Enhancer connectome in primary human cells identifies target genes of disease-associated DNA elements
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Abstract
The challenge of linking intergenic mutations to target genes has limited molecular understanding of human diseases. Here we show that H3K27ac HiChIP generates high-resolution contact maps of active enhancers and target genes in rare primary human T cell subtypes and coronary artery smooth muscle cells. Differentiation of naive T cells into T helper 17 cells or regulatory T cells creates subtype-specific enhancer-promoter interactions, specifically at regions of shared DNA accessibility. These data provide a principled means of assigning molecular functions to autoimmune and cardiovascular disease risk variants, linking hundreds of noncoding variants to putative gene targets. Target genes identified with HiChIP are further supported by CRISPR interference and activation at linked enhancers, by the presence of expression quantitative trait loci, and by allele-specific enhancer loops in patient-derived primary cells. The majority of disease-associated enhancers contact genes beyond the nearest gene in the linear genome, leading to a fourfold increase in the number of potential target genes for autoimmune and cardiovascular diseases.
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Using techniques with antibodies to enhancer- and promoter-associated histone modifications or RNA polymerase has revealed large numbers of 3D enhancer-promoter contacts.
“Using these techniques with antibodies to enhancer- and promoter-associated histone modifications or those to RNA polymerase has also revealed large numbers of 3D enhancer–promoter contacts [244, 295–301].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [244]
Predicted loops were highly specific for oligodendrocytes.
“To investigate the cell-type specificity of the predictions, we generated pileups using Oligodendrocyte H3K27ac HiChIP data and H3K27ac HiChIP performed in mouse embryonic stem cells37 and found that the predicted loops were highly specific for oligodendrocytes (Figure 6b).”
From Single-cell CUT&Tag profiles histone modifications and transcription factors in complex tissues (2021) · cites this paper as [37]
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Chromatin accessibility profiling by ATAC-seq
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Self-citationSingle-cell multiomic analysis identifies regulatory programs in mixed-phenotype acute leukemia
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Self-citationSingle-cell CUT&Tag profiles histone modifications and transcription factors in complex tissues
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Promoter of lncRNA Gene PVT1 Is a Tumor-Suppressor DNA Boundary Element
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Self-citationecDNA hubs drive cooperative intermolecular oncogene expression
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Self-citationEpigenetic regulation of T cell exhaustion
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Self-citationA new era in functional genomics screens
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A cellular and molecular view of T helper 17 cell plasticity in autoimmunity
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Identification of significant chromatin contacts from HiChIP data by FitHiChIP
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“We choose these two window sizes for compatibility with existing literature on HiChIP and Hi-C data analysis 3,5,14,16,19 .”
BackgroundMethodInfluentialTwo major mechanisms of chromosome organization
Mirny, L. A., Imakaev, M., & Abdennur, N. A. (2019) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2019.05.001 · Cited by 222 · see citing works
“TAD-related patterns may also appear to exhibit several levels of nesting [13] in transitive configurations that can produce grid-like alignments of edges and peaks [11,14,15].”
BackgroundSumida, T. S., Cheru, N. T., & Hafler, D. A. (2024) · Nature reviews. Immunology · doi:10.1038/s41577-024-00994-x · Cited by 208 · see citing works
“Analyses of conventional CD4 + T cells and T reg cells by HiChIP 110 , a tool to map enhancer–promoter architecture, revealed that FOXP3 controls T reg cell identity and stability by interacting with promoters and enhancers of core T reg cell signature genes and maintaining enhancer–promoter connectivity 111 .”
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“…IL-2 withdrawal (n = 6 in to **p < 0.01, ****p < 0.0001 by multiple t tests (with adjusted p value) (E and G) or screens (Henriksson et al., 2019; LaFleur et al., 2019; Shifrut et al., 2018; Ting et al., 2018; Dong et al., 2019; Ye et al., 2019), CRISPRa screens, being a GOF approach, can…”
BackgroundInfluentialFunctional Annotation of Animal Genomes (FAANG): Current Achievements and Roadmap
Giuffra, E., & Tuggle, C. K. (2018) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-020518-114913 · Cited by 201 · see citing works
Transformation of Accessible Chromatin and 3D Nucleome Underlies Lineage Commitment of Early T Cells
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“…and its potential regulatory roles in transcription in various cultured and primary cells of the hematopoietic systems (Bunting et al., 2016; Chepelev et al., 2012; Javierre et al., 2016; Kieffer-Kwon et al., 2013; Lin et al., 2012; Martin et al., 2015; Mumbach et al., 2017; Placek et al., 2017).”
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Self-citationChromatin alternates between A and B compartments at kilobase scale for subgenic organization
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“Using GM12878 H3K27ac HiChIP data 21 , we also found higher signal and more FitHiChIP 42 signi fi cant interactions proximal to diffuse CTCF loops (Fig.”
BackgroundMethodGiammartino, D. C. D., Kloetgen, A., Polyzos, A., Liu, Y., Kim, D., Murphy, D., Abuhashem, A., Cavaliere, P., Aronson, B. E., Shah, V., et al. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0390-6 · Cited by 174 · see citing works
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“These results motivate applying colocalization and TWAS methods to other molecular QTL; it may also be possible to prioritize other molecular QTL in gene set analyses by connecting regulatory regions to genes 44,45 .”
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Self-citationA supervised learning framework for chromatin loop detection in genome-wide contact maps
Salameh, T. J., Wang, X., Song, F., Zhang, B., Wright, S. M., Khunsriraksakul, C., Ruan, Y., & Yue, F. (2020) · Nature Communications · doi:10.1038/s41467-020-17239-9 · Cited by 165 · see citing works
Single-nucleus multiregion transcriptomic analysis of brain vasculature in Alzheimer’s disease
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“…linking evidence to evaluate the association between AD variant and candidate genes: (1) physical chromatin conformation capture (Hi-C) looping 89–92 ; (2) correlation-based enhancer–gene links 93 ; (3) brain, heart-and muscle-specific eQTLs at tissue-level resolution 94 ; and (4) vasculature…”
BackgroundHistone hyperacetylation disrupts core gene regulatory architecture in rhabdomyosarcoma
Gryder, B. E., Pomella, S., Sayers, C. M., Wu, X., Song, Y., Chiarella, A. M., Bagchi, S., Chou, H.-C., Sinniah, R., Walton, A., et al. (2019) · Nature Genetics · doi:10.1038/s41588-019-0534-4 · Cited by 162 · see citing works
How subtle changes in 3D structure can create large changes in transcription
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“…should colocalize with their active enhancers, based largely on bulk population assays such 3C and H3K27ac Hi-Chip (Bartman et al., 2016; Deng et al., 2012; Kagey et al., 2010; Mumbach et al., 2017, 2016; Rao et al., 2014; Williamson et al., 2016), for review see (Furlong and Levine, 2018).”
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The spatial organization of transcriptional control
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Transcript-indexed ATAC-seq for precision immune profiling
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A promoter interaction map for cardiovascular disease genetics
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“H3K27ac HiChIP was performed according to Mumbach et al. (2017) with only minor modifications.”
Epigenetic mechanisms regulating T-cell responses
Schmidl, C., Delacher, M., Huehn, J., & Feuerer, M. (2018) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2018.07.014 · Cited by 144 · see citing works
3D Genome of macaque fetal brain reveals evolutionary innovations during primate corticogenesis
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“Enhancer-enhancer interactions are implicated in gene control by forming enhancer cliques or spatially interaction hubs to regulate gene expression (Mumbach et al., 2017; Petrovic et al., 2019; Sanborn et al., 2015).”
BackgroundComplementary Alu sequences mediate enhancer–promoter selectivity
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Self-citationA practical view of fine-mapping and gene prioritization in the post-genome-wide association era
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“Moreover, only 14% (367) of these gene–variant interactions were with the gene closest to the variant [63].”
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Unveiling the Role of the Most Impactful Cardiovascular Risk Locus through Haplotype Editing
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“3 risk haplotype associated more strongly with the ANRIL enhancer (and also with the nearby CDKN2B enhancer) compared to the analogous region in the non-risk haplotype (Mumbach et al., 2017).”
Promoter-interacting expression quantitative trait loci are enriched for functional genetic variants
Chandra, V., Bhattacharyya, S., Schmiedel, B. J., Madrigal, A., González-Colín, C., Feupe, S. F., Crinklaw, A., Seumois, G., Mohammadi, P., Kronenberg, M., et al. (2020) · Nature Genetics · doi:10.1038/s41588-020-00745-3 · Cited by 124 · see citing works
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“We considered this may be due to technical limitations of our Hi-C analysis, which misses short-range interactions (<60kb) (see methods), underrepresents regulatory loops (Bonev et al., 2017; Di Giammartino et al., 2019; Mumbach et al., 2016; Mumbach et al., 2017), and does not cover a large fraction (>50%) of express…”
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BET inhibition disrupts transcription but retains enhancer-promoter contact
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MAPS: Model-based analysis of long-range chromatin interactions from PLAC-seq and HiChIP experiments
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Nested epistasis enhancer networks for robust genome regulation
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The Role of Noncoding Variants in Heritable Disease
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“As enhancers can physically interact with multiple target gene promoters [50,51], disease-associated variants in enhancers can also impact the expression of more than one gene.”
BackgroundEnhancer RNAs in cancer: regulation, mechanisms and therapeutic potential
Lee, J., Xiong, F., & Li, W. (2020) · RNA Biology · doi:10.1080/15476286.2020.1712895 · Cited by 107 · see citing works
“Most strategies so far in the literature, such as genomic deletion [34,35], transcription terminator insertion [36,37], transcription suppression by CRISPRi [38], will affect both transcription activity and eRNA transcripts.”
BackgroundPolycomb-mediated genome architecture enables long-range spreading of H3K27 methylation
Kraft, K., Yost, K. E., Murphy, S. E., Magg, A., Long, Y., Corces, M. R., Granja, J. M., Wittler, L., Mundlos, S., Cech, T. R., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2201883119 · Cited by 112 · see citing works
Self-citationOncogenic Notch Promotes Long-Range Regulatory Interactions within Hyperconnected 3D Cliques
Petrovic, J., Zhou, Y., Fasolino, M., Goldman, N., Schwartz, G. W., Mumbach, M. R., Nguyen, S. C., Rome, K., Sela, Y., Zapataro, Z., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.01.006 · Cited by 102 · see citing works
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“CircANRIL was found not only in many different cell lines, but also in many primary cell types, including vascular smooth muscle cells (VSMCs) and macrophages, as well as in heart and vascular tissue (22, 36).”
BackgroundInfluentialPost-GWAS in prostate cancer: from genetic association to biological contribution
Farashi, S., Kryza, T., Clements, J., & Batra, J. (2018) · Nature Reviews. Cancer · doi:10.1038/s41568-018-0087-3 · Cited by 88 · see citing works
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Self-citationHiChIRP reveals RNA-associated chromosome conformation
Mumbach, M. R., Granja, J. M., Flynn, R. A., Roake, C. M., Satpathy, A. T., Rubin, A. J., Qi, Y., Jiang, Z., Shams, S., Louie, B. H., et al. (2019) · Nature Methods · doi:10.1038/s41592-019-0407-x · Cited by 104 · see citing works
Self-citationHigh resolution genetic mapping of putative causal interactions between regions of open chromatin
Kumasaka, N., Knights, A., & Gaffney, D. (2018) · Nature Genetics · doi:10.1038/s41588-018-0278-6 · Cited by 99 · see citing works
Genetic Regulation of Atherosclerosis-Relevant Phenotypes in Human Vascular Smooth Muscle Cells
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Promoter-Enhancer Communication Occurs Primarily within Insulated Neighborhoods
Sun, F., Chronis, C., Kronenberg, M., Chen, X., Su, T., Lay, F. D., Plath, K., Kurdistani, S. K., & Carey, M. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.10.039 · Cited by 94 · see citing works
“For example, although a large percentage of intergenic disease-associated SNPs localize to enhancers, the effect of these on gene expression is not readily predictable (Elkon and Agami, 2017; Lupianez et al., 2015; Mumbach et al., 2017).”
BackgroundWidespread contribution of transposable elements to the rewiring of mammalian 3D genomes
Choudhary, M. N. K., Quaid, K., Xing, X., Schmidt, H. K., & Wang, T. (2023) · Nature Communications · doi:10.1038/s41467-023-36364-9 · Cited by 97 · see citing works
Nucleome Dynamics during Retinal Development
Norrie, J. L., Lupo, M. S., Xu, B., Aldiri, I., Valentine, M. B., Putnam, D. K., Griffiths, L. M., Zhang, J., Johnson, D. A., Easton, J. B., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.08.002 · Cited by 87 · see citing works
Trac-looping measures genome structure and chromatin accessibility
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Epigenomes of Human Hearts Reveal New Genetic Variants Relevant for Cardiac Disease and Phenotype
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SnapHiC: a computational pipeline to identify chromatin loops from single-cell Hi-C data
Yu, M., Abnousi, A., Zhang, Y., Li, G., Lee, L., Chen, Z., Fang, R., Lagler, T. M., Yang, Y., Wen, J., et al. (2021) · Nature Methods · doi:10.1038/s41592-021-01231-2 · Cited by 91 · see citing works
“cohesin 10 and H3K27ac HiChIP data 11 , all from mES cells.”
BackgroundMethodWang, S. K., Nair, S., Li, R., Kraft, K., Pampari, A., Patel, A., Kang, J. B., Luong, C., Kundaje, A. B., & Chang, H. Y. (2022) · Cell Genomics · doi:10.1016/j.xgen.2022.100164 · Cited by 88 · see citing works
“We first performed HiChIP for acetylated histone H3 lysine 27 (H3K27ac), a mark of active enhancers and promoters,(32) to characterize the three-dimensional (3D) enhancer ‘‘connectome’’ of the human retina (Figures S7A and S7B).(14,33) We uncovered 16,692 loop anchors connected by 9,670 HiChIP loops, including several…”
MethodSelf-citationSingle-Cell Multi-omics: An Engine for New Quantitative Models of Gene Regulation
Packer, J. S., & Trapnell, C. (2018) · Trends in Genetics · doi:10.1016/j.tig.2018.06.001 · Cited by 84 · see citing works
“HiChIP is a promising technology that dramatically reduces the input number of cells required compared to ChIA-PET and promoter capture HiC ( 100 000 compared to 10 million or more).”
MethodEpigenetic reprogramming of immune cells in injury, repair, and resolution
Placek, K., Schultze, J. L., & Aschenbrenner, A. C. (2019) · Journal of Clinical Investigation · doi:10.1172/jci124619 · Cited by 83 · see citing works
“DNMT3B targets the promoter of PPARG, a key transcription factor for alternative acticell activation (29, 55), and T cell development (56) and differentiation (57) are accompanied by genome-wide reorganization of chromatin loops.”
BackgroundDeterminants of transcription factor regulatory range
Chen, C.-H., Zheng, R., Tokheim, C., Dong, X., Fan, J., Wan, C., Tang, Q., Brown, M., Liu, J. S., Meyer, C. A., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-16106-x · Cited by 85 · see citing works
Human Genetics of Obesity and Type 2 Diabetes Mellitus
Ingelsson, E., & McCarthy, M. I. (2018) · Circulation Genomic and Precision Medicine · doi:10.1161/circgen.118.002090 · Cited by 83 · see citing works
Transcriptional control by enhancers and enhancer RNAs
Lewis, M. W., Shen, L., & Franco, H. L. (2019) · Transcription · doi:10.1080/21541264.2019.1695492 · Cited by 78 · see citing works
“There are several chromatin conformation techniques that enable the mapping of enhancer-promoter interactions, such as chromatin conformation capture (3C) [46,47,163], Hi-C [164,165], and recently Hi-ChIP [166,167].”
BackgroundWidespread Enhancer Activity from Core Promoters
Medina-Rivera, A., Santiago-Algarra, D., Puthier, D., & Spicuglia, S. (2018) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2018.03.004 · Cited by 78 · see citing works
An Activity-Mediated Transition in Transcription in Early Postnatal Neurons
Stroud, H., Yang, M. G., Tsitohay, Y. N., Davis, C. P., Sherman, M. A., Hrvatin, S., Ling, E., & Greenberg, M. E. (2020) · Neuron · doi:10.1016/j.neuron.2020.06.008 · Cited by 76 · see citing works
“All loops greater than 1 Mb in length were removed as previously performed (Mumbach et al., 2017).”
MethodMoonen, J.-R. A. J., Chappell, J., Shi, M., Shinohara, T., Li, D., Mumbach, M. R., Zhang, F., Nair, R. V., Nasser, J., Mai, D. H., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-32566-9 · Cited by 78 · see citing works
Self-citationUnderstanding the 3D genome: Emerging impacts on human disease
Krumm, A., & Duan, Z. (2018) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2018.07.004 · Cited by 75 · see citing works
Ray, J. P., de Boer, C. G., Fulco, C. P., Lareau, C. A., Kanai, M., Ulirsch, J. C., Tewhey, R., Ludwig, L. S., Reilly, S. K., Bergman, D. T., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15022-4 · Cited by 75 · see citing works
Transcriptional enhancers and their communication with gene promoters
Ray-Jones, H., & Spivakov, M. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03903-w · Cited by 81 · see citing works
“Finally, evidence from multiple sources including reporter assays [169, 175, 239, 240], CRISPR [240–242], chromatin mapping [243, 244] and population genetics analysis [207, 245] suggests that certain promoters, termed ‘epromoters’, can also function as enhancers (reviewed in [246]).”
BackgroundYang, J., McGovern, A., Martin, P., Duffus, K., Ge, X. J., Zarrineh, P., Morris, A. P., Adamson, A. D., Fraser, P., Rattray, M., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-18180-7 · Cited by 71 · see citing works
Dynamic chromatin regulatory landscape of human CAR T cell exhaustion
Gennert, D. G., Lynn, R. C., Granja, J. M., Weber, E. W., Mumbach, M. R., Zhao, Y., Duren, Z., Sotillo, E., Greenleaf, W. J., Wong, W. H., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2104758118 · Cited by 70 · see citing works
“To understand the 3D chromosome landscape, we performed chromatin conformation capture coupled with immunoprecipitation and sequencing (HiChIP) directed against histone H3 lysine 27 acetylation (H3K27ac), a histone mark associated with active enhancers, to construct the enhancer connectome (46).”
Self-citationApproaches and advances in the genetic causes of autoimmune disease and their implications
Inshaw, J. R. J., Cutler, A. J., Burren, O. S., Stefana, M. I., & Todd, J. A. (2018) · Nature Immunology · doi:10.1038/s41590-018-0129-8 · Cited by 70 · see citing works
DC3 is a method for deconvolution and coupled clustering from bulk and single-cell genomics data
Zeng, W., Chen, X. X., Duren, Z., Wang, Y., Jiang, R., & Wong, W. H. (2019) · Nature Communications · doi:10.1038/s41467-019-12547-1 · Cited by 69 · see citing works
Transcriptional regulation by promoters with enhancer function
Dao, L. T. M., & Spicuglia, S. (2018) · Transcription · doi:10.1080/21541264.2018.1486150 · Cited by 69 · see citing works
“By using a CRISPR/Cas9 epigenetic activation approach, another study showed that two heterologous promoters interacting with the promoter of the T cell inducible gene CD69 regulate the expression of CD69 after T cell activation [24].”
BackgroundTranscription factors: building hubs in the 3D space
Giammartino, D. C. D., Polyzos, A., & Apostolou, E. (2020) · Cell Cycle · doi:10.1080/15384101.2020.1805238 · Cited by 66 · see citing works
“Among the highest connected HiChIP anchors in pluripotent stem cells were many of the previously described super-enhancers (SE) [42] as well as known stem cell regulators, including Mycn, Esrrb, and Mir290.”
BackgroundInfluentialGene regulation in the 3D genome
Li, Y., Hu, M., & Shen, Y. (2018) · Human Molecular Genetics · doi:10.1093/hmg/ddy164 · Cited by 66 · see citing works
Zhang, S., Plummer, D., Lu, L., Cui, J., Xu, W., Wang, M., Liu, X., Prabhakar, N., Shrinet, J., Srinivasan, D., et al. (2022) · Nature Genetics · doi:10.1038/s41588-022-01116-w · Cited by 63 · see citing works
“We also collected five sets of ChIA–PET or HiChIP data in GM12878 cells performed with CTCF, PolII, RAD21, SMC1A and H3K27ac antibodies 14,40–43 .”
MethodThe interdependence of gene-regulatory elements and the 3D genome
Vermunt, M. W., Zhang, D., & Blobel, G. A. (2018) · The Journal of Cell Biology · doi:10.1083/jcb.201809040 · Cited by 65 · see citing works
- Authors
- Mumbach, M. R., Satpathy, A. T., Boyle, E. A., Dai, C., Gowen, B. G., Cho, S. W., Nguyen, M. L., Rubin, A. J., Granja, J. M., Kazane, K. R., Wei, Y., Nguyen, T., Greenside, P. G., Corces, M. R., Tycko, J., Simeonov, D. R., Suliman, N., Li, R., Xu, J., Flynn, R. A., Kundaje, A., Khavari, P. A., Marson, A., Corn, J. E., Quertermous, T., Greenleaf, W. J., & Chang, H. Y.
- Affiliations
- Stanford Medicine (US)
- Innovative Genomics Institute (US)
- University of California, San Francisco (US)
- Chan Zuckerberg Biohub San Francisco (US)
- Corresponding author
- Greenleaf, William J
- Chang, Howard Y
- ORCID
- Mumbach, Maxwell R
- Satpathy, Ansuman T
- Boyle, Evan A
- Gowen, Benjamin G
- Cho, Seung Woo
- Nguyen, Michelle L
- Rubin, Adam J
- Granja, Jeffrey M
- Kazane, Katelynn R
- Nguyen, Trieu
- Corces, M Ryan
- Tycko, Josh
- Simeonov, Dimitre R
- Li, Rui
- Xu, Jin
- Flynn, Ryan A
- Kundaje, Anshul
- Khavari, Paul A
- Marson, Alexander
- Corn, Jacob E
- Quertermous, Thomas
- Greenleaf, William J
- Chang, Howard Y
- Venue
- Nature Genetics
- Published
- 2017-09-25
- Volume
- 49
- Issue
- 11
- Pages
- 1602-1612
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- PMC
- PMC5805393
- OpenAlex
- W2952947531
- Cited by
- 490
- References
- 65
- Citations by year
- 2026: 26 · 2025: 32 · 2024: 46 · 2023: 53 · 2022: 73 · 2021: 72 · 2020: 74 · 2019: 62 · 2018: 47 · 2017: 5
- FWCI
- 20.99
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- cc-by-nc-nd
- www.springer.com/tdm (tdm)
- Locations
- Nature Genetics (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Scholarworks@UNIST (Ulsan National Institute of Science and Technology) (submittedVersion)
- Funders
- National Institutes of Health (1s10od018220-01)
- National Human Genome Research Institute (UM1HG009436, P50HG007735, T32HG000044)
- National Cancer Institute (P30CA124435)
- National Institute of General Medical Sciences (T32GM008568)
- National Institute of Allergy and Infectious Diseases (U19AI057266)
- U.S. National Library of Medicine (T15LM007033)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- enhancer-promoter interactions, causal gene identification, Th17 cells, regulatory T cells, naive T cells, coronary artery smooth muscle cells, autoimmune disease, cardiovascular disease, expression quantitative trait loci, DNA accessibility
- MeSH terms
- Alleles, Autoimmune Diseases, Cardiovascular Diseases, Cell Differentiation, Chromatin, Enhancer Elements, Genetic, T-Lymphocytes, Helper-Inducer, Histones, Humans, Mutation, Promoter Regions, Genetic, Genome, Human, K562 Cells, DNA, Intergenic, Myocytes, Smooth Muscle, Quantitative Trait Loci, Chromatin Immunoprecipitation, T-Lymphocytes, Regulatory, Primary Cell Culture, Clustered Regularly Interspaced Short Palindromic Repeats
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