Chronic interleukin-1 exposure triggers selection for Cebpa -knockout multipotent hematopoietic progenitors
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Abstract
The early events that drive myeloid oncogenesis are not well understood. Most studies focus on the cell-intrinsic genetic changes and how they impact cell fate decisions. We consider how chronic exposure to the proinflammatory cytokine, interleukin-1β (IL-1β), impacts Cebpa-knockout hematopoietic stem and progenitor cells (HSPCs) in competitive settings. Surprisingly, we found that Cebpa loss did not confer a hematopoietic cell–intrinsic competitive advantage; rather chronic IL-1β exposure engendered potent selection for Cebpa loss. Chronic IL-1β augments myeloid lineage output by activating differentiation and repressing stem cell gene expression programs in a Cebpa-dependent manner. As a result, Cebpa-knockout HSPCs are resistant to the prodifferentiative effects of chronic IL-1β, and competitively expand. We further show that ectopic CEBPA expression reduces the fitness of established human acute myeloid leukemias, coinciding with increased differentiation. These findings have important implications for the earliest events that drive hematologic disorders, suggesting that chronic inflammation could be an important driver of leukemogenesis and a potential target for intervention.
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Cebpa-deficient MPPGM show nearly identical patterns of overexpression in genes like Bmi1, Foxo3 and Mycn.
“Our previously published analysis (Higa et al., 2021) of Cebpa-deficient MPPGM shows nearly identical patterns of overexpression in genes like Bmi1, Foxo3 and Mycn (Tothova et al., 2007; Takubo et al., 2010; Merchant et al., 2011; Warr et al., 2013; Murakami et al., 2014; Scognamiglio et al., 2016).”
From PU.1 is required to restrain myelopoiesis during chronic inflammatory stress (2023) · cites this paper as Higa et al., 2021
The Results section (‘IL-1β triggers aberrant expansion potential of Cebpa-knockout MPP3s’; page unavailable) reports elevated Bmi1, Foxo3 and Mycn expression in Cebpa-deficient, GM-biased MPP3s cultured with IL-1β. The claim omits that treatment condition, and the cited paper does not establish the asserted ‘nearly identical’ pattern of overexpression. (LLM, conf=0.80)
Experimental — accuracy not yet measuredCebpa-deficient MPPGM show identical patterns of gene expression to PU.1 KI/KI MPPGM.
“It is noteworthy that we observed identical patterns of gene expression (Higa et al., 2021) in Cebpa-deficient MPPGM.”
From PU.1 is required to restrain myelopoiesis during chronic inflammatory stress (2023) · cites this paper as Higa et al., 2021
The Results section, “Chronic IL-1β–driven myeloid gene programs are Cebpa dependent” (page unavailable), reports gene-expression changes in Cebpa-deficient, GM-biased MPP3s. It does not compare those cells with PU.1 KI/KI MPPGM or establish that their expression patterns are identical. (LLM, conf=0.84)
Experimental — accuracy not yet measuredCebpa-deficient MPPGM retained high expression levels of stem cell genes including Foxo3, Mycn, Bmi1 and Bcl2 following chronic exposure to IL-1β.
“These data are strongly reminiscent of Cebpa-deficient MPPGM, which likewise retained high expression levels of stem cell genes including Foxo3, Mycn, Bmi1 and Bcl2 following chronic exposure to IL-1β (Higa et al., 2021).”
From PU.1 is required to restrain myelopoiesis during chronic inflammatory stress (2023) · cites this paper as Higa et al., 2021
The Results section, “Chronic IL-1β triggers a self-renewal gene program in Cebpa-knockout MPP3s” (page unavailable), reports elevated Bmi1, Foxo3, and Mycn in Cebpa-deficient MPP3s after chronic IL-1β exposure. It names Mpl as the fourth gene, not Bcl2; our copy does not support the claim about Bcl2. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIL-1 can trigger the selective expansion of Cebpa-deficient HSPCs in a mouse model of oncogenic BM competition.
“we found that IL-1 can trigger the selective expansion of Cebpa-deficient HSPCs in a mouse model of oncogenic BM competition (Higa et al., 2021).”
From PU.1 enforces quiescence and limits hematopoietic stem cell expansion during inflammatory stress (2021) · cites this paper as Higa et al., 2021
IL-1β-mediated repression of these genes may involve other transcriptional regulators aside from PU.1 including CEBPA.
“These data suggest IL-1β-mediated repression of these genes may involve other transcriptional regulators aside from PU.1 including CEBPA, which regulates many of the same genes (Koschmieder et al., 2005; Pundhir et al., 2018; Higa et al., 2021).”
From PU.1 is required to restrain myelopoiesis during chronic inflammatory stress (2023) · cites this paper as Higa et al., 2021
Both CEBPA and PU.1 bind genes induced or repressed by IL-1β in MPPGM, including stem cell genes and myeloid lineage determinants.
“Along these lines, we previously found that both CEBPA and PU.1 bind genes induced or repressed by IL-1β in MPPGM, including stem cell genes and myeloid lineage determinants (Higa et al., 2021).”
From PU.1 is required to restrain myelopoiesis during chronic inflammatory stress (2023) · cites this paper as Higa et al., 2021
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Clonal Architecture and Evolutionary Dynamics in Acute Myeloid Leukemias
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PU.1 is required to restrain myelopoiesis during chronic inflammatory stress
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“1 including CEBPA, which regulates many of the same genes (Koschmieder et al., 2005; Pundhir et al., 2018; Higa et al., 2021).”
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Mutant p53 promotes clonal hematopoiesis by generating a chronic inflammatory microenvironment
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TNF Receptors Choose HSC Fate in Supporting Dnmt3a -Mutant Clonal Hematopoiesis
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Alkbh5 plays indispensable roles in maintaining self-renewal of hematopoietic stem cells
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- Authors
- Higa, K. C., Goodspeed, A., Chavez, J. S., De Dominici, M., Danis, E., Zaberezhnyy, V., Rabe, J. L., Tenen, D. G., Pietras, E. M., & DeGregori, J.
- Affiliations
- University of Colorado Anschutz (US)
- University of Colorado Cancer Center (US)
- Department of Biochemistry and Molecular Genetics, University of Colorado Anschutz Medical Campus, Aurora, CO 1
- Harvard University (US)
- Corresponding author
- DeGregori, James
- ORCID
- Venue
- Journal of Experimental Medicine
- Publisher
- Rockefeller University Press
- Published
- 2021-04-29
- Volume
- 218
- Issue
- 6
- ISSN
- 0022-1007 (ISSN-L)
- 1540-9538
- PMC
- PMC8094119
- OpenAlex
- W3157426827
- Cited by
- 57
- References
- 91
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 10 · 2023: 13 · 2022: 12 · 2021: 6 · 2020: 1
- FWCI
- 6.70
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- The Journal of Experimental Medicine (publishedVersion, cc-by-nc-sa)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nd)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (R01-AG066544, R01-AG067584, R01-DK119394, R35-CA197697, P01-HL131477, F30-CA210383, T32-AG000279, F31-HL138754)
- Cleo Meador and George R. Scott Endowed Chair of Medicine in Hematology
- Department of Medicine Outstanding Early Career Scholar Program
- Leukemia and Lymphoma Society (7020-19)
- Courtenay C. and Lucy Patten Davis Endowed Chair in Lung Cancer Research
- National Cancer Institute (P30-CA046934)
- Topics
- Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Blood disorders and treatments
- Keywords
- IL-1β, CEBPA, hematopoietic stem and progenitor cells, leukemogenesis, chronic inflammation, competitive fitness, myeloid differentiation, acute myeloid leukemia
- MeSH terms
- Animals, Cell Differentiation, Cell Line, Hematopoietic Stem Cells, Humans, Inflammation, Mice, Inbred C57BL, Leukemia, Myelomonocytic, Acute, Gene Expression, Hematopoietic Stem Cell Transplantation, Cell Lineage, Myeloid Cells, CCAAT-Enhancer-Binding Proteins, Mice, Interleukin-1beta, HEK293 Cells
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