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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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ICSBP/IRF-8 retrovirus transduction rescues dendritic cell development in vitro
Tsujimura, H., Tamura, T., Gongora, C., Aliberti, J., Sousa, C. R. E., Sher, A., & Ozato, K. (2003) · Blood · doi:10.1182/blood-2002-05-1327 · Cited by 115
Regulation of the PU.1 gene by distal elements
Li, Y., Okuno, Y., Zhang, P., Radomska, H. S., Chen, H.-M., Iwasaki, H., Akashi, K., Klemsz, M. J., McKercher, S. R., Maki, R. A., et al. (2001) · Blood · doi:10.1182/blood.v98.10.2958 · Cited by 110
Mellis, D. J., Itzstein, C., Helfrich, M., & Crockett, J. C. (2011) · Journal of Endocrinology · doi:10.1530/joe-11-0212 · Cited by 117
“1 stimulates the expression of CSF1R, the receptor for CSF1, commonly referred to as macrophage colony-stimulating factor (M-CSF; DeKoter et al. 1998).”
BackgroundOikawa, T., Yamada, T., Kihara-Negishi, F., Yamamoto, H., Kondoh, N., Hitomi, Y., & Hashimoto, Y. (1999) · Cell Death & Differentiation · doi:10.1038/sj.cdd.4400534 · Cited by 109
“1 myeloid progenitors fail to respond to GM- and G-CSF, although the unresponsiveness to G-CSF is bypassed by signaling with IL-3 in vitro.(34) The expression of genes associated with terminal myeloid differentiation such as MCSFR and CD11b is eliminated in differentiated PU.”
BackgroundMicroglia in the developing retina
Li, F., Jiang, D., & Samuel, M. A. (2019) · Neural Development · doi:10.1186/s13064-019-0137-x · Cited by 116
Hematopoietic developmental pathways: on cellular basis
Iwasaki, H., & Akashi, K. (2007) · Oncogene · doi:10.1038/sj.onc.1210754 · Cited by 117
“PU.1 transactivates a number of GM- and lymphoid-related genes (Zhang et al., 1996; DeKoter et al., 1998, 2002; Iwama et al., 1998), and is necessary for generation of early GM and lymphoid progenitors such as CMPs, GMPs and CLPs (Iwasaki et al., 2005b), whereas GATA-1 is an essential transcription…”
BackgroundEnvironmental sensing by mature B cells is controlled by the transcription factors PU.1 and SpiB
Willis, S. N., Tellier, J., Liao, Y., Trezise, S., Light, A., O’Donnell, K., Garrett-Sinha, L. A., Shi, W., Tarlinton, D. M., & Nutt, S. L. (2017) · Nature Communications · doi:10.1038/s41467-017-01605-1 · Cited by 112
Mouse models in the study of the Ets family of transcription factors
Bartel, F., Higuchi, T., & Spyropoulos, D. D. (2000) · Oncogene · doi:10.1038/sj.onc.1204038 · Cited by 108
“Additionally, MCSF or GM-CSF were unable to induce in vitro di erentiation of macrophages (Anderson et al., 1998a; DeKoter et al., 1998; McKercher et al., 1996).”
BackgroundHow B cells influence bone biology in health and disease
Horowitz, M. C., Fretz, J. A., & Lorenzo, J. (2010) · Bone · doi:10.1016/j.bone.2010.06.011 · Cited by 105
“In agreement with these data, the amount of PU.1 expressed by OCs is 3 fold more than in BM macrophages (32).”
BackgroundInfluentialKrysinska, H., Hoogenkamp, M., Ingram, R., Wilson, N., Tagoh, H., Laslo, P., Singh, H., & Bonifer, C. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01915-06 · Cited by 102
“reduced numbers, but their differentiation is blocked (6).”
BackgroundSelf-citationThe Transcription Factor PU.1 is a Critical Regulator of Cellular Communication in the Immune System
Turkistany, S. A., & DeKoter, R. P. (2011) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-011-0147-9 · Cited by 96
Self-citationMicroRNAs in Osteoclastogenesis and Function: Potential Therapeutic Targets for Osteoporosis
Xiao, J., Chen, X., & Yu, X. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17030349 · Cited by 102
Visualizing PU.1 activity during hematopoiesis
Back, J., Allman, D., Chan, S., & Kastner, P. (2005) · Experimental Hematology · doi:10.1016/j.exphem.2004.12.010 · Cited by 97
Hegde, V. L., Tomar, S., Jackson, A. R., Rao, R., Yang, X., Singh, U. P., Singh, N. P., Nagarkatti, P. S., & Nagarkatti, M. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.503037 · Cited by 96
“macrophage differentiation (57), and interaction of PU.”
Cdc42 critically regulates the balance between myelopoiesis and erythropoiesis
Yang, L. C., Wang, L., Kalfa, T. A., Cancelas, J. A., Shang, X., Pushkaran, S., Mo, J., Williams, D. A., & Zheng, Y. (2007) · Blood · doi:10.1182/blood-2007-03-079582 · Cited by 97
The Transcriptional Repressor GFI-1 Antagonizes PU.1 Activity through Protein-Protein Interaction
Dahl, R. E., Iyer, S. R., Owens, K., Cuylear, D. D., & Simon, M. C. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m607613200 · Cited by 103
Ikaros regulates neutrophil differentiation
Dumortier, A., Kirstetter, P., Kastner, P., & Chan, S. H. (2003) · Blood · doi:10.1182/blood-2002-05-1336 · Cited by 100
Interconversion between Tumorigenic and Differentiated States in Acute Myeloid Leukemia
McKenzie, M. D., Ghisi, M., Oxley, E. P., Ngo, S., Cimmino, L., Esnault, C., Liu, R., Salmon, J. M., Bell, C. C., Ahmed, N., et al. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.07.001 · Cited by 91
Surprising new roles for PU.1 in the adaptive immune response
Carotta, S., Wu, L., & Nutt, S. L. (2010) · Immunological Reviews · doi:10.1111/j.1600-065x.2010.00955.x · Cited by 93
“1-deficient fetal liver cells and conditionally deleted adult HSCs lack Csf2ra expression and are unable to form GM-CSF-responsive colonies in semi-solid media (15, 91).”
BackgroundMonocyte Differentiation to Macrophage Requires Interferon Regulatory Factor 7
Lu, R., & Pitha, P. M. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.c100421200 · Cited by 89
Ye, M., Ermakova, O. V., & Graf, T. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20051089 · Cited by 94
“PU.1 / liver cell suspensions that were seeded under conditions permissive for both B and myeloid cell growth (S17 stroma cells containing IL-3, IL-7, SCF, and Flt-3L) developed into foci of small round, refractile cells within 2–3 wk from all 21 fetal livers (embryonic day [E] 14.5–18.5) tested (Fig.”
BackgroundInfluentialAnderson, K. L., Smith, K. A., Perkin, H. B., Hermanson, G., Anderson, C.-G., Jolly, D. J., Maki, R. A., & Torbett, B. E. (1999) · Blood · doi:10.1182/blood.v94.7.2310.419k34_2310_2318 · Cited by 90
PU.1: A crucial and versatile player in hematopoiesis and leukemia
Kastner, P., & Chan, S. (2008) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2007.01.026 · Cited by 101
Immunomodulatory derivatives induce PU.1 down-regulation, myeloid maturation arrest, and neutropenia
Pal, R., Monaghan, S. A., Hassett, A. C., Mapara, M. Y., Schafer, P. H., Roodman, G. D., Ragni, M. V., Moscinski, L. C., List, A. F., & Lentzsch, S. (2009) · Blood · doi:10.1182/blood-2009-05-221077 · Cited by 90
Transcriptional Control of Natural Killer Cell Development and Function
Hesslein, D. G. T., & Lanier, L. L. (2011) · Advances in immunology · doi:10.1016/b978-0-12-387664-5.00002-9 · Cited by 85
“(B) Genes primarily involved in NK cell function. direct target of PU.1 (Carotta et al., 2010; DeKoter et al., 1998; Medina et al., 2004).”
BackgroundThe origins and non-canonical functions of macrophages in development and regeneration
Théret, M., Mounier, R., & Rossi, F. M. V. (2019) · Development · doi:10.1242/dev.156000 · Cited by 90
“However, by using a conditional LysM-Cre PU.1 floxed model, it has been demonstrated that PU.1 is dispensable for HSC development, allowing the community to investigate hematopoiesis more thoroughly (McKercher et al., 1996; DeKoter et al., 1998; Dakic et al., 2005).”
MethodJin, F., Li, Y., Ren, B., & Natarajan, R. D. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1017214108 · Cited by 84
“1 (SPI1), which were specifically expressed in THP-1 cells and are known to be critical for hematopoietic development (21, 22).”
BackgroundGadd45β mediates the protective effects of CD40 costimulation against Fas-induced apoptosis
Zazzeroni, F., Papa, S., Algeciras-Schimnich, A., Alvarez, K., Melis, T., Bubici, C., Majewski, N., Hay, N., Smaele, E. D., Peter, M. E., et al. (2003) · Blood · doi:10.1182/blood-2003-03-0689 · Cited by 83
“Retrovirus production and transduction of BJAB cells High-titer retroviral preparations were produced using ΦNX-Ampho retroviral packaging cells as described previously.(35) Packaging cells were transfected with MIGR1- or pBabebased constructs (22.”
MethodKim, H.-G., de Guzman, C. G., Swindle, C. S., Cotta, C. V., Gartland, L., Scott, E. W., & Klug, C. A. (2004) · Blood · doi:10.1182/blood-2002-08-2425 · Cited by 75
Protein tyrosine phosphatase 1B negatively regulates macrophage development through CSF-1 signaling
Heinonen, K. M., Dubé, N., Bourdeau, A., Lapp, W. S., & Tremblay, M. L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508563103 · Cited by 81
Induction of granulocytic differentiation by 2 pathways
Zhang, P., Nelson, E. A., Radomska, H. S., Iwasaki-Arai, J., Akashi, K., Friedman, A. D., & Tenen, D. G. (2002) · Blood · doi:10.1182/blood.v99.12.4406 · Cited by 77
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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