Brain cell type-specific enhancer-promoter interactome maps and diseaserisk association.
paper
Cited
Public
Unavailable
- Authors
- Nott, Alexi; Holtman, Inge R; Coufal, Nicole G; Schlachetzki, Johannes C M; Yu, Miao; Hu, Rong; Han, Claudia Z; Pena, Monique; Xiao, Jiayang; Wu, Yin; Keulen, Zahara; Pasillas, Martina P; O'Connor, Carolyn; Nickl, Christian K; Schafer, Simon T; Shen, Zeyang; Rissman, Robert A; Brewer, James B; Gosselin, David; Gonda, David D; Levy, Michael L; Rosenfeld, Michael G; McVicker, Graham; Gage, Fred H; Ren, Bing; Glass, Christopher K
- Year
- 2019
- Journal
- Science (New York, N.Y.)
- PMID
- 31727856
- DOI
- 10.1126/science.aay0793
- PMCID
- PMC7028213
Noncoding genetic variation is a major driver of phenotypic diversity, but functional interpretation is challenging. To better understand common genetic variation associated with brain diseases, we defined noncoding regulatory regions for major cell types of the human brain. Whereas psychiatric disorders were primarily associated with variants in transcriptional enhancers and promoters in neurons, sporadic Alzheimer's disease (AD) variants were largely confined to microglia enhancers. Interactome maps connecting disease-risk variants in cell-type-specific enhancers to promoters revealed an extended microglia gene network in AD. Deletion of a microglia-specific enhancer harboring AD-risk variants ablated expression in microglia, but not in neurons or astrocytes. These findings revise and expand the list of genes likely to be influenced by noncoding variants in AD and suggest the probable cell types in which they function.
Cell type-specific genomic regulatory region enrichments for GWAS-risk variants for brain disorders and behavioral traits. (A) UCSC browser of ATAC-seq (top panel), H3K4me3 (middle panel) and H3K27ac ChIP-seq (bottom panel) for brain nuclei populations. Shown is a representative gene for microglia (CX3CR1), neurons (NEFL), oligodendrocytes (MOG) and astrocytes (GJA1). (B) Chow-Ruskey plot of promoter regions defined for cell populations. (C) Chow-Ruskey plot of enhancer regions defined for cell populations and PsychENCODE enhancers defined using bulk brain. (D) Heatmap of LDSC analysis for genetic variants associated with brain disorders and behavior traits displayed as βlog10(q) value for significance of enrichment for promoter and enhancer regions of cell populations and PsychENCODE bulk brain enhancers. OL, oligodendrocytes.
LLM interpretation
This figure analyzes cell type-specific genomic regulatory enrichments for brain disorders and behavioral traits across four cell types (microglia, neurons, oligodendrocytes, and astrocytes). Panel A shows genomic tracks for ATAC-seq, H3K27ac, and H3K4me3 at representative genes, while panels B and C use Chow-Ruskey plots to visualize the overlap of promoter and enhancer regions. Panel D is a heatmap displaying the $-\log_{10}(q)$ values from LDSC analysis, showing varying levels of genetic variant enrichment across neurological, psychiatric, and behavioral categories for both promoters and enhancers.
Chromatin loops link promoters to active gene regulatory regions. (A) UCSC browser of ATAC-seq, and H3K27ac and H3K4me3 ChIP-seq, and PLAC-seq loops at the SALL1 locus. The microglia-specific super-enhancer is associated with microglia interactions (highlighted yellow). (B) Violin plots of ATAC-seq, H3K27ac, H3K4me3 ChIP-seq and RNA-seq log2(CPM) values at PLAC-seq upregulated interactions shown in fig. S7B for microglia, neurons and oligodendrocytes; *** = P < 1e-12; ** = P < 1e-5; * = P < 1e-3. Kruskal-Wallis-between group test. (C) Metascape enrichment analyses of active genes identified at PLAC-seq upregulated interactions shown in fig. S6D for microglia, neurons and oligodendrocytes shown as βlog10(q) values.
LLM interpretation
This figure consists of three panels analyzing chromatin loops and gene regulation in microglia, neurons, and oligodendrocytes (OLs). Panel A shows a UCSC browser track of ATAC-seq, H3K27ac, H3K4me3, and PLAC-seq loops at the *SALL1* locus, highlighting a microglia-specific super-enhancer. Panel B uses violin plots to compare $\log_2(\text{CPM})$ values across these markers and RNA-seq, showing significant enrichment (p-values indicated by asterisks) in the respective cell-type-specific interactions. Panel C displays Metascape enrichment bar charts showing the $-\log_{10}(q)$ values for biological pathways associated with each cell type.
Expanded gene network of AD-risk loci. (A) Circos plot of AD GWAS loci, showing microglia enhancers (gold bars), promoters (turquoise), open chromatin regions (black bars) and PLAC-seq interactions (black loops). Dots show z-score values of high-confidence AD variants identified by fine mapping (Kunkle, stage 1) with log10 p-value < 6e-5 (18). Blue dots represent z-score values of the credible set of AD SNPs (95% confidence); red lines show 15 high-confidence AD SNPs with a posterior probability > 0.2. (B) Chow-Ruskey plot of genes that are GWAS-assigned and PLAC-seq linked to AD-risk credible set variants in microglia, neurons and oligodendrocytes. (C)-(E) UCSC browser of interactions at AD-risk loci demonstrating (C) reassignment of GWAS-assigned genes, (D) extension of GWAS-assigned genes and (E) cell type-specific gene regulatory regions. The AD GWAS track shows meta-analysis p-values of stage 2 variants (18); line indicates p-value = 5e-8; blue dots are fine mapped 95% credible set variants.
LLM interpretation
This figure presents a gene network of Alzheimer's Disease (AD) risk loci across different cell types. Panel A is a Circos plot mapping AD GWAS loci to microglia enhancers, promoters, and PLAC-seq interactions, with dots representing z-score values of fine-mapped variants. Panel B is a Chow-Ruskey plot illustrating the cell-type specificity of GWAS-assigned and PLAC-linked variants among microglia, neurons, and oligodendrocytes. Panels C-E are UCSC browser tracks showing genomic interactions that lead to the reassignment of genes (C), extension of gene sets (D), and identification of cell-type-specific regulatory regions (E).
Deletion of a microglia-specific enhancer harboring a lead AD-risk variant affects microglia BIN1 expression. (A) UCSC browser of the BIN1 locus showing AD-risk variants, ATAC-seq, H3K27ac, H3K4me3 ChIP-seq and PLAC-seq in brain cell types. Shared active promoter region, highlighted pink; microglia-specific enhancer region, highlighted in yellow. The AD GWAS track shows meta-analysis p-values of stage 2 variants (18); line indicates p-value = 5e-8; blue dots are fine mapped 95% credible set variants. (B) Immunohistochemistry of PSCs, microglia, neurons and astrocytes in control and BIN1enh_del lines stained for the indicated cell lineage markers. (C) BIN1 gene expression in control and BIN1enh_del PSCs (N = 8,7), microglia (N = 6,5), neurons (N = 6,5) and astrocytes (N = 4,5) as RNA-seq TPM. **** Benjamini and Hochberg adjusted p-value < 0.0001. (D) Western blot of BIN1 and GAPDH in control and BIN1enh_del PSC-derived microglia (top) and neurons (bottom). (E) Protein expression of BIN1 in control and BIN1enh_del PSCs, microglia, neurons and astrocytes determined as Western blot BIN1/GAPDH mean gray intensity. N = 4 controls, 3 BIN1enh_del per cell type. ** unpaired two-tailed t-test p-value < 0.01.
LLM interpretation
This figure examines the effect of deleting a microglia-specific enhancer on *BIN1* expression. Panel A shows a genomic browser track identifying a microglia-specific enhancer (yellow) and promoter (pink) via ATAC-seq, ChIP-seq, and PLAC-seq. Panels B, C, D, and E demonstrate that while cell lineage markers remain unchanged (B), *BIN1* mRNA (C) and protein levels (D, E) are significantly reduced specifically in microglia of the $BIN1\text{enh}_{\text{del}}$ line compared to controls (p < 0.0001 for mRNA; p < 0.01 for protein), with no significant effect in PSCs, neurons, or astrocytes.
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