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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1 retracted

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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“NF-kB is an important transcription factor that plays a critical role in the regulation of a variety of important genes in cellular responses (Liu et al., 2008).”
Background
The Glyoxalase System in Age-Related Diseases: Nutritional Intervention as Anti-Ageing Strategy
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NRF2 Activation and Downstream Effects: Focus on Parkinson’s Disease and Brain Angiotensin
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Anti-Inflammatory Therapeutic Mechanisms of Isothiocyanates: Insights from Sulforaphane
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A novel nuclear factor erythroid 2-related factor 2 (Nrf2) activator RS9 attenuates brain injury after ischemia reperfusion in mice
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Catalase Overexpression Prevents Nuclear Factor Erythroid 2–Related Factor 2 Stimulation of Renal Angiotensinogen Gene Expression, Hypertension, and Kidney Injury in Diabetic Mice
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The role of peroxiredoxin 6 in neutralization of X-ray mediated oxidative stress: effects on gene expression, preservation of radiosensitive tissues and postradiation survival of animals
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“Suppression of NRF2 activity can also be achieved by a competitive interaction of NFkb with CBP (CREB binding protein), which is a transcription co-activator of NRF2, as well as by NFkb-mediated activation of HDAC3 (histone deacetylase 3), which locally reduces histone acetylation in ARE regions, thus preventing from…”
Background
Depletion of Nrf2 Enhances Inflammation Induced by Oxyhemoglobin in Cultured Mice Astrocytes
Pan, H., Wang, H., Zhu, L., Mao, L., Qiao, L., & Su, X. (2011) · Neurochemical Research · doi:10.1007/s11064-011-0571-6 · Cited by 50
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The role of Nrf2 in periodontal disease by regulating lipid peroxidation, inflammation and apoptosis
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“Because CBP preferentially interacts with phosphorylated p65 at Ser276, the overexpression of p65 limits the availability of CBP in Nrf2 interaction (77, 78).”
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Modulation of angiotensin II signaling following exercise training in heart failure
Zucker, I. H., Schultz, H. D., Patel, K. P., & Wang, H. (2015) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00026.2015 · Cited by 49
Pyrrolidine dithiocarbamate activates the Nrf2 pathway in astrocytes
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Background
Oxidized Low-Density Lipoprotein Loading of Macrophages Downregulates TLR-Induced Proinflammatory Responses in a Gene-Specific and Temporal Manner through Transcriptional Control
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The Effects of Nuclear Factor Erythroid 2 (NFE2)-Related Factor 2 (Nrf2) Activation in Preclinical Models of Peripheral Neuropathic Pain
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BackgroundInfluential
Nutriepigenomics in Environmental-Associated Oxidative Stress
Rubio, K., Cruz, E. Y. H., Rogel-Ayala, D. G., Sarvari, P., Isidoro, C., Barreto, G., & Pedraza‐Chaverrí, J. (2023) · Antioxidants · doi:10.3390/antiox12030771 · Cited by 51
The Role of Cyclo(His-Pro) in Neurodegeneration
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Akebia Saponin D suppresses inflammation in chondrocytes via the NRF2/HO-1/NF-κB axis and ameliorates osteoarthritis in mice
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Protective effects of conventional and colon-targeted lycopene and linalool on ulcerative colitis induced by acetic acid in rats
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The molecular mechanism of AhR-ARNT-XREs signaling pathway in the detoxification response induced by polycyclic aromatic hydrocarbons (PAHs) in clam Ruditapes philippinarum
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Glyoxalase System as a Therapeutic Target against Diabetic Retinopathy
Aragonès, G., Rowan, S., Francisco, S. G., Yang, W., Weinberg, J., Taylor, A., & Bejarano, E. (2020) · Antioxidants · doi:10.3390/antiox9111062 · Cited by 48
“Downregulation of NRF2 signaling is linked to decreased expression of Glo1 and reduction of NRF2-antioxidant pathway signaling is associated with inflammation [108,157].”
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The recent advances of glucosinolates and their metabolites: Metabolism, physiological functions and potential application strategies
Wu, J., Cui, S., Liu, J., Tang, X., Zhao, J., Zhang, H., Mao, B., & Chen, W. (2022) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2022.2059441 · Cited by 45
Michael Acceptors as Anti-Cancer Compounds: Coincidence or Causality?
Andrés, C. M. C., de la Lastra, J. M. P., Munguira, E. B., Andrés, C., & Pérez‐Lebeña, E. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25116099 · Cited by 48
“The transcription factor Peroxisome Proliferator-Activated Receptor gamma (PPAR-γ ) is involved in the regulation of lipid homeostasis, inflammatory signaling and adipocyte differentiation.”
Background
Navigating the redox landscape: reactive oxygen species in regulation of cell cycle
Mackova, V., Raudenská, M., Polanska, H. H., Jakubek, M., & Masařík, M. (2024) · Redox Report · doi:10.1080/13510002.2024.2371173 · Cited by 48
“Induced by Nrf2, HO-1 inhibits NF-κB [61], while NF-κB suppresses Nrf2 by competing for the CBP–p300 complex [62].”
Possible role of methylglyoxal and glyoxalase in arthritis.
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Regulation of Myoblast Differentiation by the Nuclear Envelope Protein NET39
Liu, G., Guan, T., Datta, K., Coppinger, J. A., Yates, J. R., & Gerace, L. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.00684-09 · Cited by 47
“(Promega) following the manufacturer’s protocol (27).”
The Atypical Antipsychotic Paliperidone Regulates Endogenous Antioxidant/Anti-Inflammatory Pathways in Rat Models of Acute and Chronic Restraint Stress
MacDowell, K. S., Caso, J. R., Martín‐Hernández, D., Moreno, B. M., Madrigal, J. L. M., Micó, J. A., Leza, J. C., & García‐Bueno, B. (2016) · Neurotherapeutics · doi:10.1007/s13311-016-0438-2 · Cited by 45
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BackgroundInfluential
NRF2 as a therapeutic opportunity to impact in the molecular roadmap of ALS
Jiménez-Villegas, J., Ferraiuolo, L., Mead, R. J., Shaw, P. J., Cuadrado, A., & Rojo, A. I. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.07.022 · Cited by 44
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Background
SUMO-Modification of Human Nrf2 at K110 and K533 Regulates Its Nucleocytoplasmic Localization, Stability and Transcriptional Activity
Walters, T. S., McIntosh, D., Ingram, S., Tillery, L., Motley, E. D., Arinze, I., & Misra, S. (2021) · Cellular Physiology and Biochemistry · doi:10.33594/000000351 · Cited by 44
“Nrf2 gene expression is shown to be regulated in response to stress by different transcription factors including Nrf2 and NF-kB [2, 3].”
Ghrelin prevents 1-methyl-4-phenylpyridinium ion-induced cytotoxicity through antioxidation and NF-kappaB modulation in MES23.5 cells.
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“Some study reported that there are crosstalks between NF-κB and nuclear factor E2-related factor 2 (Nrf2) (Jin et al., 2008; Liu et al., 2008).”
Anti-oxidative and anti-inflammatory effects of cinnamaldehyde on protecting high glucose-induced damage in cultured dorsal root ganglion neurons of rats
Yang, D., Liang, X., Shi, Y., Sun, Q. Y., Liu, D., Liu, W., & Zhang, H. (2015) · Chinese Journal of Integrative Medicine · doi:10.1007/s11655-015-2103-8 · Cited by 44
“Nrf2 is critical in antioxidant response element (ARE)mediated induction of genes encoding numerous antioxidant enzymes (catalase, glutathion peroxidase, SOD and HO-1) and phase II detoxifying enzymes (GST and NQO1).((36,37)) Nrf2 and HO-1 have been shown to possess protective effect against streptozocininduced diabet…”
Background
Transcription Factors in the Cellular Response to Charged Particle Exposure
Hellweg, C. E., Spitta, L. F., Henschenmacher, B., Diegeler, S., & Baumstark‐Khan, C. (2016) · Frontiers in Oncology · doi:10.3389/fonc.2016.00061 · Cited by 46
Cardioprotective role of azafrin in against myocardial injury in rats via activation of the Nrf2-ARE pathway
Yang, S., Chou, G., & Li, Q. (2018) · Phytomedicine · doi:10.1016/j.phymed.2018.04.042 · Cited by 45
RETRACTED ARTICLE: Piceatannol protects against cisplatin nephrotoxicity via activation of Nrf2/HO-1 pathway and hindering NF-κB inflammatory cascade
Wahdan, S. A., Azab, S. S., Elsherbiny, D. A., & El‐Demerdash, E. (2019) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-019-01673-8 · Cited by 44
Retracted
Cryptotanshinone from Salvia miltiorrhiza Bunge (Danshen) inhibited inflammatory responses via TLR4/MyD88 signaling pathway
Li, X., Zheng, X., Liu, Z., Xu, Q., Tang, H., Feng, J., Yang, S., Vong, C. T., Gao, H., & Wang, Y. (2020) · Chinese Medicine · doi:10.1186/s13020-020-00303-3 · Cited by 44
Divulging the Intricacies of Crosstalk Between NF-Kb and Nrf2-Keap1 Pathway in Neurological Complications of COVID-19
Bhandari, R., Khanna, G., Kaushik, D., & Kuhad, A. (2021) · Molecular Neurobiology · doi:10.1007/s12035-021-02344-7 · Cited by 46
Anti-inflammatory and antioxidant activities of methanol extract of Piper betle Linn. (Piper betle L.) leaves and stems by inhibiting NF-κB/MAPK/Nrf2 signaling pathways in RAW 264.7 macrophages
Seo, J., Lee, U., Seo, S., Wibowo, A. E., Pongtuluran, O. B., Lee, K.-J., Han, S. B., & Cho, S. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.113734 · Cited by 51
Dietary Polyphenols Remodel DNA Methylation Patterns of NRF2 in Chronic Disease
Divyajanani, S., Harithpriya, K., Ganesan, K., & Ramkumar, K. M. (2023) · Nutrients · doi:10.3390/nu15153347 · Cited by 47
“The knockout of p65 helps promote the NRF2-CREB-binding protein (CBP), thereby decreasing the expression of NF-kB target genes such as iNOS [14].”
Background
Reductive potential — A savior turns stressor in protein aggregation cardiomyopathy
Narasimhan, M., & Rajasekaran, N. S. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2014.11.010 · Cited by 44
“Thus, we believe a sustained Nrf2 activation that is followed by one or more of these events such as heterodimerization of Bach1-MafK or homodimerization of small Mafs or p65 dependent HDAC3 recruitment that act as repressors for Nrf2/ARE transcription could presumably be compromised in the nucleus of hR120GCryAB-TG c…”
Background
Micheliolide suppresses LPS-induced neuroinflammatory responses
Sun, Z., Li, G., Tong, T., & Chen, J. (2017) · PLoS ONE · doi:10.1371/journal.pone.0186592 · Cited by 43
Inhibition of JNK Alleviates Chronic Hypoperfusion-Related Ischemia Induces Oxidative Stress and Brain Degeneration via Nrf2/HO-1 and NF-κB Signaling
Khan, M. S., Khan, A., Ahmad, S., Ahmad, R., Rehman, I. U. R., Ikram, M. A., & Kim, M. O. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/5291852 · Cited by 43
“Similarly, the suppression of NF-κB has shown promising effects on the activation of Nrf2 [46].”
Background
Retracted
Beyond direct Nrf2 activation; reinvestigating 1,2,4-oxadiazole scaffold as a master key unlocking the antioxidant cellular machinery for cancer therapy
Ayoup, M. S., Abu-Serie, M. M., Abdel‐Hamid, H., & Teleb, M. (2021) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2021.113475 · Cited by 43

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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