Cited by 795Genomics, phytochemicals, and oxidative stressRedox biology and oxidative stressBioactive Compounds and Antitumor Agents

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Small Molecule Modulators of Keap1‐ Nrf2‐ ARE Pathway as Potential Preventive and Therapeutic Agents

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Magesh, Sadagopan, Chen, Yu, Hu, Longqin·2012·Medicinal Research Reviews

DOI 10.1002/med.21257PMC PMC3393814

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Abstract

Kelch-like ECH-associated protein 1 (Keap1)-nuclear factor erythroid 2-related factor 2 (Nrf2)-antioxidant response elements (ARE) pathway represents one of the most important cellular defense mechanisms against oxidative stress and xenobiotic damage. Activation of Nrf2 signaling induces the transcriptional regulation of ARE-dependent expression of various detoxifying and antioxidant defense enzymes and proteins. Keap1-Nrf2-ARE signaling has become an attractive target for the prevention and treatment of oxidative stress-related diseases and conditions including cancer, neurodegenerative, cardiovascular, metabolic, and inflammatory diseases. Over the last few decades, numerous Nrf2 inducers have been developed and some of them are currently undergoing clinical trials. Recently, overactivation of Nrf2 has been implicated in cancer progression as well as in drug resistance to cancer chemotherapy. Thus, Nrf2 inhibitors could potentially be used to improve the effectiveness of cancer therapy. Herein, we review the signaling mechanism of Keap1-Nrf2-ARE pathway, its disease relevance, and currently known classes of small molecule modulators. We also discuss several aspects of Keap1-Nrf2 interaction, Nrf2-based peptide inhibitor design, and the screening assays currently used for the discovery of direct inhibitors of Keap1-Nrf2 interaction.

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2 retracted

Nuclear Import and Export Signals in Control of Nrf2
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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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Background
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BackgroundInfluential
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Background
Targeting Protein–Protein Interfaces with Peptides: The Contribution of Chemical Combinatorial Peptide Library Approaches
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“Magesh et al. summarized and categorized known Nrf2 inducers, and electrophilicity is one of the most common properties (Magesh et al., 2012).”
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Dithiolethiones: A Privileged Pharmacophore for Anticancer Therapy and Chemoprevention
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BackgroundInfluential
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“In addition, decrease in Keap1 and Nrf2 as well as phase 2 enzymes including Nqo-1 and Ho-1 in hyperglycemia could reduce the production of anti-oxidative enzymes including SOD, CAT, and, GPx in cerebrum (Magesh et al. 2012).”
Background
Antioxidant Therapy in Pancreatitis
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Background
Lycium barbarum polysaccharide protects rats and cardiomyocytes against ischemia/reperfusion injury via Nrf2 activation through autophagy inhibition
Pan, H., Niu, L., Wu, Y., Chen, L., Zhou, X., & Zhao, Y. (2021) · Molecular Medicine Reports · doi:10.3892/mmr.2021.12418 · Cited by 34
Momordica charantia Ethanol Extract Attenuates H2O2-Induced Cell Death by Its Antioxidant and Anti-Apoptotic Properties in Human Neuroblastoma SK-N-MC Cells
Kim, K. B., Lee, S., Kang, I., & Kim, J.-H. (2018) · Nutrients · doi:10.3390/nu10101368 · Cited by 35
“As Nrf2 induces the activation of HO-1, various terpenoids have been reported to possess antioxidant and protective effects [46,47].”
Background
Nuclear factor-like factor 2-antioxidant response element signaling activation by tert-butylhydroquinone attenuates acute heat stress in bovine mammary epithelial cells
Jin, X., Wang, K., Liu, L., Liu, H., Zhao, F., & Liu, J. (2016) · Journal of Dairy Science · doi:10.3168/jds.2016-11031 · Cited by 32
“Numerous reports have confirmed the positive roles of Nrf2 in eliciting adaptive responses to diverse stresses by upregulating cellular antioxidant defense and restoring the cellular redox status (Magesh et al., 2012).”
Background
Importance of the Keap1-Nrf2 pathway in NSCLC: Is it a possible biomarker? (Review)
Rodríguez, R. B. (2018) · Biomedical Reports · doi:10.3892/br.2018.1143 · Cited by 32
“Two reports in the last 5 years have provided a comprehensive summary of current literature relevant to small-molecule modulators of the Keap1-Nrf2 pathway and their usefulness as potential preventive and therapeutic agents (77,78).”
Quantification and cytoprotection by vanillin, 4-methylguaiacol and 4-ethylguaiacol against AAPH-induced abnormal oxidative stress in HepG2 cells
Zhao, D., Shi, D., Sun, J., Li, H., Zhao, M., & Sun, B. (2018) · RSC Advances · doi:10.1039/c8ra06505e · Cited by 32
Catalpol and panax notoginseng saponins synergistically alleviate triptolide-induced hepatotoxicity through Nrf2/ARE pathway
Feng, Z., Zhou, C., Dong, S., Liu, Z.-P., Liu, T., Zhou, L., & Zhou, X. (2019) · Toxicology in Vitro · doi:10.1016/j.tiv.2019.01.016 · Cited by 32
Identification of compounds that inhibit the binding of Keap1a/Keap1b Kelch DGR domain with Nrf2 ETGE/DLG motifs in zebrafish
Raghunath, A., Raju, N., Sundarraj, K., Palanisamy, K., & Perumal, E. (2019) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/bcpt.13222 · Cited by 33
Cyclopentenone Prostaglandins: Biologically Active Lipid Mediators Targeting Inflammation
Lee, B. R., Paing, M. H., & Sharma-Walia, N. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.640374 · Cited by 34
“…glutathione reductase (GR), glutathione peroxidase 1 (GPx) Pleurisy, atherosclerosis Diers et al., 2010; Itoh et al., 2004; Kansanen et al., 2009; Magesh et al., 2012 15d-PGJ2 15-PGDH gene expression, protein level, and its activity, AP-1 and HO-1 Human colon cancer cell line HCT-116 Park and…”
Background
Neuroprotective mechanisms of red clover and soy isoflavones in Parkinson's disease models
Jacquet, A. D. R., Ambaw, A., Tambe, M. A., Ma, S. Y., Timmers, M. A., Grace, M. H., Wu, Q., Simon, J. E., McCabe, G. P., Lila, M. A., et al. (2021) · Food & Function · doi:10.1039/d1fo00007a · Cited by 32
Effects of medical ozone upon healthy equine joints: Clinical and laboratorial aspects
Vendruscolo, C. D. P., Moreira, J. J., Seidel, S. R. T., Fülber, J., Neuenschwander, H. M., Bonagura, G., Agreste, F. R., & Baccarin, R. Y. A. (2018) · PLoS ONE · doi:10.1371/journal.pone.0197736 · Cited by 33
Rosmarinic acid exerts an antagonistic effect on vascular calcification by regulating the Nrf2 signalling pathway
Ji, R., Sun, H., Peng, J., Ma, X., Bao, L., Fu, Y., Zhang, X., Luo, C., Gao, C., Jin, Y., et al. (2019) · Free Radical Research · doi:10.1080/10715762.2018.1558447 · Cited by 31
“Following exposure of cells to electrophiles or oxidative stress, Nrf2 is able to escape Keap1-mediated degradation, translocate to the nucleus, and activate ARE-dependent gene expression of a series of antioxidative and cytoprotective proteins, which include HO-1, NQO1, GCL, and GPx [32].”
Background
Therapeutic effects of medicinal plants on isoproterenol-induced heart failure in rats
Keihanian, F., Moohebati, M., Saeidinia, A., Mohajeri, S. A., & Madaeni, S. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.111101 · Cited by 31
Ginnalin A Binds to the Subpockets of Keap1 Kelch Domain To Activate the Nrf2-Regulated Antioxidant Defense System in SH-SY5Y Cells
Zhang, Z., Peng, L., Fu, Y., Wang, W., Wang, P., & Zhou, F. (2021) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.0c00713 · Cited by 31
Minocycline inhibits sleep deprivation-induced aberrant microglial activation and Keap1-Nrf2 expression in mouse hippocampus
Ahmed, A., Misrani, A., Tabassum, S., Yang, L., & Long, C. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.05.028 · Cited by 32
Synthesis of new betulinic acid–peptide conjugates and in vivo and in silico studies of the influence of peptide moieties on the triterpenoid core activity
Govdi, A. I., Sokolova, N. V., Sorokina, I. V., Baev, D. S., Tolstikova, T. G., Mamatyuk, V. I., Fadeev, D. S., Vasilevsky, S. F., & Nenajdenko, V. G. (2014) · MedChemComm · doi:10.1039/c4md00236a · Cited by 31
Overexpression of Brg1 Alleviates Hepatic Ischemia/Reperfusion‐Induced Acute Lung Injury through Antioxidative Stress Effects
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Impairment of gill structural integrity by manganese deficiency or excess related to induction of oxidative damage, apoptosis and dysfunction of the physical barrier as regulated by NF-κB, caspase and Nrf2 signaling in fish
Jiang, W., Tang, R.-J., Liu, Y., Wu, P., Kuang, S., Jiang, J., Tang, L., Tang, W., Zhang, Y., Zhou, X., et al. (2017) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2017.09.022 · Cited by 30
Imine Resveratrol Analogues: Molecular Design, Nrf2 Activation and SAR Analysis
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“Developing small molecules with Keap1 modifying properties has been considered as a valid strategy to achieve chemoprevention of cancer [8].”
Superoxide Dismutase 3 Dysregulation in a Murine Model of Neonatal Lung Injury
Poonyagariyagorn, H. K., Metzger, S. L., Dikeman, D. A., Lopez-Mercado, A., Malinina, A., Calvi, C. L., McGrath‐Morrow, S. A., & Neptune, E. (2014) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2013-0043oc · Cited by 30
Long‐term intake of white tea prevents oxidative damage caused by adriamycin in kidney of rats
Espinosa‐Ruíz, C., López‐Jiménez, J. Á., Pérez‐Llamas, F., Guardiola, F. A., Esteban, M. Á., Arnao, M. B., & Zamora, S. (2015) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.7483 · Cited by 30
Small molecule deoxynyboquinone triggers alkylation and ubiquitination of Keap1 at Cys489 on Kelch domain for Nrf2 activation and inflammatory therapy
Linghu, K., Zhang, T., Zhang, W., Lv, P., Zhang, W., Zhao, M., Xiong, S.-H., Ma, Q.-S., Zhao, M.-M., Chen, M., et al. (2023) · Journal of Pharmaceutical Analysis · doi:10.1016/j.jpha.2023.07.009 · Cited by 29
“In a state of basal activity, Nrf2 forms a bond with the Keap1-Kelch domain and undergoes continuous ubiquitination by the Keap1-Cul3-Ligase complex, ultimately resulting in degradation of Nrf2 within the 26S proteasome [5,10].”
BackgroundInfluential
Fucosylated chondroitin sulfate from sea cucumber Stichopus chloronotus alleviate the intestinal barrier injury and oxidative stress damage in vitro and in vivo
Yin, H., Li, R., Liu, J., Sun, Y., Zhao, L., Mou, J., & Yang, J. (2023) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2023.121722 · Cited by 33
New strategies to inhibit KEAP1 and the Cul3-based E3 ubiquitin ligases
Canning, P., & Bullock, A. N. (2014) · Biochemical Society Transactions · doi:10.1042/bst20130215 · Cited by 29
Synthesis and Evaluation of Noncovalent Naphthalene-Based KEAP1-NRF2 Inhibitors
Lazzara, P. R., Jain, A. D., Maldonado, A. C., Richardson, B. G., Skowron, K. J., David, B. P., Siddiqui, Z., Ratia, K. M., & Moore, T. W. (2020) · ACS Medicinal Chemistry Letters · doi:10.1021/acsmedchemlett.9b00631 · Cited by 28
Digestive properties and effects of Chimonanthus nitens Oliv polysaccharides on antioxidant effects in vitro and in immunocompromised mice
Zhang, Y., Han, Y., He, J., Ouyang, K., Zhao, M., Cai, L., Zhao, Z., Meng, W., Chen, L., & Wang, W. (2021) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2021.06.114 · Cited by 29
Electrophile versus oxidant modification of cysteine residues: Kinetics as a key driver of protein modification
Sauerland, M. B., & Davies, M. J. (2022) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2022.109344 · Cited by 31
Neuroprotective Effects of a Smoothened Receptor Agonist against Early Brain Injury after Experimental Subarachnoid Hemorrhage in Rats
Hu, Q., Li, T., Wang, L., Xie, Y., Liu, S., Bai, X., Zhang, T., Bo, S., Xin, D., Xue, H., et al. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00306 · Cited by 29
“In the nucleus, Nrf2 binds to antioxidant-response element (ARE) and then activates ARE-dependent gene expression, such as heme oxygenase-1 (HO-1), NAD(P)H:quinone oxidoreductase 1, glutamate-cysteine ligase, glutathione peroxidase (Magesh et al., 2012).”
Background
Anti-cancer activity of Conyza blinii saponin against cervical carcinoma through MAPK/TGF-β/Nrf2 signaling pathways
Peng, L., Hu, C., Zhang, C., Lu, Y., Man, S., & Ma, L. (2019) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2019.112503 · Cited by 29
Dietary phytochemicals targeting Nrf2 for chemoprevention in breast cancer
Wang, P., Long, F., Lin, H., & Wang, T. (2022) · Food & Function · doi:10.1039/d2fo00186a · Cited by 28
Beyond Antioxidation: Keap1–Nrf2 in the Development and Effector Functions of Adaptive Immune Cells
Pant, A., Dasgupta, D., Tripathi, A., & Pyaram, K. (2023) · ImmunoHorizons · doi:10.4049/immunohorizons.2200061 · Cited by 28
Cyclic Peptide Keap1–Nrf2 Protein–Protein Interaction Inhibitors: Design, Synthesis, and In Vivo Treatment of Acute Lung Injury
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Ozone: complicated effects in central nervous system diseases
Zhang, X., Wang, S., Wan, S.-C., Li, X., & Chen, G. (2024) · Medical Gas Research · doi:10.4103/mgr.medgasres-d-24-00005 · Cited by 30
Investigation of the intermolecular recognition mechanism between the E3 ubiquitin ligase Keap1 and substrate based on multiple substrates analysis
Jiang, Z., Xu, L., Lu, M., Pan, Y., Huang, H., Zhang, X., Sun, H.-P., & You, Q. (2014) · Journal of Computer-Aided Molecular Design · doi:10.1007/s10822-014-9799-y · Cited by 28
N-Propargyl Caffeamide Skews Macrophages Towards a Resolving M2-Like Phenotype Against Myocardial Ischemic Injury via Activating Nrf2/HO-1 Pathway and Inhibiting NF-ĸB Pathway
Cheng, Y., Yang, C., Luo, D., Li, X., Le, X. C., & Rong, J. (2018) · Cellular Physiology and Biochemistry · doi:10.1159/000491651 · Cited by 28
Perspectives on the Clinical Development of NRF2-Targeting Drugs
Lastra, D., Fernández-Ginés, R., Manda, G., & Cuadrado, A. (2020) · Handbook of experimental pharmacology · doi:10.1007/164_2020_381 · Cited by 29
Reduction of Oxidative Stress through Activating the Nrf2 mediated HO-1 Antioxidant Efficacy Signaling Pathway by MS15, an Antimicrobial Peptide from Bacillus velezensis
Khan, M. M., Kim, Y. K., Bilkis, T., Suh, J., Lee, D., & Yoo, J. C. (2020) · Antioxidants · doi:10.3390/antiox9100934 · Cited by 28
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Background
The ethanol extract of flower buds of Tussilago farfara L. attenuates cigarette smoke-induced lung inflammation through regulating NLRP3 inflammasome, Nrf2, and NF-κB
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Synthesis and bioevaluation of a series of α-pyrone derivatives as potent activators of Nrf2/ARE pathway (part I)
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Identification of Non-Electrophilic Nrf2 Activators from Approved Drugs
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“To date, the activation of Nrf2 can take place through either a direct antioxidant or indirect antioxidant mechanism, and most of the research has focused on electrophilic indirect Nrf2 activators [3,23,24].”
BackgroundInfluential
Antioxidant defense mechanisms and its dysfunctional regulation in the mitochondrial disease, Friedreich's ataxia
Chiang, S., Huang, M. L. H., Park, K. C., & Richardson, D. R. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.07.019 · Cited by 27
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An insight into prodrug strategy for the treatment of Alzheimer’s disease
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Structure-activity relationships of 1,4-bis(arylsulfonamido)-benzene or naphthalene-N,N′-diacetic acids with varying C2-substituents as inhibitors of Keap1-Nrf2 protein-protein interaction
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Neuroprotective effects of dimethyl fumarate against depression-like behaviors via astrocytes and microglia modulation in mice: possible involvement of the HCAR2/Nrf2 signaling pathway
de Souza, A. G., Lopes, I. S., Filho, A. J. M. C., Cavalcante, T. M. B., Oliveira, J. V. S., de Carvalho, M. A. J., de Lima, K. A., Jucá, P. M., Mendonça, S. S., Mottin, M., et al. (2022) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-022-02247-x · Cited by 28

Authors: Magesh, S., Chen, Y., & Hu, L.
Affiliations: Rutgers, The State University of New Jersey (US)
Corresponding author: Hu, Longqin
ORCID: Chen, Yu
Hu, Longqin
Venue: Medicinal Research Reviews
Publisher: Wiley
Published: 2012-05
Volume: 32
Issue: 4
Pages: 687-726
ISSN: 0198-6325 (ISSN-L)
1098-1128
DOI: 10.1002/med.21257
PMC: PMC3393814
OpenAlex: W1767659454
Cited by: 760
References: 275
Citations by year: 2026: 30 · 2025: 39 · 2024: 52 · 2023: 61 · 2022: 69 · 2021: 58 · 2020: 85 · 2019: 81 · 2018: 54 · 2017: 63 · 2016: 41 · 2015: 56 · 2014: 42 · 2013: 28 · 2012: 1
FWCI: 3.79
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Medicinal Research Reviews (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (CA133791, CA125868, MH093197)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics, phytochemicals, and oxidative stress
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Toxicology › Bioactive Compounds and Antitumor Agents
Keywords: Nrf2/Keap1 pathway, Nrf2, Keap1, antioxidant response element, small molecule modulators, Nrf2 inducers, Nrf2 inhibitors, oxidative stress, xenobiotic detoxification, antioxidant defense, cancer chemotherapy resistance, peptide inhibitors, Keap1-Nrf2 interaction
MeSH terms: Animals, Anti-Inflammatory Agents, Antineoplastic Agents, Antioxidants, Humans, Hypoglycemic Agents, Signal Transduction, Oxidative Stress, Neuroprotective Agents, Response Elements, Intracellular Signaling Peptides and Proteins, NF-E2-Related Factor 2

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Small Molecule Modulators of Keap1‐ Nrf2‐ ARE Pathway as Potential Preventive and Therapeutic Agents

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