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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Background
Sulforaphane ameliorates cadmium induced hepatotoxicity through the up-regulation of /Nrf2/ARE pathway and the inactivation of NF-κB
He, Q., Luo, Y., & Xie, Z. (2020) · Journal of Functional Foods · doi:10.1016/j.jff.2020.104297 · Cited by 16
Potential of natural products in combination with arsenic trioxide: Investigating cardioprotective effects and mechanisms
Wang, J., Liu, Y., Hu, J., & Chen, C. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.114464 · Cited by 17
hucMSC Conditioned Medium Ameliorate Lipopolysaccharide-Induced Acute Lung Injury by Suppressing Oxidative Stress and Inflammation via Nrf2/NF-κB Signaling Pathway
Tang, Y., Ding, F., Wu, C. F., & Liu, B. (2021) · Analytical Cellular Pathology · doi:10.1155/2021/6653681 · Cited by 17
“Recent investigations have documented the Nrf2 cascade, and the NF-κB cascade is mutually inhibited at their transcriptional level by protein-protein cross-talks or by affecting the second messenger [5, 6].”
Background
Melatonin regulates antioxidant defense and inflammatory response by activating Nrf2–dependent mechanisms and inhibiting NFkappaB expression in middle-aged T. cruzi infected rats
Brazão, V., Colato, R. P., Santello, F. H., Duarte, A., Goulart, A., Sampaio, P. A., da Silva, C. B. P., Tirapelli, C. R., da Costa, R. M., Tostes, R. C., et al. (2022) · Experimental Gerontology · doi:10.1016/j.exger.2022.111895 · Cited by 17
Targeting Nrf2/HO-1 and NF-κB/TNF-α signaling pathways with empagliflozin protects against atrial fibrillation-induced acute kidney injury in rats
Badreldin, H., El-Karef, A., Ibrahim, T. M., & Elshal, M. (2024) · Toxicology · doi:10.1016/j.tox.2024.153879 · Cited by 16
Vincamine exerts hepato-protective activity during colon ligation puncture-induced sepsis by modulating oxidative stress, apoptosis, and TNFα/Nrf-2/Keap-1 signaling pathways
Alaaeldin, R., Mohyeldin, R. H., Sharata, E. E., Attya, M. E., & Fathy, M. (2024) · Scientific Reports · doi:10.1038/s41598-024-69729-1 · Cited by 16
“Additionally, TNFα, a central pro-inflammatory mediator involved in the pathogenesis of some inflammatory and autoimmune diseases, was notably reported to suppress Nrf-2 expression 40,41 .”
Cell line-specific oxidative stress in cellular toxicity: A toxicogenomics-based comparison between liver and colon cell models
Deferme, L., Briedé, J. J., Claessen, S. M. H., Cavill, R., & Kleinjans, J. C. S. (2015) · Toxicology in Vitro · doi:10.1016/j.tiv.2015.03.007 · Cited by 16
3-(3-Pyridylmethylidene)-2-indolinone Reduces the Severity of Colonic Injury in a Murine Model of Experimental Colitis
Wang, K., Zhang, C., Zhang, S., Liu, E.-D., Dong, L., Kong, X.-Z., Cao, P., Hu, C., Zhao, K., Zhan, Y., et al. (2015) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2015/959253 · Cited by 16
Preliminary Trichinella spiralis Infection Ameliorates Subsequent RSV Infection-Induced Inflammatory Response
Chu, K., Lee, H., Kang, H., Moon, E., & Quan, F. (2020) · Cells · doi:10.3390/cells9051314 · Cited by 15
“The p65 subunit involved in the NF-κB signaling has been documented to antagonize the Nrf2 expression by limiting the available CREB-binding protein (CBP), thereby suppressing the downstream expression of antioxidant enzymes [35,36].”
Background
Nrf2 and the Nrf2-Interacting Network in Respiratory Inflammation and Diseases
Carlson, J., Price, L., & Deng, H. (2020) · Progress in inflammation research · doi:10.1007/978-3-030-44599-7_3 · Cited by 17
“NF-κB can inactivate Nrf2 by competing with the CBP–Nrf2 interaction or by recruiting the transcription repressor HDAC3 to ARE [39].”
Background
Effects of a Novel Magnesium Complex on Metabolic and Cognitive Functions and the Expression of Synapse-Associated Proteins in Rats Fed a High-Fat Diet
Orhan, C., Tuzcu, M., Deeh, P. B. D., Şahin, N., Ojalvo, S. P., Sylla, S., Komorowski, J. R., & Şahin, K. (2021) · Biological Trace Element Research · doi:10.1007/s12011-021-02619-z · Cited by 16
Subacute inhalation of ultrafine particulate matter triggers inflammation without altering amyloid beta load in 5xFAD mice
Saveleva, L., Vartiainen, P., Górová, V., Chew, S., Belaya, I., Konttinen, H., Zucchelli, M., Korhonen, P., Kaartinen, E., Kortelainen, M., et al. (2022) · NeuroToxicology · doi:10.1016/j.neuro.2022.01.001 · Cited by 19
Anti-inflammatory and anti-oxidant properties of Melianodiol on DSS-induced ulcerative colitis in mice
Shen, J., Ma, X., He, Y., Wang, Y., Zhong, T., & Zhang, Y. (2022) · PeerJ · doi:10.7717/peerj.14209 · Cited by 17
Interplay between Nrf2 and NF-κB in Neuroinflammatory Diseases
Liddell, J. R. (2017) · Journal of Clinical & Cellular Immunology · doi:10.4172/2155-9899.1000489 · Cited by 16
Keap1 silencing boosts lipopolysaccharide-induced transcription of interleukin 6 via activation of nuclear factor κB in macrophages
Lv, P., Xue, P., Dong, J., Peng, H., Clewell, R. A., Wang, A., Wang, Y., Peng, S., Qu, W., Zhang, Q., et al. (2013) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2013.07.012 · Cited by 16
Involvement of Nrf2 Signaling in Lead-induced Toxicity
Arabnezhad, M., Haghani, F., Ghaffarian‐Bahraman, A., Jafarzadeh, E., Mohammadi, H., Yadegari, J. G., Farkhondeh, T., Aschner, M., Darroudi, M., Marouzi, S., et al. (2023) · Current Medicinal Chemistry · doi:10.2174/0929867330666230522143341 · Cited by 15
The untapped potential of targeting NRF2 in neurodegenerative disease
Chen, W.-T., & Dodson, M. B. (2023) · Frontiers in Aging · doi:10.3389/fragi.2023.1270838 · Cited by 18
“…2011; Khor et al., 2014), as well as transcriptional up or downregulation of NRF2 expression by other transcription factors (i.e., nuclear factor kappa B [NF-κ B] and aryl hydrocarbon receptor [AhR]) (microRNA) (Miao et al., 2005; Liu et al., 2008), have all been shown to dictate the NRF2 response.”
Combination of monoammonium glycyrrhizinate and cysteine hydrochloride ameliorated lipopolysaccharide/galactosamine-induced acute liver injury through Nrf2/ARE pathway
Chu, S., Niu, Z., Guo, Q., Bi, H., Li, X., Li, F., Zhang, Z., He, W., Cao, P., Chen, N., et al. (2020) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2020.173258 · Cited by 15
Lichen-Derived Depsides and Depsidones Modulate the Nrf2, NF-κB and STAT3 Signaling Pathways in Colorectal Cancer Cells
Papierska, K., Krajka‐Kuźniak, V., Paluszczak, J., Kleszcz, R., Skalski, M., Studzińska-Sroka, E., & Baer‐Dubowska, W. (2021) · Molecules · doi:10.3390/molecules26164787 · Cited by 15
“Activated NF-κB competes with Nrf2 for CBP coactivators and leads to Nrf2 inactivation [37].”
Background
Autophagic Flux Unleashes GATA4‐NF‐ κ B Axis to Promote Antioxidant Defense‐Dependent Survival of Colorectal Cancer Cells under Chronic Acidosis
Liu, X., Zhao, M., Sun, X., Meng, Z., Bai, X., Gong, Y., Xu, L., Hao, X., Yang, T., Wei, Z., et al. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/8189485 · Cited by 15
“The upregulation of NF-κB further argues against the role of NRF2 in antioxidant defense in CRC-AA cells because the NRF2-ARE pathway is antagonized by NF-κB [45].”
Background
Association between insulin and Nrf2 signalling pathway in Alzheimer's disease: A molecular landscape
Rahman, S. O., Khan, T. M., Iqubal, A., Agarwal, S., Akhtar, M., Parvez, S., Shah, Z. A., & Najmi, A. K. (2023) · Life Sciences · doi:10.1016/j.lfs.2023.121899 · Cited by 15
Diallyl Disulfide Blocks Cigarette Carcinogen 4-(Methylnitrosamino)-1-(3-pyridyl)-1-butanone-Induced Lung Tumorigenesis via Activation of the Nrf2 Antioxidant System and Suppression of NF-κB Inflammatory Response
Tian, J., Zhao, W., Wu, Y., Shi, Y., Yu, J., Zhang, W., Xing, C., Zhuang, C., & Qu, Z. (2023) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.3c02007 · Cited by 15
Guben Qingfei decoction attenuates LPS-induced acute lung injury by modulating the TLR4/NF-κB and Keap1/Nrf2 signaling pathways
Zeng, Z., Fu, Y., Li, M., Shi, Y., Ding, Q., & Chen, S. (2023) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2023.117674 · Cited by 15
Nanoparticles with intermediate hydrophobicity polarize macrophages to plaque-specific Mox phenotype via Nrf2 and HO-1 activation
Zhai, S., Zhang, X., Jiang, M., Liu, Y., Qu, G., Cui, X., Hirschbiegel, C., Liu, Y., Alves, C., Lee, Y.-W., et al. (2024) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2024.133590 · Cited by 15
Oxidative State in Cutaneous Melanoma Progression: A Question of Balance
Benedusi, M., Lee, H., Lim, Y., & Valacchi, G. (2024) · Antioxidants · doi:10.3390/antiox13091058 · Cited by 16
Igalan induces detoxifying enzymes mediated by the Nrf2 pathway in HepG2 cells
Lee, K., Shin, J. M., Chun, J., Song, K., Nho, C. W., & Kim, Y. S. (2019) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.22297 · Cited by 14
3 β -Hydroxysteroid- Δ 24 Reductase (DHCR24) Protects Pancreatic β Cells from Endoplasmic Reticulum Stress-Induced Apoptosis by Scavenging Excessive Intracellular Reactive Oxygen Species
Li, Y., Wang, X., Yang, B., Wang, H., Ma, Z., Lu, Z., Lu, X., & Gao, B. (2020) · Journal of Diabetes Research · doi:10.1155/2020/3426902 · Cited by 14
Yeast β-glucan Increases Etoposide Sensitivity in Lung Cancer Cell Line A549 by Suppressing Nuclear Factor Erythroid 2-Related Factor 2 via the Noncanonical Nuclear Factor Kappa B Pathway
Siswanto, F. M., Tamura, A., Sakuma, R., & Imaoka, S. (2022) · Molecular Pharmacology · doi:10.1124/molpharm.121.000475 · Cited by 14
Reactive Oxygen Species and Reactive Nitrogen Species in Epigenetic Modifications
Baird, A., O'Byrne, K. J., & Gray, S. G. (2014) · Springer eBooks · doi:10.1007/978-3-642-30018-9_32 · Cited by 14
“The repression and negative regulation of Nrf2 by p65 has been shown to occur in two ways, (a) via competitively binding to KAT3A (CBP) within the CH1-KIX domain and (b) promoting HDAC3 recruitment to antioxidant response elements (AREs) and its interaction with KAT3A (CBP) or MafK leading to histone hypoacetylation (…”
Background
Irradiation with UV ‐C inhibits TNF ‐α‐dependent activation of the NF ‐κB pathway in a mechanism potentially mediated by reactive oxygen species
Szołtysek, K., Walaszczyk, A., Janus, P., Kimmel, M., & Widłak, P. (2016) · Genes to Cells · doi:10.1111/gtc.12455 · Cited by 15
“…pathways that Genes to Cells (2017) 22, 45–58 © 2016 Molecular Biology Society of Japan and John Wiley & Sons Australia, Ltd depend on p53, JNK/AP-1 and NF-jB, and that are involved in the protection of cells against ROSrelated damage (Liu et al. 2008a,b; Ray et al. 2012; Vurusanera et al. 2012).”
Background
Redox Sensitive Transcription via Nrf2-Keap1 in Suppression of Inflammation
Bhakkiyalakshmi, E., Sireesh, D., & Ramkumar, K. M. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-805417-8.00012-3 · Cited by 14
Nrf2 and autonomic dysregulation in chronic heart failure and hypertension
Wafi, A. M. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1206527 · Cited by 16
“have shown that Nrf2 displaces NFKB from CBP through competitive interaction with a specific Creb Binding Protein (CBP) domain (Liu et al., 2008).”
Background
Pathways to therapy resistance: The sheltering effect of the bone marrow microenvironment to multiple myeloma cells
Bhowmick, K., Suskil, M. V., Al‐Odat, O. S., Elbezanti, W. O., Jonnalagadda, S. C., Budak-Alpdoǧan, T., & Pandey, M. K. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e33091 · Cited by 15
Chlorogenic acid improves SPS-induced PTSD-like behaviors in rats by regulating the crosstalk between Nrf2 and NF-κB signaling pathway
Tang, C. L., Gao, J., Li, S., Cheng, Y.-F., Peng, Y.-Y., Ding, Y., Yang, H., Ma, X.-M., Wang, H., Long, Z., et al. (2025) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2025.02.034 · Cited by 14
The Complicated Role of Nuclear Factor Erythroid-Derived 2-Like 2 in Allergy and Asthma
Rockwell, C. E., Jin, Y., Boss, A. P., Kaiser, L. M., & Awali, S. (2021) · Drug Metabolism and Disposition · doi:10.1124/dmd.121.000414 · Cited by 13
Dietary and Synthetic Activators of the Antistress Gene Response in Treatment of Renal Disease
Thornalley, P. J., & Rabbani, N. (2011) · Journal of Renal Nutrition · doi:10.1053/j.jrn.2011.10.012 · Cited by 13
Targeting the Nrf2/HO-1 aixs: A therapeutic strategy against regulated cell death in Alzheimer’s disease
Wang, Z., Feng, W., Li, X., Yun, X., Wu, S., Du, L., & Wang, H. (2026) · Ageing Research Reviews · doi:10.1016/j.arr.2026.103035 · Cited by 15
Adenophora Stricta Root Extract Protects Lung Injury from Exposure to Particulate Matter 2.5 in Mice
Park, S.-M., Jung, C.-J., Lee, D.-G., Choi, B., Ku, T.-H., La, I.-J., Cho, I. J., & Ku, S. (2022) · Antioxidants · doi:10.3390/antiox11071376 · Cited by 12
“, CREB binding protein) and Keap1-mediated sequestration of inhibitory κB kinase β [54,55].”
Background
Nrf2 Drives Hepatocellular Carcinoma Progression through Acetyl-CoA–Mediated Metabolic and Epigenetic Regulatory Networks
Xi, C., Pang, J., Barrett, A., Horuzsko, A., Ande, S., Mivechi, N. F., & Zhu, X. (2023) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-22-0935 · Cited by 12
The Role of NRF2 in Trinucleotide Repeat Expansion Disorders
Chang, K., & Chen, C. (2024) · Antioxidants · doi:10.3390/antiox13060649 · Cited by 12
“Moreover, P65 inhibits NRF2 activity by competitive association with cAMP response element-binding protein (CREB)-binding protein (CBP) [135], which is required for the transactivation of NRF2 [79].”
Background
Reno-protective effect of fenofibrate and febuxostat against vancomycin-induced acute renal injury in rats: Targeting PPARγ/NF-κB/COX-II and AMPK/Nrf2/HO-1 signaling pathways
El‐Shoura, E. A. M., Sharkawi, S. M. Z., Abdelzaher, L. A., Abdel-Wahab, B. A., Ahmed, Y. H., & Abdel-Sattar, A. R. (2024) · Immunopharmacology and Immunotoxicology · doi:10.1080/08923973.2024.2373216 · Cited by 12
“By inhibiting the CREB-binding protein from binding to the Nrf2 promoter, the NF-κB-p65 subunit can prevent transcription of the Nrf2-antioxidant response element pathway [48].”
Protective role of melatonin against diclofenac-induced acute kidney injury
Agaty, S. M. E., Khedr, S., Mostafa, D. K. M., Wanis, N. A., & Abou-Bakr, D. A. (2024) · Life Sciences · doi:10.1016/j.lfs.2024.122936 · Cited by 12
Epigenetic regulation of Nrf2-Mediated angiogenesis in diabetic foot ulcer progression: Role of histone deacetylases
Harithpriya, K., Jayasuriya, R., Milan, K. L., Juttada, U., Kumpatla, S., Viswanathan, V., & Ramkumar, K. M. (2024) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2024.110133 · Cited by 12
Maslinic Acid Ameliorates Myocardial Ischemia Reperfusion Injury-Induced Oxidative Stress via Activating Nrf2 and Inhibiting NF-κB Pathways
Li, Q., Li, Z., Liu, C., Xu, M., Li, T., Wang, Y., Feng, J., Yin, X., Du, X., & Lu, C. (2023) · The American Journal of Chinese Medicine · doi:10.1142/s0192415x2350043x · Cited by 12

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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