Lineage-specific and single-cell chromatin accessibility charts human hematopoiesis and leukemia evolution
Open accessAbstract
We define the chromatin accessibility and transcriptional landscapes in 13 human primary blood cell types that span the hematopoietic hierarchy. Exploiting the finding that the enhancer landscape better reflects cell identity than mRNA levels, we enable 'enhancer cytometry' for enumeration of pure cell types from complex populations. We identify regulators governing hematopoietic differentiation and further show the lineage ontogeny of genetic elements linked to diverse human diseases. In acute myeloid leukemia (AML), chromatin accessibility uncovers unique regulatory evolution in cancer cells with a progressively increasing mutation burden. Single AML cells exhibit distinctive mixed regulome profiles corresponding to disparate developmental stages. A method to account for this regulatory heterogeneity identified cancer-specific deviations and implicated HOX factors as key regulators of preleukemic hematopoietic stem cell characteristics. Thus, regulome dynamics can provide diverse insights into hematopoietic development and disease.
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Wider-ranging epigenetic alterations, especially perturbing key enhancer landscapes with high similarity to human disease, support a role in the myeloid disease.
“our molecular analyses into gene regulatory circuits support a role for wider-ranging epigenetic alterations, especially perturbing key enhancer landscapes with high similarity to human disease (29).”
From PU.1-Dependent Enhancer Inhibition Separates <i>Tet2</i> -Deficient Hematopoiesis from Malignant Transformation (2022) · cites this paper as [29]
The Results section ('Synthetic normal analogs uncover AML-specific biology'; page unavailable) identifies altered regulatory modules in human acute myeloid leukemia, and the Discussion describes cancer-specific changes in chromatin accessibility. This supports the relevance of enhancer-associated epigenetic alterations to myeloid disease, but the source does not establish that the citing authors’ alterations have high similarity to those in human disease. (LLM, conf=0.82)
Experimental — accuracy not yet measuredGenome-wide datasets of TF binding and chromatin accessibility are not informative regarding the functional role of each TF in a given sequence context.
“Genome-wide datasets of TF binding and chromatin accessibility13,22,23 are not informative regarding the functional role of each TF in a given sequence context.”
From Design principles of cell-state-specific enhancers in hematopoiesis (2025) · cites this paper as [23]
The Results section ('Regulatory networks of normal hematopoiesis') says a motif sequence alone cannot identify the precise TF causing accessibility, especially when TFs share similar motifs. That supports a limitation of accessibility data, but not the broader claim that genome-wide TF-binding and accessibility datasets are uninformative about each TF’s functional role in a given sequence context. The paper also uses accessibility data, integrated with RNA-seq, to identify putative regulators. (LLM, conf=0.85)
Experimental — accuracy not yet measuredARCH HSCs showed no discernible alterations of PU.1 mRNA levels compared with age-matched healthy individual-derived control cells.
“ARCH HSCs, closely resembling the regulatory landscape that defines the transcriptional make-up, of non-ARCH, healthy multipotent progenitor (MPP) cells (29), showed no discernible alterations of PU.1 mRNA levels compared with age-matched healthy individual-derived control cells (Fig. 1A).”
From PU.1-Dependent Enhancer Inhibition Separates <i>Tet2</i> -Deficient Hematopoiesis from Malignant Transformation (2022) · cites this paper as [29]
In LSCs, PU.1 mRNA expression was found reduced to sub-haploinsufficient levels by 21% ± 4% (P < 0.01) compared with their healthy counterparts.
“However, in LSCs, mostly sharing transcriptional programs with healthy granulocytic–monocytic progenitors (GMPs; ref. 29), PU.1 mRNA expression was found reduced to sub-haploinsufficient levels [by 21% ± 4% (P < 0.01) compared with their healthy counterparts; Fig. 1B].”
From PU.1-Dependent Enhancer Inhibition Separates <i>Tet2</i> -Deficient Hematopoiesis from Malignant Transformation (2022) · cites this paper as [29]
The strong effects of p300 inhibition on promoter activation support previous reports on the role of p300 catalytic activity in assembling the pre-initiation complex and recruiting RNA polymerase.
“also supports previous reports on the role of the catalytic activity of p300 in assembling the pre-initiation complex (PIC) and recruiting RNA polymerase51.”
From Single-molecule states link transcription factor binding to gene expression (2024) · cites this paper as [51]
The Results section on regulatory networks of normal hematopoiesis discusses transcription-factor motifs and chromatin accessibility, not p300 catalytic activity. Searches for p300, pre-initiation complex assembly, and RNA polymerase recruitment found no passage addressing the attributed mechanism in our copy. (LLM, conf=0.76)
Experimental — accuracy not yet measured
Recent observations indicate that inhibiting p300 catalytic activity stabilizes interactions with chromatin.
“and is instead consistent with recent observations that inhibiting p300 catalytic activity actually stabilizes interactions with chromatin51,52.”
From Single-molecule states link transcription factor binding to gene expression (2024) · cites this paper as [51]
The Results passages on chromatin accessibility discuss hematopoietic regulatory motifs and AML, not p300 inhibition or p300–chromatin interactions. Searches for p300 catalytic inhibition and chromatin binding returned no passage addressing the claimed stabilization. (LLM, conf=0.76)
Experimental — accuracy not yet measuredscATAC-seq studies revealed regulatory heterogeneity within immunophenotypically sorted cellular populations that are governed by diverse regulatory programmes at individual cis-regulatory elements and by relatively simple transcription factor motif dynamics.
“These studies revealed regulatory heterogeneity within immunophenotypically sorted cellular populations that are governed by diverse regulatory programmes at individual cis-regulatory elements and by relatively simple TF motif dynamics.”
From Mapping gene regulatory networks from single-cell omics data (2018) · cites this paper as [61]
Earlier work proposed that regulatory element activity may better reflect cell potential and be more cell-type specific than gene expression.
“previous work has suggested that activity of regulatory elements may be a more accurate reflection of cell potential and perhaps provide higher cell-type specificity than measurements of gene expression17.”
From Droplet-based combinatorial indexing for massive-scale single-cell chromatin accessibility (2019) · cites this paper as [17]
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“Currently, chromatin accessibility pro fi ling (e.g., ATAC-seq) is being explored as a biomarker tool in psychiatry (44).”
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- Authors
- Corces, M. R., Buenrostro, J. D., Wu, B., Greenside, P. G., Chan, S. M., Koenig, J. L., Snyder, M. P., Pritchard, J. K., Kundaje, A., Greenleaf, W. J., Majeti, R., & Chang, H. Y.
- Affiliations
- Stanford Medicine (US)
- Broad Institute (US)
- Stanford University (US)
- University Health Network (CA)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Majeti, Ravindra
- Chang, Howard Y
- ORCID
- Venue
- Nature Genetics
- Published
- 2016-08-15
- Volume
- 48
- Issue
- 10
- Pages
- 1193-1203
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- PMC
- PMC5042844
- OpenAlex
- W2514448720
- Cited by
- 1,151
- References
- 64
- Citations by year
- 2026: 63 · 2025: 92 · 2024: 123 · 2023: 120 · 2022: 157 · 2021: 156 · 2020: 146 · 2019: 132 · 2018: 90 · 2017: 66 · 2016: 6
- FWCI
- 50.92
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Genetics (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- National Human Genome Research Institute (P50HG007735, K22HG000044, T32HG000044)
- National Cancer Institute (R25CA180993, F31CA180659, R01CA188055, P30CA124435)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (UH2AR067676)
- 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 › Molecular Biology › Chromatin Remodeling and Cancer
- Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
- Keywords
- chromatin accessibility, hematopoiesis, acute myeloid leukemia, enhancer landscape, hematopoietic differentiation, regulatory evolution, mutational burden, transcriptional landscape, single-cell chromatin accessibility
- MeSH terms
- Chromatin, Clone Cells, Enhancer Elements, Genetic, Hematopoiesis, Humans, Regulatory Sequences, Nucleic Acid, Tumor Cells, Cultured, Leukemia, Myeloid, Acute, Gene Expression Regulation, Neoplastic, Sequence Analysis, DNA, Cell Lineage, Gene Expression Profiling, Myelopoiesis
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