The DOI matches its Crossref record; 46 of the 46 references it cites were found in a registry or an index.
Chromosome conformation elucidates regulatory relationships in developing human brain
Open accessAbstract
Three-dimensional physical interactions within chromosomes dynamically regulate gene expression in a tissue-specific manner. However, the 3D organization of chromosomes during human brain development and its role in regulating gene networks dysregulated in neurodevelopmental disorders, such as autism or schizophrenia, are unknown. Here we generate high-resolution 3D maps of chromatin contacts during human corticogenesis, permitting large-scale annotation of previously uncharacterized regulatory relationships relevant to the evolution of human cognition and disease. Our analyses identify hundreds of genes that physically interact with enhancers gained on the human lineage, many of which are under purifying selection and associated with human cognitive function. We integrate chromatin contacts with non-coding variants identified in schizophrenia genome-wide association studies (GWAS), highlighting multiple candidate schizophrenia risk genes and pathways, including transcription factors involved in neurogenesis, and cholinergic signalling molecules, several of which are supported by independent expression quantitative trait loci and gene expression analyses. Genome editing in human neural progenitors suggests that one of these distal schizophrenia GWAS loci regulates FOXG1 expression, supporting its potential role as a schizophrenia risk gene. This work provides a framework for understanding the effect of non-coding regulatory elements on human brain development and the evolution of cognition, and highlights novel mechanisms underlying neuropsychiatric disorders.
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In the citing paper
“In contrast, this interaction was not observed in Hi-C experiments performed in cells neither from adult human dorsolateral prefrontal cortex (Schmitt et al. 2016; supplementary fig. S9, Supplementary Material online) nor from developing human cerebral cortex at mid-gestation (Won et al. 2016; supplementary fig. S10, Supplementary Material online).”
From The Human Accelerated Region HAR202 Controls NPAS3 Expression in the Developing Forebrain Displaying Differential Enhancer Activity Between Modern and Archaic Human Sequences (2024) · cites this paper as Won et al. 2016
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In the citing paper
“new methodologies, such as Hi-C and single-cell sequencing, have yet to be fully integrated at scale with brain genomics data (13–16).”
From Comprehensive functional genomic resource and integrative model for the human brain (2018) · cites this paper as [13]
Experimental — accuracy not yet measuredIn the citing paper
“MAGMA assigns SNPs to the nearest genes, which has two major pitfalls. First, it is becoming increasingly recognized that non-coding SNPs can regulate distal genes via long range (>10 kb) regulatory interactions, whereby distal enhancers are brought into contact with the gene promoter3,4.”
From A computational tool (H-MAGMA) for improved prediction of brain-disorder risk genes by incorporating brain chromatin interaction profiles (2020) · cites this paper as [4]
In the citing paper
“Since 3D chromatin loops are highly tissue-specific4, it is important to decide which Hi-C datasets are appropriate to identify target genes for each disorder.”
From A computational tool (H-MAGMA) for improved prediction of brain-disorder risk genes by incorporating brain chromatin interaction profiles (2020) · cites this paper as [4]
In the citing paper
“SCZ and BD-associated genes were also enriched for acetylcholinergic signaling, supporting previous studies that altered cholinergic signaling contributes to SCZ and BD pathogenesis4,22.”
From A computational tool (H-MAGMA) for improved prediction of brain-disorder risk genes by incorporating brain chromatin interaction profiles (2020) · cites this paper as [4]
In the citing paper
“Only ~31% of the interactions in our adult Hi-C data were detected in the fetal dataset (figs. S39 and S40) (13).”
From Comprehensive functional genomic resource and integrative model for the human brain (2018) · cites this paper as [13]
In the citing paper
“The majority of SCZ genes were not even in LD with the index SNPs (~67%, or 748 of 1111 genes with r2 < 0.6) (fig. S45), consistent with the fact that regulatory relationships often do not follow linear genome organization (13).”
From Comprehensive functional genomic resource and integrative model for the human brain (2018) · cites this paper as [13]
In the citing paper
“Brain Hi-C data (Wang et al., 2018; Won et al., 2016) detected a direct interaction of the cross-disorder association region with NOX4 in both adult and fetal brain (interaction p = 3.2 3 10 16 and 9.3 3 10 6 , respectively).”
From Genomic Relationships, Novel Loci, and Pleiotropic Mechanisms across Eight Psychiatric Disorders (2019) · cites this paper as Won et al., 2016
In the citing paper
“Crucially, recent studies have shown that genes located far outside of a locus are often implicated (see functional architecture section below) (Wang et al., 2018a; Won et al., 2016).”
From Defining the genetic, genomic, cellular, and diagnostic architectures of psychiatric disorders (2019) · cites this paper as Won et al., 2016
In the citing paper
“assigning even well-annotated genomic regions to specific genes is not as simple as choosing the closest gene or genes containing variation that is highly correlated with the associated SNPs which is usually the default approach (Whalen et al., 2016; Won et al., 2016)”
From Defining the genetic, genomic, cellular, and diagnostic architectures of psychiatric disorders (2019) · cites this paper as Won et al., 2016
In the citing paper
“around half of non-coding regions have regulatory functions that are shared across tissues meaning that half of the regulatory elements in a given tissue may be relatively specific to a tissue, cell type, or developmental stage (Liu et al., 2017a; Roadmap Epigenomics Consortium, 2015; Won et al., 2016)”
From Defining the genetic, genomic, cellular, and diagnostic architectures of psychiatric disorders (2019) · cites this paper as Won et al., 2016
In the citing paper
“disease-associated SNPs in non-coding areas of the genome influence genes associated with diseases including Alzheimer’s Disease (AD)”
From Neuronal DNA double-strand breaks lead to genome structural variations and 3D genome disruption in neurodegeneration (2023) · cites this paper as [46]
In the citing paper
“We detected 187,674 and 167,551 promoter-based interactions3,4 from NeuN+ and NeuN− cells, respectively (Fig. 2a).”
From Neuronal and glial 3D chromatin architecture informs the cellular etiology of brain disorders (2021) · cites this paper as [4]
In the citing paper
“We identified 24,544 unique loops from published Hi-C data created in human brain tissue derived from the germinal zone and cortical plate41”
From Three-dimensional genome restructuring across timescales of activity-induced neuronal gene expression (2020) · cites this paper as [41]
In the citing paper
“We and others have shown that enhancers often regulate distal genes4,15,16”
From Neuronal and glial 3D chromatin architecture informs the cellular etiology of brain disorders (2021) · cites this paper as [4]
In the citing paper
“Cortical plate and germinal zone loops were then merged to create a master set of 24,544 loops spanning the two brain tissues.”
From Three-dimensional genome restructuring across timescales of activity-induced neuronal gene expression (2020) · cites this paper as [41]
In the citing paper
“we observed a similar increase in insulation around SOX11 (Figure S3M).”
From Multiscale 3D Genome Rewiring during Mouse Neural Development (2017) · cites this paper as Won et al., 2016
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Citations
Cites
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Integrative analysis of 111 reference human epigenomes
Roadmap Epigenomics Consortium, Kundaje, A., Meuleman, W., Ernst, J., Bilenky, M., Yen, A., Heravi-Moussavi, A., Kheradpour, P., Zhang, Z., Wang, J., et al. (2015) · Nature · doi:10.1038/nature14248 · Cited by 6,368
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GREAT improves functional interpretation of cis-regulatory regions
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The accessible chromatin landscape of the human genome
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Metadata
- Authors
- Won, H., de la Torre-Ubieta, L., Stein, J. L., Parikshak, N. N., Huang, J., Opland, C. K., Gandal, M. J., Sutton, G. J., Hormozdiari, F., Lu, D., Lee, C., Eskin, E., Voineagu, I., Ernst, J., & Geschwind, D. H.
- Affiliations
- University of California, Los Angeles (US)
- UNSW Sydney (AU)
- Corresponding author
- Geschwind, Daniel H.
- ORCID
- Venue
- Nature
- Published
- 2016-10
- Volume
- 538
- Issue
- 7626
- Pages
- 523-527
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC5358922
- OpenAlex
- W2534005127
- Cited by
- 584
- References
- 46
- Citations by year
- 2026: 24 · 2025: 45 · 2024: 51 · 2023: 45 · 2022: 62 · 2021: 79 · 2020: 78 · 2019: 76 · 2018: 72 · 2017: 46 · 2016: 3
- FWCI
- 34.12
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- UNC Libraries
- Funders
- National Science Foundation (1254200, CAREER)
- National Research Foundation
- National Research Foundation of Korea
- National Institutes of Health (TG2-01169, 5r01mh094714-04, AI028697)
- Center for AIDS Research, University of Washington (5P30AI028697, AI028697)
- National Health and Medical Research Council (1062510)
- National Institute of Mental Health (K99MH102357, U01MH103339, R01-MH094714, F30MH099886, R01MH110927, R01MH100027, R01MH101782, U01MH105991, R01MH060233, R00MH102357, T32MH073526, R37MH060233)
- National Institute of Allergy and Infectious Diseases (P30AI028697)
- National Institute of Environmental Health Sciences (R01ES022282, R01ES024995)
- Center for AIDS Research, University of California Los Angeles (AI028697)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genomic variations and chromosomal abnormalities
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Keywords
- chromosome conformation, 3D genome organization, human brain development, cortical development, enhancer-promoter interactions, non-coding variants, schizophrenia risk genes, autism spectrum disorder, neurodevelopmental disorders, FOXG1, purifying selection, human cognitive evolution, neural progenitor cells, Hi-C, gene regulatory networks
- MeSH terms
- Brain, Chromatin, Chromosomes, Human, Cognition, Enhancer Elements, Genetic, Humans, Nerve Tissue Proteins, Nucleic Acid Conformation, Organ Specificity, Promoter Regions, Genetic, Schizophrenia, Reproducibility of Results, Gene Expression Regulation, Developmental, Genetic Predisposition to Disease, Polymorphism, Single Nucleotide, Epigenesis, Genetic, Forkhead Transcription Factors, Genome-Wide Association Study, Neurogenesis, Neural Stem Cells
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