Cited by 699Genomics, phytochemicals, and oxidative stressNF-κB Signaling PathwaysNuclear Receptors and Signaling

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NF-κB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and facilitating recruitment of HDAC3 to MafK

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Liu, Guang-Hui, Qu, Jing, Shen, Xun·2008·Biochimica et Biophysica Acta (BBA) - Molecular Cell Research

DOI 10.1016/j.bbamcr.2008.01.002

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Abstract

Constitutively activated NF-kappaB occurs in many inflammatory and tumor tissues. Does it interfere with anti-inflammatory or anti-tumor signaling pathway? Here, we report that NF-kappaB p65 subunit repressed the Nrf2-antioxidant response element (ARE) pathway at transcriptional level. In the cells where NF-kappaB and Nrf2 were simultaneously activated, p65 unidirectionally antagonized the transcriptional activity of Nrf2. In the p65-overexpressing cells, the ARE-dependent expression of heme oxygenase-1 was strongly suppressed. However, p65 inhibited the ARE-driven gene transcription in a way that was independent of its own transcriptional activity. Two mechanisms were found to coordinate the p65-mediated repression of ARE: (1) p65 selectively deprives CREB binding protein (CBP) from Nrf2 by competitive interaction with the CH1-KIX domain of CBP, which results in inactivation of Nrf2. The inactivation depends on PKA catalytic subunit-mediated phosphorylation of p65 at S276. (2) p65 promotes recruitment of histone deacetylase 3 (HDAC3), the corepressor, to ARE by facilitating the interaction of HDAC3 with either CBP or MafK, leading to local histone hypoacetylation. This investigation revealed the participation of NF-kappaB p65 in the negative regulation of Nrf2-ARE signaling, and might provide a new insight into a possible role of NF-kappaB in suppressing the expression of anti-inflammatory or anti-tumor genes.

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Cytokines suppress adipogenesis and PPAR-γ function through the TAK1/TAB1/NIK cascade
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Signaling to NF-κB
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Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain
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“Nrf2 is amember of theCNC-basic leucine zipper (CNC-bZIP) family of transcription factors, which coordinately regulates the constitutive and inducible expression of antioxidant and phase 2 detoxification enzymes, such as heme oxygenase-1 (HO-1) and NAD(P)H:quinone oxidoreductase 1 (NQO1), via a cis-acting DNA element…”
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“The latter was proved to act as a negative regulator of the Nrf2 pathway by competing with it for binding to the transcriptional co-activator CREB-binding protein (CBP) and also to promote the binding of the co-repressor histone deacetylase 3 (HDAC3) to the antioxidant response element (ARE) [62]; these effects may re…”
Background
Desoxyrhapontigenin up-regulates Nrf2-mediated heme oxygenase-1 expression in macrophages and inflammatory lung injury
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Crocin ameliorates arsenic trioxide‑induced cardiotoxicity via Keap1-Nrf2/HO-1 pathway: Reducing oxidative stress, inflammation, and apoptosis
Liang, Y., Zheng, B., Li, J., Shi, J., Chu, L., Han, X., Chu, X., Zhang, J., & Zhang, J. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110713 · Cited by 76
A-kinase-interacting Protein 1 (AKIP1) Acts as a Molecular Determinant of PKA in NF-κB Signaling
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MafK positively regulates NF-κB activity by enhancing CBP-mediated p65 acetylation
Hwang, Y.-J., Lee, E., Song, J., Kim, H.-R., Jun, Y.-C., & Hwang, K. (2013) · Scientific Reports · doi:10.1038/srep03242 · Cited by 74
Concerted redox modulation by sulforaphane alleviates diabetes and cardiometabolic syndrome
Patel, B., Mann, G. E., & Chapple, S. J. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.02.004 · Cited by 77
Nrf2 Involvement in Chemical-Induced Skin Innate Immunity
Helou, D. G., Martin, S. F., Pallardy, M. J., Chollet‐Martin, S., & Kerdine‐Römer, S. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01004 · Cited by 74
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Gonchar, O. O., Maznychenko, A. V., Bulgakova, N. V., Vereshchaka, I. V., Tomiak, T., Ritter, U., Prylutskyy, Y. І., Im, M., & Kostyukov, A. I. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/2518676 · Cited by 73
“Under stress condition, C60FAS administration promotes Nrf2 nuclear accumulation and triggers the protein expression of a panel of antioxidant and phase II enzymes, at least partially, through the Nrf2/ARE signaling pathway.”
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Baicalein acts as a nephroprotectant that ameliorates colistin-induced nephrotoxicity by activating the antioxidant defence mechanism of the kidneys and down-regulating the inflammatory response
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Nrf2 deficiency influences susceptibility to steroid resistance via HDAC2 reduction
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“It is possible that loss of Nrf2 leads to activation of NF-κB by increasing the pool of CREB-binding protein (CBP) available to interact with RelA/p65 [26,27], and thus causing induction of NF-κB-dependent pro-inflammatory genes.”
BackgroundInfluential
Sumoylation Regulates Nuclear Localization of Lipin-1α in Neuronal Cells
Liu, G., & Gerace, L. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007031 · Cited by 71
“Lucifease assay The luciferase assay was performed as previously described [45,46].”
Method
Cyclo(His-Pro) exerts anti-inflammatory effects by modulating NF-κB and Nrf2 signalling
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NFκB promotes oxidative stress-induced necrosis and ischemia/reperfusion injury by inhibiting Nrf2-ARE pathway
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Regulation of innate immunity by Nrf2
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“Analogously, Neh4 and Neh5 can modulate ARE-dependent genes via binding to another transcriptional co-activator cAMP response element-binding protein (CREB)-binding protein (CBP) (Nioi et al., 2005; Katoh et al., 2001).”
Background
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“In addition to activating antioxidant enzyme expression by binding to the AREs on antioxidant promoters, Nrf2 has been shown to reduce inflammatory mediators by competing with NF-kB (Li et al., 2008; Liu et al., 2008; Kim et al., 2013).”
BackgroundInfluential
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“At the same time, the Nrf2 pathway can modify the antiinflammatory pathways by the inhibition of the NF-κB pathway [76].”
BackgroundInfluential
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“Additionally, NF-κB can restrain NRF2 signaling activity by recruiting histone deacetylase 3 (HDAC3) to NRF2-antioxidant response element (ARE), interacting with either CREBP or small MAF protein K (MAFK), and causing local histone hypoacetylation [30] (Figure 1).”
Background
PROGRESS IN UREMIC TOXIN RESEARCH: Highlights and Hotspots of Protein Glycation in End‐Stage Renal Disease
Thornalley, P. J., & Rabbani, N. (2009) · Seminars in Dialysis · doi:10.1111/j.1525-139x.2009.00589.x · Cited by 68
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Wang, H., Pan, L., Xu, R., Si, L., & Zhang, X. (2019) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2019.06.006 · Cited by 65
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Background
Polystyrene microplastics induce apoptosis in chicken testis via crosstalk between NF-κB and Nrf2 pathways
Hou, L., Wang, D., Yin, K., Zhang, Y., Lu, H., Guo, T., Li, J., Zhao, H., & Xing, M. (2022) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/j.cbpc.2022.109444 · Cited by 65
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Background
Dihydromyricetin reverses MRP2-induced multidrug resistance by preventing NF-κB-Nrf2 signaling in colorectal cancer cell
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Antioxidant Systems as Modulators of Ferroptosis: Focus on Transcription Factors
Punziano, C., Trombetti, S., Cesaro, E., Grosso, M., & Faraonio, R. (2024) · Antioxidants · doi:10.3390/antiox13030298 · Cited by 75

Authors: Liu, G.-H., Qu, J., & Shen, X.
Affiliations: Chinese Academy of Sciences (CN)
Corresponding author: Shen, Xun
ORCID: Liu, Guang-Hui
Qu, Jing
Shen, Xun
Venue: Biochimica et Biophysica Acta (BBA) - Molecular Cell Research
Publisher: Elsevier BV
Published: 2008-05
Volume: 1783
Issue: 5
Pages: 713-727
ISSN: 0167-4889 (ISSN-L)
DOI: 10.1016/j.bbamcr.2008.01.002
OpenAlex: W2113024198
Cited by: 697
References: 77
Citations by year: 2026: 54 · 2025: 45 · 2024: 51 · 2023: 47 · 2022: 68 · 2021: 51 · 2020: 59 · 2019: 59 · 2018: 47 · 2017: 38 · 2016: 32 · 2015: 33 · 2014: 15 · 2013: 28 · 2012: 13
FWCI: 7.82
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)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 1904 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Biochimica et Biophysica Acta (BBA) - Molecular Cell Research (publishedVersion)
PubMed (publishedVersion)
Funders: National Natural Science Foundation of China (30330250, 30570462)
Shanghai Municipal Education Commission (E-04010)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics, phytochemicals, and oxidative stress
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › NF-κB Signaling Pathways
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Receptors and Signaling
Keywords: NF-κB p65, Nrf2, antioxidant response element, CBP, HDAC3, MafK, heme oxygenase-1, transcriptional repression, histone deacetylation, histone hypoacetylation, PKA phosphorylation, corepressor recruitment, anti-inflammatory signaling
MeSH terms: Histone Deacetylase 3, Antioxidants, Cell Line, Gene Expression Regulation, Histone Deacetylases, Humans, Transcription, Genetic, Trans-Activators, NF-kappa B, Response Elements, CREB-Binding Protein, MafK Transcription Factor, NF-E2-Related Factor 2, Transcription Factor RelA

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NF-κB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and facilitating recruitment of HDAC3 to MafK

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