When NRF2 talks, who's listening?

Antioxidants and Redox Signaling

Volumn 13, Issue 11, 2010, Pages 1649-1663

  Wakabayashi, Nobunao ^a,b   Slocum, Stephen L ^c   Skoko, John J ^d   Shin, Soona ^d   Kensler, Thomas W ^a,b,c,d  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NOTCH1 RECEPTOR; TRANSCRIPTION FACTOR NRF2; UBIQUITIN PROTEIN LIGASE E3;

CELL FATE; CELL SURVIVAL; HUMAN; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL SURVIVAL; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, KNOCKOUT; NEOPLASMS; NF-E2-RELATED FACTOR 2; NF-KAPPA B; RECEPTOR, NOTCH1; RECEPTORS, ARYL HYDROCARBON; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA;

EID: 77956915802     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2010.3216     Document Type: Review

References (168)

1. Ahmad R, Raina D, Meyer C, Kharbanda S, and Kufe D. Triterpenoid CDDO-Me blocks the NF-kappaB pathway by direct inhibition of IKKbeta on Cys-179. J Biol Chem 281: 35764-35769, 2006.
2. Ahn KS and Aggarwal BB. Transcription factor NF-kappaB: a sensor for smoke and stress signals. Ann N Y Acad Sci 1056: 218-2133, 2005.
3. Alam J, Stewart D, Touchard C, Boinapally S, Choi AM, and Cook JL. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 274: 26071-26078, 1999.
4. Albakri QA and Stuehr DJ. Intracellular assembly of in-ducible NO synthase is limited by nitric oxide-mediated changes in heme insertion and availability. J Biol Chem 271: 5414-5421, 1996.
5. Alexander DL, Ganem LG, Fernandez-Salguero P, Gonza-lez F, and Jefcoate CR. Aryl-hydrocarbon receptor is an inhibitory regulator of lipid synthesis and of commitment to adipogenesis. J Cell Sci 111: 3311-3322, 1998.
6. Ansell PJ, Lo SC, Newton LG, Espinosa-Nicholas C, Zhang DD, Liu JH, Hannink M, and Lubahn DB. Repression of cancer protective genes by 17beta-estradiol: ligand-dependent interaction between human Nrf2 and estrogen receptor alpha. Mol Cell Endocrinol 243: 27-34, 2005.
7. Anwar AA, Li FY, Leake DS, Ishii T, Mann GE, and Siow RC. Induction of heme oxygenase 1 by moderately oxi-dized low-density lipoproteins in human vascular smooth muscle cells: role of mitogen-activated protein kinases and Nrf2. Free Radic Biol Med 39: 227-236, 2005.
8. Arinze IJ and Kawai Y. Transcriptional activation of the human Galphai2 gene promoter through nuclear factor-kappaB and antioxidant response elements. J Biol Chem 280: 9786-9795, 2005.
9. Banning A, Brigelius-Flohe R. NF-kappaB, Nrf2, and HO-1 interplay in redox-regulated VCAM-1 expression. Antioxid Redox Signal 7: 889-899, 2005.
10. Bensaad K, Tsuruta A, Selak MA, Vidal MN, Nakano K, Bartrons R, Gottlieb E, Vousden KH. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 126: 107-120, 2006.
11. Beyer TA, Xu W, Teupser D, Aufdem Keller U, Bugnon P, Hildt E, Thiery J, Kan YW, and Werner S. Impaired liver regeneration in Nrf2 knockout mice: role of ROS-mediated insulin/IGF-1 resistance. EMBO J 27: 212-223, 2008.
12. Braun S, Hanselmann C, Gassmann MG, Aufdem Keller U, Born-Berclaz C, Chan K, Kan YW, and Werner S. Nrf2 transcription factor, a novel target of keratinocyte growth factor action which regulates gene expression and inflam-mation in the healing skin wound. Mol Cell Biol 22: 5492-5505, 2002.
13. Brown SL, Sekhar KR, Rachakonda G, Sasi S, and Freeman ML. Activating transcription factor 3 is a novel repressor of the nuclear factor erythroid-derived 2-related factor 2 (Nrf2)-regulated stress pathway. Cancer Res 68: 364-368, 2008.
14. Canalis E. Notch signaling in osteoblasts. Sci Signal 1: pe17, 2008.
15. Cao S, Zhang X, Edwards JP, and Mosser DM. NF-kappaB1 (p50) homodimers differentially regulate pro-and anti-inflammatory cytokines in macrophages. J Biol Chem 281: 26041-26050, 2006.
16. Carayol N, Chen J, Yang F, Jin T, Jin L, States D, and Wang CY. A dominant function of IKK/NF-kappaB signaling in global lipopolysaccharide- induced gene expression. J Biol Chem 281: 31142-31151, 2006.
17. Carlson EA, McCulloch C, Koganti A, Goodwin SB, Sutter TR, and Silkworth JB. Divergent transcriptomic responses to aryl hydrocarbon receptor agonists between rat and human primary hepatocytes. Toxicol Sci 112: 257-272, 2009.
18. Carvajal-Gonzalez JM, Roman AC, Cerezo-Guisado MI, Rico-Leo EM, Martin-Partido G, and Fernandez-Salguero PM. Loss of dioxin-receptor expression accelerates wound healing in vivo by a mechanism involving TGFbeta. J Cell Sci 122: 1823-1833, 2009.
19. Chen W, Sun Z, Wang XJ, Jiang T, Huang Z, Fang D, and Zhang DD. Direct interaction between Nrf2 and p21(Cip1/WAF1) upregulates the Nrf2-mediated antioxi-dant response. Mol Cell 34: 663-673, 2009.
20. Chen XL, Dodd G, Thomas S, Zhang X, Wasserman MA, Rovin BH, and Kunsch C. Activation of Nrf2/ARE path-way protects endothelial cells from oxidant injury and in-hibits inflammatory gene expression. Am J Physiol Heart Circ Physiol 290: H1862-H1870, 2006.
21. Chen XL, Varner SE, Rao AS, Grey JY, Thomas S, Cook CK, Wasserman MA, Medford RM, Jaiswal AK, and Kunsch C. Laminar flow induction of antioxidant response element-mediated genes in endothelial cells: a novel anti-inflammatory mechanism. J Biol Chem 278: 703-711, 2003.
22. Chen ZJ, Parent L, and Maniatis T. Site-specific phosphor-ylation of IkappaBalpha by a novel ubiquitination-dependent protein kinase activity. Cell 84: 853-862, 1996.
23. Cho HY, Imani F, Miller-DeGraff L, Walters D, Melendi GA, Yamamoto M, Polack FP, and Kleeberger SR. Antiviral activity of Nrf2 in a murine model of respiratory syncytial virus disease. AmJRespir Crit Care Med 179: 138-150, 2009.
24. Chuang HC, Chang CW, Chang GD, Yao TP, and Chen H. Histone deacetylase 3 binds to and regulates the GCMa transcription factor. Nucleic Acids Res 34: 1459-1469, 2006.
25. Cousins DJ, McDonald J, and Lee TH. Therapeutic ap-proaches for control of transcription factors in allergic dis-ease. JAllergy Clin Immunol 121:803-809; quiz 810-811,2008.
26. Das KC. c-Jun NH2-terminal kinase-mediated redox-dependent degradation of IkappaB: role of thioredoxin in NF-kappaB activation. J Biol Chem 276: 4662-4670, 2001.
27. de la Pompa JL, Wakeham A, Correia KM, Samper E, Brown S, Aguilera RJ, Nakano T, Honjo T, Mak TW, Ros-sant J, and Conlon RA. Conservation of the Notch signal-ling pathway in mammalian neurogenesis. Development 124: 1139-1148, 1997.
28. DiDonato JA, Hayakawa M, Rothwarf DM, Zandi E, and Karin M. A cytokine-responsive IkappaB kinase that acti-vates the transcription factor NF-kappaB. Nature 388: 548-554, 1997.
29. Dotto GP. p21(WAF1/Cip1): more than a break to the cell cycle? Biochim Biophys Acta 1471: M43-M56, 2000.
30. el-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, Lin D, Mercer WE, Kinzler KW, and Vogelstein B. WAF1, a potential mediator of p53 tumor suppression. Cell 75: 817-825, 1993.
31. Esposito F, Cuccovillo F, Russo L, Casella F, Russo T, and Cimino F. A new p21waf1/cip1 isoform is an early event of cell response to oxidative stress. Cell Death Differ 5: 940-945, 1998.
32. Fan Y, Boivin GP, Knudsen ES, Nebert DW, Xia Y, and Puga A. The aryl hydrocarbon receptor functions as a tumor suppressor of liver carcinogenesis. Cancer Res 70: 212-222, 2010.
33. Faraonio R, Vergara P, Di Marzo D, Pierantoni MG, Na-politano M, Russo T, and Cimino F. p53 suppresses the Nrf2-dependent transcription of antioxidant response genes. J Biol Chem 281: 39776-39784, 2006.
34. Foresti R, Clark JE, Green CJ, and Motterlini R. Thiol compounds interact with nitric oxide in regulating heme oxygenase-1 induction in endothelial cells. Involvement of superoxide and peroxynitrite anions. J Biol Chem 272: 18411-18417, 1997.
35. Fre S, Huyghe M, Mourikis P, Robine S, Louvard D, and Artavanis-Tsakonas S. Notch signals control the fate of immature progenitor cells in the intestine. Nature 435: 964-968, 2005. (Pubitemid 40896323)
36. Freemerman AJ, Gallegos A, and Powis G. Nuclear factor kappaB transactivation is increased but is not involved in the proliferative effects of thioredoxin overexpression in MCF-7 breast cancer cells. Cancer Res 59: 4090-4094, 1999.
37. Garg V, Muth AN, Ransom JF, Schluterman MK, Barnes R, King IN, Grossfeld PD, and Srivastava D. Mutations in NOTCH1 cause aortic valve disease. Nature 437: 270-274, 2005.
38. Gartel AL and Tyner AL. The role of the cyclin-dependent kinase inhibitor p21 in apoptosis. Mol Cancer Ther 1: 639-649, 2002.
39. Gatz SA and Wiesmuller L. p53 in recombination and re-pair. Cell Death Differ 13: 1003-1016, 2006.
40. Gil A, Maria Aguilera C, Gil-Campos M, and Canete R. Altered signalling and gene expression associated with the immune system and the inflammatory response in obesity. Br J Nutr 98(suppl 1): S121-S126, 2007.
41. Gilmore T, Gapuzan ME, Kalaitzidis D, and Starczynowski D. Rel/NF-kappa B/I kappa B signal transduction in the generation and treatment of human cancer. Cancer Lett 181: 1-9, 2002.
42. Go YM, Gipp JJ, Mulcahy RT, and Jones DP. H2O2-dependent activation of GCLC-ARE4 reporter occurs by mitogen-activated protein kinase pathways without oxi-dation of cellular glutathione or thioredoxin-1. J Biol Chem 279: 5837-5845, 2004.
43. Green DR and Kroemer G. Cytoplasmic functions of the tumour suppressor p53. Nature 458: 1127-1130, 2009.
44. Gu YZ, Hogenesch JB, and Bradfield CA. The PAS super-family: sensors of environmental and developmental sig-nals. Annu Rev Pharmacol Toxicol 40: 519-561, 2000.
45. Harper JW, Adami GR, Wei N, Keyomarsi K, and Elledge SJ. The p21 Cdk-interacting protein Cip1 is a potent inhib-itor of G1 cyclin-dependent kinases. Cell 75: 805-816, 1993.
46. Hayashi T and Faustman D. Defective function of the proteasome in autoimmunity: involvement of impaired NF-kappaB activation. Diabetes Technol Ther 2: 415-428, 2000.
47. Hayashi T, Ueno Y, and Okamoto T. Oxidoreductive reg-ulation of nuclear factor kappa B. Involvement of a cellular reducing catalyst thioredoxin.JBiol Chem 268:11380-11388, 1993.
48. Hayes JD and McMahon M. NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer. Trends Biochem Sci 34: 176-188, 2009.
49. Healy ZR, Lee NH, Gao X, Goldring MB, Talalay P, Kensler TW, and Konstantopoulos K. Divergent responses of chondrocytes and endothelial cells to shear stress: cross-talk among COX-2, the phase 2 response, and apoptosis. Proc Natl Acad Sci USA 102: 14010-14015, 2005.
50. Heiss E, Herhaus C, Klimo K, Bartsch H, and Gerhauser C. Nuclear factor kappa B is a molecular target for sulfor-aphane-mediated anti-inflammatory mechanisms. J Biol Chem 276: 32008-32015, 2001.
51. Herrmann O, Baumann B, de Lorenzi R, Muhammad S, Zhang W, Kleesiek J, Malfertheiner M, Kohrmann M, Po-trovita I, Maegele I, Beyer C, Burke JR, Hasan MT, Bujard H, Wirth T, Pasparakis M, and Schwaninger M. IKK me-diates ischemia-induced neuronal death. Nat Med 11: 1322-1329, 2005.
52. Hinoi E, Fujimori S, Wang L, Hojo H, Uno K, and Yoneda Y. Nrf2 negatively regulates osteoblast differentiation via interfering with Runx2-dependent transcriptional activa-tion. J Biol Chem 281: 18015-18024, 2006.
53. Hinoi E, Takarada T, Fujimori S, Wang L, Iemata M, Uno K, and Yoneda Y. Nuclear factor E2 p45-related factor 2 negatively regulates chondrogenesis. Bone 40: 337-344, 2007.
54. Hirota K, Murata M, Sachi Y, Nakamura H, Takeuchi J, Mori K, and Yodoi J. Distinct roles of thioredoxin in the cytoplasm and in the nucleus: a two-step mechanism of redox regulation of transcription factor NF-kappaB. J Biol Chem 274: 27891-27897, 1999.
55. Hollstein M, Sidransky D, Vogelstein B, and Harris CC. p53 mutations in human cancers. Science 253: 49-53, 1991.
56. Hosoya T, Maruyama A, Kang MI, Kawatani Y, Shibata T, Uchida K, Warabi E, Noguchi N, Itoh K, and Yamamoto M. Differential responses of the Nrf2-Keap1 system to laminar and oscillatory shear stresses in endothelial cells. J Biol Chem 280: 27244-27250, 2005.
57. Huppert SS, Le A, Schroeter EH, Mumm JS, Saxena MT, Milner LA, and Kopan R. Embryonic lethality in mice homozygous for a processing-deficient allele of Notch1. Nature 405: 966-970, 2000.
58. Iida K, Itoh K, Maher JM, Kumagai Y, Oyasu R, Mori Y, Shimazui T, Akaza H, and Yamamoto M. Nrf2 and p53 cooperatively protect against BBN-induced urinary bladder carcinogenesis. Carcinogenesis 28: 2398-2403, 2007.
59. Ikeda Y, Sugawara A, Taniyama Y, Uruno A, Igarashi K, Arima S, and Ito S, Takeuchi K. Suppression of rat throm-boxane synthase gene transcription by peroxisome pro-liferator-activated receptor gamma in macrophages via an interaction with NRF2. J Biol Chem 275: 33142-33150, 2000.
60. Immenschuh S, Tan M, and Ramadori G. Nitric oxide mediates the lipopolysaccharide dependent regulation of the heme oxygenase-1 gene expression in cultured rat Kupffer cells. J Hepatol 30: 61-69, 1999.
61. Iskander K, Li J, Han S, Zheng B, and Jaiswal AK. NQO1 and NQO2 regulation of humoral immunity and autoim-munity. J Biol Chem 281: 30917-30924, 2006.
62. Iso T, Kedes L, and Hamamori Y. HES and HERP families: multiple effectors of the Notch signaling pathway. J Cell Physiol 194: 237-255, 2003.
63. Itoh K, Mochizuki M, Ishii Y, Ishii T, Shibata T, Kawamoto Y, Kelly V, Sekizawa K, Uchida K, and Yamamoto M. Transcription factor Nrf2 regulates inflammation by me-diating the effect of 15-deoxy-Delta(12,14)-prostaglandin j(2). Mol Cell Biol 24: 36-45, 2004.
64. Jensen CH, Jauho EI, Santoni-Rugiu E, Holmskov U, Teis-ner B, Tygstrup N, and Bisgaard HC. Transit-amplifying ductular (oval) cells and their hepatocytic progeny are characterized by a novel and distinctive expression of delta-like protein/preadipocyte factor 1/fetal antigen 1. Am J Pathol 164: 1347-1359, 2004.
65. Jin W, Zhu L, Guan Q, Chen G, Wang QF, Yin HX, Hang CH, Shi JX, and Wang HD. Influence of Nrf2 genotype on pulmonary NF-kappaB activity and inflammatory response after traumatic brain injury. Ann Clin Lab Sci 38: 221-227, 2008.
66. Jun CD, Kim Y, Choi EY, Kim M, Park B, Youn B, Yu K, Choi KS, Yoon KH, Choi SC, Lee MS, Park KI, Choi M, Chung Y, and Oh J. Gliotoxin reduces the severity of tri-nitrobenzene sulfonic acid-induced colitis in mice: evidence of the connection between heme oxygenase-1 and the nuclear factor-kappaB pathway in vitro and in vivo. In-flamm Bowel Dis 12: 619-629, 2006.
67. Kageyama R, Ohtsuka T, and Tomita K. The bHLH gene Hes1 regulates differentiation of multiple cell types. Mol Cells 10: 1-7, 2000.
68. Kanninen K, Heikkinen R, Malm T, Rolova T, Kuhmonen S, Leinonen H, Yla-Herttuala S, Tanila H, Levonen AL, Koistinaho M, and Koistinaho J. Intrahippocampal injection of a lentiviral vector expressing Nrf2 improves spatial learning in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 106: 16505-10510, 2009.
69. Karuri AR, Huang Y, Bodreddigari S, Sutter CH, Roebuck BD, Kensler TW, and Sutter TR. 3H-1,2-dithiole-3-thione targets nuclear factor kappaB to block expression of in-ducible nitric-oxide synthase, prevents hypotension, and improves survival in endotoxemic rats. J Pharmacol Exp Ther 317: 61-67, 2006.
70. Katoh M and Katoh M. Notch signaling in gastrointestinal tract (review). Int J Oncol 30: 247-251, 2007.
71. Kaur H, Hughes MN, Green CJ, Naughton P, Foresti R, and Motterlini R. Interaction of bilirubin and biliverdin with reactive nitrogen species. FEBS Lett 543: 113-119, 2003.
72. Kawajiri K, Kobayashi Y, Ohtake F, Ikuta T, Matsush-ima Y, Mimura J, Pettersson S, Pollenz RS, Sakaki T, Hirokawa T, Akiyama T, Kurosumi M, Poellinger L, Kato S, and Fujii-Kuriyama Y. Aryl hydrocarbon re-ceptor suppresses intestinal carcinogenesis in ApcMin/+ mice with natural ligands. Proc Natl Acad Sci USA 106: 13481-13486, 2009.
73. Kensler TW, Wakabayashi N, and Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47: 89-116, 2007.
74. Kim YC, Masutani H, Yamaguchi Y, Itoh K, Yamamoto M, and Yodoi J. Hemin-induced activation of the thioredoxin gene by Nrf 2: a differential regulation of the antioxidant responsive element by a switch of its binding factors. J Biol Chem 276: 18399-18406, 2001.
75. Kimura A, Naka T, Nakahama T, Chinen I, Masuda K, Nohara K, Fujii-Kuriyama Y, and Kishimoto T. Aryl hy-drocarbon receptor in combination with Stat1 regulates LPS-induced inflammatory responses. J Exp Med 206: 2027-2035, 2009.
76. Kimura T, Kawasaki Y, Okumura F, Sone T, Natsuki R, and Isobe M. Ethanol-induced expression of glutamate-cysteine ligase catalytic subunit gene is mediated by NF-kappaB. Toxicol Lett 185: 110-115, 2009.
77. Knorr-Wittmann C, Hengstermann A, Gebel S, Alam J, and Muller T. Characterization of Nrf2 activation and heme oxygenase-1 expression in NIH3T3 cells exposed to aque-ous extracts of cigarette smoke. Free Radic Biol Med 39: 1438-1448, 2005.
78. Kobayashi A, Kang MI, Okawa H, Ohtsuji M, Zenke Y, Chiba T, Igarashi K, and Yamamoto M. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol Cell Biol 24: 7130-7139, 2004.
79. Kohle C and Bock KW. Coordinate regulation of Phase I and II xenobiotic metabolisms by the Ah receptor and Nrf2. Biochem Pharmacol 73: 1853-1862, 2007.
80. Kohler C, Bell AW, Bowen WC, Monga SP, Fleig W, and Michalopoulos GK. Expression of Notch-1 and its ligand Jagged-1 in rat liver during liver regeneration. Hepatology 39: 1056-1065, 2004.
81. Kong AN, Owuor E, Yu R, Hebbar V, Chen C, Hu R, and Mandlekar S. Induction of xenobiotic enzymes by the MAP kinase pathway and the antioxidant or electrophile re-sponse element (ARE/EpRE). Drug Metab Rev 33: 255-271, 2001.
82. Kunsch C and Rosen CA. NF-kappa B subunit-specific regulation of the interleukin-8 promoter. Mol Cell Biol 13: 6137-6146, 1993.
83. Kwak MK, Itoh K, Yamamoto M, and Kensler TW. En-hanced expression of the transcription factor Nrf2 by cancer chemopreventive agents: role of antioxidant response ele-ment-like sequences in the nrf2 promoter. Mol Cell Biol 22: 2883-2892, 2002.
84. Kwak MK, Wakabayashi N, Greenlaw JL, Yamamoto M, and Kensler TW. Antioxidants enhance mammalian pro-teasome expression through the Keap1-Nrf2 signaling pathway. Mol Cell Biol 23: 8786-8794, 2003.
85. Kwak MK, Wakabayashi N, Itoh K, Motohashi H, Yama-moto M, Kensler TW. Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway: identification of novel gene clusters for cell survival. J Biol Chem 278: 8135-8145, 2003.
86. Lavrovsky Y, Schwartzman ML, Levere RD, Kappas A, and Abraham NG. Identification of binding sites for transcrip-tion factors NF-kappa B and AP-2 in the promoter region of the human heme oxygenase 1 gene. Proc Natl Acad SciUS A 91: 5987-5991, 1994.
87. Lee TS and Chau LY. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med 8: 240-246, 2002.
88. Lernbecher T, Muller U, and Wirth T. Distinct NF-kappa B/Rel transcription factors are responsible for tissue-specific and inducible gene activation. Nature 365: 767-770,1993.
89. Letai AG. Diagnosing and exploiting cancer's addiction to blocks in apoptosis. Nat Rev Cancer 8: 121-132, 2008.
90. Levonen AL, Inkala M, Heikura T, Jauhiainen S, Jyrkkanen HK, Kansanen E, Maatta K, Romppanen E, Turunen P, Rutanen J, and Yla-Herttuala S. Nrf2 gene transfer induces antioxidant enzymes and suppresses smooth muscle cell growth in vitro and reduces oxidative stress in rabbit aorta in vivo. Arterioscler Thromb Vasc Biol 27: 741-747, 2007.
91. Lin R, Gewert D, and Hiscott J. Differential transcriptional activation in vitro by NF-kappa B/Rel proteins. J Biol Chem 270: 3123-3131, 1995.
92. Linzer DI and Levine AJ. Characterization of a 54K dalton cellular SV40 tumor antigen present in SV40-transformed cells and uninfected embryonal carcinoma cells. Cell 17:43-52,1979.
93. Liu GH, Qu J, and Shen X. NF-kappaB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and fa-cilitating recruitment of HDAC3 to MafK. Biochim Biophys Acta 1783: 713-727, 2008.
94. Liu YC, Hsieh CW, Wu CC, and Wung BS. Chalcone inhibits the activation of NF-kappaB and STAT3 in endo-thelial cells via endogenous electrophile. Life Sci 80: 1420-1430, 2007.
95. Ma Q, Kinneer K, Bi Y, Chan JY, and Kan YW. Induction of murine NAD(P)H:quinone oxidoreductase by 2,3,7,8-tetra-chlorodibenzo-p-dioxin requires the CNC (cap 'n' collar) basic leucine zipper transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2): cross-interaction between AhR (aryl hydrocarbon receptor) and Nrf2 signal transduction. Biochem J 377: 205-213, 2004.
96. Matthews JR, Wakasugi N, Virelizier JL, Yodoi J, and Hay RT. Thioredoxin regulates the DNA binding activity of NF-kappa B by reduction of a disulphide bond involving cys-teine 62. Nucleic Acids Res 20: 3821-3830, 1992.
97. Mattson MP and Camandola S. NF-kappaB in neuronal plasticity and neurodegenerative disorders. J Clin Invest 107: 247-254, 2001.
98. Miao W, Hu L, Scrivens PJ, and Batist G. Transcriptional regulation of NF-E2 p45-related factor (NRF2) expression by the aryl hydrocarbon receptor-xenobiotic response ele-ment signaling pathway: direct cross-talk between phase I and II drug-metabolizing enzymes. J Biol Chem 280: 20340-20348, 2005.
99. Mochizuki M, Ishii Y, Itoh K, Iizuka T, Morishima Y, Ki-mura T, Kiwamoto T, Matsuno Y, Hegab AE, Nomura A, Sakamoto T, Uchida K, Yamamoto M, and Sekizawa K. Role of 15-deoxy delta(12,14) prostaglandin J2 and Nrf2 pathways in protection against acute lung injury. Am J Respir Crit Care Med 171: 1260-1266, 2005.
100. Moll UM, Marchenko N, and Zhang XK. p53 and Nur77/TR3: transcription factors that directly target mitochondria for cell death induction. Oncogene 25: 4725-4743, 2006.
101. Mulcahy RT, Wartman MA, Bailey HH, and Gipp JJ. Constitutive and beta-naphthoflavone-induced expression of the human gamma-glutamylcysteine synthetase heavy subunit gene is regulated by a distal antioxidant response element/TRE sequence. J Biol Chem 272: 7445-7454, 1997.
102. Nair S, Doh ST, Chan JY, Kong AN, and Cai L. Regulatory potential for concerted modulation of Nrf2-and Nfkb1-mediated gene expression in inflammation and carcino-genesis. Br J Cancer 99: 2070-2082, 2008.
103. Nguyen T, Huang HC, and Pickett CB. Transcriptional regu-lation of the antioxidant response element: activation by Nrf2 and repression by MafK. J Biol Chem 275: 15466-15473, 2000.
104. Nioi P and Hayes JD. Contribution of NAD(P)H:quinone oxidoreductase 1 to protection against carcinogenesis, and regulation of its gene by the Nrf2 basic-region leucine zipper and the arylhydrocarbon receptor basic helix-loop-helix transcription factors. Mutat Res 555: 149-171, 2004.
105. Noda S, Harada N, Hida A, Fujii-Kuriyama Y, Motohashi H, and Yamamoto M. Gene expression of detoxifying en-zymes in AhR and Nrf2 compound null mutant mouse. Biochem Biophys Res Commun 303: 105-111, 2003.
106. O'Dwyer PJ, Johnson SW, Khater C, Krueger A, Matsu-moto Y, Hamilton TC, and Yao KS. The chemopreventive agent oltipraz stimulates repair of damaged DNA. Cancer Res 57: 1050-1053, 1997.
107. O'Reilly MA. Redox activation of p21Cip1/WAF1/Sdi1: a multifunctional regulator of cell survival and death. Anti-oxid Redox Signal 7: 108-118, 2005.
108. Ohtake F, Baba A, Takada I, Okada M, Iwasaki K, Miki H, Takahashi S, Kouzmenko A, and Nohara K, Chiba T, Fujii-Kuriyama Y, Kato S. Dioxin receptor is a ligand-dependent E3 ubiquitin ligase. Nature 446: 562-566, 2007.
109. Ohtake F, Fujii-Kuriyama Y, and Kato S. AhR acts as an E3 ubiquitin ligase to modulate steroid receptor functions. Biochem Pharmacol 77: 474-484, 2009.
110. Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA, and Choi AM. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 6: 422-428, 2000.
111. Pae HO, Oh GS, Lee BS, Rim JS, Kim YM, and Chung HT. 3-Hydroxyanthranilic acid, one of L-tryptophan metabo-lites, inhibits monocyte chemoattractant protein-1 secretion and vascular cell adhesion molecule-1 expression via heme oxygenase-1 induction in human umbilical vein endothelial cells. Atherosclerosis 187: 274-284, 2006.
112. Pahl HL. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18: 6853-6866, 1999.
113. Pan MH, Lin-Shiau SY, Lin JK. Comparative studies on the suppression of nitric oxide synthase by curcumin and its hydrogenated metabolites through down-regulation of IkappaB kinase and NFkappaB activation in macrophages. Biochem Pharmacol 60: 1665-1676, 2000.
114. Pena AS and Penate M. Genetic susceptibility and regulation of inflammation in Crohn's disease relationship with the in-nate immune system. Rev Esp Enferm Dig 94: 351-360, 2002.
115. Prochaska HJ and Talalay P. Regulatory mechanisms of monofunctional and bifunctional anticarcinogenic enzyme inducers in murine liver. Cancer Res 48: 4776-4782, 1988.
116. Qin J, Clore GM, Kennedy WM, Huth JR, and Gronenborn AM. Solution structure of human thioredoxin in a mixed disulfide intermediate complex with its target peptide from the transcription factor NF kappa B. Structure 3:289-297,1995.
117. Ramos-Gomez M, Kwak MK, Dolan PM, Itoh K, Yama-moto M, Talalay P, and Kensler TW. Sensitivity to carci-nogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc Natl Acad Sci USA 98: 3410-3415, 2001.
118. Rangarajan A, Talora C, Okuyama R, Nicolas M, Mam-mucari C, Oh H, Aster JC, Krishna S, Metzger D, Chambon P, Miele L, Aguet M, Radtke F, and Dotto GP. Notch sig-naling is a direct determinant of keratinocyte growth arrest and entry into differentiation. EMBO J 20: 3427-3436, 2001.
119. Rangasamy T, Guo J, Mitzner WA, Roman J, Singh A, Fryer AD, Yamamoto M, Kensler TW, Tuder RM, Georas SN, and Biswal S. Disruption of Nrf2 enhances susceptibility to se-vere airway inflammation and asthma in mice. J Exp Med 202: 47-59, 2005.
120. Reddy NM, Kleeberger SR, Bream JH, Fallon PG, Kensler TW, Yamamoto M, and Reddy SP. Genetic disruption of the Nrf2 compromises cell-cycle progression by impairing GSH-induced redox signaling. Oncogene 27: 5821-5832, 2008.
121. Reddy NM, Kleeberger SR, Yamamoto M, Kensler TW, Scollick C, Biswal S, and Reddy SP. Genetic dissection of the Nrf2-dependent redox signaling-regulated transcrip-tional programs of cell proliferation and cytoprotection. Physiol Genomics 32: 74-81, 2007.
122. Rosen ED. The transcriptional basis of adipocyte develop-ment. Prostaglandins Leukot Essent Fatty Acids 73: 31-34,2005.
123. Roshak AK, Callahan JF, and Blake SM. Small-molecule inhibitors of NF-kappaB for the treatment of inflammatory joint disease. Curr Opin Pharmacol 2: 316-321, 2002.
124. Ross DA, Hannenhalli S, Tobias JW, Cooch N, Shiekhattar R, and Kadesch T. Functional analysis of Hes-1 in pre-adipocytes. Mol Endocrinol 20: 698-705, 2006.
125. Ross JS, Stagliano NE, Donovan MJ, Breitbart RE, and Ginsburg GS. Atherosclerosis: a cancer of the blood ves-sels? Am J Clin Pathol 1160(suppl): S97-S107, 2001.
126. Rossi A, Kapahi P, Natoli G, Takahashi T, Chen Y, Karin M, and Santoro MG. Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IkappaB kinase. Nature 403: 103-108, 2000.
127. Rushworth SA, Chen XL, Mackman N, Ogborne RM, and O'Connell MA. Lipopolysaccharide-induced heme oxyge-nase-1 expression in human monocytic cells is mediated via Nrf2 and protein kinase C. J Immunol 175: 4408-4415, 2005.
128. Rushworth SA, MacEwan DJ, and O'Connell MA. Lipo-polysaccharide-induced expression of NAD(P)H:quinone oxidoreductase 1 and heme oxygenase-1 protects against excessive inflammatory responses in human monocytes. J Immunol 181: 6730-6737, 2008.
129. Sablina AA, Budanov AV, Ilyinskaya GV, Agapova LS, Kravchenko JE, and Chumakov PM. The antioxidant function of the p53 tumor suppressor. Nat Med 11: 1306-1313, 2005.
130. Sander GR and Powell BC. Expression of notch receptors and ligands in the adult gut. J Histochem Cytochem 52: 509-516, 2004.
131. Sarady JK, Zuckerbraun BS, Bilban M, Wagner O, Usheva A, Liu F, Ifedigbo E, Zamora R, Choi AM, and Otterbein LE. Carbon monoxide protection against endotoxic shock involves reciprocal effects on iNOS in the lung and liver. FASEB J 18: 854-856, 2004.
132. Sartor MA, Schnekenburger M, Marlowe JL, Reichard JF, Wang Y, Fan Y, Ma C, Karyala S, Halbleib D, Liu X, Medvedovic M, and Puga A. Genomewide analysis of aryl hydrocarbon receptor binding targets reveals an extensive array of gene clusters that control morphogenetic and de-velopmental programs. Environ Health Perspect 117: 1139-1146, 2009.
133. Schmidt JV, Su GH, Reddy JK, Simon MC, and Bradfield CA. Characterization of a murine Ahr null allele: involve-ment of the Ah receptor in hepatic growth and develop-ment. Proc Natl Acad Sci USA 93: 6731-6736, 1996.
134. Schroder N and Gossler A. Expression of Notch pathway components in fetal and adult mouse small intestine. Gene Expr Patterns 2: 247-250, 2002.
135. Seldon MP, Silva G, Pejanovic N, Larsen R, Gregoire IP, Filipe J, Anrather J, and Soares MP. Heme oxygenase-1 inhibits the expression of adhesion molecules associated with endothelial cell activation via inhibition of NF-kappaB RelA phosphorylation at serine 276. J Immunol 179: 7840-7851, 2007.
136. Shimba S, Wada T, and Tezuka M. Arylhydrocarbon re-ceptor (AhR) is involved in negative regulation of adipose differentiation in 3T3-L1 cells: AhR inhibits adipose dif-ferentiation independently of dioxin. J Cell Sci 114: 2809-2817, 2001.
137. Shin S, Wakabayashi J, Yates MS, Wakabayashi N, Dolan PM, Aja S, Liby KT, Sporn MB, Yamamoto M, and Kensler TW. Role of Nrf2 in prevention of high-fat diet-induced obesity by synthetic triterpenoid CDDO-imidazolide. Eur J Pharmacol 620: 138-144, 2009.
138. Shin S, Wakabayashi N, Misra V, Biswal S, Lee GH, Agoston ES, Yamamoto M, and Kensler TW. NRF2 mod-ulates aryl hydrocarbon receptor signaling: influence on adipogenesis. Mol Cell Biol 27: 7188-7197, 2007.
139. Soares MP, Seldon MP, Gregoire IP, Vassilevskaia T, Berberat PO, Yu J, Tsui TY, and Bach FH. Heme oxygenase-1 modu-lates the expression of adhesion molecules associated with endothelial cell activation. JImmunol 172: 3553-23563, 2004.
140. Sriram N, Kalayarasan S, and Sudhandiran G. Epigalloca-techin-3-gallate augments antioxidant activities and inhib-its inflammation during bleomycin-induced experimental pulmonary fibrosis through Nrf2-Keap1 signaling. Pulm Pharmacol Ther 22: 221-236, 2009.
141. Srisook K and Cha YN. Super-induction of HO-1 in mac-rophages stimulated with lipopolysaccharide by prior de-pletion of glutathione decreases iNOS expression and NO production. Nitric Oxide 12: 70-79, 2005.
142. Stier S, Cheng T, Dombkowski D, Carlesso N, and Scadden DT. Notch1 activation increases hematopoietic stem cell self-renewal in vivo and favors lymphoid over myeloid lineage outcome. Blood 99: 2369-2378, 2002.
143. Surh YJ, Kundu JK, and Na HK. Nrf2 as a master redox switch in turning on the cellular signaling involved in the induction of cytoprotective genes by some chemo-preventive phytochemicals. Planta Med 74: 1526-1539, 2008.
144. Tanaka Y, Aleksunes LM, Yeager RL, Gyamfi MA, Esterly N, Guo GL, and Klaassen CD. NF-E2-related factor 2 in-hibits lipid accumulation and oxidative stress in mice fed a high-fat diet. J Pharmacol Exp Ther 325: 655-664, 2008.
145. Tenhunen R, Marver HS, and Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxy-genase. Proc Natl Acad Sci USA 61: 748-755, 1968.
146. Tennant RW, French JE, and Spalding JW. Identifying chemical carcinogens and assessing potential risk in short-term bioassays using transgenic mouse models. Environ Health Perspect 103: 942-950, 1995.
147. Thimmulappa RK, Lee H, Rangasamy T, Reddy SP, Ya-mamoto M, Kensler TW, and Biswal S. Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J Clin Invest 116: 984-995, 2006.
148. Thompson JE, Phillips RJ, Erdjument-Bromage H, Tempst P, and Ghosh S. I kappa B-beta regulates the persistent response in a biphasic activation of NF-kappa B. Cell 80: 573-582, 1995.
149. Tien AC, Rajan A, and Bellen HJ. A Notch updated. J Cell Biol 184: 621-629, 2009.
150. Traenckner EB, Pahl HL, Henkel T, Schmidt KN, Wilk S, and Baeuerle PA. Phosphorylation of human I kappa B-alpha on serines 32 and 36 controls I kappa B-alpha pro-teolysis and NF-kappa B activation in response to diverse stimuli. EMBO J 14: 2876-2883, 1995.
151. Venugopal R and Jaiswal AK. Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:qui-none oxidoreductase1 gene. Proc Natl Acad Sci USA 93: 14960-14965, 1996.
152. Wakabayashi N, Itoh K, Wakabayashi J, Motohashi H, Noda S, Takahashi S, Imakado S, Kotsuji T, Otsuka F, Roop DR, Harada T, Engel JD, and Yamamoto M. Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat Genet 35: 238-245, 2003.
153. Wakabayashi N, Shin S, Slocum S, Agoston ES, Waka-bayashi J, Kwak MK, Misra V, Biswal S, Yamamoto M, and Kensler TW. Regulation of Notch1 signaling by Nrf2: implications for tissue regeneration. Sci Signal (in press, 2010).
154. Wang XD, Shou J, Wong P, French DM, and Gao WQ. Notch1-expressing cells
155. Wang XJ, Hayes JD, Henderson CJ, and Wolf CR. Iden-tification of retinoic acid as an inhibitor of transcrip-tion factor Nrf2 through activation of retinoic acid receptor alpha. Proc Natl Acad Sci USA 104: 19589-19594, 2007.
156. Weiss G, Werner-Felmayer G, Werner ER, Grunewald K, Wachter H, and Hentze MW. Iron regulates nitric oxide synthase activity by controlling nuclear transcription. J Exp Med 180: 969-976, 1994.
157. Whiteside ST, Epinat JC, Rice NR, and Israel A. I kappa B epsilon, a novel member of the I kappa B family, controls RelA and cRel NF-kappa B activity. EMBO J 16: 1413-1426,1997.
158. Wilson A and Radtke F. Multiple functions of Notch sig-naling in self-renewing organs and cancer. FEBS Lett 580: 2860-2868, 2006.
159. Wu Z, Bucher NL, and Farmer SR. Induction of peroxisome proliferator-activated receptor gamma during the conver-sion of 3T3 fibroblasts into adipocytes is mediated by C/EBPbeta, C/EBPdelta, and glucocorticoids. Mol Cell Biol 16: 4128-4136, 1996.
160. Xiong Y, Hannon GJ, Zhang H, Casso D, Kobayashi R, and Beach D. p21 is a universal inhibitor of cyclin kinases. Nature 366: 701-704, 1993.
161. Yang H, Magilnick N, Lee C, Kalmaz D, Ou X, Chan JY, and Lu SC. Nrf1 and Nrf2 regulate rat glutamate-cysteine ligase catalytic subunit transcription indirectly via NF-kappaB and AP-1. Mol Cell Biol 25: 5933-5946, 2005.
162. Yates MS, Tran QT, Dolan PM, Osburn WO, Shin S, McCulloch CC, Silkworth JB, Taguchi K, Yamamoto M, Williams CR, Liby KT, Sporn MB, Sutter TR, and Kensler TW. Genetic versus chemoprotective activation of Nrf2 signaling: overlapping yet distinct gene expression profiles between Keap1 knockout and triterpenoid-treated mice. Carcinogenesis 30: 1024-1031, 2009.
163. Yeager RL, Reisman SA, Aleksunes LM, and Klaassen CD. Introducing the "TCDD-inducible AhR-Nrf2 gene battery." Toxicol Sci 111: 2382-2346, 2009.
164. Yuan M, Konstantopoulos N, Lee J, Hansen L, Li ZW, Karin M, and Shoelson SE. Reversal of obesity-and diet-induced insulin resistance with salicylates or targeted dis-ruption of IKKbeta. Science 293: 1673-1677, 2001.
165. Zabel U and Baeuerle PA. Purified human I kappa B can rapidly dissociate the complex of the NF-kappa B tran-scription factor with its cognate DNA. Cell 61: 255-265, 1990.
166. Zhang X, Chen X, Song H, Chen HZ, and Rovin BH. Activation of the Nrf2/antioxidant response pathway increases IL-8 expression. Eur J Immunol 35: 3258-3267, 2005.
167. Zhang Y, Lian JB, Stein JL, van Wijnen AJ, and Stein GS. The Notch-responsive transcription factor Hes-1 attenuates osteocalcin promoter activity in osteoblastic cells. J Cell Biochem 108: 651-659, 2009.
168. Zhou W, Lo SC, Liu JH, Hannink M, and Lubahn DB. ERRbeta: a potent inhibitor of Nrf2 transcriptional activity. Mol Cell Endocrinol 278: 52-62, 2007