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
Jain, A. K., Bloom, D. A., & Jaiswal, A. K. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m502083200 · Cited by 195
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RETRACTED: Sulforaphane protects brains against hypoxic–ischemic injury through induction of Nrf2-dependent phase 2 enzyme
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“Sesquiterpenes such as zumberone (18)180 and isoalantolactone (19),181 and terpenoids containing α,β-unsaturated fragrant aldehydes182 such as perillaldehyde (20) and citral (21) were shown to induce Nrf2-mediated expression of detoxifying enzymes.”
Background
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Background
Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain
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“Sesquiterpenes such as zumberone (18)180 and isoalantolactone (19),181 and terpenoids containing α,β-unsaturated fragrant aldehydes182 such as perillaldehyde (20) and citral (21) were shown to induce Nrf2-mediated expression of detoxifying enzymes.”
Background
Cell Survival Responses to Environmental Stresses Via the Keap1-Nrf2-ARE Pathway
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BackgroundInfluential
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BackgroundInfluential
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“Compounds such as resveratrol, for example, are known to activate Nrf2 indirectly by promoting the modulation of enzymes, including AMP-activated kinase 1 (AMPK), which phosphorylates and activates Nrf2 (Figure 1) [4].”
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“The Keap1 protein contains 27 cysteine residues, some of which are accessible for redox oxidation or electrophile conjugation and act as a stress sensor (Dinkova-Kostova et al., 2002; Eggler et al., 2005; Holland and Fishbein, 2010; Kansanen et al., 2013; Magesh et al., 2012; Suzuki et al., 2019; Zhang and Hannink, 20…”
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“for the activation of this pathway could be that some chemical compounds with antioxidant properties have the ability to be redox active and activate the Nrf2-ARE pathway [42].”
Background
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Background
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“28 Recent studies have documented that Nrf2 provides protection targets in many diseases.”
Background
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“It is well known that Nrf2 increases the ARE-dependent gene expression of a series of antioxidant proteins [67] and regulatory T cells to release anti-inflammatory cytokines [68], which enter the gut–spleen axis by patrolling CD8 T cells and ameliorating severe cytotoxicity and inflammation [36,39].”
Background
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Covalent Inhibitors of KEAP1 with Exquisite Selectivity
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“Enone and ketone groups of Curcumin react as a Michael acceptor with key cysteine thiolate residues in Kelch-like ECH-associated protein 1 (Keap1), a protein that suppresses Nrf2 activity by binding (Magesh et al. 2012).”
Effects of different-intensity exercise and creatine supplementation on mitochondrial biogenesis and redox status in mice.
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“to exercise training, is an important transcription factor that regulates the expression of anti-oxidant proteins and enhances the anti-oxidant defense system against oxidative damage (10).”
Background
Structural basis of Nrf2 activation by flavonolignans from silymarin
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Renoprotective Effect of Thymoquinone against Streptozotocin-Induced Diabetic Nephropathy: Role of NOX2 and Nrf2 Signals
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Influential
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Discovery of polypodiside as a Keap1-dependent Nrf2 activator attenuating oxidative stress and accumulation of extracellular matrix in glomerular mesangial cells under high glucose
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Design, synthesis and evaluation of novel small molecules acting as Keap1-Nrf2 protein-protein interaction inhibitors
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Synthetic Triterpenoid RTA dh404 (CDDO-dhTFEA) Ameliorates Acute Pancreatitis
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“The phase II genes are involved in the inactivation of ROS, increased antioxidant capacity, and suppression of inflammation.(18,39)While ROS act as critical signaling messengers in cellular redox reactions, sustained oxidative stress leads to cellular damage.”
Background
Biological activity of organoselenium compounds in heavy metal intoxication
Rusetskaya, N. Y., & Бородулин, В. Б. (2015) · Biochemistry (Moscow) Supplement Series B Biomedical Chemistry · doi:10.1134/s1990750815010072 · Cited by 12
Synthesis and evaluation of novel ethyl ferulate derivatives as potent Keap1 inhibitors to activate the Nrf2/ARE pathway in Parkinson's disease
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Flavonoids from Polypodium hastatum as neuroprotective agents attenuate cerebral ischemia/reperfusion injury in vitro and in vivo via activating Nrf2
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“As the soft Lewis acids, they can react with the critical cysteine thiolate (soft base) groups in Keap1 to hinder the formation of Keap1-Nrf2 complex and activate Nrf2 [17].”
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Neuroprotection in Parkinson Disease
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Eletrophilic Chemistry of Tranilast Is Involved in Its Anti-Colitic Activity via Nrf2-HO-1 Pathway Activation
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Discovery and Anti-Inflammatory Activity of a Cyanobacterial Fatty Acid Targeting the Keap1/Nrf2 Pathway
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“Analysis of regulator effect networks at 32 µ M identiﬁed the known ARE activators ﬁngolimod, resveratrol and curcumin to have similar effects as 1 [6,48].”
Background
Effects of ubiquitin-proteasome inhibitor on the expression levels of TNF-α and TGF-β1 in mice with viral myocarditis
Zhang, H., Yu, J., Sun, H., Zhao, Y., Wang, J., Zhang, J., & Meng, B. (2019) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2019.7895 · Cited by 9
“However, some studies (22) have obtained different results when different UPS inhibitors were applied in the intervention of ischemic cardiomyopathy, and the reason is not clear at present.”
Result
Dietary Phytochemicals in Neurodegenerative Disease
Jacquet, A. D. R., Tambe, M. A., & Rochet, J. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-802928-2.00018-7 · Cited by 8
Impact of epigallocatechin‑3‑gallate on expression of nuclear factor erythroid 2‑related factor 2 and γ‑glutamyl cysteine synthetase genes in oxidative stress‑induced mouse renal tubular epithelial cells
Du, X., Yu, J., Sun, X., Qu, S., Zhang, H., Hu, M., Yang, S., & Zhou, P. H. (2018) · Molecular Medicine Reports · doi:10.3892/mmr.2018.8798 · Cited by 9
“Experiments have demonstrated that Nrf2 is able to interact with ARE to regulate the expression of antioxidant proteins and phase II detoxifying enzymes (28).”
Vernonia patula (Dryand.) Merr. and Leucas chinensis (Retz.) R. Brown exert anti-inflammatory activities and relieve oxidative stress via Nrf2 activation
Wu, P.-S., Jeng, J., Yang, J.-J., Kao, V. Y.-Y., Yen, J.-H., & Wu, M. (2020) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2020.113155 · Cited by 9
The identification and characterization of non-reactive inhibitor of Keap1-Nrf2 interaction through HTS using a fluorescence polarization assay
Wang, L., Lewis, T. A., Zhang, Y., Khodier, C., Magesh, S., Chen, L., Inoyama, D., Chen, Y., Zhen, J., Hu, L., et al. (2013) · Europe PMC (PubMed Central) · Cited by 9
Discovery of β-amino acid substituted naphthalene sulfonamide derivatives as potent Kelch-like ECH-associated protein 1−nuclear factor erythroid 2-related factor 2 (Keap1−Nrf2) protein−protein interaction inhibitors for ulcerative colitis management
Zhao, Z., Lu, H., Wang, J., Wu, T., Xu, S., Ge, Y., You, Q., Jiang, Z., & Lu, M. (2025) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2025.117384 · Cited by 11
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da Silva, R. C., Polegato, B. F., Azevedo, P. S., Fernandes, A. A. H., Okoshi, K., de Paiva, S. A. R., Minicucci, M. F., & Zornoff, L. A. M. (2022) · Antioxidants · doi:10.3390/antiox11020249 · Cited by 8
“However, in stressful situations, Nrf-2 migrates to the nucleus and combines with a small protein, forming a heterodimer and initiating the transcription of genes involved in the antioxidant response [36].”
Background
Swinhoeic acid from Potentilla fragarioides ameliorates high glucose-induced oxidative stress and accumulation of ECM in mesangial cells via Keap1-dependent activation of Nrf2
Yao, H., Kong, M., Du, D., Ai, F., Li, J., & Li, Y. (2022) · Redox Report · doi:10.1080/13510002.2022.2134755 · Cited by 8
“And they can react with the key thiol groups (soft base) in cysteine residues of Keap1 through Michael addition reaction, which gives rise to the activation of Nrf2 [31].”
Background
What is the role of Von Willebrand factor in chronic hepatitis B virus infection to hepatocellular carcinoma: a review article
Xiang, Q., Tao, J., Li, J., Tian, R.-B., & Li, X.-H. (2022) · Therapeutic Advances in Chronic Disease · doi:10.1177/20406223221125683 · Cited by 8
A recent update on the connection between dietary phytochemicals and skin cancer: emerging understanding of the molecular mechanism
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“This pathway is involved in the regulation of antioxidant enzymes and can help to protect cells against oxidative damage [397 – 399] .”
Background
Design and synthesis of novel iminothiazinylbutadienols and divinylpyrimidinethiones as ARE inducers
Chen, L., Magesh, S., Wang, H., Yang, C. S., Kong, A. T., & Hu, L. (2013) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2013.12.072 · Cited by 8
Dexmedetomidine Attenuates Orthotopic Liver Transplantation-Induced Acute Gut Injury via α2-Adrenergic Receptor-Dependent Suppression of Oxidative Stress
Lv, P., Chen, T., Liu, P., Zheng, L., Tian, J., Tan, F., Chen, J., Deng, Y., Li, J., Cai, J., et al. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/9426368 · Cited by 8
“exposure to oxidative stress and activates the gene expression of many antioxidases and cytoprotective proteins, including GCL, HO-1, GPX, and NQO1 [28].”
Background
Design and evaluation of Nrf2 activators with 1,3,4-oxa/thiadiazole core as neuro-protective agents against oxidative stress in PC-12 cells
Lin, H., Qiao, Y., Yang, H., Li, Q., Chen, Y., Qu, W., Liu, W., Feng, F., & Sun, H. (2019) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2019.126853 · Cited by 8
Development of Keap1-interactive small molecules that regulate Nrf2 transcriptional activity
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“…the importance of HMOX2 in oxidative stress-related diseases, the activation of cytoprotective enzymes, including HMOX2, by the KEAP1-NRF2-ARE pathway highlights the potential of this pathway as a therapeutic target for oxidative stress-related chronic diseases, such as SMA (Magesh et al. 2012).”
Background
Focusing on Keap1, IKKβ, and Bcl2 proteins: predicted targets of stigmasterol in neurodegeneration
Soni, M., Kumar, A., Kumar, R., Dangi, M., Kumar, A., & Kumar, V. J. (2025) · Journal of Receptors and Signal Transduction · doi:10.1080/10799893.2025.2465243 · Cited by 7
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“[48] 2.2.”
Influential
CB5712809, a novel Keap1 inhibitor upregulates SQSTM1/p62 mediated Nrf2 activation to induce cell death in colon cancer cells
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Glycyrrhizin regulates antioxidation through Nrf2 signaling pathway in rat temporomandibular joint osteoarthritis
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Preclinical studies of natural flavonoids in inflammatory bowel disease based on macrophages: a systematic review with meta-analysis and network pharmacology
Shi, S., Jiang, H., Ma, W., Guan, Z., Han, M., Man, S., Wu, Z., & He, S. (2024) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-024-03501-0 · Cited by 7
“In addition, the downstream enzymes of Nrf2 also have the potential to inhibit the activation of NLRP3, such as NQO1, HO-1, Trx1, and SOD2 (Magesh et al. 2012).”

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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