STAT3 controls myeloid progenitor growth during emergency granulopoiesis

Zhang, Huiyuan; Nguyen-Jackson, Hoainam; Panopoulos, Athanasia D.; Li, Haiyan S.; Murray, Peter J.; Watowich, Stephanie S.

doi:10.1182/blood-2009-12-259630

Cited by 233Cytokine Signaling Pathways and InteractionsBlood disorders and treatmentsHematopoietic Stem Cell Transplantation

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STAT3 controls myeloid progenitor growth during emergency granulopoiesis

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Zhang, Huiyuan, Nguyen-Jackson, Hoainam, Panopoulos, Athanasia D., Li, Haiyan S., Murray, Peter J., Watowich, Stephanie S.·2010·Blood

DOI 10.1182/blood-2009-12-259630PMC PMC2953883

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Abstract

Granulocyte colony-stimulating factor (G-CSF) mediates “emergency” granulopoiesis during infection, a process that is mimicked by clinical G-CSF use, yet we understand little about the intracellular signaling cascades that control demand-driven neutrophil production. Using a murine model with conditional deletion of signal transducer and activator of transcription 3 (STAT3) in bone marrow, we investigated the cellular and molecular mechanisms of STAT3 function in the emergency granulopoiesis response to G-CSF administration or infection with Listeria monocytogenes, a pathogen that is restrained by G-CSF signaling in vivo. Our results show that STAT3 deficiency renders hematopoietic progenitor cells and myeloid precursors refractory to the growth-promoting functions of G-CSF or L monocytogenes infection. STAT3 is necessary for accelerating granulocyte cell-cycle progression and maturation in response to G-CSF. STAT3 directly controls G-CSF–dependent expression of CCAAT-enhancer-binding protein β (C/EBPβ), a crucial factor in the emergency granulopoiesis response. Moreover, STAT3 and C/EBPβ coregulate c-Myc through interactions with the c-myc promoter that control the duration of C/EBPα occupancy during demand-driven granulopoiesis. These results place STAT3 as an essential mediator of emergency granulopoiesis by its regulation of transcription factors that direct G-CSF–responsive myeloid progenitor expansion.

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G-CSF-mediated activation of STAT3 induces granulocytic progenitor proliferation through transcriptional upregulation of C/EBPβ and c-Myc.
“granulocyte cell-stimulating factor–mediated activation of STAT3 induces granulocytic progenitor proliferation through transcriptional upregulation of CCAAT/enhancer-binding protein (C/EBP)β and c-Myc”
From Targeting Janus Kinases and Signal Transducer and Activator of Transcription 3 To Treat Inflammation, Fibrosis, and Cancer: Rationale, Progress, and Caution (2020) · cites this paper as Zhang et al., 2010
AD-HIES patients do not demonstrate quantitative defects in basal or stress hematopoiesis, including production of neutrophils, total lymphocyte numbers, red blood cells, or platelets.
“AD-HIES patients do not demonstrate quantitative defects in basal or stress hematopoiesis, including the production of neutrophils, total lymphocyte numbers, red blood cells, or platelets”
From Targeting Janus Kinases and Signal Transducer and Activator of Transcription 3 To Treat Inflammation, Fibrosis, and Cancer: Rationale, Progress, and Caution (2020) · cites this paper as Zhang et al., 2010
The Discussion (page not provided) mentions patients with hyper-IgE syndrome but says their emergency granulopoiesis and neutrophil function have not been investigated extensively. The reported blood-cell and progenitor findings concern mice, not AD-HIES patients. Searches for AD-HIES blood-cell counts and hematopoiesis found no passage establishing the claimed absence of quantitative defects in patients. (LLM, conf=0.78)
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Authors: Zhang, H., Nguyen-Jackson, H., Panopoulos, A. D., Li, H. S., Murray, P. J., & Watowich, S. S.
Affiliations: The University of Texas MD Anderson Cancer Center (US)
St. Jude Children's Research Hospital (US)
ORCID: Zhang, Huiyuan
Panopoulos, Athanasia D.
Li, Haiyan S.
Murray, Peter J.
Watowich, Stephanie S.
Venue: Blood
Publisher: American Society of Hematology
Published: 2010-10-07
Volume: 116
Issue: 14
Pages: 2462-2471
ISSN: 0006-4971 (ISSN-L)
1528-0020
DOI: 10.1182/blood-2009-12-259630
PMC: PMC2953883
OpenAlex: W2041168245
Semantic Scholar: 911cf5f012ca2c41275c386f29013395eb9d6499
Cited by: 232
References: 50
Citations by year: 2026: 9 · 2025: 10 · 2024: 11 · 2023: 13 · 2022: 12 · 2021: 17 · 2020: 24 · 2019: 19 · 2018: 12 · 2017: 16 · 2016: 18 · 2015: 12 · 2014: 16 · 2013: 15 · 2012: 13
FWCI: 6.49
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Blood (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Cancer Institute (P30CA16672, T32CA009598, P30CA016672, T32 CA09598-16)
National Institute of Allergy and Infectious Diseases (R21AI073587, AI073587)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Cytokine Signaling Pathways and Interactions
Health Sciences › Medicine › Hematology › Blood disorders and treatments
Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
Keywords: STAT3, emergency granulopoiesis, granulocyte colony-stimulating factor, myeloid progenitor cells, neutrophil production, Listeria monocytogenes infection, C/EBPβ, c-Myc, C/EBPα, cell cycle progression, transcriptional regulation, bone marrow
MeSH terms: Animals, Cell Cycle, Gene Expression Regulation, Granulocytes, Hematopoietic Stem Cells, Listeria monocytogenes, Promoter Regions, Genetic, Signal Transduction, Granulocyte Colony-Stimulating Factor, Proto-Oncogene Proteins c-myc, Leukopoiesis, CCAAT-Enhancer-Binding Proteins, CCAAT-Enhancer-Binding Protein-beta, STAT3 Transcription Factor, Mice

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STAT3 controls myeloid progenitor growth during emergency granulopoiesis

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