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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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Schütte, J., Moignard, V., & Göttgens, B. (2012) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1163 · Cited by 12
AML1/RUNX1 gene point mutations in childhood myeloid malignancies
Migas, A. A., Savva, N. N., Mishkova, V., & Aleinikova, O. (2011) · Pediatric Blood & Cancer · doi:10.1002/pbc.22980 · Cited by 13
Chiang, M. Y., & Monroe, J. (2001) · Journal of Immunology · doi:10.4049/jimmunol.166.10.6091 · Cited by 16
“1 in developing B cells appears to be at odds with its myeloid lineage-determining functions (38) and its ability to up-regulate the expression of the GM-CSFRa-chain (39).”
BackgroundMulet‐Lazaro, R., van Herk, S., Nuetzel, M., Sijs‐Szabó, A., Díaz, N., Kelly, K., Erpelinck-Verschueren, C. A. J., Schwarzfischer, L., Stanewsky, H., Ackermann, U., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-49811-y · Cited by 17
Herbst, F., Lang, T. J. L., Eckert, E., Wünsche, P., Wurm, A. A., Kindinger, T., Laaber, K., Hemmati, S., Hotz‐Wagenblatt, A., Zavidij, O., et al. (2021) · Leukemia · doi:10.1038/s41375-021-01267-5 · Cited by 14
Ohmori, S., Ishijima, Y., Numata, S., Takahashi, M., Sekita, M., Sato, T., Chugun, K., Yamamoto, M., & Ohneda, K. (2019) · Molecular and Cellular Biology · doi:10.1128/mcb.00314-19 · Cited by 15
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
Ano, S., Pereira, R., Pironin, M., Lesault, I., Milley, C., Lebigot, I., Quang, C. T., & Ghysdael, J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m303816200 · Cited by 14
Nielsen, J., Doyonnas, R., & McNagny, K. (2002) · Cells Tissues Organs · doi:10.1159/000057691 · Cited by 15
“In order to study the role of PU.1 in hematopoiesis, an E26 construct containing PU.1 expressed from an IRES element was used to infect 2-day chicken blastoderms [Nerlov and Graf, 1998].”
BackgroundMethodInfluentialMapping of complex regulatory elements by pufferfish/zebrafish transgenesis
Rothenberg, E. (2001) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.131199098 · Cited by 15
The Cell Biology of Stem Cells
Meshorer, E., & Plath, K. (2010) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-7037-4 · Cited by 20
Transcriptional Factor PU.1 Regulates Decidual C1q Expression in Early Pregnancy in Human
Madhukaran, S. P., Kishore, U., Jamil, K., Teo, B. H. D., Choolani, M. A., & Lu, J. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00053 · Cited by 13
Lineage-specific combinatorial action of enhancers regulates mouse erythroid Gata1 expression.
Drissen, R., Guyot, B., Zhang, L., Atzberger, A., Sloane-Stanley, J., Wood, B., Porcher, C., & Vyas, P. (2010) · Blood · doi:10.1182/blood-2009-07-232876 · Cited by 14
Young, P. P., Ardestani, S., & Li, B. (2010) · Cancer Microenvironment · doi:10.1007/s12307-010-0045-4 · Cited by 15
“1 gene, an ETS transcription factor [20, 23–26].”
BackgroundMultiple ways of C/EBPα inhibition in myeloid leukaemia
Trivedi, A. K., Pal, P., Behre, G., & Singh, S. M. (2008) · European Journal of Cancer · doi:10.1016/j.ejca.2008.04.022 · Cited by 16
Enos, M., Bancos, S., Bushnell, T. P., & Crispe, I. N. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.6.3699 · Cited by 16
Li, X., Li, Z., Cai, D., Li, Y., Zhu, Y., Jiao, R., Lai, C., Sun, J., & Bai, W. (2023) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.3c03119 · Cited by 13
Horváth, A., Dániel, B., Széles, L., Cuaranta‐Monroy, I., Czimmerer, Z., Ozgyin, L., Steiner, L., Kiss, M., Simándi, Z., Póliska, S., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz118 · Cited by 13
“1 is known as an inducer of myeloid differentiation (10), CEBPA/B and PU.”
BackgroundOmrani, M., Yaqubi, M., & Mohammadnia, A. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.03.033 · Cited by 13
Olig2 is expressed late in human eosinophil development and controls Siglec-8 expression
Hwang, S. M., Uhm, T. G., Lee, S. K., Kong, S.-K., Jung, K. H., Binas, B., Chai, Y. G., Park, S., & Chung, I. Y. (2016) · Journal of Leukocyte Biology · doi:10.1189/jlb.1a0715-314rrr · Cited by 16
Functional genomics of the inflammatory response: where are we now?
Simonatto, M., & Natoli, G. (2013) · Briefings in Functional Genomics · doi:10.1093/bfgp/elt023 · Cited by 8
CTCF depletion alters chromatin structure and transcription of myeloid-specific factors.
Ouboussad, L., Kreuz, S., & Lefevre, P. (2013) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjt023 · Cited by 13
“1 (Nerlov and Graf, 1998; Seshasayee et al., 1998; Heyworth et al., 2002).”
Remen, K. M. R., Gustafsson, J.-Α., & Andersson, G. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.11.021 · Cited by 12
Zhao, M. L., Duan, X.-F., Wen, D., & Chen, G. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.03.024 · Cited by 14
Molecular biology of hematopoietic stem cells.
Steidl, U., Kronenwett, R., Martin, S., & Haas, R. (2003) · Vitamins and hormones · doi:10.1016/s0083-6729(03)01001-x · Cited by 13
mTORC1 activity is essential for erythropoiesis and B cell lineage commitment
Malik, N., Dunn, K. M., Cassels, J. E., Hay, J., Estell, C., Sansom, O. J., & Michie, A. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-53141-1 · Cited by 13
Kim, M. S., Kang, J.-W., Park, Y. S., Lee, D. H., Bak, Y., Kwon, T., & Yoon, D. (2015) · Oncotarget · doi:10.18632/oncotarget.3013 · Cited by 12
Uchiumi, F., Enokida, K., Shiraishi, T., Masumi, A., & Tanuma, S.-I. (2010) · Gene · doi:10.1016/j.gene.2010.04.014 · Cited by 11
“PU.1, which is also known as the proto-oncogene product Spi-1 (Ray et al., 1990), is a regulator of myeloid lineage commitment (Nerlov and Graf, 1998) and graded reduction of PU.1 was suggested to induce AML (Rosenbauer et al., 2004).”
BackgroundInfluentialRegulation of the transcription factor GATA-1 at the gene and protein level
Tang, X., Liu, D.-P., & Liang, C. (2001) · Cellular and Molecular Life Sciences · doi:10.1007/pl00000833 · Cited by 10
Reprogramming Somatic Cells to a Kidney Fate
Takasato, M., Vanslambrouck, J. M., & Little, M. H. (2014) · Seminars in Nephrology · doi:10.1016/j.semnephrol.2014.06.012 · Cited by 8
Stress hematopoiesis is regulated by the Krüppel-like transcription factor ZBP-89
Li, X.-G., Romain, R. D., Park, D., Scadden, D. T., Merchant, J., & Arnaout, M. (2014) · Stem Cells · doi:10.1002/stem.1598 · Cited by 11
Wilson, N. K., Tijssen, M., & Göttgens, B. (2011) · Experimental Hematology · doi:10.1016/j.exphem.2011.07.005 · Cited by 11
Seo, H.-Y., Han, J.-K., & Kim, Y.-H. (2011) · doi:10.7778/jpkm.2011.25.1.001 · Cited by 11
Mas, V. M.-D., de Thonel, A., Gaulin, V., Demur, C., Laurent, G., & Quillet-Mary, A. (2002) · British Journal of Haematology · doi:10.1046/j.1365-2141.2002.03625.x · Cited by 11
“Indeed, this ETS familymember transcription factor, which is essentially distributed in monocytic and granulocytic lineage (Fisher & Scott, 1998), plays an important function in myeloid lineage commitment (Nerlov & Graf, 1998; Nerlov et al, 2000).”
BackgroundWayman, G. A., Walters, M. J., Kolibaba, K. S., Soderling, T. R., & Christian, J. L. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.4.811 · Cited by 13
“…as transcriptional regulators that are required for commitment of progenitors to the erythroid lineage (for review see Sieweke and Graf, 1998), whereas the Ets family member PU.1 can instruct pluripotent hematopoietic progenitors to differentiate along the myeloid lineage (Nerlov and Graf, 1998).”
Background
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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