Ischemia/reperfusion induces interferon stimulated gene expression in microglia
Open accessAbstract
Innate immune signaling is important in the pathophysiology of ischemia/reperfusion (stroke)-induced injury and recovery. Several lines of evidence support a central role for microglia in these processes. Recent work has identified Toll-like receptors (TLRs) and type I interferon (IFN) signaling in both ischemia/reperfusion-induced brain injury and ischemic preconditioning-mediated neuroprotection. To determine the effects of “ischemia/reperfusion-like” conditions on microglia, we performed genomic analyses on wild-type (WT) and TLR4−/− cultured microglia after sequential exposure to hypoxia/hypoglycemia and normoxia/normoglycemia (H/H–N/N). We observed increased expression of type 1 IFN-stimulated genes (ISGs) as the predominant transcriptomal feature of H/H–N/N-exposed WT, but not TLR4−/−, microglia. Microarray analysis on ex vivo sorted microglia from ipsilateral male mouse cortex after a transient in vivo ischemic pulse also demonstrated robust expression of ISGs. Type 1 IFNs, including the IFN-αs and IFN-β, activate the interferon-α/β receptor (IFNAR) complex. We confirmed both in vitro H/H–N/N- and in vivo ischemia/reperfusion-induced microglial ISG responses by quantitative real-time PCR and demonstrated that both were dependent on IFNAR1. We characterized the effects of hypoxia/hypoglycemia on phosphorylation of signal transducer and activator of transcription 1 (STAT1), release of type 1 IFNs, and surface expression of IFNAR1 in microglia. We demonstrated that IFN-β induces dose-dependent secretion of ISG chemokines in cultured microglia and robust ISG expression in microglia both in vitro and in vivo. Finally, we demonstrated that the microglial ISG chemokine responses to TLR4 agonists were dependent on TLR4 and IFNAR1. Together, these data suggest novel ischemia/reperfusion-induced pathways for both TLR4-dependent and -independent, IFNAR1-dependent, type 1 IFN signaling in microglia. SIGNIFICANCE STATEMENT Stroke is the fifth leading cause of death in the United States and is a leading cause of serious long-term disability worldwide. Innate immune responses are critical in stroke pathophysiology, and microglia are key cellular effectors in the CNS response to ischemia/reperfusion. Using a transcriptional analysis approach, we identified a robust interferon (IFN)-stimulated gene response within microglia exposed to ischemia/reperfusion in both in vitro and in vivo experimental paradigms. Using a number of complementary techniques, we have demonstrated that these responses are dependent on innate immune signaling components including Toll-like receptor-4 and type I IFNs. We have also elucidated several novel ischemia/reperfusion-induced microglial signaling mechanisms.
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In the brain, under sterile inflammatory conditions, there are increasing reports showing activation of the Type I IFN response in ischemia, spinal cord injury, and in two different AD mouse models as well as in AD patients.
“However, in the brain, and under sterile inflammatory conditions, there are increasing numbers of reports showing activation of the Type I IFN response in ischemia (McDonough et al., 2017), spinal cord injury (Impellizzeri et al., 2015) and in two different AD mouse models, the 5xFAD (Landel et al., 2014) and APP/PS1 (Taylor et al., 2014), as well as in AD patients (Taylor et al., 2014).”
From TET2 Regulates the Neuroinflammatory Response in Microglia (2019) · cites this paper as McDonough et al., 2017
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- Authors
- McDonough, A., Lee, R. V., Noor, S., Lee, C., Le, T., Iorga, M., Phillips, J. L. H., Murphy, S., Möller, T., & Weinstein, J. R.
- Affiliations
- University of Washington (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2017-07-26
- Volume
- 37
- Issue
- 34
- Pages
- 8292-8308
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC5566872
- OpenAlex
- W2738570053
- Cited by
- 71
- References
- 94
- Citations by year
- 2026: 8 · 2025: 8 · 2024: 11 · 2023: 9 · 2022: 8 · 2021: 7 · 2020: 8 · 2019: 6 · 2018: 5 · 2017: 1
- FWCI
- 2.72
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (F32NS100245, R01NS076620, K02NS065008)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54HD083091)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- microglia, interferon-stimulated genes, type I interferon, IFNAR1, TLR4, hypoxia/hypoglycemia, STAT1 phosphorylation, interferon-beta, chemokines, stroke, innate immune signaling, ischemic preconditioning, neuroprotection, TLR4 agonist
- MeSH terms
- Animals, Animals, Newborn, Cells, Cultured, Brain Ischemia, Dose-Response Relationship, Drug, Female, Interferons, Male, Mice, Inbred C57BL, Reperfusion Injury, Gene Expression, Microglia, Mice, Knockout, Toll-Like Receptor 4, Mice, Receptor, Interferon alpha-beta
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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