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PU.1 regulates both cytokine‐dependent proliferation and differentiation of granulocyte/macrophage progenitors
Open accessAbstract
PU.1 is a unique regulatory protein required for the generation of both the innate and the adaptive immune system. It functions exclusively in a cell-intrinsic manner to control the development of granulocytes, macrophages, and B and T lymphocytes. We demonstrate that mutation of the PU.1 gene causes a severe reduction in myeloid (granulocyte/macrophage) progenitors. PU.1 -/- myeloid progenitors can proliferate in vitro in response to the multilineage cytokines interleukin-3 (IL-3), IL-6 and stem cell factor but are unresponsive to the myeloid-specific cytokines granulocyte-macrophage colony-stimulating factor (GM-CSF), G-CSF and M-CSF. The failure of PU.1 -/- progenitors to respond to G-CSF is bypassed by transient signaling with IL-3. In the presence of IL-3 and G-CSF, PU.1 -/- progenitors can differentiate into granulocytic precursors containing myeloperoxidase-positive granules. Thus PU.1 is not essential for specification of granulocytic precursors, but is required for their further differentiation. The failure of PU.1 -/- progenitors to respond to M-CSF is due to lack of c-fms gene transcription. Transduction of c-fms into PU.1 -/- myeloid progenitors bypasses the block to M-CSF-dependent proliferation but does not induce detectable macrophage differentiation. Therefore, PU. 1 appears to be essential for specification of monocytic precursors. Importantly, retroviral transduction of PU.1 into mutant progenitors restores responsiveness to myeloid-specific cytokines and development of mature granulocytes and macrophages. Thus PU.1 controls myelopoiesis by regulating both proliferation and differentiation pathways.
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“These findings are consistent with prior work indicating PU.1 can constrain myelopoietic activity (DeKoter et al., 1998; Dakic et al., 2005)”
From PU.1 is required to restrain myelopoiesis during chronic inflammatory stress (2023) · cites this paper as DeKoter et al., 1998
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“We and others have previously shown that the myeloid ‘master regulator’ transcription factor PU.1 (DeKoter et al., 1998; Singh et al., 1999) is upregulated at the transcriptional and protein levels in HSC by chronic inflammatory signals such as the pro-inflammatory cytokine IL-1β (Algeciras-Schimnich et al., 2003; Pietras et al., 2016; Hernandez et al., 2020; Rabe et al., 2020; Chavez et al., 2021”
From PU.1 is required to restrain myelopoiesis during chronic inflammatory stress (2023) · cites this paper as DeKoter et al., 1998
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“Consistent with this, PU.1 is expressed at low levels in hematopoietic stem cells and is relatively more abundant during monocyte versus neutrophil differentiation (43).”
From PU.1, Interferon Regulatory Factor (IRF) 2, and the Interferon Consensus Sequence-binding Protein (ICSBP/IRF8) Cooperate to Activate NF1 Transcription in Differentiating Myeloid Cells (2007) · cites this paper as [43]
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Variety matters: Diverse functions of monocyte subtypes in vascular inflammation and atherogenesis
Vlacil, A.-K., Schuett, J., Schieffer, B., & Grote, K. (2018) · Vascular Pharmacology · doi:10.1016/j.vph.2018.12.002 · Cited by 29
Santo, J. P. D., Radtke, F., & Rodewald, H.-R. (2000) · Current Opinion in Immunology · doi:10.1016/s0952-7915(99)00066-7 · Cited by 29
Functional significance of mononuclear phagocyte populations generated through adult hematopoiesis
Gutknecht, M. F., & Bouton, A. H. (2014) · Journal of Leukocyte Biology · doi:10.1189/jlb.1ri0414-195r · Cited by 30
The transcription factor PU.1 does not regulate lineage commitment but has lineage-specific effects
McKercher, S. R., Henkel, G. W., & Maki, R. A. (1999) · Journal of Leukocyte Biology · doi:10.1002/jlb.66.5.727 · Cited by 28
“These results demonstrate expression of early myeloid genes in embryos and ES cells [36], in vitro proliferation of granulocytic precursors in response to growth factors [ 37 ], and the expression of some eosinophil mRNA species in fetal liver [30].”
ResultDeng, G., Wang, P., Su, R., Sun, X., Wu, Z., Huang, Z., Gu, L., Yu, H., Zhao, Z., He, Y., et al. (2024) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2024-009983 · Cited by 32
“SPI1 + CD68 + TAMs have shown promising effects in combined antiangiogenic and immunotherapy, thereby providing a novel therapeutic strategy in the treatment of GC. 49”
Bonifer, C., Hoogenkamp, M., Krysinska, H., & Tagoh, H. (2008) · Seminars in Immunology · doi:10.1016/j.smim.2008.05.001 · Cited by 27
Chromatin-based regulation of cytokine transcription in Th2 cells and mast cells
Monticelli, S., Lee, D. U., Nardone, J., Bolton, D. L., & Rao, A. (2005) · International Immunology · doi:10.1093/intimm/dxh329 · Cited by 27
Riemschneider, S., Kohlschmidt, J., Fueldner, C., Esser, C., Hauschildt, S., & Lehmann, J. (2018) · Toxicology Letters · doi:10.1016/j.toxlet.2018.07.050 · Cited by 26
PU.1 supports proliferation of immature erythroid progenitors
Fisher, R. C., Slayton, W. B., Chien, C. D., Guthrie, S. M., Bray, C. L., & Scott, E. W. (2003) · Leukemia Research · doi:10.1016/s0145-2126(03)00178-4 · Cited by 29
Mechanisms Underlying the Selection and Function of Macrophage-Specific EnhancersPreprint
Link, V. M., Gosselin, D., & Glass, C. K. (2015) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2015.80.027367 · Cited by 25
“Indeed, despite the fact that every subset of resident tissue macrophages in the body depends on PU.1 activity (McKercher et al. 1996; DeKoter et al. 1998; Schulz et al. 2012), gene expression in these cells varies greatly from one subset to another (Gautier et al. 2012).”
BackgroundYang, G. C. H., Besanceney, C., & Tam, W. (2009) · Diagnostic Cytopathology · doi:10.1002/dc.21215 · Cited by 24
Hu, L., Huang, W., Hjort, E. E., Bei, L., Platanias, L. C., & Eklund, E. A. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.681361 · Cited by 23
Bone Development and Remodeling
Maes, C., & Kronenberg, H. M. (2015) · Elsevier eBooks · doi:10.1016/b978-0-323-18907-1.00060-3 · Cited by 26
Lapko, N., Zawadka, M., Połosak, J., Worthen, G. S., Danet-Desnoyers, G. A., Puzianowska‐Kuźnicka, M., & Laudański, K. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00401 · Cited by 25
Sourki, P. A., Pourfathollah, A. A., Kaviani, S., Zomorrod, M. S., Ajami, M., Wollenberg, B., Multhoff, G., & Dezfouli, A. B. (2023) · Experimental Gerontology · doi:10.1016/j.exger.2023.112142 · Cited by 26
“Since PU-1 is highly expressed in granulocyte/monocyte progenitors and induces myeloid cytokine receptors such as granulocyte/macrophage colony-stimulating factor receptor α (DeKoter et al., 1998), the high PU-1 expression is another consequence of the elderly EVs effect on aging-induced myeloid differentiation.”
The early transcription factor GATA‐2 is expressed in classical Hodgkin's lymphoma
Schneider, E., Torlakovic, E., Stühler, A., Diehl, V., Tesch, H., & Giebel, B. (2004) · The Journal of Pathology · doi:10.1002/path.1664 · Cited by 23
“1, which directs the differentiation of haematopoietic progenitors into macrophages, neutrophils, and B lymphocytes [36,37], interacts with GATA proteins; that is, they antagonize each other’s activities by direct protein–protein interactions.”
BackgroundMolecular and functional characterization of erythropoietin of the goldfish (Carassius auratus L.)
Katakura, F., Katzenback, B. A., & Belosevic, M. (2013) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2013.02.007 · Cited by 21
“1, mafb, cjun, egr1 and cebpa) (DeKoter et al., 1998; Friedman, 2002; Krishnaraju et al., 2001; Sarrazin et al., 2009; Zhang et al., 1997), erythropoies is (gata1 and lmo2) (Brandt and Koury, 2009; Takahashi et al.”
The genome-wide molecular signature of transcription factors in leukemia
Prange, K. H. M., Singh, A. A., & Martens, J. H. A. (2014) · Experimental Hematology · doi:10.1016/j.exphem.2014.04.012 · Cited by 19
Katakura, F., Katzenback, B. A., & Belosevic, M. (2014) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2014.02.017 · Cited by 20
Das, A., Wang, X., Kang, J. M., Coulter, A. M., Shetty, A. C., Bachu, M., Brooks, S. R., Dell’Orso, S., Foster, B. L., Fan, X., et al. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4165 · Cited by 19
“Proc Natl Acad Sci U S A 107, 2193121936. DeKoter, R.P., Walsh, J.C., and Singh, H. (1998). PU.”
BackgroundInfluentialFukuchi, Y., Ito, M., Shibata, F., Kitamura, T., & Nakajima, H. (2008) · Stem Cells · doi:10.1634/stemcells.2008-0320 · Cited by 20
Malu, K., Garhwal, R., Pelletier, M. G. H., Gotur, D., Halene, S., Zwerger, M., Yang, Z., Rosmarin, A. G., & Gaines, P. C. W. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1402285 · Cited by 19
Molecular resolution of the B cell landscape
Santos, P. M. L., & Borghesi, L. (2011) · Current Opinion in Immunology · doi:10.1016/j.coi.2010.11.014 · Cited by 19
Delgado, M. D., Gutiérrez, P., Richard, C., Cuadrado, M. A., Moreau-Gachelin, F., & León, J. (1998) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1998.9587 · Cited by 20
Engulfing by lipids: a matter of taste?
Chimini, G. (2001) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400833 · Cited by 19
TLR7 activation at epithelial barriers promotes emergency myelopoiesis and lung antiviral immunity
Jackson, W. D., Giacomassi, C., Ward, S., Owen, A., Luis, T. C., Spear, S., Woollard, K. J., Johansson, C., Strid, J., & Botto, M. (2023) · eLife · doi:10.7554/elife.85647 · Cited by 19
Dendritic Cell Development: A Choose-Your-Own-Adventure Story
Moore, A. J., & Anderson, M. K. (2013) · Advances in Hematology · doi:10.1155/2013/949513 · Cited by 18
“Interestingly, there is an accumulation of CD24hi cKitint Sca1− DN1 precursors, corresponding phenotypically to the DN1c population, in PU.1−/− animals [80], suggesting that it is needed for the developmental progression of DN1c cells to CD8+ tDCs. PU.1 induces the expression of many DCpromoting factors, such as M-CSF…”
Background
Metadata
- Authors
- DeKoter, R. P., Walsh, J. C., & Singh, H.
- Affiliations
- Howard Hughes Medical Institute (US)
- University of Chicago (US)
- Corresponding author
- Singh, Harinder
- Venue
- The EMBO Journal
- Published
- 1998-08-03
- Volume
- 17
- Issue
- 15
- Pages
- 4456-4468
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC1170777
- OpenAlex
- W2081654176
- Cited by
- 296
- References
- 77
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 4 · 2023: 6 · 2022: 1 · 2021: 3 · 2020: 5 · 2019: 9 · 2018: 4 · 2017: 6 · 2016: 12 · 2015: 11 · 2014: 10 · 2013: 13 · 2012: 6
- FWCI
- 7.14
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The EMBO Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- University of Toronto
- National Institutes of Health
- National Heart, Lung, and Blood Institute (T32HL007237)
- National Institute of General Medical Sciences (T32GM007151)
- Topics
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- PU.1, ETS transcription factors, myeloid progenitor cells, granulocytic differentiation, macrophage differentiation, myelopoiesis, cytokine responsiveness, interleukin-3, granulocyte colony-stimulating factor, macrophage colony-stimulating factor, c-fms, granulocytic precursors, retroviral transduction
- MeSH terms
- Proto-Oncogene Protein Spi-1, Animals, Cell Differentiation, Cell Division, Colony-Forming Units Assay, Female, Gene Expression Regulation, Granulocytes, Hematopoietic Stem Cells, Interleukin-3, Macrophages, Male, Mutation, Proto-Oncogene Proteins, Retroviridae, Transduction, Genetic, Trans-Activators, Interleukin-6, Macrophage Colony-Stimulating Factor, Granulocyte-Macrophage Colony-Stimulating Factor, Granulocyte Colony-Stimulating Factor, Cytokines, Genes, fms, Mice, Knockout, Stem Cell Factor, Mice
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