Cited by 262Mast cells and histamineHematopoietic Stem Cell TransplantationGenomics and Chromatin Dynamics

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Cooperative and Antagonistic Interplay between PU.1 and GATA-2 in the Specification of Myeloid Cell Fates

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Walsh, Jonathan C., DeKoter, Rodney P., Lee, Hyun-Jun, Smith, Erica D., Lancki, David W., Gurish, Michael F., Friend, Daniel S., Stevens, Richard L., Anastasi, John, Singh, Harinder·2002·Immunity

DOI 10.1016/s1074-7613(02)00452-1

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Abstract

PU.1 and GATA transcription factors appear to antagonize each other's function in the development of distinct lineages of the hematopoietic system. In contrast, we demonstrate that PU.1, like GATA-2, is essential for the generation of mast cells. PU.1-/- hematopoietic progenitors can be propagated in IL-3 and differentiate into mast cells or macrophages upon restoration of PU.1 activity. Using these progenitors and a conditionally activatable PU.1 protein, we show that PU.1 can negatively regulate expression of the GATA-2 gene. In the absence of GATA-2, PU.1 promotes macrophage but not mast cell differentiation. Reexpression of GATA-2 in such progenitors enables the generation of mast cells. We propose a developmental model in which cooperative function or antagonistic crossregulation by PU.1 of GATA-2 promotes distinct myeloid cell fates.

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Overproduction of PU.1 in mast cell progenitors: its effect on monocyte- and mast cell-specific gene expression
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“1, positively or negatively, in certain contexts.(113) PU.”
Background
Bone marrow hematopoietic dysfunction in untreated chronic lymphocytic leukemia patients
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Mast Cells Acquire Monocyte-Specific Gene Expression and Monocyte-Like Morphology by Overproduction of PU.1
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“1 is involved in mast cell-specific gene regulation (7, 37, 39), we speculate that this synergistic effect may be essential for mast cell development.”
Background
Transcription factors controlling the beginning and end of B-cell differentiation
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“In addition, GATA-2 transcription can be regulated by several other transcription factors, including V-ets ETS1, 14 BMP4, 15 NOTCH1 , 16,17 PU.1 , 18 and EVI1, 19,20 and cytokines, such as IL-1 and TNF α .”
Chromatin regulation by RUNX1
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Molecular complexities of stem cells
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Roles of PU.1 in monocyte- and mast cell-specific gene regulation: PU.1 transactivates CIITA pIV in cooperation with IFN-
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Involvement of PU.1 in mast cell/basophil-specific function of the human IL1RL1/ST2 promoter.
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Chromatin Remodeler Recruitment during Macrophage Differentiation Facilitates Transcription Factor Binding to Enhancers in Mature Cells
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“4 days) in the presence of tamoxifen leads to differentiation of these cells into macrophage-like cells (24).”
Background
The analysis of novel distal Cebpa enhancers and silencers using a transcriptional model reveals the complex regulatory logic of hematopoietic lineage specification
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“PUER cells are blocked at a progenitor state and can be differentiated into either macrophage-or neutrophil-like cells by inducing the translocation of PU.1 (PUER) protein into the nucleus with 4-hydroxy-tamoxifen (OHT) (Dahl et al., 2003; Laslo et al., 2006; Walsh et al., 2002).”
BackgroundMethodInfluential
The proximal promoter of the human cathepsin G gene conferring myeloid-specific expression includes C/EBP, c-myb and PU.1 binding sites
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Causal Gene Regulatory Network Modeling and Genomics: Second-Generation Challenges
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“Modest levels of both PU.1 and GATA-1 establish a stable convivencia , as in mast cells (Walsh et al., 2002), whereas higher levels of either one will tip the balance.”
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Essential role of PU .1 in maintenance of mixed lineage leukemia‐associated leukemic stem cells
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“…instance, although GATA1 and PU.1 act reciprocally in the lineage determination of hematopoietic stem ⁄progenitor cells (Arinobu et al. 2007), a co-operative interplay between PU.1 and the GATA factors has been reported in mast cells (Henkel & Brown 1994; Walsh et al. 2002; Takemoto et al. 2010).”
Background
PU.1 Positively Regulates GATA-1 Expression in Mast Cells
Takemoto, C. M., Brandal, S., Jegga, A. G., Lee, Y.-N., Shahlaee, A. H., Ye, Y., DeKoter, R. P., & McDevitt, M. A. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0900927 · Cited by 15
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“1 also interacts synergistically or antagonistically with c-Jun, C/EBPδ, GATA-1, GATA-2, C/EBPα, c-Myb, CBP, AML-1B, AML-1/ETO, NF-EMS/Pip/IRF-4, and ICSBP/IRF-8, which governs most of the genes [37-47].”
Background
Navigating Transcriptional Coregulator Ensembles to Establish Genetic Networks
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“…act in cytokine pathways but may also affect TLR signaling crosstalk), or by acting as components of E3 ubiquitin ligase complexes to mediate the ubiquitination and proteasomal degradation of signaling molecules (such as IRAK1, TRAF6, and MyD88 itself), thereby terminating the signal [61].”
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Myeloid-derived NF-κB negative regulation of PU.1 and c/EBP-β-driven pro-inflammatory cytokine production restrains LPS-induced shock
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“1 and C/EBP family member transcriptional regulation of cell fate decisions have identified an important contribution from antagonistic and cooperative relationships between transcription factors.(54) The underlying molecular processes involved in the antagonism–cooperative switch are not yet clear; however, the conce…”
Background
Genome-scale definition of the transcriptional programme associated with compromised PU.1 activity in acute myeloid leukaemia
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“The reporter assays were carried out in PUER cells (Walsh et al., 2002), which act as bipotential granulocyte-monocyte progenitors (GMPs) and can be differentiated into macrophages or neutrophils by treatment with 4-OH-tamoxifen (OHT) in the presence of IL-3 or G-CSF respectively (Dahl et al.,…”
BackgroundMethod
Chromatin Dynamics during Differentiation of Myeloid Cells
Schönheit, J., Leutz, A., & Rosenbauer, F. (2014) · Journal of Molecular Biology · doi:10.1016/j.jmb.2014.08.015 · Cited by 15
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PU.1 is required to restrain myelopoiesis during chronic inflammatory stress
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“Our previously published analysis (Higa et al., 2021) of Cebpa-deficient MPPGM shows nearly identical patterns of overexpression in genes like Bmi1, Foxo3 andMycn (Tothova et al., 2007; Takubo et al., 2010; Merchant et al., 2011; Warr et al., 2013; Murakami et al., 2014; Scognamiglio et al., 2016).”
Background
Pathogenic human variant that dislocates GATA2 zinc fingers disrupts hematopoietic gene expression and signaling networks
Jung, M. M., Shen, S., Botten, G. A., Olender, T., Katsumura, K. R., Johnson, K. D., Soukup, A. A., Liu, P., Zhang, Q., Jensvold, Z. D., et al. (2023) · Journal of Clinical Investigation · doi:10.1172/jci162685 · Cited by 19
“Although the ETS factor PU.1 can antagonize GATA1 or GATA2 (74, 93, 94), it can cooperate with GATA2 in activation (95).”
Lung Function in African American Children with Asthma Is Associated with Novel Regulatory Variants of the KIT Ligand KITLG/SCF and Gene-By-Air-Pollution Interaction
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“However, these two factors collaborate in mast-cell development and function (106).”
Background
Data-driven modeling predicts gene regulatory network dynamics during the differentiation of multipotential hematopoietic progenitors
Handzlik, J. E., & Manu (2022) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1009779 · Cited by 11
A Novel GATA2 Protein Reporter Mouse Reveals Hematopoietic Progenitor Cell Types
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“This is in agreement with recent single-cell RNA sequencing analysis confirming heterogeneousMPPGata2 expression at themRNA level (Weinreb et al., 2020).”
BackgroundResult
Bone Marrow Monocytes and Derived Dendritic Cells from Myelodysplastic Patients Have Functional Abnormalities Associated with Defective Response to Bacterial Infection
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Authors: Walsh, J. C., DeKoter, R. P., Lee, H.-J., Smith, E. D., Lancki, D. W., Gurish, M. F., Friend, D. S., Stevens, R. L., Anastasi, J., & Singh, H.
Affiliations: University of Chicago (US)
Howard Hughes Medical Institute (US)
Brigham and Women's Hospital (US)
Corresponding author: Singh, Harinder
ORCID: DeKoter, Rodney P.
Lee, Hyun-Jun
Smith, Erica D.
Gurish, Michael F.
Singh, Harinder
Venue: Immunity
Publisher: Elsevier BV
Published: 2002-11
Volume: 17
Issue: 5
Pages: 665-676
ISSN: 1074-7613 (ISSN-L)
DOI: 10.1016/s1074-7613(02)00452-1
OpenAlex: W2145064410
Cited by: 262
References: 0
Citations by year: 2026: 4 · 2025: 8 · 2024: 7 · 2023: 7 · 2022: 3 · 2021: 10 · 2020: 7 · 2019: 7 · 2018: 7 · 2017: 8 · 2016: 11 · 2015: 16 · 2014: 18 · 2013: 8 · 2012: 11
FWCI: 4.01
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 3911 d)
Locations: Immunity (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Heart, Lung, and Blood Institute (HL07237, HL-36110, P01HL036110)
National Institute of General Medical Sciences (GM07151, T32GM007151)
National Institute of Allergy and Infectious Diseases (AI-23483, AI31599, R01AI023483)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Mast cells and histamine
Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords: PU.1, GATA2, mast cell differentiation, macrophage differentiation, hematopoietic progenitor cells, transcription factors
MeSH terms: Proto-Oncogene Protein Spi-1, Animals, DNA-Binding Proteins, Macrophages, Mast Cells, Proto-Oncogene Proteins, Transcription Factors, Trans-Activators, Zinc Fingers, Gene Expression Regulation, Developmental, Cell Lineage, Myelopoiesis, GATA2 Transcription Factor, Mice

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Cooperative and Antagonistic Interplay between PU.1 and GATA-2 in the Specification of Myeloid Cell Fates

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