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PU.1 (Spi-1) and C/EBPα Regulate Expression of the Granulocyte-Macrophage Colony-Stimulating Factor Receptor α Gene
Open accessAbstract
Growth factor receptors play an important role in hematopoiesis. In order to further understand the mechanisms directing the expression of these key regulators of hematopoiesis, we initiated a study investigating the transcription factors activating the expression of the granulocyte-macrophage colony-stimulating factor (GM-CSF) receptor alpha gene. Here, we demonstrate that the human GM-CSF receptor alpha promoter directs reporter gene activity in a tissue-specific fashion in myelomonocytic cells, which correlates with its expression pattern as analyzed by reverse transcription PCR. The GM-CSF receptor alpha promoter contains an important functional site between positions -53 and -41 as identified by deletion analysis of reporter constructs. We show that the myeloid and B cell transcription factor PU.1 binds specifically to this site. Furthermore, we demonstrate that a CCAAT site located upstream of the PU.1 site between positions -70 and -54 is involved in positive-negative regulation of the GM-CSF receptor alpha promoter activity. C/EBP alpha is the major CCAAT/enhancer-binding protein (C/EBP) form binding to this site in nuclear extracts of U937 cells. Point mutations of either the PU.1 site or the C/EBP site that abolish the binding of the respective factors result in a significant decrease of GM-CSF receptor alpha promoter activity in myelomonocytic cells only. Furthermore, we demonstrate that in myeloid and B cell extracts, PU.1 forms a novel, specific, more slowly migrating complex (PU-SF) when binding the GM-CSF receptor alpha promoter PU.1 site. This is the first demonstration of a specific interaction with PU.1 on a myeloid PU.1 binding site. The novel complex is distinct from that described previously as binding to B cell enhancer sites and can be formed by addition of PU.1 to extracts from certain nonmyeloid cell types which do not express PU.1, including T cells and epithelial cells, but not from erythroid cells. Furthermore, we demonstrate that the PU-SF complex binds to PU.1 sites found on a number of myeloid promoters, and its formation requires an intact PU.1 site adjacent to a single-stranded region. Expression of PU.1 in nonmyeloid cells can activate the GM-CSF receptor alpha promoter. Deletion of the amino-terminal region of PU.1 results in a failure to form the PU-SF complex and in a concomitant loss of transactivation, suggesting that formation of the PU-SF complex is of functional importance for the activity of the GM-CSF receptor alpha promoter. Finally, we demonstrate that C/EBP alpha can also active the GM-CSF receptor alpha promoter in nonmyeloid cells. These results suggest that PU.1 and C/EBP alpha direct the cell-type-specific expression of GM-CSF receptor alpha, further establish the role of PU.1 as a key regulator of hematopoiesis, and point to C/EBP alpha as an additional important factor in this process.
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“PU.1 imparts its key functions by regulating vast number of myeloid gene promoters that include GM-CSF receptor a, M-CSF receptor (M-CSFR), scavenger receptor CD163, and CD11b, etc (6,7).”
From FBW7 Inhibits Myeloid Differentiation in Acute Myeloid Leukemia via GSK3-Dependent Ubiquitination of PU.1 (2021) · cites this paper as [6]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“In cotransfection experiments, RUNX1, PU.1, and CEBPA play essential roles in activation of the hematopoietic differentiation genes MCSFR and GMCSFR.7,8,31”
From RUNX1 regulates corepressor interactions of PU.1 (2011) · cites this paper as [31]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“The block in the development of these lineages occurs at very early stages, because the mutant animals completely lack lymphoid and myeloid progenitor cells, rendering it difficult to determine the precise role of PU.1 during stage- and lineage-specific gene expression.”
From AKT Induces Transcriptional Activity of PU.1 through Phosphorylation-mediated Modifications within Its Transactivation Domain (2001) · cites this paper as [67]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“Targeted disruption of PU.1 in mice severely impairs the development of lymphoid (B cells) and myeloid (macrophages and neutrophils) lineages.”
From AKT Induces Transcriptional Activity of PU.1 through Phosphorylation-mediated Modifications within Its Transactivation Domain (2001) · cites this paper as [67]
In the citing paper
“In myeloid lineages, the putative PU.1 target genes include G-SCF receptor [23], GM-CSF receptor [24] and M-CSF receptor [25].”
From PU.1 and partners: regulation of haematopoietic stem cell fate in normal and malignant haematopoiesis (2009) · cites this paper as [24]
In the citing paper
“C/EBP-α expression is prominent in immature myeloid cells [24, 101].”
From PU.1 and partners: regulation of haematopoietic stem cell fate in normal and malignant haematopoiesis (2009) · cites this paper as [24]
In the citing paper
“Each factor has been shown to synergize on various promoters, including M-CSF receptor promoter and neutrophil elastase (NE) promoter [24, 63].”
From PU.1 and partners: regulation of haematopoietic stem cell fate in normal and malignant haematopoiesis (2009) · cites this paper as [24]
In the citing paper
“C/EBP-␣ minimally activates several myeloid cell-specific promoters, including those for cytokine receptors (e.g., GM-CSF, G-CSF, and M-CSF receptors) (26,65,78,79) and granule proteins (e.g., NE) (50).”
From The t(8;21) Fusion Product, AML-1–ETO, Associates with C/EBP-α, Inhibits C/EBP-α-Dependent Transcription, and Blocks Granulocytic Differentiation (1998) · cites this paper as [26]
In the citing paper
“Moreover, C/EBP-␣ cooperates with other myeloid transcription factors, including AML-1B and PU.1, to synergistically upregulate the expression of several myeloid cellspecific promoters (26,50,78).”
From The t(8;21) Fusion Product, AML-1–ETO, Associates with C/EBP-α, Inhibits C/EBP-α-Dependent Transcription, and Blocks Granulocytic Differentiation (1998) · cites this paper as [26]
In the citing paper
“Each factor has been shown to synergize on various promoters, including M-CSF receptor promoter and neutrophil elastase promoter.15,35”
From Granulocyte inducer C/EBPα inactivates the myeloid master regulator PU.1: possible role in lineage commitment decisions (2002) · cites this paper as [15]
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“C/EBP is important in the regulation of myeloid differentiation, being expressed particularly in early myeloid cells, in addition to regulating a number of granulocyte-specific genes (Hohaus et al., 1995; Oelgeschlager et al., 1996; Smith et al., 1996; Petrovick et al., 1998).”
BackgroundThe RUNX1–PU.1 axis in the control of hematopoiesis
Imperato, M. R., Cauchy, P., Obier, N., & Bonifer, C. (2015) · International Journal of Hematology · doi:10.1007/s12185-015-1762-8 · Cited by 94
“1 is a master regulator of later hematopoiesis and is required for commitment to the myeloid lineage since together with C/EBPα it controls the expression of the receptors for GM-CSF [46], and of CSF-1 which are critical cytokines for myelopoiesis [47, 48].”
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The Transcription Factor PU.1 is a Critical Regulator of Cellular Communication in the Immune System
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“1/Spi-1 is involved in myeloid lineage determination via regulation of target genes, including granulocyte colony-stimulating factor receptor (31), granulocyte-macrophage colony-stimulating factor receptor (32) and macrophage colony-stimulating factor receptor (33).”
BackgroundUse of RDA analysis of knockout mice to identify myeloid genes regulated in vivo by PU.1 and C/EBP
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Surprising new roles for PU.1 in the adaptive immune response
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“1 is Csf2ra, the gene coding for the GM-CSFRa chain (26).”
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“Each factor has been shown to synergize on various promoters, including M-CSF receptor promoter and neutrophil elastase (NE) promoter [24, 63].”
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PU.1 Is Essential for p47 Promoter Activity in Myeloid Cells
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RUNX1 regulates corepressor interactions of PU.1
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c-Jun Homodimers Can Function as a Context-Specific Coactivator
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“1 or C/EBP is enhanced through association with multiple protein partners (26, 53, 60, 61).”
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Metadata
- Authors
- Hohaus, S., Petrovick, M. S., Voso, M. T., Sun, Z., Zhang, D.-E., & Tenen, D. G.
- Affiliations
- Harvard University (US)
- Corresponding author
- Tenen, Daniel G.
- Venue
- Molecular and Cellular Biology
- Publisher
- Informa UK Limited
- Published
- 1995-10-01
- Volume
- 15
- Issue
- 10
- Pages
- 5830-5845
- ISSN
- 0270-7306 (ISSN-L)
- 1098-5549
- PMC
- PMC230835
- OpenAlex
- W2161743101
- Cited by
- 284
- References
- 73
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 4 · 2023: 5 · 2022: 8 · 2021: 3 · 2020: 6 · 2019: 6 · 2018: 7 · 2017: 5 · 2016: 5 · 2015: 8 · 2014: 5 · 2013: 7 · 2012: 6
- FWCI
- 5.58
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Molecular and Cellular Biology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
- Funders
- American Lung Association
- National Cancer Institute (CA 41456, R01CA041456)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK048660, DK48660)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Immunology and Microbiology › Immunology › Cytokine Signaling Pathways and Interactions
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Keywords
- PU.1, SPI-1, C/EBPα, GM-CSF receptor alpha, transcription factor binding sites, myelomonocytic cells, B cells, promoter regulation, transcriptional activation, hematopoiesis, single-stranded DNA binding, U937 cells
- MeSH terms
- Amino Acid Sequence, B-Lymphocytes, Base Sequence, Cell Line, DNA, DNA-Binding Proteins, DNA, Single-Stranded, Hematopoiesis, Humans, Methylation, Molecular Sequence Data, Monocytes, Mutation, Nuclear Proteins, Promoter Regions, Genetic, T-Lymphocytes, Transcription Factors, Transcriptional Activation, Retroviridae Proteins, Oncogenic, Receptors, Granulocyte-Macrophage Colony-Stimulating Factor, Genes, Reporter, CCAAT-Enhancer-Binding Proteins
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