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Mechanism of chemical activation of Nrf2
Yun Li1, Joseph D Paonessa, Yuesheng Zhang
1Department of Cancer Prevention and Control, Roswell Park Cancer Institute, Buffalo, New York, United States of America.
Abstract:
NF-E2 related factor-2 (Nrf2) promotes the transcription of many cytoprotective genes and is a major drug target for prevention of cancer and other diseases. Indeed, the cancer-preventive activities of several well-known chemical agents were shown to depend on Nrf2 activation. It is well known that chemopreventive Nrf2 activators stabilize Nrf2 by blocking its ubiquitination, but previous studies have indicated that this process occurs exclusively in the cytoplasm. Kelch-like ECH-associated protein 1 (Keap1) binds to Nrf2 and orchestrates Nrf2 ubiquitination, and it has been a widely-held view that inhibition of Nrf2 ubiquitination by chemopreventive agents results from the dissociation of Nrf2 from its repressor Keap1. Here, we show that while the activation of Nrf2 by prototypical chemical activators, including 5,6-dihydrocyclopenta-1,2-dithiole-3-thione (CPDT) and sulforaphane (SF), results solely from inhibition of its ubiquitination, such inhibition occurs predominantly in the nucleus. Moreover, the Nrf2 activators promote Nrf2 association with Keap1, rather than disassociation, which appears to result from inhibition of Nrf2 phosphorylation at Ser40. Available evidence suggests the Nrf2 activators may block Nrf2 ubiquitination by altering Keap1 conformation via reaction with the thiols of specific Keap1 cysteines. We further show that while the inhibitory effects of CPDT and SF on Nrf2 ubiquitination depend entirely on Keap1, Nrf2 is also degraded by a Keap1-independent mechanism. These findings provide significant new insight about Nrf2 activation and suggest that exogenous chemical activators of Nrf2 enter the nucleus to exert most of their inhibitory impact on Nrf2 ubiquitination and degradation.
Insights
Chemical activators stabilize NF-E2 related factor-2 (Nrf2) by inhibiting its ubiquitination in the nucleus, not the cytoplasm. This process involves Nrf2 association with Keap1, challenging previous understanding of Nrf2 activation.
Area of Science:
- Molecular Biology
- Cellular Biology
- Biochemistry
Background:
- NF-E2 related factor-2 (Nrf2) is a key transcription factor for cytoprotective genes and a significant drug target for cancer prevention.
- Nrf2 activators stabilize Nrf2 by blocking ubiquitination, a process previously thought to occur exclusively in the cytoplasm.
- Kelch-like ECH-associated protein 1 (Keap1) is the primary repressor of Nrf2, orchestrating its ubiquitination and degradation.
Purpose of the Study:
- To investigate the subcellular localization of Nrf2 ubiquitination inhibition by chemical activators.
- To elucidate the mechanism by which chemopreventive agents activate Nrf2.
- To challenge the established model of Nrf2 regulation by Keap1.
Main Methods:
- Treatment of cells with chemical Nrf2 activators like 5,6-dihydrocyclopenta-1,2-dithiole-3-thione (CPDT) and sulforaphane (SF).
- Analysis of Nrf2 ubiquitination status in cytoplasmic and nuclear fractions.
- Assessment of Nrf2-Keap1 association and Nrf2 phosphorylation.
- Investigating Keap1-dependent and independent Nrf2 degradation pathways.
Main Results:
- Nrf2 ubiquitination inhibition by CPDT and SF occurs predominantly in the nucleus, not the cytoplasm.
- Nrf2 activators promote Nrf2-Keap1 association, contrary to the dissociation hypothesis.
- Activation appears to result from inhibition of Nrf2 phosphorylation at Ser40, potentially via Keap1 cysteine modification.
- A Keap1-independent Nrf2 degradation pathway also exists.
Conclusions:
- Chemopreventive Nrf2 activators function primarily in the nucleus to inhibit Nrf2 ubiquitination and degradation.
- The mechanism involves enhanced Nrf2-Keap1 interaction and altered Keap1 conformation.
- These findings necessitate a revised understanding of Nrf2 regulation and therapeutic targeting.
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