MicroRNA-17/20a/106a modulate macrophage inflammatory responses through targeting signal-regulatory protein α

Zhu, Dihan; Pan, Chaoyun; Li, Limin; Bian, Zhen; Lv, Zhiyuan; Shi, Lei; Zhang, Jing; Li, Donghai; Gu, Hongwei; Zhang, Chen-Yu; Liu, Yuan; Zen, Ke

doi:10.1016/j.jaci.2013.02.005

Cited by 140Phagocytosis and Immune RegulationMicroRNA in disease regulationNeuroinflammation and Neurodegeneration Mechanisms

MicroRNA-17/20a/106a modulate macrophage inflammatory responses through targeting signal-regulatory protein α

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Zhu, Dihan, Pan, Chaoyun, Li, Limin, Bian, Zhen, Lv, Zhiyuan, Shi, Lei, Zhang, Jing, Li, Donghai +4 more·2013·Journal of Allergy and Clinical Immunology

DOI 10.1016/j.jaci.2013.02.005PMC PMC5882493

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Abstract

Background Signal-regulatory protein α (SIRPα) is an essential signaling molecule that modulates leukocyte inflammatory responses. However, the regulation of selective SIRPα synthesis and its dynamic changes in leukocytes under inflammatory stimulation remain incompletely understood. Objective We sought to identify the microRNAs (miRNAs) that posttranscriptionally regulate SIRPα synthesis and their roles in modulating macrophage inflammatory responses. Methods SIRPα was induced in SIRPα-negative promyelocytic cells by retinoic acid or phorbol 12-myristate 13-acetate, and the differential expression of miRNAs was assessed by means of microarray and quantitative RT-PCR assays. The roles of identified miRNAs in controlling SIRPα synthesis in leukocytes and leukocyte inflammatory responses were determined. Results We identified SIRPα as a common target gene of miR-17, miR-20a, and miR-106a. During SIRPα induction, levels of these 3 miRNAs were all reduced, and their downregulation by retinoic acid or phorbol 12-myristate 13-acetate occurred through suppression of the c-Myc signaling pathway. All miR-17, miR-20a, and miR-106a specifically bound to the same seed sequence within the SIRPα 3' untranslated region and correlated inversely with SIRPα protein levels in various cells. In macrophages upregulation of miR-17, miR-20a, and miR-106a by LPS served as the mechanism underlying LPS-induced SIRPα reduction and macrophage activation. Both in vitro and in vivo assays demonstrate that miR-17, miR-20a, and miR-106a regulate macrophage infiltration, phagocytosis, and proinflammatory cytokine secretion through targeting SIRPα. Conclusion These findings demonstrate for the first time that miR-17, miR-20a, and miR-106a regulate SIRPα synthesis and SIRPα-mediated macrophage inflammatory responses in a redundant fashion, providing a novel pathway in which a panel of miRNAs can modulate immune polarization through regulation of macrophage activation.

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LPS stimulation leads to upregulation of miR-17, miR-20a, and miR-106a, which suppresses SIRPα, resulting in macrophage activation.
“LPS stimulation, responsible for M1 phenotype differentiation, leads to upregulation of miR-17, miR-20a, and miR-106a, which suppresses SIRPα, resulting in macrophage activation [114].”
From MicroRNAs as Regulators of Phagocytosis (2022) · cites this paper as [114]
Inhibition of miR-17, miR-20a, and miR-106a derepresses SIRPα, decreasing phagocytic capacity measured as zymosan uptake.
“inhibition of the abovementioned microRNAs leads to derepression of SIRPα, resulting in decreased phagocytic capacity measured as zymosan uptake [114]”
From MicroRNAs as Regulators of Phagocytosis (2022) · cites this paper as [114]

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Authors: Zhu, D., Pan, C., Li, L., Bian, Z., Lv, Z., Shi, L., Zhang, J., Li, D., Gu, H., Zhang, C.-Y., Liu, Y., & Zen, K.
Affiliations: Nanjing General Hospital of Nanjing Military Command (CN)
State Key Laboratory of Pharmaceutical Biotechnology (CN)
Georgia State University (US)
Corresponding author: Zhang, Chen-Yu
Liu, Yuan
Zen, Ke
ORCID: Pan, Chaoyun
Li, Limin
Bian, Zhen
Lv, Zhiyuan
Shi, Lei
Zhang, Jing
Li, Donghai
Zhang, Chen-Yu
Liu, Yuan
Zen, Ke
Venue: Journal of Allergy and Clinical Immunology
Publisher: Elsevier BV
Published: 2013-08
Volume: 132
Issue: 2
Pages: 426-436.e8
ISSN: 0091-6749 (ISSN-L)
DOI: 10.1016/j.jaci.2013.02.005
PMC: PMC5882493
OpenAlex: W2070985562
Cited by: 140
References: 41
Citations by year: 2026: 3 · 2025: 6 · 2024: 12 · 2023: 12 · 2022: 8 · 2021: 20 · 2020: 11 · 2019: 14 · 2018: 9 · 2017: 12 · 2016: 16 · 2015: 7 · 2014: 6 · 2013: 3
FWCI: 5.90
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Journal of Allergy and Clinical Immunology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Allergy and Infectious Diseases (R01AI106839)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: microRNA-17, microRNA-20a, SIRPα, macrophage activation, macrophage inflammation, 3' untranslated region, post-transcriptional regulation, lipopolysaccharide, phagocytosis, macrophage infiltration, inflammatory cytokines, immune polarization
MeSH terms: Animals, Antigens, Differentiation, Cell Line, Gene Expression Regulation, Humans, Inflammation, Macrophage Activation, Macrophages, Male, Mice, Inbred C57BL, Receptors, Immunologic, Signal Transduction, HL-60 Cells, U937 Cells, MicroRNAs, Mice

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MicroRNA-17/20a/106a modulate macrophage inflammatory responses through targeting signal-regulatory protein α

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