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Am. J. Respir. Cell Mol. Biol., Volume 26, Number 2, February, 2002 175-182

Role of NRF2 in Protection Against Hyperoxic Lung Injury in Mice

Hye-Youn Cho, Anne E. Jedlicka, Sekhar P. M. Reddy, Thomas W. Kensler, Masayuki Yamamoto, Liu-Yi Zhang, and Steven R. Kleeberger

Department of Environmental Health Sciences, The Bloomberg School of Hygiene and Public Health, Johns Hopkins University, Baltimore, Maryland; and Institute of Basic Medical Sciences and Center for Tsukuba Advanced Research Alliance, University of Tsukuba Tennoudai, Tsukuba, Japan

NRF2 is a transcription factor important in the protection against carcinogenesis and oxidative stress through antioxidant response element (ARE)-mediated transcriptional activation of several phase 2 detoxifying and antioxidant enzymes. This study was designed to determine the role of NRF2 in the pathogenesis of hyperoxic lung injury by comparing pulmonary responses to 95-98% oxygen between mice with site-directed mutation of the gene for NRF2 (Nrf2-/-) and wild-type mice (Nrf2+/+). Pulmonary hyperpermeability, macrophage inflammation, and epithelial injury in Nrf2-/- mice were 7.6-fold, 47%, and 43% greater, respectively, compared with Nrf2+/+ mice after 72 h hyperoxia exposure. Hyperoxia markedly elevated the expression of NRF2 mRNA and DNA-binding activity of NRF2 in the lungs of Nrf2+/+ mice. mRNA expression for ARE- responsive lung antioxidant and phase 2 enzymes was evaluated in both genotypes of mice to identify potential downstream molecular mechanisms of NRF2 in hyperoxic lung responses. Hyperoxia-induced mRNA levels of NAD(P)H:quinone oxidoreductase 1 (NQO1), glutathione-S-transferase (GST)-Ya and -Yc subunits, UDP glycosyl transferase (UGT), glutathione peroxidase-2 (GPx2), and heme oxygenase-1 (HO-1) were significantly lower in Nrf2-/- mice compared with Nrf2+/+ mice. Consistent with differential mRNA expression, NQO1 and total GST activities were significantly lower in Nrf2-/- mice compared with Nrf2+/+ mice after hyperoxia. Results demonstrated that NRF2 has a significant protective role against pulmonary hyperoxic injury in mice, possibly through transcriptional activation of lung antioxidant defense enzymes.

Abbreviations: antioxidant response element, ARE; bronchoalveolar lavage fluid, BALF; butylated hydroxyanisole, BHA; butylated hydroxytoluene, BHT; 1-chloro 2,4-dinitrobenzene, CDNB; alpha -dithiothreitol, DTT; ethylenediaminetetraacetic acid, EDTA; electrophoretic mobility shift assay, EMSA; flavine adenine dinucleotide, FAD; gamma -glutamate cystein ligase regulatory subunit, GCLS; glutathione peroxidase, GPx; glutathione reductase, GR; glutathione-S-transferase, GST; N-[2-hydroxyethyl]piperazine-N'-[2-ethanesulfonic acid, HEPES; tris buffered EDTA, TBE; heme oxygenase-1, HO-1; 3-(N-morpholino)propanesulfonic, MOPS; nicotinamide adenine dinucleotide, reduced form, NADH; nuclear factor, erythroid 2, NF-E2; NAD(P)H:quinone oxidoreductase 1, NQO1; NF-E2-related factor 2, NRF2; ICR/Sv129 mice, Nrf2+/+; ICR/Sv129 mice with site-directed mutation in Nrf2, Nrf2-/-; polymorphonuclear leukocyte, PMN; phenylmethanesulfonyl fluoride, PMSF; polydeoxyinosinic-deoxycytidylic acid, polydI-dC; reactive oxygen species, ROS; reverse transcriptase polymerase chain reaction, RT-PCR; standard error of the mean, SEM; superoxide dismutase, SOD; UDP glycosyl transferase, UGT.




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[Abstract] [Full Text] [PDF]

Home page
 J. Biol. Chem.Home page
S. Papaiahgari, S. R. Kleeberger, H.-Y. Cho, D. V. Kalvakolanu, and S. P. Reddy
NADPH Oxidase and ERK Signaling Regulates Hyperoxia-induced Nrf2-ARE Transcriptional Response in Pulmonary Epithelial Cells
J. Biol. Chem., October 1, 2004; 279(40): 42302 - 42312.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
K. Iida, K. Itoh, Y. Kumagai, R. Oyasu, K. Hattori, K. Kawai, T. Shimazui, H. Akaza, and M. Yamamoto
Nrf2 Is Essential for the Chemopreventive Efficacy of Oltipraz against Urinary Bladder Carcinogenesis
Cancer Res., September 15, 2004; 64(18): 6424 - 6431.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
N. Li, J. Alam, M. I. Venkatesan, A. Eiguren-Fernandez, D. Schmitz, E. Di Stefano, N. Slaughter, E. Killeen, X. Wang, A. Huang, et al.
Nrf2 Is a Key Transcription Factor That Regulates Antioxidant Defense in Macrophages and Epithelial Cells: Protecting against the Proinflammatory and Oxidizing Effects of Diesel Exhaust Chemicals
J. Immunol., September 1, 2004; 173(5): 3467 - 3481.
[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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 Proc. Natl. Acad. Sci. USAHome page
X. Gao and P. Talalay
Induction of phase 2 genes by sulforaphane protects retinal pigment epithelial cells against photooxidative damage
PNAS, July 13, 2004; 101(28): 10446 - 10451.
[Abstract] [Full Text] [PDF]

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 GENES CELLSHome page
T. Yanagawa, K. Itoh, J. Uwayama, Y. Shibata, A. Yamaguchi, T. Sano, T. Ishii, H. Yoshida, and M. Yamamoto
Nrf2 deficiency causes tooth decolourization due to iron transport disorder in enamel organ
Genes Cells, July 1, 2004; 9(7): 641 - 651.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
J.-M. Lee, K. Chan, Y. W. Kan, and J. A. Johnson
Targeted disruption of Nrf2 causes regenerative immune-mediated hemolytic anemia
PNAS, June 29, 2004; 101(26): 9751 - 9756.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
A. Derjuga, T. S. Gourley, T. M. Holm, H. H. Q. Heng, R. A. Shivdasani, R. Ahmed, N. C. Andrews, and V. Blank
Complexity of CNC Transcription Factors As Revealed by Gene Targeting of the Nrf3 Locus
Mol. Cell. Biol., April 15, 2004; 24(8): 3286 - 3294.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
J. P. Russell, J. B. Engiles, and J. L. Rothstein
Proinflammatory Mediators and Genetic Background in Oncogene Mediated Tumor Progression
J. Immunol., April 1, 2004; 172(7): 4059 - 4067.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
T. Ishii, K. Itoh, E. Ruiz, D. S. Leake, H. Unoki, M. Yamamoto, and G. E. Mann
Role of Nrf2 in the Regulation of CD36 and Stress Protein Expression in Murine Macrophages: Activation by Oxidatively Modified LDL and 4-Hydroxynonenal
Circ. Res., March 19, 2004; 94(5): 609 - 616.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Renal Physiol.Home page
E. M. Sikorski, T. Hock, N. Hill-Kapturczak, and A. Agarwal
The story so far: molecular regulation of the heme oxygenase-1 gene in renal injury
Am J Physiol Renal Physiol, March 1, 2004; 286(3): F425 - F441.
[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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 CarcinogenesisHome page
S. Gebel, B. Gerstmayer, A. Bosio, H.-J. Haussmann, E. V. Miert, and T. Muller
Gene expression profiling in respiratory tissues from rats exposed to mainstream cigarette smoke
Carcinogenesis, February 1, 2004; 25(2): 169 - 178.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
K. Itoh, M. Mochizuki, Y. Ishii, T. Ishii, T. Shibata, Y. Kawamoto, V. Kelly, K. Sekizawa, K. Uchida, and M. Yamamoto
Transcription Factor Nrf2 Regulates Inflammation by Mediating the Effect of 15-Deoxy-{Delta}12,14-Prostaglandin J2
Mol. Cell. Biol., January 1, 2004; 24(1): 36 - 45.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
L. Leung, M. Kwong, S. Hou, C. Lee, and J. Y. Chan
Deficiency of the Nrf1 and Nrf2 Transcription Factors Results in Early Embryonic Lethality and Severe Oxidative Stress
J. Biol. Chem., November 28, 2003; 278(48): 48021 - 48029.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J.-M. Lee, A. Y. Shih, T. H. Murphy, and J. A. Johnson
NF-E2-related Factor-2 Mediates Neuroprotection against Mitochondrial Complex I Inhibitors and Increased Concentrations of Intracellular Calcium in Primary Cortical Neurons
J. Biol. Chem., September 26, 2003; 278(39): 37948 - 37956.
[Abstract] [Full Text] [PDF]

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 Mol. Interv.Home page
C. J. Henderson and C. R. Wolf
Transgenic Analysis of Human Drug-Metabolizing Enzymes: Preclinical Drug Development and Toxicology
Mol. Interv., September 1, 2003; 3(6): 331 - 343.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Cell Mol. Bio.Home page
N. R. Hackett, A. Heguy, B.-G. Harvey, T. P. O'Connor, K. Luettich, D. B. Flieder, R. Kaplan, and R. G. Crystal
Variability of Antioxidant-Related Gene Expression in the Airway Epithelium of Cigarette Smokers
Am. J. Respir. Cell Mol. Biol., September 1, 2003; 29(3): 331 - 343.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
A. Baulig, M. Garlatti, V. Bonvallot, A. Marchand, R. Barouki, F. Marano, and A. Baeza-Squiban
Involvement of reactive oxygen species in the metabolic pathways triggered by diesel exhaust particles in human airway epithelial cells
Am J Physiol Lung Cell Mol Physiol, September 1, 2003; 285(3): L671 - L679.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Cell Mol. Bio.Home page
S. Perkowski, J. Sun, S. Singhal, J. Santiago, G. D. Leikauf, and S. M. Albelda
Gene Expression Profiling of the Early Pulmonary Response to Hyperoxia in Mice
Am. J. Respir. Cell Mol. Biol., June 1, 2003; 28(6): 682 - 696.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
A. Y. Shih, D. A. Johnson, G. Wong, A. D. Kraft, L. Jiang, H. Erb, J. A. Johnson, and T. H. Murphy
Coordinate Regulation of Glutathione Biosynthesis and Release by Nrf2-Expressing Glia Potently Protects Neurons from Oxidative Stress
J. Neurosci., April 15, 2003; 23(8): 3394 - 3406.
[Abstract] [Full Text] [PDF]

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 CarcinogenesisHome page
M. Ramos-Gomez, P. M. Dolan, K. Itoh, M. Yamamoto, and T. W. Kensler
Interactive effects of nrf2 genotype and oltipraz on benzo[a]pyrene-DNA adducts and tumor yield in mice
Carcinogenesis, March 1, 2003; 24(3): 461 - 467.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
Y.-S. Ho
Transgenic and Knockout Models for Studying the Role of Lung Antioxidant Enzymes in Defense against Hyperoxia
Am. J. Respir. Crit. Care Med., December 15, 2002; 166(12): S51 - 56.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
S. P. M. Reddy and B. T. Mossman
Role and regulation of activator protein-1 in toxicant-induced responses of the lung
Am J Physiol Lung Cell Mol Physiol, December 1, 2002; 283(6): L1161 - L1178.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
L. M. Zipper and R. T. Mulcahy
The Keap1 BTB/POZ Dimerization Function Is Required to Sequester Nrf2 in Cytoplasm
J. Biol. Chem., September 20, 2002; 277(39): 36544 - 36552.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
A. T. Dinkova-Kostova, W. D. Holtzclaw, R. N. Cole, K. Itoh, N. Wakabayashi, Y. Katoh, M. Yamamoto, and P. Talalay
Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants
PNAS, September 3, 2002; 99(18): 11908 - 11913.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
M.-K. Kwak, K. Itoh, M. Yamamoto, and T. W. Kensler
Enhanced Expression of the Transcription Factor Nrf2 by Cancer Chemopreventive Agents: Role of Antioxidant Response Element-Like Sequences in the nrf2 Promoter
Mol. Cell. Biol., May 1, 2002; 22(9): 2883 - 2892.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Cell Mol. Bio.Home page
L. E. Otterbein and A. M. K. Choi
The Saga of Leucine Zippers Continues . In Response to Oxidative Stress
Am. J. Respir. Cell Mol. Biol., February 1, 2002; 26(2): 161 - 163.
[Full Text] [PDF]


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