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Cooperative and Antagonistic Interplay between PU.1 and GATA-2 in the Specification of Myeloid Cell Fates
Open accessAbstract
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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PU-ER cells constitutively express a low level of PU.1 from the transgene, with 4-OHT rapidly inducing PU.1 protein activation.
“These cells constitutively express a low level of PU.1 from the transgene, with 4-OHT rapidly inducing PU.1 protein activation (Walsh et al., 2002).”
From PU.1 enforces quiescence and limits hematopoietic stem cell expansion during inflammatory stress (2021) · cites this paper as Walsh et al., 2002
The PUER experiments and Figure 4 caption describe a transgene-encoded PU.1 fusion protein whose activity is induced by OHT. But the paper describes high levels of PUER protein with low basal activity, not a low level of protein expression; the cited passages also do not establish that activation is rapid. Our copy provides no page numbers for these passages. (LLM, conf=0.86)
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BackgroundTwo distinct auto-regulatory loops operate at the PU.1 locus in B cells and myeloid cells
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“However, these patterns distinguished levels of expression, not response category or direction of response—the patterns were the same for induced or repressed genes.”
BackgroundPU.1 Level-Directed Chromatin Structure Remodeling at the Irf8 Gene Drives Dendritic Cell Commitment
Schönheit, J., Kuhl, C., Gebhardt, M. L., Klett, F. F., Riemke, P., Scheller, M., Huang, G., Naumann, R., Leutz, A., Stocking, C., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.04.007 · Cited by 127
“7, NIH 3T3, 416B, PU.1–/–ERT-PU.1, and PU.1–/– cell lines were cultured as described before (Leddin et al., 2011; Walsh et al., 2002).”
MethodGraded repression of PU.1/Sfpi1 gene transcription by GATA factors regulates hematopoietic cell fate
Chou, S. T., Khandros, E., Bailey, L. C., Nichols, K. E., Vakoc, C. R., Yao, Y., Huang, Z., Crispino, J. D., Hardison, R. C., Blobel, G. A., et al. (2009) · Blood · doi:10.1182/blood-2009-03-207944 · Cited by 126
PU.1 determines the self-renewal capacity of erythroid progenitor cells
Back, J., Dierich, A., Bronn, C., Kastner, P., & Chan, S. (2004) · Blood · doi:10.1182/blood-2003-11-4089 · Cited by 123
The emerging roles of DOT1L in leukemia and normal development
McLean, C. M., Karemaker, I. D., & van Leeuwen, F. (2014) · Leukemia · doi:10.1038/leu.2014.169 · Cited by 118
MIR-23A microRNA cluster inhibits B-cell development
Kong, K. Y., Owens, K. S., Rogers, J. H., Mullenix, J., Velu, C. S., Grimes, H. L., & Dahl, R. (2010) · Experimental Hematology · doi:10.1016/j.exphem.2010.04.004 · Cited by 89
“1 protein [9,18].”
The STAT5-GATA2 Pathway Is Critical in Basophil and Mast Cell Differentiation and Maintenance
Li, Y.-P., Qi, X.-P., Liu, B., & Huang, H. (2015) · Journal of Immunology · doi:10.4049/jimmunol.1500018 · Cited by 113
Origin, development, and homeostasis of tissue‐resident macrophages
Haldar, M., & MURPHY, K. M. M. (2014) · Immunological Reviews · doi:10.1111/imr.12215 · Cited by 125
“1 and GATA2 antagonism in myeloid versus mast cell fate (86).”
BackgroundChen, R., Bélanger, S., Frederick, M. A., Li, B., Johnston, R. J., Xiao, N., Liu, Y., Sharma, S., Peters, B., Rao, A., et al. (2014) · Immunity · doi:10.1016/j.immuni.2014.08.002 · Cited by 118
Gu, X., Ebrahem, Q., Mahfouz, R. Z., Hasipek, M., Enane, F. O., Radivoyevitch, T., Rapin, N., Przychodzen, B. P., Hu, Z., Balusu, R., et al. (2018) · Journal of Clinical Investigation · doi:10.1172/jci97117 · Cited by 118
“1-ER (53), activating terminal monocytic fates (Supplemental Figure 7) and suppressing Hox gene expression.”
MicroRNA-221–222 Regulate the Cell Cycle in Mast Cells
Mayoral, R. J., Pipkin, M. E., Pachkov, M. V., van Nimwegen, E., Rao, A., & Monticelli, S. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.182.1.433 · Cited by 95
“1 / cells (39) that were reconstituted with either GFP or PU.”
BackgroundRole of NFAT Proteins in IL13 Gene Transcription in Mast Cells
Monticelli, S., Solymar, D. C., & Rao, A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m406354200 · Cited by 98
Krysinska, 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
“1 in PUER cells (PUER OHT) led to induction of c-fms mRNA expression, as previously observed (3, 36).”
BackgroundMethodSelf-citationSCL is required for normal function of short-term repopulating hematopoietic stem cells
Curtis, D. J., Hall, M. A., van Stekelenburg, L., Robb, L. G., Jane, S. M., & Begley, C. G. (2004) · Blood · doi:10.1182/blood-2003-09-3202 · Cited by 89
PU.1-mediated upregulation of CSF1R is crucial for leukemia stem cell potential induced by MOZ-TIF2
Aikawa, Y., Katsumoto, T., Zhang, P., Shima, H., Shino, M., Terui, K., Ito, E., Ohno, H., Stanley, E. R., Singh, H., et al. (2010) · Nature Medicine · doi:10.1038/nm.2122 · Cited by 96
“The [35S]-MOZ (1-664) protein was incubated with GST-, GST-PU.”
Self-citationMechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development
Rothenberg, E. V., Hosokawa, H., & Ungerbäck, J. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00228 · Cited by 99
“1 can work in an all-or-none gene network switch through mutual antagonism with GATA-1 (20–24), which has been much discussed as a possible mechanism for the irreversibility of erythro-myeloid lineage commitment [(25–29); but also see (30, 31)].”
BackgroundCdc42 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
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
“1 is required for mast and dendritic cell differentiation, and plays a role in early T lymphopoiesis [4–8].”
BackgroundRothenberg, E. V. (2007) · Immunity · doi:10.1016/j.immuni.2007.06.005 · Cited by 87
Pospisil, V., Vargova, K., Kokavec, J., Rybarova, J., Savvulidi, F., Jonasova, A., Necas, E., Zavadil, J., Laslo, P., & Stopka, T. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.317 · Cited by 93
“PUER (Walsh et al, 2002), shEgr2, shNab2 (Laslo et al, 2006) and HL60 cells were cultured as described.”
BackgroundMethodNAMPT: A pleiotropic modulator of monocytes and macrophages
Travelli, C., Colombo, G., Mola, S., Genazzani, A. A., & Porta, C. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2018.06.022 · Cited by 91
PU.1 enforces quiescence and limits hematopoietic stem cell expansion during inflammatory stress
Chavez, J. S., Rabe, J. L., Loeffler, D., Higa, K. C., Hernandez, G., Mills, T. S., Ahmed, N., Gessner, R. L., Ke, Z., Idler, B. M., et al. (2021) · Journal of Experimental Medicine · doi:10.1084/jem.20201169 · Cited by 91
Redirecting differentiation of hematopoietic progenitors by a transcription factor, GATA-2
Kitajima, K., Tanaka, M., Zheng, J., Yen, H., Sato, A., Sugiyama, D., Umehara, H., Sakai, E., & Nakano, T. (2005) · Blood · doi:10.1182/blood-2005-06-2527 · Cited by 82
Antagonism of FOG-1 and GATA factors in fate choice for the mast cell lineage
Cantor, A. B., Iwasaki, H., Arinobu, Y., Moran, T. B., Shigematsu, H., Sullivan, M. R., Akashi, K., & Orkin, S. H. (2008) · The Journal of Experimental Medicine · doi:10.1084/jem.20070544 · Cited by 77
Bonifer, C. (2007) · Frontiers in bioscience · doi:10.2741/2700 · Cited by 72
Weigelt, K., Carvalho, L. A., Drexhage, R. C., Wijkhuijs, A. J. M., de Wit, H., van Beveren, N. J. M., Birkenhäger, T. K., Bergink, V., & Drexhage, H. A. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.03.006 · Cited by 76
“1 is involved in the development and specific gene regulation of the myeloid- and lymphoid-lineages, including macrophages, dendritic cells (DC), neutrophils, mast cells (MC) and lymphoid cells (Anderson et al., 2000; Guerriero et al., 2000; Lloberas et al., 1999; McKercher et al., 1996; Scott et al., 1997, 1994; Wals…”
de Pooter, R. F., Schmitt, T. M., de la Pompa, J. L., Fujiwara, Y., Orkin, S. H., & Zúñiga‐Pflücker, J. C. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.9.5267 · Cited by 63
Gupta, P., Gurudutta, G. U., Saluja, D., & Tripathi, R. P. (2009) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2009.00757.x · Cited by 74
Molecular Mechanisms of Mast Cell Development
Kitamura, Y., Oboki, K., & Ito, A. (2006) · Immunology and Allergy Clinics of North America · doi:10.1016/j.iac.2006.05.004 · Cited by 73
Key regulators control distinct transcriptional programmes in blood progenitor and mast cells
Calero‐Nieto, F. J., Ng, F. S., Wilson, N. K., Hannah, R., Moignard, V., Leal-Cervantes, A. I., Jimenez-Madrid, I., Diamanti, E., Wernisch, L., & Göttgens, B. (2014) · The EMBO Journal · doi:10.1002/embj.201386825 · Cited by 71
“Some of these factors, like SCL/TAL1 (Salmon et al , 2007), GATA2 (Tsai & Orkin, 1997) and PU.1 (Walsh et al , 2002), had been implicated in mast cell function before, but no such information had been provided for the other HSC regulators.”
InfluentialModulators of MicroRNA Function in the Immune System
Jia, Y., & Wei, Y. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21072357 · Cited by 83
“1, are essential to determine myeloid cell diversity and functional specificity during differentiation [28,31,32].”
BackgroundJun Blockade of Erythropoiesis: Role for Repression of GATA-1 by HERP2
Elagib, K. E., Xiao, M., Hussaini, I. M., Delehanty, L. L., Palmer, L. A., Racke, F. K., Birrer, M. J., Ganapathy‐Kanniappan, S., McDevitt, M. A., & Goldfarb, A. N. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.17.7779-7794.2004 · Cited by 71
“1 binds and represses both GATA-1 and GATA-2, with the net phenotypic result of erythroid blockade (33, 47, 48, 62, 71).”
BackgroundRegulatory coding of lymphoid lineage choice by hematopoietic transcription factors
Warren, L. A., & Rothenberg, E. V. (2003) · Current Opinion in Immunology · doi:10.1016/s0952-7915(03)00011-6 · Cited by 61
Hoogenkamp, M., Krysinska, H., Ingram, R., Huang, G., Barlow, R. E. L., Clarke, D., Ebralidze, A. K., Zhang, P., Tagoh, H., Cockerill, P. N., et al. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00905-07 · Cited by 62
“PU.1 also functions in balance with C/EBP and GATA-2 to regulate granulocyte and mast cell development, respectively (7, 41 ).”
BackgroundMethodInfluentialGregory, G. D., Miccio, A., Bersenev, A., Wang, Y., Wei, H., Zhang, Z., Poncz, M., Tong, W., & Blobel, G. A. (2010) · Blood · doi:10.1182/blood-2009-10-251280 · Cited by 75
Cis-regulatory mechanisms governing stem and progenitor cell transitions
Johnson, K. D., Kong, G., Gao, X., Chang, Y., Hewitt, K. J., Sanalkumar, R., Prathibha, R., Ranheim, E. A., Dewey, C. N., Zhang, J., et al. (2015) · Science Advances · doi:10.1126/sciadv.1500503 · Cited by 67
Epigenetic program and transcription factor circuitry of dendritic cell development
Lin, Q., Chauvistré, H., Costa, I. G., Gusmao, E. G., Mitzka, S., Hänzelmann, S., Baying, B., Klisch, T., Moriggl, R., Hennuy, B., et al. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1056 · Cited by 68
Sakata‐Yanagimoto, M., Nakagami‐Yamaguchi, E., Saito, T., Kumano, K., Yasutomo, K., Ogawa, S., Kurokawa, M., & Chiba, S. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0801074105 · Cited by 63
“GATA2 upregulation (4), and C/EBPα downregulation (5).”
BackgroundInfluentialThe hematopoietic transcription factor PU.1 regulates RANK gene expression in myeloid progenitors
Kwon, O. H., Lee, C., Lee, Y. I., Paik, S., & Lee, H. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.07.092 · Cited by 55
Self-citationTranscriptional control of B cell development and function
Bartholdy, B., & Matthias, P. (2003) · Gene · doi:10.1016/j.gene.2003.11.008 · Cited by 78
RUNX1 regulates corepressor interactions of PU.1
Hu, Z., Gu, X., Baraoidan, K., Ibanez, V., Sharma, A., Kadkol, S., Munker, R., Ackerman, S., Nucifora, G., & Saunthararajah, Y. (2011) · Blood · doi:10.1182/blood-2010-10-312512 · Cited by 63
Sullivan, A. L., Benner, C. W., Heinz, S., Huang, W. J. M., Xie, L., Miano, J. M., & Glass, C. K. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.00836-10 · Cited by 58
Transcription factor PU.1 is expressed in white adipose and inhibits adipocyte differentiation
Wang, F., & Tong, Q. (2008) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00422.2007 · Cited by 63
Huber, R., Pietsch, D., Günther, J., Welz, B., Vogt, N., & Brand, K. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1322-4 · Cited by 62
“1-dependent downregulation of GATA2 gene expression induces macrophage formation and a block of mast cell development [206].”
BackgroundRothenberg, E. V., Ungerbäck, J., & Champhekar, A. (2016) · Advances in Immunology · doi:10.1016/bs.ai.2015.09.002 · Cited by 61
Transcriptional determination and functional specificity of myeloid cells: making sense of diversity
Monticelli, S., & Natoli, G. (2017) · Nature reviews. Immunology · doi:10.1038/nri.2017.51 · Cited by 63
GATA2 and Sp1 Positively Regulate the c-kit Promoter in Mast Cells
Maeda, K., Nishiyama, C., Ogawa, H., & Okumura, K. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1001228 · Cited by 55
Granulocytes: effector cells or immunomodulators in the immune response to helminth infection?
Cadman, E., & Lawrence, R. (2010) · Parasite immunology (Print) · doi:10.1111/j.1365-3024.2009.01147.x · Cited by 58
Transcriptional Regulation of the Cyclooxygenase-2 Gene in Macrophages by PU.1
Joo, M., Park, G. Y., Wright, J. G., Blackwell, T. S., Atchison, M. L., & Christman, J. W. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m306267200 · Cited by 56
Bert, A., Johnson, B., Baxter, E. W., & Cockerill, P. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.02323-06 · Cited by 57
“Mast cells are known to utilize both GATA and NFAT family transcription factors in the regulation of other cytokine genes located near the GM-CSF locus (24, 30), and GATA-2 is a major factor directing mast cell differentiation (35).”
BackgroundGATA2 regulates dendritic cell differentiation
Onodera, K., Fujiwara, T., Onishi, Y., Itoh‐Nakadai, A., Okitsu, Y., Fukuhara, N., Ishizawa, K., Shimizu, R., Yamamoto, M. P., & Harigae, H. (2016) · Blood · doi:10.1182/blood-2016-02-698118 · Cited by 53
“1 expression in an IL-3–dependent cell line favored macrophage generation.(15) These studies may support our observation of macrophage expansion in GATA2-knockout mice.”
Context-dependent function of “GATA switch” sites in vivo
Snow, J. W., Trowbridge, J. J., Johnson, K. D., Fujiwara, T., Emambokus, N. E., Grass, J. A., Orkin, S. H., & Bresnick, E. H. (2011) · Blood · doi:10.1182/blood-2010-10-313031 · Cited by 53
Maeda, K., Nishiyama, C., Tokura, T., Nakano, H., Kanada, S., Nishiyama, M., Okumura, K., & Ogawa, H. (2006) · Blood · doi:10.1182/blood-2005-07-2878 · Cited by 59
Notch signaling in differentiation and function of dendritic cells
Cheng, P., & Gabrilovich, D. I. (2007) · Immunologic Research · doi:10.1007/s12026-007-8011-z · Cited by 53
Metadata
- 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
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2002-11
- Volume
- 17
- Issue
- 5
- Pages
- 665-676
- ISSN
- 1074-7613 (ISSN-L)
- 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
- 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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