes from each experimental group, compared to APOE3 group. Bar plot shows the number of differentially expressed genes (DEGs) common between different DE analyses (overlapping sets indicated by black dots in column below the bars). Bars are coloured according to statistical significance of intersection of DEGs. (B) Volcano plot showing differentially expressed genes between telencephalon astrocytes and APOE3 expressing telencephalon astrocytes. Data points for significant genes are coloured (Red for UP and blue for DOWN). Significance assigned based on |Log2(Fold Change)| > 0.2 and adjusted p-value < 0.05. (C) Violin plot showing normalized gene expression for Pde10a in telencephalon astrocytes from the experimental groups. (n = 2–3 mice per group) (D) Quadrant plot comparing differential expression of genes in telencephalon astrocytes in APOE2 vs APOE3 (along x-axis) and in APOE4 vs APOE3 (along y-axis). Colours in legend key indicate significance of genes up- or downregulated in APOE2 or APOE4 or both. Significance of differentially expressed genes based on |Log2(Fold Change)| > 0.2 and adjusted p-value < 0.05). Pearson’s correlation, R = 0.5. Statistical tests: MAST differential expression test in (A), (B) and (D), p-values were adjusted with Bonferroni correction based on the total number of genes in the dataset. SuperExactTest (Wang et al, 2015) in (A). Source data are available online for this figure.
Figure 3 APOE isoforms modulate astrocyte transcriptome in AppNL-G-F mouse brain. (A) Upset plot showing number of differentially expressed genes (UP or DOWN) in telencephalon astrocytes from each experimental group, compared to APOE3 group. Bar plot shows the number of differentially expressed genes (DEGs) common between different DE analyses (overlapping sets indicated by black dots in column below the bars). Bars are coloured according to statistical significance of intersection of DEGs. (B) Volcano plot showing differentially expressed genes between telencephalon astrocytes and APOE3 expressing telencephalon astrocytes. Data points for significant genes are coloured (Red for UP and blue for DOWN). Significance assigned based on |Log2(Fold Change)| > 0.2 and adjusted p-value < 0.05. (C) Violin plot showing normalized gene expression for Pde10a in telencephalon astrocytes from the experimental groups. (n = 2–3 mice per group) (D) Quadrant plot comparing differential expression of genes in telencephalon astrocytes in APOE2 vs APOE3 (along x-axis) and in APOE4 vs APOE3 (along y-axis). Colours in legend key indicate significance of genes up- or downregulated in APOE2 or APOE4 or both. Significance of differentially expressed genes based on |Log2(Fold Change)| > 0.2 and adjusted p-value < 0.05). Pearson’s correlation, R = 0.5. Statistical tests: MAST differential expression test in (A), (B) and (D), p-values were adjusted with Bonferroni correction based on the total number of genes in the dataset. SuperExactTest (Wang et al, 2015) in (A). Source data are available online for this figure.CC BY · PubMed Central
Figure 4 Apoe-deficient microglia mount reactive responses to fibrillar amyloid plaques. (A) IF images of AAV-transduced cortical regions (see Appendix Fig. S2A), at 6 months of age. mCherry (red) shows the transduced astrocytes. X-34 staining (white) shows the fibrillar plaque deposits. Co-staining with anti-Iba1 antibody shows microglial cells (green). Scale bar: 100 µm. (B) IF images of AAV-APOE4 transduced cortical regions (see Appendix Fig. S2A) at 6 months of age. X-34 staining (white) shows the fibrillar plaque deposits. Co-staining with anti-Iba1 antibody shows microglial cells (green) and anti-Cd68 antibody shows phagocytic structures (red) inside microglia surrounding plaques. Scale bar: 100 µm. (C) IF images of AAV-APOE4 transduced cortical regions at 6 months of age. X-34 staining (white) shows the fibrillar plaque deposits. Co-staining with anti-Iba1 antibody shows microglia (green) and anti-CtsD antibody shows lysosomal structures (red) inside clustered microglia surrounding plaques. Scale bar: 100 µm. (D) (i) Bar plot showing total number of microglia per field of view (FOV, 40× magnification) in AAV-transduced regions. Data points show mean value of 3 fields of view per mouse (n = 6–7 mice per group). For APOEKO vs APOE2 **p = 0.0056; APOEKO vs APOE3 p = 0.3957; APOEKO vs APOE4 ****p < 0.0001; APOE2 vs APOE3 p = 0.1562; APOE2 vs APOE4 ****p < 0.0001; APOE3 vs APOE4 ****p < 0.0001. (ii) Scatter plot showing linear regression between area of X-34+ staining (as fraction of total area in FOV) and total number of microglia (solid triangle), or number of plaque-associated microglia (solid circle), or number of non-plaque-associated microglia (hollow circle), for each experimental group. Data points show mean value 3 fields of view per mouse (n = 6–7 mice per group). Shape legends for different categories of microglia in (i) and (ii) are indicated. Statistical tests: Data presented as mean ± SEM (Di). One-way ANOVA and Tukey’s multiple comparison test in (Di). Source data are available online for this figure.
Figure 4 Apoe-deficient microglia mount reactive responses to fibrillar amyloid plaques. (A) IF images of AAV-transduced cortical regions (see Appendix Fig. S2A), at 6 months of age. mCherry (red) shows the transduced astrocytes. X-34 staining (white) shows the fibrillar plaque deposits. Co-staining with anti-Iba1 antibody shows microglial cells (green). Scale bar: 100 µm. (B) IF images of AAV-APOE4 transduced cortical regions (see Appendix Fig. S2A) at 6 months of age. X-34 staining (white) shows the fibrillar plaque deposits. Co-staining with anti-Iba1 antibody shows microglial cells (green) and anti-Cd68 antibody shows phagocytic structures (red) inside microglia surrounding plaques. Scale bar: 100 µm. (C) IF images of AAV-APOE4 transduced cortical regions at 6 months of age. X-34 staining (white) shows the fibrillar plaque deposits. Co-staining with anti-Iba1 antibody shows microglia (green) and anti-CtsD antibody shows lysosomal structures (red) inside clustered microglia surrounding plaques. Scale bar: 100 µm. (D) (i) Bar plot showing total number of microglia per field of view (FOV, 40× magnification) in AAV-transduced regions. Data points show mean value of 3 fields of view per mouse (n = 6–7 mice per group). For APOEKO vs APOE2 **p = 0.0056; APOEKO vs APOE3 p = 0.3957; APOEKO vs APOE4 ****p < 0.0001; APOE2 vs APOE3 p = 0.1562; APOE2 vs APOE4 ****p < 0.0001; APOE3 vs APOE4 ****p < 0.0001. (ii) Scatter plot showing linear regression between area of X-34+ staining (as fraction of total area in FOV) and total number of microglia (solid triangle), or number of plaque-associated microglia (solid circle), or number of non-plaque-associated microglia (hollow circle), for each experimental group. Data points show mean value 3 fields of view per mouse (n = 6–7 mice per group). Shape legends for different categories of microglia in (i) and (ii) are indicated. Statistical tests: Data presented as mean ± SEM (Di). One-way ANOVA and Tukey’s multiple comparison test in (Di). Source data are available online for this figure.CC BY · PubMed Central
Figure EV2 Astrocyte-derived APOE influences the expression of microglial cell state markers. (A) UMAP plot showing 18,569 APOE-deficient microglia (Cd11b+/Cd45-low) sorted from 6 months old mouse brains from the four experimental groups (n = 2 or 3 mice per group). Different sub-populations identified through unbiased clustering have been assigned cluster numbers. (B) Dot plot showing the top 10 differentially expressed genes in each cluster. Colour scale indicates normalized expression level, scaled per gene (z-score). Dot size indicates percentage of cells, in each cluster, expressing the gene. (C) Bar plot showing the proportion of microglia from each experimental group present in the different clusters.
Figure EV2 Astrocyte-derived APOE influences the expression of microglial cell state markers. (A) UMAP plot showing 18,569 APOE-deficient microglia (Cd11b+/Cd45-low) sorted from 6 months old mouse brains from the four experimental groups (n = 2 or 3 mice per group). Different sub-populations identified through unbiased clustering have been assigned cluster numbers. (B) Dot plot showing the top 10 differentially expressed genes in each cluster. Colour scale indicates normalized expression level, scaled per gene (z-score). Dot size indicates percentage of cells, in each cluster, expressing the gene. (C) Bar plot showing the proportion of microglia from each experimental group present in the different clusters.CC BY · PubMed Central
Figure EV3 Astrocyte-derived APOE modulates gene expression in microglia. (A) Upset plot showing number of differentially expressed genes (UP or DOWN) in microglia from each experimental group, compared to APOE3 group. Bar plot shows the number of differentially expressed genes (DEGs) common between different DE analyses (overlapping sets indicated by black dots in column below the bars). Bars are coloured according to statistical significance of intersection of DEGs. (B) Volcano plot showing differentially expressed genes between APOEKO telencephalon astrocytes and APOE3 expressing telencephalon astrocytes. Data points for significant genes are coloured (Red for UP and blue for DOWN). Significance assigned based on |Log2(Fold Change)| > 0.2 and adjusted p-value < 0.05. Genes discussed in text are indicated in red. (C) Dot plot showing expression of the 52 genes (Fig. 2A) commonly upregulated in APOEKO and APOE4 microglia, split by experimental groups. Colour scale indicates normalized expression level, scaled per gene (z-score). Dot size indicates percentage of cells, in each group, expressing the gene. Plaque-induced genes (PIGs) (Chen et al, 2020) are coloured in red on y-axis. (D) Quadrant plot comparing differential expression of genes in microglia in APOE2 vs APOE3 (along x-axis) and in APOE4 vs APOE3 (along y-axis). Colours in legend key indicate statistical significance of genes up- or downregulated in APOE2 or APOE4 or both. Significance of differentially expressed genes based on |Log2(Fold Change)| > 0.2 and adjusted p-value < 0.05). Pearson’s correlation, R = 0.52. Statistical tests: MAST differential expression test in (B), (C) and (D), p-values were adjusted with Bonferroni correction based on the total number of genes in the dataset.
Figure EV3 Astrocyte-derived APOE modulates gene expression in microglia. (A) Upset plot showing number of differentially expressed genes (UP or DOWN) in microglia from each experimental group, compared to APOE3 group. Bar plot shows the number of differentially expressed genes (DEGs) common between different DE analyses (overlapping sets indicated by black dots in column below the bars). Bars are coloured according to statistical significance of intersection of DEGs. (B) Volcano plot showing differentially expressed genes between APOEKO telencephalon astrocytes and APOE3 expressing telencephalon astrocytes. Data points for significant genes are coloured (Red for UP and blue for DOWN). Significance assigned based on |Log2(Fold Change)| > 0.2 and adjusted p-value < 0.05. Genes discussed in text are indicated in red. (C) Dot plot showing expression of the 52 genes (Fig. 2A) commonly upregulated in APOEKO and APOE4 microglia, split by experimental groups. Colour scale indicates normalized expression level, scaled per gene (z-score). Dot size indicates percentage of cells, in each group, expressing the gene. Plaque-induced genes (PIGs) (Chen et al, 2020) are coloured in red on y-axis. (D) Quadrant plot comparing differential expression of genes in microglia in APOE2 vs APOE3 (along x-axis) and in APOE4 vs APOE3 (along y-axis). Colours in legend key indicate statistical significance of genes up- or downregulated in APOE2 or APOE4 or both. Significance of differentially expressed genes based on |Log2(Fold Change)| > 0.2 and adjusted p-value < 0.05). Pearson’s correlation, R = 0.52. Statistical tests: MAST differential expression test in (B), (C) and (D), p-values were adjusted with Bonferroni correction based on the total number of genes in the dataset.CC BY · PubMed Central
Figure 5 Astrocyte-derived APOE initiates, and microglia modify, fibrillar Aβ plaque pathology. (A) Experimental design illustrating PLX3397 treatment for microglial depletion in AppNL-G-F x Apoe−/− mice. Treatment started at 2 months of age by mixing PLX3397 (600 mg/kg) in chow and samples were collected for analysis at 6 months of age. (B) IF images of AAV-transduced cortical regions (see Appendix Fig. S2A) at 6 months of age from control and PLX3397-treated groups. Please note that the control group is the same cohort as used in Fig. 1. mCherry (red) shows the transduced astrocytes. X-34 staining (white) shows the fibrillar plaque deposits in mouse brain cortex. Co-staining with anti-Iba1 antibody shows microglial cells (green). Scale bar: 100 µm. The images of the control experimental group were re-captured from the same mouse cohort samples used for experimental groups in Fig. 1B which is the reason why panel 2 in column 1 partially overlaps with panel 3 in column 3 of Fig. 1. (C) Bar plots showing number of X-34+ plaques per field of view (FOV, 20× magnification) and area of X-34+ plaques (as fraction of total area in FOV, 20× magnification), in the AAV-transduced cortical region for (i) APOE2, (ii) APOE3 and (iii) APOE4 groups and their respective PLX3397-treated groups. Data points show mean value of 3 fields of view per mouse (n = 4–10 mice per group). Data points for control non-treated groups are the same as shown in Fig. 1C. (D) Scatter plot showing linear regression between total APOE levels (x-axis) and corresponding guanidine-soluble Aβ42 levels (y-axis), measured by MSD-ELISA for PLX3397-treated and control mice from (i) APOE2, (ii) APOE3 and (iii) APOE4 groups. Data points show mean value for each mouse (n = 4–10 mice per group. 2 technical replicates per mouse). Data points for control non-treated groups are the same as shown in Fig. 1E. Statistical tests: Data represented as mean ± SEM in (C). Unpaired t-test in (C). p-values are indicated. Source data are available online for this figure.
Figure 5 Astrocyte-derived APOE initiates, and microglia modify, fibrillar Aβ plaque pathology. (A) Experimental design illustrating PLX3397 treatment for microglial depletion in AppNL-G-F x Apoe−/− mice. Treatment started at 2 months of age by mixing PLX3397 (600 mg/kg) in chow and samples were collected for analysis at 6 months of age. (B) IF images of AAV-transduced cortical regions (see Appendix Fig. S2A) at 6 months of age from control and PLX3397-treated groups. Please note that the control group is the same cohort as used in Fig. 1. mCherry (red) shows the transduced astrocytes. X-34 staining (white) shows the fibrillar plaque deposits in mouse brain cortex. Co-staining with anti-Iba1 antibody shows microglial cells (green). Scale bar: 100 µm. The images of the control experimental group were re-captured from the same mouse cohort samples used for experimental groups in Fig. 1B which is the reason why panel 2 in column 1 partially overlaps with panel 3 in column 3 of Fig. 1. (C) Bar plots showing number of X-34+ plaques per field of view (FOV, 20× magnification) and area of X-34+ plaques (as fraction of total area in FOV, 20× magnification), in the AAV-transduced cortical region for (i) APOE2, (ii) APOE3 and (iii) APOE4 groups and their respective PLX3397-treated groups. Data points show mean value of 3 fields of view per mouse (n = 4–10 mice per group). Data points for control non-treated groups are the same as shown in Fig. 1C. (D) Scatter plot showing linear regression between total APOE levels (x-axis) and corresponding guanidine-soluble Aβ42 levels (y-axis), measured by MSD-ELISA for PLX3397-treated and control mice from (i) APOE2, (ii) APOE3 and (iii) APOE4 groups. Data points show mean value for each mouse (n = 4–10 mice per group. 2 technical replicates per mouse). Data points for control non-treated groups are the same as shown in Fig. 1E. Statistical tests: Data represented as mean ± SEM in (C). Unpaired t-test in (C). p-values are indicated. Source data are available online for this figure.CC BY · PubMed Central

Verification

Claims the paper makes

45 Own result · 43 Own method · 35 Own interpretation · 20 Partly supported · 16 Supported · 6 Supported so far · 5 No basis given · 3 No full text of the sources · 1 Mixed support · 1 Couldn’t confirm · 1 Sources not found · accuracy not yet measured

Show all 61 claims

  • Probably not a substantial claim. 73
  • It may state two separate claims as one. 62
115 of 115
  • The paper relies on this without support.

    The AppNL-G-F x Apoe−/− mouse model is a valid model for studying APOE’s role in amyloid plaque pathology in Alzheimer’s disease.

    “In order to study the role of astrocyte-derived APOE on amyloid plaque pathology, we expressed the different human APOE isoforms (further referred to as APOE2, APOE3 and APOE4), along with reporter mCherry protein, specifically in astrocytes in an Apoe-deficient AD mouse model (AppNL-G-F x Apoe−/−)”
  • The paper relies on this without support.

    The human APOE isoforms expressed in mouse astrocytes reproduce the isoform-specific effects of human APOE in Alzheimer’s disease.

    “We express here the human APOE isoforms in astrocytes in an Apoe-deficient AD mouse model.”
  • The paper relies on this without support.

    APOE3 is neutral.

    “APOE3 that is considered neutral”
  • The paper relies on this without support.

    APOE is secreted by astrocytes and taken up via LDL receptors into endosomal compartments of all cell types in the brain, including microglia and astrocytes.

    “For the interpretation of the data, it is important to take into account that APOE is secreted here only by astrocytes but is taken up via LDL receptors into the endosomal compartments of all cell types in the brain, including the microglia and astrocytes.”
  • The paper relies on this without support.

    APOE is under a constitutive promoter based on viral transduction and is not part of the normal transcriptional regulatory networks.

    “In this overexpression model, since APOE is under a constitutive promoter based on viral transduction, and hence not a part of the normal transcriptional regulatory networks, we excluded human APOE gene expression from both astrocyte and microglia datasets prior to the following steps.”
5 of 5

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

1 of 1

Citations

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Metadata

Authors
Preman, P., Moechars, D., Fertan, E., Wolfs, L., Serneels, L., Shah, D., Lamote, J., Poovathingal, S., Snellinx, A., Mancuso, R., Balusu, S., Klenerman, D., Arranz, A. M., Fiers, M., & De Strooper, B.
Affiliations
  • VIB-KU Leuven Center for Brain & Disease Research (BE)
  • University of Cambridge (GB)
  • VIB-KU Leuven Center for Cancer Biology (BE)
  • University of Antwerp (BE)
  • Ikerbasque (ES)
Corresponding author
Fiers, Mark
Venue
EMBO Molecular Medicine
Published
2024-11-11
Volume
16
Issue
12
Pages
3113-3141
ISSN
  • 1757-4676 (ISSN-L)
  • 1757-4684
OpenAlex
W4404242617
Cited by
32
References
203
Citations by year
2026: 21 · 2025: 9 · 2024: 2
FWCI
9.04
Type
journal article
Language
en
Open access
Locations
  • EMBO Molecular Medicine (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • UCL Discovery (University College London) (submittedVersion, cc-by)
  • Lirias (KU Leuven) (submittedVersion, cc-by)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • UK Research and Innovation (MR/Y014847/1)
  • EC | European Research Council (ERC-834682)
  • Vlaams Instituut voor Biotechnologie
  • KU Leuven
  • UK Dementia Research Institute
  • Fonds voor Wetenschappelijk Onderzoek
  • The Queen Elisabeth Medical Foundation for Neurosciences
  • Leuven Universitair Fonds
  • The Belgian Alzheimer Research Foundation
  • Alzheimer's Association USA
  • Ministerio de Ciencia e Innovación (MCIN/AEI/10.13039/501100011033)
  • Basque government, Spain (PIBA-2020-1-0030)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
  • Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Keywords
apolipoprotein E, Alzheimer's disease, astrocytes, microglia, amyloid plaques, APOE ε4, APOE2, ApoE-deficient mice, astrocyte-microglia interaction, APOE isoforms
MeSH terms
Alzheimer Disease, Animals, Apolipoproteins E, Astrocytes, Disease Models, Animal, Humans, Mice, Transgenic, Amyloid beta-Peptides, Microglia, Mice, Apolipoprotein E4, Plaque, Amyloid

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