Chromatin accessibility: a window into the genome.
- Authors
- Tsompana, Maria; Buck, Michael J
- Year
- 2014
- Journal
- Epigenetics & chromatin
- PMID
- 25473421
- DOI
- 10.1186/1756-8935-7-33
- PMCID
- PMC4253006
Transcriptional activation throughout the eukaryotic lineage has been tightly linked with disruption of nucleosome organization at promoters, enhancers, silencers, insulators and locus control regions due to transcription factor binding. Regulatory DNA thus coincides with open or accessible genomic sites of remodeled chromatin. Current chromatin accessibility assays are used to separate the genome by enzymatic or chemical means and isolate either the accessible or protected locations. The isolated DNA is then quantified using a next-generation sequencing platform. Wide application of these assays has recently focused on the identification of the instrumental epigenetic changes responsible for differential gene expression, cell proliferation, functional diversification and disease development. Here we discuss the limitations and advantages of current genome-wide chromatin accessibility assays with especial attention on experimental precautions and sequence data analysis. We conclude with our perspective on future improvements necessary for moving the field of chromatin profiling forward.
Schematic diagram of current chromatin accessibility assays performed with typical experimental conditions. Representative DNA fragments generated by each assay are shown, with end locations within chromatin defined by colored arrows. Bar diagrams represent data signal obtained from each assay across the entire region. The footprint created by a transcription factor (TF) is shown for ATAC-seq and DNase-seq experiments.
Chromatin accessibility high-throughput data analysis workflow. Chromatin accessibility data analysis involves a number of stages with progressively increased level of difficulty and advanced requirements for computational and genomics expertise. All major steps of analyses, from sequence tags to data annotation/integration are shown in a comprehensive workflow format (read text for additional details).
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External
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| Human transposons are an abundant supply of transcription factor binding sites and promoter activities in breast cancer cell lines. | Jiang JC et al. | β | 2019 | β |
| Integrated Epigenetic Mapping of Human and Mouse Salivary Gene Regulation. | Michael DG et al. | β | 2019 | β |
| Intercalation of small molecules into DNA in chromatin is primarily controlled by superhelical constraint. | Bosire R et al. | β | 2019 | β |
| MeCP2 inhibits cell functionality through FoxO3a and autophagy in endothelial progenitor cells. | Zha S et al. | β | 2019 | β |
| Modulating chromatin accessibility by transactivation and targeting proximal dsgRNAs enhances Cas9 editing efficiency in vivo. | Liu G et al. | β | 2019 | β |
| Multi-study inference of regulatory networks for more accurate models of gene regulation. | Castro DM et al. | β | 2019 | β |
| Nascent transcript analysis of glucocorticoid crosstalk with TNF defines primary and cooperative inflammatory repression. | Sasse SK et al. | β | 2019 | β |
| Nucleosome Crowding in Chromatin Slows the Diffusion but Can Promote Target Search of Proteins. | Kanada R et al. | β | 2019 | β |
| Profiling of chromatin accessibility and identification of general cis-regulatory mechanisms that control two ocular lens differentiation pathways. | Zhao Y et al. | β | 2019 | β |
| SCALE method for single-cell ATAC-seq analysis via latent feature extraction. | Xiong L et al. | β | 2019 | β |
| Specific chromatin changes mark lateral organ founder cells in the Arabidopsis inflorescence meristem. | Frerichs A et al. | β | 2019 | β |
| The role of chromatin dynamics under global warming response in the symbiotic coral model Aiptasia. | Weizman E et al. | β | 2019 | β |
| Advances of DNase-seq for mapping active gene regulatory elements across the genome in animals. | Chen A et al. | β | 2018 | β |
| Analysis of rat cardiac myocytes and fibroblasts identifies combinatorial enhancer organization and transcription factor families. | Golan-Lagziel T et al. | β | 2018 | β |
| An optimized FAIRE procedure for low cell numbers in yeast. | Segorbe D et al. | β | 2018 | β |
| ATACseqQC: a Bioconductor package for post-alignment quality assessment of ATAC-seq data. | Ou J et al. | β | 2018 | β |
| CATaDa reveals global remodelling of chromatin accessibility during stem cell differentiation in vivo. | Aughey GN et al. | β | 2018 | β |
| Chromatin accessibility is associated with CRISPR-Cas9 efficiency in the zebrafish (Danio rerio). | Uusi-MΓ€kelΓ€ MIE et al. | β | 2018 | β |
| Computational Methods for Assessing Chromatin Hierarchy. | Chang P et al. | β | 2018 | β |
| Developmental Chromatin Restriction of Pro-Growth Gene Networks Acts as an Epigenetic Barrier to Axon Regeneration in Cortical Neurons. | Venkatesh I et al. | β | 2018 | β |
| Epigenetic Applications in Adverse Outcome Pathways and Environmental Risk Evaluation. | Angrish MM et al. | β | 2018 | β |
| Epigenome in Early Mammalian Development: Inheritance, Reprogramming and Establishment. | Xu Q et al. | β | 2018 | β |
| Human Papillomavirus Replication Regulation by Acetylation of a Conserved Lysine in the E2 Protein. | Thomas Y et al. | β | 2018 | β |
| Identification of cis-regulatory elements by chromatin structure. | Lu Z et al. | β | 2018 | β |
| Integrating ChIP-seq with other functional genomics data. | Jiang S et al. | β | 2018 | β |
| Interferon regulatory factor 1 and a variant of heterogeneous nuclear ribonucleoprotein L coordinately silence the gene for adhesion protein CEACAM1. | Dery KJ et al. | β | 2018 | β |
| Investigating Nucleosome Accessibility for MNase, Fe<sup>II</sup> β Peplomycin, and Duocarmycinβ B<sub>2</sub> by Using Capillary Electrophoresis. | Zou T et al. | β | 2018 | β |
| MeCP2-mediated epigenetic regulation in senescent endothelial progenitor cells. | Wang C et al. | β | 2018 | β |
| Phenotype loss is associated with widespread divergence of the gene regulatory landscape in evolution. | Roscito JG et al. | β | 2018 | β |
| Proliferation of Regulatory DNA Elements Derived from Transposable Elements in the Maize Genome. | Zhao H et al. | β | 2018 | β |
| Quantitative imaging of chromatin decompaction in living cells. | Dultz E et al. | β | 2018 | β |
| Regulatory chromatin landscape in <i>Arabidopsis thaliana</i> roots uncovered by coupling INTACT and ATAC-seq. | Tannenbaum M et al. | β | 2018 | β |
| Single-Cell (Multi)omics Technologies. | Chappell L et al. | β | 2018 | β |
| Single Copy Transgene Integration in a Transcriptionally Active Site for Recombinant Protein Synthesis. | O'Brien SA et al. | β | 2018 | β |
| Study of mitotic chromatin supports a model of bookmarking by histone modifications and reveals nucleosome deposition patterns. | Javasky E et al. | β | 2018 | β |
| The Identification and Interpretation of <i>cis</i>-Regulatory Noncoding Mutations in Cancer. | Patel MB et al. | β | 2018 | β |
| Translating GWAS in rheumatic disease: approaches to establishing mechanism and function for genetic associations with ankylosing spondylitis. | Osgood JA et al. | β | 2018 | β |
| Cell identity bookmarking through heterogeneous chromatin landscape maintenance during the cell cycle. | Luo H et al. | β | 2017 | β |
| Chromatin accessibility dynamics reveal novel functional enhancers in <i>C. elegans</i>. | Daugherty AC et al. | β | 2017 | β |
| Chromosomal dynamics predicted by an elastic network model explains genome-wide accessibility and long-range couplings. | Sauerwald N et al. | β | 2017 | β |
| Computational inference of gene regulatory networks: Approaches, limitations and opportunities. | Banf M et al. | β | 2017 | β |
| Contribution of Neuroepigenetics to Huntington's Disease. | Francelle L et al. | β | 2017 | β |
| dCATCH-Seq: improved sequencing of large continuous genomic targets with double-hybridization. | Zhang Y et al. | β | 2017 | β |
| Dynamic chromatin accessibility modeled by Markov process of randomly-moving molecules in the 3D genome. | Wang Y et al. | β | 2017 | β |
| Enhanced chromatin accessibility of the dosage compensated Drosophila male X-chromosome requires the CLAMP zinc finger protein. | Urban J et al. | β | 2017 | β |
| Epigenetic Landscape during Coronavirus Infection. | SchΓ€fer A et al. | β | 2017 | β |
| High fat diet-induced changes of mouse hepatic transcription and enhancer activity can be reversed by subsequent weight loss. | SiersbΓ¦k M et al. | β | 2017 | β |
| I-ATAC: interactive pipeline for the management and pre-processing of ATAC-seq samples. | Ahmed Z et al. | β | 2017 | β |
| Metazoan Nuclear Pores Provide a Scaffold for Poised Genes and Mediate Induced Enhancer-Promoter Contacts. | Pascual-Garcia P et al. | β | 2017 | β |
| NicE-seq: high resolution open chromatin profiling. | Ponnaluri VKC et al. | β | 2017 | β |
| Nucleosome Positioning Assay. | Zhao Z et al. | β | 2017 | β |
| Polymorphisms in sex steroid receptors: From gene sequence to behavior. | Maney DL | β | 2017 | β |
| Prediction of Chromatin Accessibility in Gene-Regulatory Regions from Transcriptomics Data. | Jung S et al. | β | 2017 | β |
| Regulatory and evolutionary signatures of sex-biased genes on both the X chromosome and the autosomes. | Shen JJ et al. | β | 2017 | β |
| Sasquatch: predicting the impact of regulatory SNPs on transcription factor binding from cell- and tissue-specific DNase footprints. | Schwessinger R et al. | β | 2017 | β |
| STAG-CNS: An Order-Aware Conserved Noncoding Sequences Discovery Tool for Arbitrary Numbers of Species. | Lai X et al. | β | 2017 | β |
| Towards genome-wide prediction and characterization of enhancers in plants. | Marand AP et al. | β | 2017 | β |
| Understanding nucleosome dynamics and their links to gene expression and DNA replication. | Lai WKM et al. | β | 2017 | β |
| Characterization, correction and de novo assembly of an Oxford Nanopore genomic dataset from Agrobacterium tumefaciens. | Deschamps S et al. | β | 2016 | β |
| ChIP bias as a function of cross-linking time. | Baranello L et al. | β | 2016 | β |
| Enhanced Identification of Transcriptional Enhancers Provides Mechanistic Insights into Diseases. | Murakawa Y et al. | β | 2016 | β |
| Epigenetic Changes During Food-Specific Immunotherapy. | Bunning BJ et al. | β | 2016 | β |
| Genetics of congenital heart disease: the contribution of the noncoding regulatory genome. | Postma AV et al. | β | 2016 | β |
| Genetics of movement disorders in the next-generation sequencing era. | Olgiati S et al. | β | 2016 | β |
| Genome-Scale Analysis of Cell-Specific Regulatory Codes Using Nuclear Enzymes. | Baek S et al. | β | 2016 | β |
| Genome-wide epigenomic profiling for biomarker discovery. | Dirks RA et al. | β | 2016 | β |
| High-throughput small molecule screen identifies inhibitors of aberrant chromatin accessibility. | Pattenden SG et al. | β | 2016 | β |
| Insights into the Ecology and Evolution of Polyploid Plants through Network Analysis. | Gallagher JP et al. | β | 2016 | β |
| Integration of ATAC-seq and RNA-seq identifies human alpha cell and beta cell signature genes. | Ackermann AM et al. | β | 2016 | β |
| Molecular Actions of Glucocorticoids in Cartilage and Bone During Health, Disease, and Steroid Therapy. | Hartmann K et al. | β | 2016 | β |
| Occupancy of RNA Polymerase II Phosphorylated on Serine 5 (RNAP S5P) and RNAP S2P on Varicella-Zoster Virus Genes 9, 51, and 66 Is Independent of Transcript Abundance and Polymerase Location within the Gene. | Henderson HH et al. | β | 2016 | β |
| Open chromatin reveals the functional maize genome. | Rodgers-Melnick E et al. | β | 2016 | β |
| Pax6 associates with H3K4-specific histone methyltransferases Mll1, Mll2, and Set1a and regulates H3K4 methylation at promoters and enhancers. | Sun J et al. | β | 2016 | β |
| Persistent Chromatin Modifications Induced by High Fat Diet. | Leung A et al. | β | 2016 | β |
| Protein Palmitoylation Regulates Neural Stem Cell Differentiation by Modulation of EID1 Activity. | Chen X et al. | β | 2016 | β |
| Self-renewal of tumor cells: epigenetic determinants of the cancer stem cell phenotype. | Ravasio R et al. | β | 2016 | β |
| The Functionality and Evolution of Eukaryotic Transcriptional Enhancers. | Buffry AD et al. | β | 2016 | β |
| An increased expression of PI-PLCΞ²1 is associated with myeloid differentiation and a longer response to azacitidine in myelodysplastic syndromes. | Cocco L et al. | β | 2015 | β |
| Chemical tagging and customizing of cellular chromatin states using ultrafast trans-splicing inteins. | David Y et al. | β | 2015 | β |
| Chromatin features, RNA polymerase II and the comparative expression of lens genes encoding crystallins, transcription factors, and autophagy mediators. | Sun J et al. | β | 2015 | β |
| Do changes in the BDNF promoter methylation indicate the risk of alcohol relapse? | Heberlein A et al. | β | 2015 | β |
| Histone profiles in cancer. | Riedel SS et al. | β | 2015 | β |
| Improved DNase-seq protocol facilitates high resolution mapping of DNase I hypersensitive sites in roots in Arabidopsis thaliana. | Cumbie JS et al. | β | 2015 | β |
| On Accounting for Sequence-Specific Bias in Genome-Wide Chromatin Accessibility Experiments: Recent Advances and Contradictions. | Madrigal P | β | 2015 | β |
| Regulation of catalase expression in healthy and cancerous cells. | Glorieux C et al. | β | 2015 | β |
| Three-dimensional regulation of transcription. | Cao J et al. | β | 2015 | β |