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NF-κB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1α
Open accessAbstract
The hypoxic response is an ancient stress response triggered by low ambient oxygen (O2) (ref. 1) and controlled by hypoxia-inducible transcription factor-1 (HIF-1), whose alpha subunit is rapidly degraded under normoxia but stabilized when O2-dependent prolyl hydroxylases (PHDs) that target its O2-dependent degradation domain are inhibited. Thus, the amount of HIF-1alpha, which controls genes involved in energy metabolism and angiogenesis, is regulated post-translationally. Another ancient stress response is the innate immune response, regulated by several transcription factors, among which NF-kappaB plays a central role. NF-kappaB activation is controlled by IkappaB kinases (IKK), mainly IKK-beta, needed for phosphorylation-induced degradation of IkappaB inhibitors in response to infection and inflammation. IKK-beta is modestly activated in hypoxic cell cultures when PHDs that attenuate its activation are inhibited. However, defining the relationship between NF-kappaB and HIF-1alpha has proven elusive. Using in vitro systems, it was reported that HIF-1alpha activates NF-kappaB, that NF-kappaB controls HIF-1alpha transcription and that HIF-1alpha activation may be concurrent with inhibition of NF-kappaB. Here we show, with the use of mice lacking IKK-beta in different cell types, that NF-kappaB is a critical transcriptional activator of HIF-1alpha and that basal NF-kappaB activity is required for HIF-1alpha protein accumulation under hypoxia in cultured cells and in the liver and brain of hypoxic animals. IKK-beta deficiency results in defective induction of HIF-1alpha target genes including vascular endothelial growth factor. IKK-beta is also essential for HIF-1alpha accumulation in macrophages experiencing a bacterial infection. Hence, IKK-beta is an important physiological contributor to the hypoxic response, linking it to innate immunity and inflammation.
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“Additionally, numerous studies have shown that NF-κB regulates the hypoxic response by stimulating the transcription of HIF-1α and HIF-1β, and by inducing IKK-dependent stabilization of HIF-2α [15–17].”
From The HIF Axes in Cancer - Angiogenesis, Metabolism and Immune-Modulation (2025) · cites this paper as [15]
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In the citing paper
“The ERN1 and CAPG genes might also be involved in the innate immune response since hypoxia triggers innate immunity responses through the activation of the hypoxia induced factor α1 (HIF-1α) (Oosthuyse et al., 2001; Rius et al., 2008; Singh et al., 2016).”
From Identification of Candidate Signature Genes and Key Regulators Associated With Trypanotolerance in the Sheko Breed (2019) · cites this paper as Rius et al., 2008
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“HIF-1α activation acts in concert with NF-κB activation and boosts antimicrobial immunity (Nizet and Johnson, 2009;Rius et al., 2008).”
From Iron in infection and immunity (2020) · cites this paper as Rius et al., 2008
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“In macrophages, lipopolysaccharide (LPS)-induced HIF1 a accumulation requires nuclear factor (NF)k B- and p42/44 MAPK-dependent transcriptional events (Frede et al., 2006; Rius et al., 2008).”
From Ferritin-Mediated Iron Sequestration Stabilizes Hypoxia-Inducible Factor-1α upon LPS Activation in the Presence of Ample Oxygen (2015) · cites this paper as Rius et al., 2008
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“NF-kB, which is a master regulator of inflammatory responses, is essential for the induction of baseline Hif-1α mRNA [55]”
From Hypoxia and hypoxia-inducible factors as regulators of T cell development, differentiation, and function (2013) · cites this paper as [55]
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“Recent studies indicate that transcription of HIF-1α is activated by NF-κB-mediated signaling51.”
From Hypoxia: an alarm signal during intestinal inflammation (2010) · cites this paper as [51]
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Metadata
- Authors
- Rius, J., Guma, M., Schachtrup, C., Akassoglou, K., Zinkernagel, A. S., Nizet, V., Johnson, R. S., Haddad, G. G., & Karin, M.
- Affiliations
- University of California San Diego (US)
- Corresponding author
- Karin, Michael
- ORCID
- Venue
- Nature
- Published
- 2008-04-23
- Volume
- 453
- Issue
- 7196
- Pages
- 807-811
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC2669289
- OpenAlex
- W2162121911
- Cited by
- 1,614
- References
- 34
- Citations by year
- 2026: 89 · 2025: 85 · 2024: 79 · 2023: 78 · 2022: 81 · 2021: 107 · 2020: 79 · 2019: 77 · 2018: 82 · 2017: 70 · 2016: 97 · 2015: 95 · 2014: 105 · 2013: 91 · 2012: 89
- FWCI
- 35.14
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institutes of Health
- National Cancer Institute (R01CA118165)
- National Institute of Allergy and Infectious Diseases (R01AI043477)
- National Center for Research Resources (P41RR004050)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › NF-κB Signaling Pathways
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Signaling Pathways in Disease
- Keywords
- NF-κB, HIF-1α, hypoxia response, innate immunity, IKKβ, transcriptional regulation, prolyl hydroxylase, oxygen-dependent degradation, inflammation, liver, brain, hypoxia-inducible factor, IκB kinase, oxygen sensing
- MeSH terms
- Animals, Hypoxia, Brain, Gene Expression Regulation, Immunity, Innate, Inflammation, Liver, Macrophages, Transcription, Genetic, Cell Hypoxia, NF-kappa B, Mice, I-kappa B Kinase, Hypoxia-Inducible Factor 1, alpha Subunit
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