A computational tool (H-MAGMA) for improved prediction of brain-disorder risk genes by incorporating brain chromatin interaction profiles.
paper
Cited
Public
- Authors
- Sey, Nancy Y A; Hu, Benxia; Mah, Won; Fauni, Harper; McAfee, Jessica Caitlin; Rajarajan, Prashanth; Brennand, Kristen J; Akbarian, Schahram; Won, Hyejung
- Year
- 2020
- Journal
- Nature neuroscience
- PMID
- 32152537
- DOI
- 10.1038/s41593-020-0603-0
- PMCID
- PMC7131892
Most risk variants for brain disorders identified by genome-wide association studies reside in the noncoding genome, which makes deciphering biological mechanisms difficult. A commonly used tool, multimarker analysis of genomic annotation (MAGMA), addresses this issue by aggregating single nucleotide polymorphism associations to nearest genes. Here we developed a platform, Hi-C-coupled MAGMA (H-MAGMA), that advances MAGMA by incorporating chromatin interaction profiles from human brain tissue across two developmental epochs and two brain cell types. By analyzing gene regulatory relationships in the disease-relevant tissue, H-MAGMA identified neurobiologically relevant target genes. We applied H-MAGMA to five psychiatric disorders and four neurodegenerative disorders to interrogate biological pathways, developmental windows and cell types implicated for each disorder. Psychiatric-disorder risk genes tended to be expressed during mid-gestation and in excitatory neurons, whereas neurodegenerative-disorder risk genes showed increasing expression over time and more diverse cell-type specificities. H-MAGMA adds to existing analytic frameworks to help identify the neurobiological principles of brain disorders.
Schematics of H-MAGMA approach.a. H-MAGMA leverages chromatin interaction profiles (Hi-C) to assign intergenic and intronic SNPs to cognate genes. We have applied this framework to five psychiatric disorders and four degenerative disorders using Hi-C datasets from the fetal and adult brain. In return, H-MAGMA provides gene-level association statistics, which can be used to elucidate biological mechanisms underlying brain disorders. b. Intronic and intergenic SNPs are often annotated to distal genes. c. SNPs mapped to H-MAGMA selective genes explain a significant proportion of heritability. Top graph: Heritability enrichment Β± standard error; enrichment denotes proportion of heritability/proportion of SNPs; red dotted line, enrichment=1. Bottom graph: false discovery rate (FDR) of heritability enrichment; red dotted line, FDR=0.05. d. Overlap between SCZ-associated genes identified by H-MAGMA, TWAS, and coloc.
Overlap between brain disorder risk genes derived from neuronal and astrocytic H-MAGMABrain disorder risk genes (FDR<0.05) were compared between neuronal and astrocytic H-MAGMA results.
Psychiatric disorder risk genes predicted by H-MAGMA are dysregulated in postmortem brains of individuals with psychiatric disorders.a. Overlap between common variation associated genes and genes differentially expressed (DEG) in postmortem brains with psychiatric disorders. b. Overlap between common variation associated genes and co-expression (co-exp) modules differentially regulated in psychiatric disorders. Down, modules are downregulated in disorders; Up, modules are upregulated in disorders.
Genetic relationships among brain disorders.a. Psychiatric disorders show strong genetic relationships both at the level of genetic correlations (bottom left, rg) and gene-level overlaps (top right, RRHO). BY FDR, P-values adjusted by the Benjamini and Yekutieli procedure. b. Genetic correlations measured with Pearsonβs correlation (rg) and gene-level overlaps (RRHO Z) are highly correlated, indicating that gene-level overlaps obtained by H-MAGMA recapitulate genetic correlations. Brain disorders that show strong genetic correlations (rg > 0.2) and gene-level overlaps (RRHO Z > 15) are marked in blue. Linear regression line with 95% confidence bands.
Spatiotemporal dynamics of brain disorder risk genes.a. Heritability enrichment of brain disorders in active regulatory elements of the fetal and adult brain. Enrichment Β± standard error (circle) and significance of heritability enrichment (triangle) are depicted. b-c. Developmental expression trajectories of brain disorder risk genes. PCW, post-conception week; M, month; Y, year. (Left) N = 410 and 453 for prenatal and postnatal samples, respectively. Center, median; box = 1st-3rd quartiles (Q); minima, Q1 β 1.5 x interquartile range (IQR); maxima, Q3 + 1.5 x IQR. (Right) LOESS smooth curve with 95% confidence bands.
Cellular expression profiles of brain disorder risk genes.a. We used neuronal and astrocytic H-MAGMA to annotate psychiatric disorder and degenerative disorder GWAS, respectively. Psychiatric disorder-associated genes are highly expressed in neurons, while neurogenerative disorder-associated genes exhibit glial signatures. Astro, astrocytes; Micro, microglia; Endo, endothelial cells; Oligo, oligodendrocytes; OPC, oligodendrocytes progenitor cells; Ex, excitatory neurons; In, inhibitory neurons; GBM, glioblastoma multiforme tumor. b-c. Developmental expression trajectories of psychiatric disorder-associated genes (b) and degenerative disorder-associated genes (c). PCW, post-conception week; M, month; Y, year. (Left) N = 410 and 453 for prenatal and postnatal samples, respectively. Center, median; box=Q1-Q3; minima, Q1 β 1.5 x IQR; maxima, Q3 + 1.5 x IQR. (Right) LOESS smooth curve with 95% confidence bands.
Characteristics of brain disorder risk genes.a. AD-associated genes are dysregulated in oligodendrocytes and microglia from AD postmortem brains (single-cell RNA-seq DEG). b. Comparison of brain disorder risk genes with common and rare variation. Only significant associations (FDR<0.1) were depicted.
Pleiotropic genes reveal shared molecular mechanisms of psychiatric disorders.a. Comparison between pleiotropic genes and genes mapped to non-pleiotropic and pleiotropic GWS loci. Odds ratio (OR) and 95% confidence intervals (CI). b. Gene ontology enrichment of pleiotropic genes. c. A developmental expression trajectory of pleiotropic genes. LOESS smooth curve with 95% confidence bands. d. Cell-type specific expression profiles of pleiotropic genes.
Comparison between H-MAGMA and cMAGMAa. The number and proportion of intronic and intergenic SNPs annotated to proximal and distal genes. SNPs mapped to proximal genes may also have distal associations, while SNPs mapped to distal genes do not have any association with proximal genes. b. The number of brain disorder risk genes (genes that are significantly associated with each brain disorder at a threshold of FDR<0.05) predicted by H-MAGMA and cMAGMA. % H-MAGMA denotes the percentage of H-MAGMA selective genes (genes that were identified by H-MAGMA but not by cMAGMA). c. The number of SNPs assigned to each gene for H-MAGMA and cMAGMA. Center, median; box=1st-3rd quartiles (Q); minima, Q1 β 1.5 x interquartile range (IQR); maxima, Q3 + 1.5 x IQR. d. The number and proportion of SNPs annotated to the cognate genes by H-MAGMA and cMAGMA. e. H-MAGMA selective SNPs (SNPs assigned to H-MAGMA selective genes in H-MAGMA β SNPs assigned to H-MAGMA selective genes in cMAGMA) explain a significant proportion of heritability. Top graph: Heritability enrichment Β± standard error; enrichment denotes proportion of heritability/proportion of SNPs; red dotted line, enrichment=1. Bottom graph: false discovery rate (FDR) of heritability enrichment: red dotted line, FDR=0.05.
Heritability enrichment of brain disorders in active regulatory elements of multiple tissue/cell types.(Top) Scaled enrichment values. (Bottom) Significance of heritability enrichment (P-values). ESC, embryonic stem cells. ESDR, embryonic stem cell derived cell lines.
Developmental expression trajectories of brain disorder risk genes derived from cMAGMAPCW, post-conception week; M, month; Y, year. (Left) N = 410 and 453 for prenatal and postnatal samples, respectively. Center, median; box=Q1-Q3; lower whisker, Q1 β 1.5 x IQR; upper whisker, Q3 + 1.5 x IQR. (Right) LOESS smooth curve with 95% confidence bands.
Cellular expression profiles of brain disorder risk genes.a. Cellular expression profiles of brain disorder risk genes derived from H-MAGMA and cMAGMA. Psychiatric disorder-associated genes are highly expressed in neurons, while neurogenerative disorder-associated genes show glial signatures. Astro, astrocytes; Micro, microglia; Endo, endothelial cells; Oligo, oligodendrocytes; OPC, oligodendrocytes progenitor cells. b. Psychiatric disorder-associated genes are highly expressed in radial glia and excitatory neurons in the developing cortex. RG, radial glia, vRG; ventricular RG; oRG, outer RG; tRG, truncated RG; IPC, intermediate progenitor cells; Ex, excitatory neurons; In, inhibitory neurons; nEx/nIn, newly born excitatory/inhibitor neurons; PFC, prefrontal cortex; V1, visual cortex; CGE, caudal ganglionic eminence; MGE, medial ganglionic eminence.
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