Interferon-γ Represses M2 Gene Expression in Human Macrophages by Disassembling Enhancers Bound by the Transcription Factor MAF
Open accessAbstract
Mechanisms by which interferon (IFN)-γ activates genes to promote macrophage activation are well studied, but little is known about mechanisms and functions of IFN-γ-mediated gene repression. We used an integrated transcriptomic and epigenomic approach to analyze chromatin accessibility, histone modifications, transcription-factor binding, and gene expression in IFN-γ-primed human macrophages. IFN-γ suppressed basal expression of genes corresponding to an "M2"-like homeostatic and reparative phenotype. IFN-γ repressed genes by suppressing the function of enhancers enriched for binding by transcription factor MAF. Mechanistically, IFN-γ disassembled a subset of enhancers by inducing coordinate suppression of binding by MAF, lineage-determining transcription factors, and chromatin accessibility. Genes associated with MAF-binding enhancers were suppressed in macrophages isolated from rheumatoid-arthritis patients, revealing a disease-associated signature of IFN-γ-mediated repression. These results identify enhancer inactivation and disassembly as a mechanism of IFN-γ-mediated gene repression and reveal that MAF regulates the macrophage enhancer landscape and is suppressed by IFN-γ to augment macrophage activation.
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WWOX and MAF were both prioritized for the WWOX locus, with MAF highly expressed in microglia and WWOX expressed most highly in astrocytes and neurons.
“WWOX and MAF, which surround an intergenic signal in an obesity associated locus91, were both prioritized for the WWOX locus, with MAF, another important regulator of macrophages92,93, being highly expressed in microglia in the Brain RNA-seq database, and WWOX, a high-density-lipoprotein cholesterol and triglyceride–associated gene94,95, being expressed most highly in astrocytes and neurons.”
From Genetic meta-analysis of diagnosed Alzheimer’s disease identifies new risk loci and implicates Aβ, tau, immunity and lipid processing (2019) · cites this paper as [92]
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- Authors
- Kang, K., Park, S. H., Chen, J., Qiao, Y., Giannopoulou, E., Berg, K., Hanidu, A., Li, J., Nabozny, G., Kang, K., Park-Min, K.-H., & Ivashkiv, L. B.
- Affiliations
- Hospital for Special Surgery (US)
- Boehringer Ingelheim (United States) (US)
- Corresponding author
- Ivashkiv, Lionel B.
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2017-08
- Volume
- 47
- Issue
- 2
- Pages
- 235-250.e4
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC5568089
- OpenAlex
- W2749286615
- Cited by
- 196
- References
- 64
- Citations by year
- 2026: 26 · 2025: 16 · 2024: 21 · 2023: 19 · 2022: 23 · 2021: 30 · 2020: 24 · 2019: 15 · 2018: 18 · 2017: 3
- FWCI
- 6.70
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Scholarworks@UNIST (Ulsan National Institute of Science and Technology) (submittedVersion)
- Funders
- Tow Foundation
- National Institutes of Health (2r01ai046712-26)
- National Institute of Allergy and Infectious Diseases (R01-AI046712, R01AI044938)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR046713)
- National Institute of Dental and Craniofacial Research (R01DE019420)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
- Keywords
- interferon-gamma, M2 macrophage phenotype, gene repression, Maf transcription factors, chromatin accessibility, histone modifications, transcription factor binding, macrophage activation, rheumatoid arthritis, enhancer landscape
- MeSH terms
- Arthritis, Rheumatoid, Cell Differentiation, Cells, Cultured, Enhancer Elements, Genetic, Gene Expression Regulation, Histones, Humans, Interferon-gamma, Macrophages, Protein Binding, Cytokines, Cell Lineage, Chromatin Assembly and Disassembly, Proto-Oncogene Proteins c-maf, Transcriptome
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