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Originally published In Press as doi:10.1074/jbc.M300931200 on April 7, 2003

J. Biol. Chem., Vol. 278, Issue 24, 21592-21600, June 13, 2003
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Keap1-dependent Proteasomal Degradation of Transcription Factor Nrf2 Contributes to the Negative Regulation of Antioxidant Response Element-driven Gene Expression*

Michael McMahon {ddagger}, Ken Itoh §, Masayuki Yamamoto § and John D. Hayes

From the Biomedical Research Centre, Ninewells Hospital and Medical School, University of Dundee, Dundee DD1 9SY, Scotland, United Kingdom, § Centre for Tsukuba Advanced Research Alliance and Institute of Basic Medical Sciences, University of Tsukuba, Tsukuba 305-8577, Japan

Keap1 is a negative regulator of Nrf2, a bZIP transcription factor that mediates adaptation to oxidative stress. Previous studies suggested this negative regulation is a consequence of Keap1 controlling the subcellular distribution of Nrf2. We now report that Keap1 also controls the total cellular level of Nrf2 protein. In the RL34 non-transformed rat liver cell line, Nrf2 was found to accumulate rapidly in response to oxidative stress caused by treatment with sulforaphane, and the accumulation resulted from inhibition of proteasomal-mediated degradation of the bZIP protein. By heterologously expressing in COS1 cells epitope-tagged Nrf2 and an Nrf2{Delta}ETGE mutant lacking the Keap1-binding site, in both the presence and absence of Keap1 we demonstrate that Nrf2 is subject to ubiquitination and proteasomal degradation independently of both Keap1 and the redox environment of the cell. In oxidatively stressed cells, this is the sole mechanism responsible for Nrf2 degradation. However, under homeostatic conditions Nrf2 is subject to a substantially more rapid mode of proteasomal degradation than it is in oxidatively stressed cells, and this rapid turnover of Nrf2 requires it to interact with Keap1. Within Nrf2, the N-terminal Neh2 domain is identified as the redox-sensitive degron. These data suggest that Keap1 negatively regulates Nrf2 by both enhancing its rate of proteasomal degradation and altering its subcellular distribution.

Received for publication, January 28, 2003 , and in revised form, March 29, 2003.

* This work was funded by grants from the Association for International Cancer Research (99-041 and 02-049) (to M. Y. and J. D. H.). The TaqMan® analyses described herein were obtained with equipment provided by a Medical Research Council Cooperative Group Grant G0000281. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

{ddagger} To whom correspondence should be addressed: Biomedical Research Centre, Ninewells Hospital and Medical School, Dundee DD1 9SY, Scotland, UK. Tel.: 44-1382-660111; Fax: 44-1382-669993; E-mail: m.j.m.mcmahon{at}dundee.ac.uk.


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Distinct roles of c-Abl and Atm in oxidative stress response are mediated by protein kinase C {delta}
Genes & Dev., August 1, 2004; 18(15): 1824 - 1837.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. McMahon, N. Thomas, K. Itoh, M. Yamamoto, and J. D. Hayes
Redox-regulated Turnover of Nrf2 Is Determined by at Least Two Separate Protein Domains, the Redox-sensitive Neh2 Degron and the Redox-insensitive Neh6 Degron
J. Biol. Chem., July 23, 2004; 279(30): 31556 - 31567.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
Y. Zhang and G. B. Gordon
A strategy for cancer prevention: Stimulation of the Nrf2-ARE signaling pathway
Mol. Cancer Ther., July 1, 2004; 3(7): 885 - 893.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
G. Shen, V. Hebbar, S. Nair, C. Xu, W. Li, W. Lin, Y.-S. Keum, J. Han, M. A. Gallo, and A.-N. T. Kong
Regulation of Nrf2 Transactivation Domain Activity: THE DIFFERENTIAL EFFECTS OF MITOGEN-ACTIVATED PROTEIN KINASE CASCADES AND SYNERGISTIC STIMULATORY EFFECT OF Raf AND CREB-BINDING PROTEIN
J. Biol. Chem., May 28, 2004; 279(22): 23052 - 23060.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
H. Motohashi, F. Katsuoka, J. D. Engel, and M. Yamamoto
Small Maf proteins serve as transcriptional cofactors for keratinocyte differentiation in the Keap1-Nrf2 regulatory pathway
PNAS, April 27, 2004; 101(17): 6379 - 6384.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
D. Martin, A. I. Rojo, M. Salinas, R. Diaz, G. Gallardo, J. Alam, C. M. R. de Galarreta, and A. Cuadrado
Regulation of Heme Oxygenase-1 Expression through the Phosphatidylinositol 3-Kinase/Akt Pathway and the Nrf2 Transcription Factor in Response to the Antioxidant Phytochemical Carnosol
J. Biol. Chem., March 5, 2004; 279(10): 8919 - 8929.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
N. Wakabayashi, A. T. Dinkova-Kostova, W. D. Holtzclaw, M.-I. Kang, A. Kobayashi, M. Yamamoto, T. W. Kensler, and P. Talalay
Protection against electrophile and oxidant stress by induction of the phase 2 response: Fate of cysteines of the Keap1 sensor modified by inducers
PNAS, February 17, 2004; 101(7): 2040 - 2045.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
M.-I. Kang, A. Kobayashi, N. Wakabayashi, S.-G. Kim, and M. Yamamoto
Scaffolding of Keap1 to the actin cytoskeleton controls the function of Nrf2 as key regulator of cytoprotective phase 2 genes
PNAS, February 17, 2004; 101(7): 2046 - 2051.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
D. D. Zhang and M. Hannink
Distinct Cysteine Residues in Keap1 Are Required for Keap1-Dependent Ubiquitination of Nrf2 and for Stabilization of Nrf2 by Chemopreventive Agents and Oxidative Stress
Mol. Cell. Biol., November 15, 2003; 23(22): 8137 - 8151.
[Abstract] [Full Text] [PDF]

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 Mol. Pharmacol.Home page
I. R. Jowsey, Q. Jiang, K. Itoh, M. Yamamoto, and J. D. Hayes
Expression of the Aflatoxin B1-8,9-Epoxide-Metabolizing Murine Glutathione S-Transferase A3 Subunit Is Regulated by the Nrf2 Transcription Factor through an Antioxidant Response Element
Mol. Pharmacol., November 1, 2003; 64(5): 1018 - 1028.
[Abstract] [Full Text] [PDF]


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