Positive Feedback Between PU.1 and the Cell Cycle Controls Myeloid Differentiation
Open accessAbstract
Regulatory gene circuits with positive-feedback loops control stem cell differentiation, but several mechanisms can contribute to positive feedback. Here, we dissect feedback mechanisms through which the transcription factor PU.1 controls lymphoid and myeloid differentiation. Quantitative live-cell imaging revealed that developing B cells decrease PU.1 levels by reducing PU.1 transcription, whereas developing macrophages increase PU.1 levels by lengthening their cell cycles, which causes stable PU.1 accumulation. Exogenous PU.1 expression in progenitors increases endogenous PU.1 levels by inducing cell cycle lengthening, implying positive feedback between a regulatory factor and the cell cycle. Mathematical modeling showed that this cell cycle-coupled feedback architecture effectively stabilizes a slow-dividing differentiated state. These results show that cell cycle duration functions as an integral part of a positive autoregulatory circuit to control cell fate.
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Specific cellular levels of PU.1 are critical for distinct cell fates; highest PU.1 amounts drive macrophage development and lower concentrations are required for granulocytic/B-cell fate adoption.
“Volumes of evidences indicate that specific cellular levels of PU.1 are critical for distinct cell fates, where highest PU.1 amounts drive macrophage development and lower concentrations are required for granulocytic/B-cell fate adoption (4,5).”
From FBW7 Inhibits Myeloid Differentiation in Acute Myeloid Leukemia via GSK3-Dependent Ubiquitination of PU.1 (2021) · cites this paper as [5]
The supplied passage labeled Abstract (page not provided) reports that macrophages up-regulated PU.1, B cells down-regulated it, and developing granulocytes maintained progenitor-like levels. The paper also reports that increased PU.1 promotes macrophage differentiation and inhibits B-cell development. It does not establish that a lower PU.1 concentration is required for granulocyte fate. (LLM, conf=0.84)
Experimental — accuracy not yet measuredPU.1 protein is highly stable, which can magnify its impact on cells despite modest RNA transcript levels.
“although the RNA transcript levels are modest in absolute terms, the impact of PU.1 on the cells can be magnified by the high stability of PU.1 protein (82).”
From Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development (2019) · cites this paper as [82]
The passage discussing PU.1 removal (Fig. 1E; page unavailable) says its protein half-life is substantially longer than the progenitor cell cycle. The passages discussing cell-cycle lengthening (Figs. 1F–H and 3C–D; page unavailable) show that PU.1 can accumulate to higher levels without increased synthesis, supporting the proposed magnifying effect. Our copy does not establish that PU.1 RNA transcript levels are modest in absolute terms. (LLM, conf=0.84)
Experimental — accuracy not yet measuredTarget genes stimulated by PU.1 include both pro-proliferative and G1-prolonging cell cycle effectors, whereas some important proliferative genes are repressed when PU.1 levels are high.
“The target genes stimulated by PU.1 include both pro-proliferative and G1-prolonging cell cycle effectors, whereas some important proliferative genes are repressed when PU.1 levels are high (82, 83).”
From Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development (2019) · cites this paper as [82]
In the passage on regulatory gene expression (indexed as Abstract; page unavailable), PU.1 transduction reduced Cyclin D2, Cdc25a, Myb, and Myc, supporting the repression of proliferative genes. The paper says PU.1 promotes growth in some progenitors and notes that p21 and Gfi1 are up-regulated by PU.1 in stem cells, but it does not establish here that PU.1 stimulates both pro-proliferative and G1-prolonging target genes. (LLM, conf=0.87)
Experimental — accuracy not yet measuredPU.1 can restrict proliferation in hematopoietic stem and progenitor cells (HSPCs), likely a mechanism to promote PU.1 accumulation during myeloid differentiation.
“Interestingly, PU.1 can also restrict proliferation in hematopoietic stem and progenitor cells (HSPCs), likely a mechanism to promote PU.1 accumulation during myeloid differentiation (Fukuchi et al., 2008; Kueh et al., 2013).”
From PU.1 enforces quiescence and limits hematopoietic stem cell expansion during inflammatory stress (2021) · cites this paper as Kueh et al., 2013
The paper’s Abstract reports that PU.1 lengthens the cell cycle in progenitors, allowing PU.1 to accumulate and promoting macrophage differentiation. It does not establish this mechanism across HSPCs: it distinguishes cell-cycle arrest during macrophage differentiation from stem-cell quiescence and notes that PU.1 promotes growth in some progenitor types. No page number is available in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredPU.1 represses cell cycle genes in T cell progenitors.
“PU.1 similarly represses cell cycle genes in T cell progenitors”
From PU.1 is required to restrain myelopoiesis during chronic inflammatory stress (2023) · cites this paper as Kueh et al., 2013
The gene-expression passage (indexed under Abstract; page unavailable) reports that PU.1 transduction reduced the cell-cycle-promoting factors Cyclin D2 and Cdc25a. But the paper describes experiments in progenitors cultured for macrophage and B-cell differentiation, not T-cell progenitors, so it does not establish the claimed T-cell setting. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Cell cycle restriction may play a similar role in lymphoid development.
“and thus cell cycle restriction may play a similar role in lymphoid development (Kueh et al., 2013; Staber et al., 2013; Champhekar et al., 2015).”
From PU.1 is required to restrain myelopoiesis during chronic inflammatory stress (2023) · cites this paper as Kueh et al., 2013
The discussion (page unavailable) suggests that cell-cycle-linked mechanisms may operate in other differentiation systems, supporting the cautious possibility in the claim. It does not specifically propose this role in lymphoid development: its B-cell observations instead show similar cell-cycle lengths to progenitors and reduced PU.1 transcription, unlike the cell-cycle lengthening seen in macrophages. (LLM, conf=0.78)
Experimental — accuracy not yet measuredCellular levels of PU.1 direct different cell fates from hematopoietic progenitors, with highest amounts required for macrophage and lower concentrations for granulocyte or B-cell differentiation.
“cellular levels of PU.1 direct different cell fates from these hematopoietic progenitors where the highest amounts of PU.1 are required for macrophage and lower concentrations for granulocyte or B-cell differentiation (4,5).”
From FBW7 Inhibits Myeloid Differentiation in Acute Myeloid Leukemia via GSK3-Dependent Ubiquitination of PU.1 (2021) · cites this paper as [5]
The long half-life of PU.1 protein can mask some loss effects at time points less than 2 days after deletion, while development can proceed to new stages if time windows are extended.
“One problem is that the long half-life of PU.1 protein (82) can mask some loss effects at time points <2 days after deletion, while development of the pro-T cells can proceed to new stages if time windows are extended further.”
From Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development (2019) · cites this paper as [82]
Because PU.1 protein can persist longer than a cell cycle, the slowdown of cell division caused by Spi1 deletion can interfere with the dilution needed to complete clearance of PU.1 protein.
“Ironically, because PU.1 protein can persist longer than a cell cycle (82), the very slowdown of cell division caused by deletion of Spi1 (see above) can also interfere with the dilution needed to complete the clearance of the PU.1 protein.”
From Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development (2019) · cites this paper as [82]
The connection between cell cycle inhibition and myeloid differentiation likely centers on cell cycle lengthening as a mechanism to promote PU.1 accumulation and myeloid differentiation in hematopoietic progenitors.
“The connection between cell cycle inhibition and myeloid differentiation likely centers on cell cycle lengthening as a mechanism to promote PU.1 accumulation and myeloid differentiation in hematopoietic progenitors (Kueh et al., 2013).”
From PU.1 enforces quiescence and limits hematopoietic stem cell expansion during inflammatory stress (2021) · cites this paper as Kueh et al., 2013
PU.1 restricts the cell cycle activity of myeloid-committed progenitors, thereby facilitating homeostatic myeloid differentiation via accumulation of sufficient myeloid lineage determinants prior to cell division.
“Previous work has shown that PU.1 restricts the cell cycle activity of myeloid-committed progenitors (Kueh et al., 2013), thereby facilitating homeostatic myeloid differentiation via accumulation of sufficient myeloid lineage determinants prior to cell division.”
From PU.1 is required to restrain myelopoiesis during chronic inflammatory stress (2023) · cites this paper as Kueh et al., 2013
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- Authors
- Kueh, H. Y., Champhekar, A., Nutt, S. L., Elowitz, M. B., & Rothenberg, E. V.
- Affiliations
- California Institute of Technology (US)
- Walter and Eliza Hall Institute of Medical Research (AU)
- Corresponding author
- Kueh, Hao Yuan
- Rothenberg, Ellen V.
- Venue
- Science
- Published
- 2013-08-09
- Volume
- 341
- Issue
- 6146
- Pages
- 670-673
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC3913367
- OpenAlex
- W2083385452
- Cited by
- 273
- References
- 46
- Citations by year
- 2026: 13 · 2025: 18 · 2024: 16 · 2023: 17 · 2022: 14 · 2021: 21 · 2020: 26 · 2019: 19 · 2018: 20 · 2017: 20 · 2016: 29 · 2015: 28 · 2014: 23 · 2013: 8
- FWCI
- 13.06
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Heart, Lung, and Blood Institute (R33HL089123)
- National Cancer Institute (R01CA090233, RC2CA148278)
- National Institute of Allergy and Infectious Diseases (R01AI083514)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- PU.1, positive feedback loop, cell cycle, myeloid differentiation, lymphoid differentiation, B cell development, macrophage development, transcriptional regulation, cell fate determination, mathematical modeling, live-cell imaging
- MeSH terms
- Proto-Oncogene Protein Spi-1, Animals, Cell Cycle, Cell Differentiation, Cells, Cultured, Gene Expression Regulation, Macrophages, Mice, Inbred Strains, Proto-Oncogene Proteins, Trans-Activators, Myeloid Cells, Feedback, Physiological, Mice, Gene Regulatory Networks, Precursor Cells, B-Lymphoid
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