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PU.1 induces myeloid lineage commitment in multipotent hematopoietic progenitors
Open accessAbstract
Little is known about the transcription factors that mediate lineage commitment of multipotent hematopoietic precursors. One candidate is the Ets family transcription factor PU.1, which is expressed in myeloid and B cells and is required for the development of both these lineages. We show here that the factor specifically instructs transformed multipotent hematopoietic progenitors to differentiate along the myeloid lineage. This involves not only the up-regulation of myeloid-specific cell surface antigens and the acquisition of myeloid growth-factor dependence but also the down-regulation of progenitor/thrombocyte-specific cell-surface markers and GATA-1. Both effects require an intact PU.1 transactivation domain. Whereas sustained activation of an inducible form of the factor leads to myeloid lineage commitment, short-term activation leads to the formation of immature eosinophils, indicating the existence of a bilineage intermediate. Our results suggest that PU.1 induces myeloid lineage commitment by the suppression of a master regulator of nonmyeloid genes (such as GATA-1) and the concomitant activation of multiple myeloid genes.
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In the citing paper
“PU.1 regulates lineage-specific gene expression in a dose-dependent manner21–23.”
From Lymphoid gene expression supports neuroprotective microglia function (2025) · cites this paper as [21]
Experimental — accuracy not yet measuredIn the citing paper
“All activated macrophages, regardless of polarization state, express high levels of the transcription factors runt-related transcription factor 1 (RUNX1) and PU.1, which are thought to represent global regulators of macrophage phenotypic expression [20–22].”
From Macrophage polarization: an opportunity for improved outcomes in biomaterials and regenerative medicine (2012) · cites this paper as [22]
In the citing paper
“Interestingly, C/EBP-α is also known to cooperate with PU.1 in controlling the expression of the GM-CSF receptor [108].”
From PU.1 and partners: regulation of haematopoietic stem cell fate in normal and malignant haematopoiesis (2009) · cites this paper as [108]
In the citing paper
“During lineage commitment, activation of specific transcription factors has been shown to direct precursor cells to a particular differentiation pathway (3, 41).”
From Negative cross-talk between hematopoietic regulators: GATA proteins repress PU.1 (1999) · cites this paper as [41]
In the citing paper
“and C/EBP⑀ in particular) are essential for the commitment and/or terminal differentiation of myeloid progenitors to the eosinophil lineage (1)(2)(3)(4)(5)(6)(7)(8)(9).”
From Novel Combinatorial Interactions of GATA-1, PU.1, and C/EBPε Isoforms Regulate Transcription of the Gene Encoding Eosinophil Granule Major Basic Protein (2002) · cites this paper as [1]
In the citing paper
“PU.1 probably plays an important role at several stages in the differentiation process, and there is evidence that it is active at an early stage, mediating commitment of multipotential progenitor cells to the myeloid lineage.8”
From Granulocyte inducer C/EBPα inactivates the myeloid master regulator PU.1: possible role in lineage commitment decisions (2002) · cites this paper as [8]
In the citing paper
“PU.1 has been demonstrated to instruct transformed chicken multipotent hematopoietic progenitors to differentiate along the myeloid lineage.8”
From Granulocyte inducer C/EBPα inactivates the myeloid master regulator PU.1: possible role in lineage commitment decisions (2002) · cites this paper as [8]
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Citations
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BackgroundIshikawa, Y., Gamo, K., Yabuki, M., Takagi, S., Toyoshima, K., Nakayama, K., Nakayama, A., Morimoto, M., Miyashita, H., Dairiki, R., et al. (2016) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-16-0471 · Cited by 113
“1, is a DNA-binding transcription factor that plays a critical role in myeloid development and activates lineage-specific gene expression (19); our finding suggests that T-3775440 induces the ectopic upregulation of myeloid lineage genes in erythroid and megakaryocytic lineage cells.”
BackgroundRedirecting differentiation of hematopoietic progenitors by a transcription factor, GATA-2
Kitajima, K., Tanaka, M., Zheng, J., Yen, H., Sato, A., Sugiyama, D., Umehara, H., Sakai, E., & Nakano, T. (2005) · Blood · doi:10.1182/blood-2005-06-2527 · Cited by 82
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“The ETS family of transcription factors consists of a large number of proteins that perform diverse functions, such as serum stimulation of the c-fos promoter (52), activation of the herpes simplex virus immediate-early promoter (36), regulation of immunoglobulin light-chain enhancers (13), control of lymphoid and mye…”
BackgroundMicroRNA-155 Implication in M1 Polarization and the Impact in Inflammatory Diseases
Paşca, S., Jurj, A. M., Petrushev, B., Tomuleasa, C., & Matei, D. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00625 · Cited by 85
Eosinophils in Infection and Intestinal Immunity
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“These cluster-specific peaks were enriched for lineage-determining TF motifs, such as RUNX and ETS factors in T lymphocytes 23,24 , SPI (PU.1) factors in myeloid lineage cells 25 , TP63 in keratinocytes 26 and MITF in melanocytes 27 (Fig.”
Bellantuono, I. (2004) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2003.10.008 · Cited by 77
The mechanism of repression of the myeloid-specific c-fms gene by Pax5 during B lineage restriction.
Tagoh, H., Ingram, R., Wilson, N., Salvagiotto, G., Warren, A. J., Clarke, D., Busslinger, M., & Bonifer, C. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7600997 · Cited by 74
“Overexpression of the transcription factor PU.1 in multipotent progenitor cells shifts differentiation toward myeloid cells (Nerlov and Graf, 1998; DeKoter and Singh, 2000; Yamada et al, 2001; McIvor et al, 2003).”
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BSAP Can Repress Enhancer Activity by Targeting PU.1 Function
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“1 also appears to play a role in terminal differentiation within the macrophage lineage (14, 21, 38, 44) and may be crucial for the proper tissue-specific and temporal regulation of immunoglobulin k chain (Igk) gene rearrangement (20, 22).”
BackgroundInhibition of CBP-Mediated Protein Acetylation by the Ets Family Oncoprotein PU.1
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“1 in multipotent progenitor cells leads to myeloid differentiation at the expense of erythroid cell formation and GATA-1 expression (53).”
BackgroundPI3K: A master regulator of brain metastasis‐promoting macrophages/microglia
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“Moreover, it has been established that the macrophage-specific enhancer selection is largely dependent on binding of PU.1, which occupies most enhancers in the macrophage genome as a myeloid master TF (Bowman et al., 2016; Nerlov & Graf, 1998; Vangala et al., 2003).”
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The activity of medicinal plants and secondary metabolites on eosinophilic inflammation
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“1 in cells cannot drive further differentiation of myeloblasts to monocytes (43, 48), suggesting that PU.”
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Gata1 regulates dendritic-cell development and survival
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PU.1 regulates TCR expression by modulating GATA-3 activity
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“1 is an ETS family transcription factor that regulates various genes, including cytokine receptors required for the development of lymphoid and myeloid lineages (10).”
Backgroundc-Jun Homodimers Can Function as a Context-Specific Coactivator
Grondin, B., Lefrançois, M., Tremblay, M. R., Saint-Denis, M., Haman, A., Waga, K., Bédard, A., Tenen, D. G., & Hoang, T. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00936-06 · Cited by 62
“myelomonocytic genes (6, 32, 40, 42, 64) and plays essential roles in the development of myeloid and lymphoid cells (13, 28, 48, 52, 68).”
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“1 in both normal myelopoiesis and the genesis of murine erythroleukemias, the role of this factor in myeloerythroid commitment decision has been investigated only indirectly by the analysis of cell lines representing one or the other lineage [12,13,15–17].”
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“GATA3 (HSC-MPP model), PU.1 and SPI-B (GMP model) and GATA1 (MEP model) had lineage-specific expression patterns consistent with known expression and activity of these factors 53,56,49,57–60 (Figure S12A-C).”
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“Notably, although high PU.1 levels are associated with myeloid commitment 64 , loss of PU.1 in vivo leads to increased myelopoiesis, impaired lym-phopoiesis, and induces myeloid leukemia 65,66 , which is compatible with the aging cellular phenotype.”
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“1 induce the commitment of multiple myeloid lineages(22), suggesting that PU.”
BackgroundUltrastructural evidence for human mast cell-eosinophil interactions in vitro
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“1 [4], Notch1 [67], Cdkn2a [68, 69], and Egr2 [70].”
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“Besides regulation of proliferation and differentiation pathways of myeloid and lymphoid lineages, graded concentrations of PU.1 protein function to specify distinct cell fates (B cell or macrophage) from a common lym-phoid-myeloid progenitor (30,38,50,51).”
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“The importance of Ets-genes in the di erentiation of lymphoid, myeloid and erythroid lineages has been abundantly illustrated (Pereira et al., 1999; Nerlov and Graf, 1998; for review, see Bassuk and Leyden, 1997; Ghysdael and Boureux, 1997).”
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Different Faces for Different Places: Heterogeneity of Neutrophil Phenotype and Function
Yang, P., Li, Y., Xie, Y., & Liu, Y. (2019) · Journal of Immunology Research · doi:10.1155/2019/8016254 · Cited by 65
Sp1/Sp3 and PU.1 Differentially Regulate β5Integrin Gene Expression in Macrophages and Osteoblasts
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HLS7, a hemopoietic lineage switch gene homologous to the leukemia‐inducing gene MLF1
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Elements of Transcription Factor Network Design for T-Lineage Specification
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Isocitrate ameliorates anemia by suppressing the erythroid iron restriction response
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“Consistent with this, ectopic expression of PU.1 in multipotent progenitors also promotes myeloid differentiation (Nerlov & Graf, 1998).”
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A Novel Retinoic Acid-Responsive Element Regulates Retinoic Acid-Induced BLR1 Expression
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“1 converts erythroid-megakaryocytic cells into myeloid cells (4).”
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PU.1 is regulated by NF-κB through a novel binding site in a 17 kb upstream enhancer element
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“1 has a crucial role during myeloid differentiation (Voso et al., 1994; Nerlov and Graf, 1998).”
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“1 is a transcription factor of the ETS family, whose members are essential for macrophage and B-cell differentiation.((37,38)) Essential roles for PU.”
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“In myeloid lineage precursor cells, PU.1 instructs hematopoietic progenitors to upregulate myeloid-specific cell surface antigens and to downregulate other cell-specific markers and transcription factors (Nerlov & Graf 1998).”
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Protein Acetylation Regulates Both PU.1 Transactivation and Igκ 3′ Enhancer Activity
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“Additionally, PU.1 can inhibit the expression of Gata factor encoding genes (Nerlov and Graf, 1998; Rekhtman et al., 1999; Zhang et al., 1999, 2000; Nerlov et al., 2000; Walsh et al., 2002).”
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“Recently PU1 and CEBPb were shown to be capable of inducing myeloid and eosinophil lineage commitment respectively in MEP cells [46,47].”
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Pioneer factors in development and cancer
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“1, a pioneer TF highly expressed in macrophages that binds to macrophage-specific enhancers and is essential for establishing and maintaining macrophage identity and viability (67).”
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“Conversely, GATA-1 inhibits binding of PU.1 to c-Jun, a critical coactivator of PU.1 transactivation of myeloid promoters [ 46-48 ].”
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Lentiviral PU.1 overexpression restores differentiation in myeloid leukemic blasts
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Metadata
- Authors
- Nerlov, C., & Graf, T.
- Affiliations
- European Molecular Biology Laboratory (DE)
- Venue
- Genes & Development
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 1998-08-01
- Volume
- 12
- Issue
- 15
- Pages
- 2403-2412
- ISSN
- 0890-9369 (ISSN-L)
- 1549-5477
- PMC
- PMC317050
- OpenAlex
- W1974612283
- Cited by
- 449
- References
- 46
- Citations by year
- 2026: 13 · 2025: 9 · 2024: 12 · 2023: 16 · 2022: 7 · 2021: 22 · 2020: 18 · 2019: 19 · 2018: 13 · 2017: 21 · 2016: 16 · 2015: 17 · 2014: 15 · 2013: 27 · 2012: 17
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genes & Development (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Sundhed og Sygdom, Det Frie Forskningsråd
- Medical Research Council
- Topics
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
- Keywords
- PU.1, ETS transcription factors, myeloid lineage commitment, hematopoietic progenitor cells, GATA-1, transactivation domain, eosinophils, cell surface markers
- MeSH terms
- Proto-Oncogene Protein Spi-1, Alleles, Animals, Cell Differentiation, Chick Embryo, DNA-Binding Proteins, Hematopoiesis, Hematopoietic Stem Cells, Humans, Proto-Oncogene Proteins, Transcription Factors, Transformation, Genetic, Trans-Activators, Gene Expression Regulation, Developmental, Erythroid-Specific DNA-Binding Factors, GATA1 Transcription Factor
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