Simple Combinations of Lineage-Determining Transcription Factors Prime cis-Regulatory Elements Required for Macrophage and B Cell Identities
Open accessAbstract
Genome-scale studies have revealed extensive, cell type-specific colocalization of transcription factors, but the mechanisms underlying this phenomenon remain poorly understood. Here, we demonstrate in macrophages and B cells that collaborative interactions of the common factor PU.1 with small sets of macrophage- or B cell lineage-determining transcription factors establish cell-specific binding sites that are associated with the majority of promoter-distal H3K4me1-marked genomic regions. PU.1 binding initiates nucleosome remodeling, followed by H3K4 monomethylation at large numbers of genomic regions associated with both broadly and specifically expressed genes. These locations serve as beacons for additional factors, exemplified by liver X receptors, which drive both cell-specific gene expression and signal-dependent responses. Together with analyses of transcription factor binding and H3K4me1 patterns in other cell types, these studies suggest that simple combinations of lineage-determining transcription factors can specify the genomic sites ultimately responsible for both cell identity and cell type-specific responses to diverse signaling inputs.
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PU.1 can bind as a collaboration-dependent partner with NF-κB or with C/EBPα/β or IRF4/8.
“or as a collaboration-dependent partner in binding complexes, either with activation-dependent factors like NF-κB or with lineage-defining partners like C/EBPα (or β) or IRF4/8 (13–15)”
From Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development (2019) · cites this paper as [13]
The section “PU.1 binds in the vicinity of other lineage-determining transcription factors” (page unavailable) reports nearby PU.1 and C/EBPα/β binding sites and describes a PU.1–IRF4/8 ternary complex. “Combinatorial interplay delineates stage-specific cistromes” (page unavailable) further reports reciprocal effects of PU.1 and C/EBPβ on binding. For NF-κB, however, the paper reports nearby motifs and its activation in TLR4 signaling, not a collaboration-dependent PU.1–NF-κB binding complex. (LLM, conf=0.87)
Experimental — accuracy not yet measuredPU.1 binding sites and binding partners are not the same in early T-cell precursors as in myeloid cells or B lineage cells.
“PU.1 binding sites and PU.1 binding partners are not the same in early T-cell precursors as in myeloid cells or B lineage cells (13, 80, 84, 85)”
From Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development (2019) · cites this paper as [13]
The sections “Distinct PU.1 binding programs in macrophages and B cells” and “PU.1 binds in the vicinity of other lineage-determining transcription factors” report different PU.1 binding sites and nearby factor motifs in macrophages and B cells (page numbers unavailable). Our copy does not compare either lineage with early T-cell precursors, so it does not establish the claimed T-cell difference. (LLM, conf=0.86)
Experimental — accuracy not yet measuredMLL4 binding at enhancers coincides with the binding of master regulators.
“MLL4 binding at enhancers has been shown to coincide with the binding of master regulators42–44.”
From HNF4A guides the MLL4 complex to establish and maintain H3K4me1 at gene regulatory elements (2024) · cites this paper as [42]
The section ‘PU.1 induces sequential nucleosome remodelling and histone H3K4 monomethylation’ reports that distal sites bound by lineage-determining factors are associated with H3K4me1, a mark of enhancer-like regions. That supports the enhancer–regulator association, but the paper does not establish that MLL4 itself binds at those sites or coincides with the regulators. (LLM, conf=0.82)
Experimental — accuracy not yet measuredThe intronic Myc peak was also present in two independent published macrophage datasets.
“The intronic Myc peak was also present in two independent published macrophage datasets (Heinz et al., 2010; GEO accession no. GSE21512).”
From PU.1 enforces quiescence and limits hematopoietic stem cell expansion during inflammatory stress (2021) · cites this paper as Heinz et al., 2010
The “Distinct PU.1 binding programs in macrophages and B cells” section describes a macrophage ChIP-seq dataset with intragenic peaks, so Heinz et al. is a relevant published dataset. Our copy does not identify an intronic Myc peak or establish its presence in that dataset; the other dataset is separately identified by the GEO accession in the citing sentence. (LLM, conf=0.83)
Experimental — accuracy not yet measuredDifferentially regulated H3K27ac or STAT3 sites were identified from three (H3K27ac) or two (STAT3) biological replicates using DESeq.
“Differentially regulated H3K27ac or STAT3 sites were identified from three (H3K27ac) or two (STAT3) biological replicates using DESeq65 in the default parameters through HOMER66 (http://homer.salk.edu/homer/).”
From Synergistic gene expression during the acute phase response is characterized by transcription factor assisted loading (2017) · cites this paper as [66]
In myeloid and B-lymphoid cells, SPI1 activates lineage-specific genes due to lineage-specific coactivators at enhancers.
“In myeloid and B-lymphoid cells, SPI1 activates lineage-specific genes due to lineage-specific coactivators at enhancers (6,7,68).”
From HDAC1 and PRC2 mediate combinatorial control in SPI1/PU.1-dependent gene repression in murine erythroleukaemia (2022) · cites this paper as [7]
Activation of common housekeeping genes is associated with an enrichment of SPI1 occupancy at promoters without requiring lineage-specific coactivators but with a higher affinity of binding to chromatin compared to enhancers.
“Instead, activation of common housekeeping genes is associated with an enrichment of SPI1 occupancy at promoters without requiring lineage-specific coactivators but with a higher affinity of binding to chromatin compared to enhancers (6,7,68).”
From HDAC1 and PRC2 mediate combinatorial control in SPI1/PU.1-dependent gene repression in murine erythroleukaemia (2022) · cites this paper as [7]
Differentially bound sites between macrophages and B cells were mostly located at enhancers, whereas similar occupancy levels in both cell types were observed at TSS-proximal regions.
“A parallel analysis of Spi-1 genomic occupancy in macrophages and B cells showed that differentially bound sites between the two lineages were mostly located at the enhancers, whereas similar occupancy levels in both cell types were observed at TSS-proximal regions (13,14).”
From Spi-1/PU.1 activates transcription through clustered DNA occupancy in erythroleukemia (2012) · cites this paper as [14]
Several Spi-1 motifs within 100 bp of the central Spi-1 motif inside a Spi-1 binding site were identified in macrophages-specific or macrophages and B cells commonly bound sites of Spi-1.
“Moreover, in a recent study, several Spi-1 motifs within 100 bp of the central Spi-1 motif inside a Spi-1 binding site were identified in macrophages-specific or macrophages and B cells commonly bound sites of Spi-1 (14), but the impact of the Spi-1 motif multiplicity was not investigated in regard to the gene transactivation and binding regions in this study.”
From Spi-1/PU.1 activates transcription through clustered DNA occupancy in erythroleukemia (2012) · cites this paper as [14]
Top de novo motifs identified by HOMER within vitC deMRs were for PU.1 (34%), CEBPβ (15%), HIF1α (68%) and RUNX1 (30%).
“Consistent with the observed GO associations, the top de novo motifs identified by HOMER35 were for PU.1 (34%), CEBPβ (15%), HIF1α (68%) and RUNX1 (30% Figure 2d).”
From Vitamin C-induced epigenomic remodelling in IDH1 mutant acute myeloid leukaemia (2018) · cites this paper as [35]
Microglial enhancers are primed by relatively simple combinations of lineage-determining transcription factors to become sites of activity of broadly expressed signal-dependent transcription factors.
“Microglial enhancers are primed by relatively simple combinations of LDTFs (31, 32) to become sites of activity of broadly expressed signal-dependent transcription factors (SDTFs).”
From An environment-dependent transcriptional network specifies human microglia identity (2017) · cites this paper as [31]
Within cell-specific enhancers, DNA sequences provide information about the identities of key lineage-determining transcription factors and the activity states of signaling pathways that control the functions of signal-dependent transcription factors.
“Within cell-specific enhancers, DNA sequences provide information about the identities of key LDTFs and the activity states of signaling pathways that control the functions of SDTFs (31, 33–35).”
From An environment-dependent transcriptional network specifies human microglia identity (2017) · cites this paper as [31]
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- Authors
- Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y. C., Laslo, P., Cheng, J. X., Murre, C., Singh, H., & Glass, C. K.
- Affiliations
- University of California San Diego (US)
- University of Chicago (US)
- University of Leeds (GB)
- Genentech (US)
- Corresponding author
- Glass, Christopher K.
- ORCID
- Venue
- Molecular Cell
- Publisher
- Elsevier BV
- Published
- 2010-05
- Volume
- 38
- Issue
- 4
- Pages
- 576-589
- ISSN
- 1097-2765 (ISSN-L)
- PMC
- PMC2898526
- OpenAlex
- W2014677321
- Cited by
- 13,382
- References
- 49
- Citations by year
- 2026: 1075 · 2025: 1447 · 2024: 1483 · 2023: 1473 · 2022: 1305 · 2021: 1435 · 2020: 1177 · 2019: 939 · 2018: 791 · 2017: 653 · 2016: 461 · 2015: 422 · 2014: 309 · 2013: 188 · 2012: 109
- FWCI
- 50.91
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Molecular Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Heart, Lung, and Blood Institute (F32HL083752, HC088093)
- National Cancer Institute (R01CA078384, R01CA052599, R01CA054198, CA 52599)
- National Institute of General Medical Sciences (P50GM081892)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK063491, DK62434, U19DK062434, P30DK063491, R01DK091183)
- 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
- PU.1, cis-regulatory elements, macrophage identity, B cell identity, H3K4me1, H3K4 monomethylation, nucleosome remodeling, liver X receptor, transcription factor binding sites
- MeSH terms
- Proto-Oncogene Protein Spi-1, Animals, B-Lymphocytes, Binding Sites, Macrophages, Male, Mice, Inbred C57BL, Proto-Oncogene Proteins, Transcription Factors, Trans-Activators, Cell Lineage, Oligonucleotide Array Sequence Analysis, Regulatory Elements, Transcriptional, Mice
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