Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position
Open accessAbstract
We describe an assay for transposase-accessible chromatin using sequencing (ATAC-seq), based on direct in vitro transposition of sequencing adaptors into native chromatin, as a rapid and sensitive method for integrative epigenomic analysis. ATAC-seq captures open chromatin sites using a simple two-step protocol with 500-50,000 cells and reveals the interplay between genomic locations of open chromatin, DNA-binding proteins, individual nucleosomes and chromatin compaction at nucleotide resolution. We discovered classes of DNA-binding factors that strictly avoided, could tolerate or tended to overlap with nucleosomes. Using ATAC-seq maps of human CD4(+) T cells from a proband obtained on consecutive days, we demonstrated the feasibility of analyzing an individual's epigenome on a timescale compatible with clinical decision-making.
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ATAC-seq is a landmark breakthrough that utilizes Tn5 transposase to fragment open chromatin and labels the genome with sequencing adaptors.
“ATAC-seq barges to the forefront as a landmark breakthrough that utilizes the Tn5 transposase to fragment open chromatin and labels the genome with sequencing adaptors [110].”
From Single-cell sequencing to multi-omics: technologies and applications (2024) · cites this paper as [110]
PU.1 binding sites are enriched for open chromatin as defined by DNase accessibility or ATAC-seq.
“The sites where PU.1 binds are enriched for open chromatin as defined by DNase accessibility or ATAC-seq [assay of transposase-accessible chromatin (94)]”
From Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development (2019) · cites this paper as [94]
ATAC-seq uses a hyperactive Tn5 transposase to measure the activity of regulatory DNA elements.
“We recently developed the assay for transposase-accessible chromatin with sequencing (ATAC-seq), which utilizes a hyperactive transposase (Tn5) to measure the activity of regulatory DNA elements (Buenrostro et al., 2013).”
From Coupled Single-Cell CRISPR Screening and Epigenomic Profiling Reveals Causal Gene Regulatory Networks (2019) · cites this paper as Buenrostro et al., 2013
ATAC-seq informs the identification of enhancers, nucleosome positioning, and inference of transcription factor binding.
“This method informs the identification of enhancers, the positioning of nucleosomes, and the inference of transcription factor binding (Buenrostro et al., 2013; Schep et al., 2015, 2017).”
From Coupled Single-Cell CRISPR Screening and Epigenomic Profiling Reveals Causal Gene Regulatory Networks (2019) · cites this paper as Buenrostro et al., 2013
Using DNase hypersensitivity or ATAC-seq data to infer open chromatin, followed by combining transcription factor binding with open chromatin footprinting, can provide a powerful and comprehensive way to identify tissue-specific transcription factor regulation.
“There is compelling evidence that using DNase hypersensitivity or ATAC-seq data to infer open chromatin, followed by combining transcription factor binding with open chromatin footprinting, can provide a powerful and comprehensive way to identify tissue-specific transcription factor regulation60,61.”
From Systems biology and gene networks in neurodevelopmental and neurodegenerative disorders (2015) · cites this paper as [60]
Assays that combine enzymatic digestion with sequencing to measure chromatin accessibility give an integrated map of chromatin states covering many functional regulatory elements.
“Thus, methods that measure chromatin accessibility by combining sensitivity to enzymatic digestion with sequencing6–8 provide an integrated map of chromatin states that encompasses a diverse repertoire of functional regulatory elements2,5.”
From Droplet-based combinatorial indexing for massive-scale single-cell chromatin accessibility (2019) · cites this paper as [8]
Chromatin accessibility from bulk ATAC-seq and DNase-seq and the aggregate chromatin accessibility across different single-cell technologies were highly correlated.
“We found that chromatin accessibility from bulk ATAC-seq8 and DNase-seq2 and the aggregate chromatin accessibility across the different single-cell technologies18,19,24,25 were highly correlated (Fig. 1c,d).”
From Droplet-based combinatorial indexing for massive-scale single-cell chromatin accessibility (2019) · cites this paper as [8]
Many newer single-cell multi-omics methods for chromatin accessibility derive from ATAC-seq, which employs Tn5 transposase to cut open chromatin and attach adaptors.
“Most recent single-cell multi-omics technologies that profile chromatin accessibility are primarily adapted from assay for transposase-accessible chromatin sequencing (ATAC-seq37), which uses the transposase Tn5 to fragment open chromatin and tag adaptors to the DNA38–42.”
From The technological landscape and applications of single-cell multi-omics (2023) · cites this paper as [37]
ATAC-seq can find open chromatin regions linked to transcription even with few cells, and it is simple and fast because it skips extraction and enzymatic digestion.
“ATAC-seq allows the identification of regions within the genome that have open chromatin states associated with transcription in low numbers of cells and is an easy and time-friendly method as it does not include extraction or enzymatic-digestion steps.”
From The technological landscape and applications of single-cell multi-omics (2023) · cites this paper as [37]
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Self-citation
- Authors
- Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y., & Greenleaf, W. J.
- Affiliations
- Howard Hughes Medical Institute (US)
- Stanford Medicine (US)
- Corresponding author
- Chang, Howard Y
- Greenleaf, William J
- Venue
- Nature Methods
- Published
- 2013-10-06
- Volume
- 10
- Issue
- 12
- Pages
- 1213-1218
- ISSN
- 1548-7091 (ISSN-L)
- 1548-7105
- PMC
- PMC3959825
- OpenAlex
- W2117757143
- Cited by
- 6,422
- References
- 38
- Citations by year
- 2026: 462 · 2025: 557 · 2024: 681 · 2023: 691 · 2022: 711 · 2021: 799 · 2020: 683 · 2019: 583 · 2018: 496 · 2017: 361 · 2016: 218 · 2015: 126 · 2014: 46 · 2013: 4
- FWCI
- 58.87
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Methods (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (U19AI057229)
- National Institute of Diabetes and Digestive and Kidney Diseases (U01DK089532, P30DK116074)
- National Institute of Neurological Disorders and Stroke (RC4NS073015)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (T32AR050942)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- ATAC-seq, open chromatin, DNA-binding proteins, nucleosome positioning, chromatin condensation, epigenetic profiling, CD4+ T cells, single-cell epigenomics
- MeSH terms
- Cell Separation, Chromatin, DNA-Binding Proteins, Enhancer Elements, Genetic, Flow Cytometry, Humans, Interleukin-2, Nucleosomes, Transcription Factors, CD4-Positive T-Lymphocytes, Polymerase Chain Reaction, Dimerization, Computational Biology, Epigenomics
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