Nrf2: Friend and Foe in preventing cigarette smoking-dependent lung disease

Chemical Research in Toxicology

Volumn 25, Issue 9, 2012, Pages 1805-1824

  Müller, Thomas ^a   Hengstermann, Arnd ^a  

^a Molecular Toxicology Department   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2 CYANO 3,12 DIOXOOLEAN 1,9 (11)DIEN 28 OYL) IMIDAZOLE; AMINO ACID TRANSPORTER; AURORA A KINASE; AURORA B KINASE; CATECHOL; CATHEPSIN E; CIGARETTE SMOKE; CIGARETTE SMOKE CONDENSATE; CYCLIN A2; CYCLIN B2; CYSTEINE; ELECTROPHILE; GLUTATHIONE PEROXIDASE 2; HEAVY METAL; HEME OXYGENASE 1; HYDROQUINONE; KELCH LIKE ECH ASSOCIATED PROTEIN 1; PEROXIREDOXIN 1; POLYCYCLIC AROMATIC HYDROCARBON; POLYENE; PROTEIN KINASE C; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SUPEROXIDE DISMUTASE; SYNAPTOPHYSIN; THIOL DERIVATIVE; THIOREDOXIN REDUCTASE 1; TRANSCRIPTION FACTOR NRF2; TRITERPENOID; UNCLASSIFIED DRUG;

CANCER PREVENTION; CELL DAMAGE; CELL STRESS; CHEMICAL STRESS; CHEMOPROPHYLAXIS; CHRONIC OBSTRUCTIVE LUNG DISEASE; CIGARETTE SMOKING; DISEASE COURSE; ENDOPLASMIC RETICULUM STRESS; FORCED EXPIRATORY VOLUME; GENE ACTIVATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE MUTATION; GENETIC ASSOCIATION; GENOTYPE; HUMAN; LUNG CANCER; LUNG CARCINOGENESIS; LUNG COMPLIANCE; LUNG EMPHYSEMA; LUNG PARENCHYMA; MICROARRAY ANALYSIS; MOLECULAR INTERACTION; MORPHOMETRICS; NITROSYLATION; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RETICULOPHAGY; REVIEW; TOTAL LUNG CAPACITY;

ANIMALS; EMPHYSEMA; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LUNG DISEASES; MODELS, ANIMAL; NF-E2-RELATED FACTOR 2; OXIDANTS; OXIDATIVE STRESS; PROTEIN KINASE C; SMOKING; SULFHYDRYL COMPOUNDS;

EID: 84866398376     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx300145n     Document Type: Review

References (179)

1. U.S. Department of Health and Human Services (2004) 2004 Surgeon General's Report: The Health Consequences of Smoking. A Report of the Surgeon General, U.S. Department of Health and Human Services, Centers for Disease Control and Prevention and Health Promotion, Office on Smoking and Health, Atlanta, Georgia.
2. Doll, R. and Hill, B. G. (1952) A study of the aetiology of carcinoma of the lung Br. Med. J. 2 (4797) 1271-1286
3. Vineis, P., Alavanja, M., and Garte, S. (2004) Dose-response relationship in tobacco-related cancers of bladder and lung: A biochemical interpretation Int. J. Cancer 108 (1) 2-7 (Pubitemid 37444436)
4. Rodgman, A. and Perfetti, T. A. (2009) The Chemical Compounds of Tobacco and Tobacco Smoke, CRC Press, Boca Raton, London, NY.
5. Nakayama, T., Kaneko, M., Kodama, M., and Nagata, C. (1985) Cigarette smoke induces DNA single-strand breaks in human cells Nature 314 (6010) 462-464 (Pubitemid 15145590)
6. Müller, T., Haussmann, H. J., and Schepers, G. (1997) Evidence for peroxynitrite as an oxidative stress-inducing compound of aqueous cigarette smoke fractions Carcinogenesis 18 (2) 295-301 (Pubitemid 28132421)
7. Squadrito, G. L. and Pryor, W. A. (1998) Oxidative chemistry of nitric oxide: the roles of superoxide, peroxynitrite, and carbon dioxide Free Radical Biol. Med. 25 (4-5) 392-403 (Pubitemid 28390297)
8. Hecht, S. S. (2003) Tobacco carcinogens, their biomarkers and tobacco-induced cancer Nat. Rev. Cancer 3, 733-744 (Pubitemid 37328812)
9. Müller, T. and Gebel, S. (2006) Cigarette Smoke-Induced Redox Signaling and Gene Expression in In Vitro and In Vivo Models. In Cigarette Smoke & Oxidative Stress (Halliwell, B. B. and Poulsen, H. E., Eds.) pp 75-111, Springer, Heidelberg.
10. Fenner, M. L. and Braven, J. (1968) The mechanism of carcinogenesis by tobacco smoke. Further experimental evidence and a prediction from the thiol-defence hypothesis Br. J. Cancer 22 (3) 474-479
11. Lange, R. (1961) Inhibiting effect of tobacco smoke on some crystalline enzymes Science 134, 52-53
12. Sato, T., Suruki, T., and Fukijama, T. (1962) Cigarette Smoke: Mode of Adhesion and Haemolyzing and SH-inhibiting Factors Br. J. Cancer 16, 7-14
13. Green, G. M. (1968) Cigarette smoke: Protection of alveolar macrophages by glutathione and cysteine Science 162, 810-811
14. Stauffer, H. P. (1974) The interaction of cigarette smoke with thiol groups, a model study Soz. Präv. Med. 19, 55-58
15. Leuchtenberger, C., Leuchtenberger, R., and Zbinden, I. (1974) Gas vapour phase constituents and SH reactivity of cigarette smoke influence lung cultures Nature 247, 565-567
16. Leuchtenberger, C., Leuchtenberger, R., Zbinden, I., and Schleh, E. (1976) SH Reactivity of cigarette smoke and its correlation with carcinogenic effects on hamster lung cultures Soz. Präv. Med. 21 (1) 47-50
17. MacNee, W. (2010) Oxidative stress and chronic obstructive pulmonary disease Eur. Resp. Monogr. 46, 100-129
18. van der Vliet, A. (2006) Oxidative Modifications of Proteins and Lipids by Cigarette Smoke (CS). A Central Role for Unsaturated Aldehydes in CS-Mediated Airway Inflammation. In Cigarette Smoke and Oxidative Stress (Halliwell, B. B. and Poulsen, H. E., Eds.) pp 47-73, Springer, Berlin Heidelberg.
19. Müller, T. and Gebel, S. (1998) The cellular stress response induced by aqueous extracts of cigarette smoke is critically dependent on the intracellular glutathione concentration Carcinogenesis 19 (5) 797-801 (Pubitemid 28376769)
20. Kehrer, J. P. and Biswal, S. S. (2000) The molecular effects of acrolein Toxicol. Sci. 57, 6-15
21. Andersen, M. E., Clewell, H. J., Bermudez, E., Dodd, D. E., Willson, G. A., Campbell, J. L., and Thomas, R. S. (2010) Formaldehyde: Integrating Dosimetry, Cytotoxicity, and Genomics to Understand Dose-Dependent Transitions for an Endogenous Compound Toxicol. Sci. 118 (2) 716-731
22. Reddy, S., Finkelstein, E. I., Wong, P. S.-Y., Phung, A., Cross, C. E., and van der Vliet, A. (2002) Identification of glutathione modifications by cigarette smoke Free Radical Biol. Med. 33 (11) 1490-1498 (Pubitemid 35351592)
23. Liu, J., Qu, W., and Kadiiska, M. B. (2009) Role of oxidative stress in cadmium toxicity and carcinogenesis Toxicol. Appl. Pharmacol. 238 (3) 209-214
24. Abdelmohsen, K., Gerber, P. A., von Montfort, C., Sies, H., and Klotz, L. O. (2003) Epidermal Growth Factor Receptor Is a Common Mediator of Quinone-induced Signaling Leading to Phosphorylation of Connexin-43 - role of Glutathione and Tyrosine Phosphatases J. Biol. Chem. 278 (40) 38360-38367 (Pubitemid 37221728)
25. Bolton, J. L., Trush, M. A., Penning, T. M., Dryhurst, G., and Monks, T. J. (2000) Role of Quinones in Toxicology Chem. Res. Toxicol. 13 (3) 135-160 (Pubitemid 30169958)
26. Müller, T. and Gebel, S. (1994) Heme oxygenase expression in Swiss 3T3 cells following exposure to aqueous cigarette smoke fractions Carcinogenesis 15 (1) 67-72 (Pubitemid 24121626)
27. Schafer, F. Q. and Buettner, G. R. (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple Free Radical Biol. Med. 30 (11) 1191-1212 (Pubitemid 32463931)
28. Matthews, J. R., Wakasugi, N., Virelizier, J. L., Yodoi, J., and Hay, R. T. (1992) Thioredoxin regulates the DNA binding activity of NF-κB by reduction of a disulphide bond involving cysteine 62 Nucleic Acids Res. 20, 3821-3830
29. Abate, C., Patel, L., Rauscher, F. J., III, and Curran, T. (1990) Redox regulation of fos and jun DNA-binding activity in vitro Science 249 (4973) 1157-1161
30. Brigelius-Flohé, R. and Flohé, L. (2011) Basic Principles and Emerging Concepts in the Redox Control of Transcription Factors Antioxid. Redox Signaling 15 (8) 2335-2381
31. Taguchi, K., Motohashi, H., and Yamamoto, M. (2011) Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution Genes Cells 16 (2) 123-140
32. Itoh, K., Wakabayashi, N., Katoh, Y., Ishii, T., Igarashi, K., Engel, J. D., and Yamamoto, M. (1999) Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain Genes Dev. 13, 76-86 (Pubitemid 29045117)
33. Eaton, P. (2006) Protein thiol oxidation in health and disease: Techniques for measuring disulfides and related modifications in complex protein mixtures Free Radical Biol. Med. 40 (11) 1889-1899 (Pubitemid 43744434)
34. Ferrer-Sueta, G., Manta, B., Botti, H., Radi, R., Trujillo, M., and Denicola, A. (2011) Factors Affecting Protein Thiol Reactivity and Specificity in Peroxide Reduction Chem. Res. Toxicol. 24 (4) 434-450
35. Wakabayashi, N., Dinkova-Kostova, A. T., Holtzclaw, W. D., Kang, M. I., Kobayashi, A., Yamamoto, M., Kensler, T. W., and Talalay, P. (2004) Protection against electrophile and oxidant stress by induction of the phase 2 response: Fate of cysteines of the Keap1 sensor modified by inducers Proc. Natl. Acad. Sci. 101 (7) 2040-2045 (Pubitemid 38229011)
36. Zhang, D. D. and Hannink, M. (2003) 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. 23 (22) 8137-8151 (Pubitemid 37377505)
37. Levonen, A. L., Landar, A., Ramachandran, A., Ceaser, E. K., Dickinson, D. A., Zanoni, G., Morrow, J. D., and Darley-Usmar, V. M. (2004) Cellular mechanisms of redox cell signalling: Role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products Biochem. J. 378 (Pt 2) 373-382 (Pubitemid 38367228)
38. Eggler, A. L., Liu, G., Pezzuto, J. M., van Breemen, R. B., and Mesecar, A. D. (2005) Modifying specific cysteines of the electrophile-sensing human Keap1 protein is insufficient to disrupt binding to the Nrf2 domain Neh2 Proc. Natl. Acad. Sci. 102 (29) 10070-10075 (Pubitemid 41023327)
39. Holland, R. and Fishbein, J. C. (2010) Chemistry of the Cysteine Sensors in Kelch-Like ECH-Associated Protein 1 Antioxid. Redox Signaling 13 (11) 1749-1761
40. Yamamoto, T., Suzuki, T., Kobayashi, A., Wakabayashi, J., Maher, J., Motohashi, H., and Yamamoto, M. (2008) Physiological Significance of Reactive Cysteine Residues of Keap1 in Determining Nrf2 Activity Mol. Cell. Biol. 28 (8) 2758-2770 (Pubitemid 351542373)
41. Kobayashi, M., Li, L., Iwamoto, N., Nakajima-Takagi, Y., Kaneko, H., Nakayama, Y., Eguchi, M., Wada, Y., Kumagai, Y., and Yamamoto, M. (2009) The Antioxidant Defense System Keap1-Nrf2 Comprises a Multiple Sensing Mechanism for Responding to a Wide Range of Chemical Compounds Mol. Cell. Biol. 29 (2) 493-502
42. Holtzclaw, W. D., Dinkova-Kostova, A. T., and Talalay, P. (2004) Protection against electrophile and oxidative stress by induction of phase 2 genes: the quest for the elusive sensor that responds to inducers Adv. Enzyme Regul. 44 (1) 335-367 (Pubitemid 39568181)
43. Prestera, T., Holtzclaw, W. D., Zhang, Y., and Talalay, P. (1993) Chemical and Molecular Regulation of Enzymes that Detoxify Carcinogens Proc. Natl. Acad. Sci. 90 (7) 2965-2969 (Pubitemid 23113538)
44. Wooten, J. B., Chouchane, S., and McGrath, T. E. (2006) Tobacco Smoke Constituents Affecting Oxidative Stress. In Cigarette Smoke and Oxidative Stress (Halliwell, B. and Poulsen, H., Eds.) pp 5-46, Springer, Heidelberg.
45. Katoh, Y., Iida, K., Kang, M.-I., Kobayashi, A., Mizukami, M., Tong, K. I., McMahon, M., Hayes, J. D., Itoh, K., and Yamamoto, M. (2005) Evolutionary conserved N-terminal domain of Nrf2 is essential for the Keap1-mediated degradation of the protein by proteasome Arch. Biochem. Biophys. 433 (2) 342-350 (Pubitemid 39592789)
46. Kobayashi, A., Kang, M. I., Watai, Y., Tong, K. I., Shibata, T., Uchida, K., and Yamamoto, M. (2006) Oxidative and Electrophilic Stresses Activate Nrf2 through Inhibition of Ubiquitination Activity of Keap1 Mol. Cell. Biol. 26 (1) 221-229
47. Hayes, J. D. and McMahon, M. (2009) NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer Trends Biochem. Sci. 34 (4) 176-188
48. Hayes, J. D., McMahon, M., Chowdhry, S., and Dinkova-Kostova, A. T. (2010) Cancer Chemoprevention Mechanisms Mediated Through the Keap1-Nrf2 Pathway Antioxid. Redox Signaling 13 (11) 1713-1748
49. Zhang, D. D. (2010) The Nrf2-Keap1-ARE Signaling Pathway: The Regulation and Dual Function of Nrf2 in Cancer Antioxid. Redox Signaling 13 (11) 1623-1626
50. Huang, H. C., Nguyen, T., and Pickett, C. B. (2002) Phosphorylation of Nrf2 at Ser-40 by Protein Kinase C Regulates Antioxidant Response Element-mediated Transcription J. Biol. Chem. 277 (45) 42769-42774 (Pubitemid 35285650)
51. Jaiswal, A. K. (2004) Nrf2 signaling in coordinated activation of antioxidant gene expression Free Radical Biol. Med. 36 (10) 1199-1207 (Pubitemid 38526313)
52. Bloom, D. A. and Jaiswal, A. K. (2003) Phosphorylation of Nrf2 at Ser40 by Protein Kinase C in Response to Antioxidants Leads to the Release of Nrf2 from INrf2, but Is Not Required for Nrf2 Stabilization/Accumulation in the Nucleus and Transcriptional Activation of Antioxidant Response Element-mediated NAD(P)H:Quinone Oxidoreductase-1 Gene Expression J. Biol. Chem. 278 (45) 44675-44682 (Pubitemid 37377224)
53. Bobrovnikova-Marjon, E., Grigoriadou, C., Pytel, D., Zhang, F., Ye, J., Koumenis, C., Cavener, D., and Diehl, J. A. (2010) PERK promotes cancer cell proliferation and tumor growth by limiting oxidative DNA damage Oncogene 29 (27) 3881-3895
54. Cullinan, S. B., Zhang, D., Hannink, M., Arvisais, E., Kaufman, R. J., and Diehl, J. A. (2003) Nrf2 Is a Direct PERK Substrate and Effector of PERK-Dependent Cell Survival Mol. Cell. Biol. 23 (20) 7198-7209 (Pubitemid 37211002)
55. Shen, G., Hebbar, V., Nair, S., Xu, C., Li, W., Lin, W., Keum, Y. S., Han, J., Gallo, M. A., and Kong, A. N. T. (2004) 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. 279 (22) 23052-23060 (Pubitemid 38685609)
56. Kang, K. W., Lee, S. J., Park, J. W., and Kim, S. G. (2002) Phosphatidylinositol 3-Kinase Regulates Nuclear Translocation of NF-E2-Related Factor 2 through Actin Rearrangement in Response to Oxidative Stress Mol. Pharmacol. 62, 1001-1010 (Pubitemid 35222491)
57. Bartalis, J., Zhao, Y. L., Flora, J. W., Paine, J. B., and Wooten, J. B. (2008) Carbon-Centered Radicals in Cigarette Smoke: Acyl and Alkylaminocarbonyl Radicals Anal. Chem. 81 (2) 631-641
58. Flicker, T. M. and Green, S. A. (2001) Comparison of gas-phase free-radical populations in tobacco smoke and model systems by HPLC Environ. Health Perspect. 109 (8) 765-771 (Pubitemid 32910297)
59. Pryor, W. A., Prier, D. G., and Church, D. F. (1983) Electron-spin resonance study of mainstream and sidestream cigarette smoke: Nature of the free radicals in gas-phase smoke and in cigarette tar Environ. Health Perspect. 47, 345-355 (Pubitemid 13134676)
60. Nguyen, T., Sherratt, P. J., and Pickett, C. B. (2003) Regulatory Mechanisms Controlling Gene Expression Mediated by the Antioxidant Response Element Annu. Rev. Pharmacol. Toxicol. 43, 233-260 (Pubitemid 37372641)
61. Nebert, D. W., Dalton, T. P., Okey, A. B., and Gonzalez, F. J. (2004) Role of Aryl Hydrocarbon Receptor-mediated Induction of the CYP1 Enzymes in Environmental Toxicity and Cancer J. Biol. Chem. 279 (23) 23847-23850 (Pubitemid 38725238)
62. Wakabayashi, N., Slocum, S. L., Skoko, J. J., Shin, S., and Kensler, T. W. (2010) When Nrf2 Talks, Who's Listening? Antioxid. Redox Signaling 13 (11) 1649-1663
63. Miao, W., Hu, L., Scrivens, P. J., and Batist, G. (2005) Transcriptional Regulation of NF-E2 p45-related Factor (NRF2) Expression by the Aryl Hydrocarbon Receptor-Xenobiotic Response Element Signaling Pathway: Direct Cross-Talk between Phase I and II Drug-Metabolizing Enzymes J. Biol. Chem. 280 (21) 20340-20348 (Pubitemid 40776732)
64. Prochaska, H. J. and Talalay, P. (1988) Regulatory Mechanisms of Monofunctional and Bifunctional Anticarcinogenic Enzyme Inducers in Murine Liver Cancer Res. 48 (17) 4776-4782
65. Dinkova-Kostova, A. T., Holtzclaw, W. D., Cole, R. N., Itoh, K., Wakabayashi, N., Katoh, Y., Yamamoto, M., and Talalay, P. (2002) Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants Proc. Natl. Acad. Sci. 99 (18) 11908-11913 (Pubitemid 34994497)
66. Holland, R., Hawkins, A. E., Eggler, A. L., Mesecar, A. D., Fabris, D., and Fishbein, J. C. (2008) Prospective Type 1 and Type 2 Disulfides of Keap1 Protein Chem. Res. Toxicol. 21 (10) 2051-2060
67. Bosio, A., Knörr, C., Janssen, U., Gebel, S., Haussmann, H. J., and Müller, T. (2002) Kinetics of gene expression profiling in Swiss 3T3 cells exposed to aqueous extracts of cigarette smoke Carcinogenesis 23 (5) 741-748 (Pubitemid 34567512)
68. Wright, W. R., Parzych, K., Crawford, D., Mein, C., Mitchell, J. A., and Paul-Clark, M. J. (2012) Inflammatory Transcriptome Profiling of Human Monocytes Exposed Acutely to Cigarette Smoke PLoS One 7 (2) e30120
69. Knörr-Wittmann, C., Hengstermann, A., Gebel, S., Alam, J., and Müller, T. (2005) Characterization of Nrf2 activation and heme oxygenase-1 expression in NIH3T3 cells exposed to aqueous extracts of cigarette smoke Free Radical Biol. Med. 39 (11) 1438-1448 (Pubitemid 41547224)
70. Kutty, R. K. and Maines, M. D. (1981) Purification and characterization of biliverdin reductase from rat liver J. Biol. Chem. 256 (8) 3956-3962
71. Stocker, R. (2004) Antioxidant activities of bile pigments Antioxid. Redox Signaling 6 (5) 841-849 (Pubitemid 39237937)
72. Sedlak, T. W., Saleh, M., Higginson, D. S., Paul, B. D., Juluri, K. R., and Snyder, S. H. (2009) Bilirubin and glutathione have complementary antioxidant and cytoprotective roles Proc. Natl. Acad. Sci. 106 (13) 5171-5176
73. Goven, D., Boutten, A., Leçon-Malas, V., Boczkowski, J., and Bonay, M. (2009) Prolonged cigarette smoke exposure decreases heme oxygenase-1 and alters Nrf2 and Bach1 expression in human macrophages: Roles of the MAP kinases ERK1/2 and JNK FEBS Lett. 583 (21) 3508-3518
74. Cheng, S.-E., Lee, I.-T., Lin, C.-C., Kou, Y. R., and Yang, C.-M. (2010) Cigarette smoke particle-phase extract induces HO-1 expression in human tracheal smooth muscle cells: role of the c-Src/NADPH oxidase/MAPK/Nrf2 signaling pathway Free Radical Biol. Med. 48 (10) 1410-1422
75. Um, H. C., Jang, J. H., Kim, D. H., Lee, C., and Surh, Y. J. (2011) Nitric oxide activates Nrf2 through S -nitrosylation of Keap1 in PC12 cells Nitric Oxide 25 (2) 161-168
76. Buckley, B. J., Marshall, Z. M., and Whorton, A. R. (2003) Nitric oxide stimulates Nrf2 nuclear translocation in vascular endothelium Biochem. Biophys. Res. Commun. 307 (4) 973-979 (Pubitemid 36871668)
77. McMahon, M., Lamont, D. J., Beattie, K. A., and Hayes, J. D. (2010) Keap1 perceives stress via three sensors for the endogenous signaling molecules nitric oxide, zinc, and alkenals Proc. Natl. Acad. Sci. 107 (44) 18838-18843
78. Joseph, P. (2009) Mechanisms of cadmium carcinogenesis Toxicol. Appl. Pharmacol. 238 (3) 272-279
79. Wild, P., Bourgkard, E., and Paris, C. (2009) Lung Cancer and Exposure to Metals: The Epidemiological Evidence Methods Mol. Biol. 472, 139-167
80. Alam, J., Wicks, C., Stewart, D., Gong, P. F., Touchard, C., Otterbein, S., Choi, A. M. K., Burow, M. E., and Tou, J. S. (2000) Mechanism of heme oxygenase-1 gene activation by cadmium in MCF-7 mammary epithelial cells - Role of p38 kinase and Nrf2 transcription factor J. Biol. Chem. 275 (36) 27694-27702
81. He, X., Chen, M. G., Lin, G. X., and Ma, Q. (2006) Arsenic Induces NAD(P)H-quinone Oxidoreductase I by Disrupting the Nrf2·Keap1·Cul3 Complex and Recruiting Nrf2·Maf to the Antioxidant Response Element Enhancer J. Biol. Chem. 281 (33) 23620-23631 (Pubitemid 44274137)
82. Wang, X.-J., Sun, Z., Chen, W., Li, Y., Villeneuve, N. F., and Zhang, D. D. (2008) Activation of Nrf2 by arsenite and monomethylarsonous acid is independent of Keap1-C151: Enhanced Keap1-Cul3 interaction Toxicol. Appl. Pharmacol. 230 (3) 383-389
83. He, X. and Ma, Q. (2009) NRF2 Cysteine Residues Are Critical for Oxidant/Electrophile-Sensing, Kelch-Like ECH-Associated Protein-1-Dependent Ubiquitination-Proteasomal Degradation, and Transcription Activation Mol. Pharmacol. 76 (6) 1265-1278
84. Cai, J., Bhatnagar, A., and Pierce, W. M. (2009) Protein Modification by Acrolein: Formation and Stability of Cysteine Adducts Chem. Res. Toxicol. 22 (4) 708-716
85. Tirumalai, R., Kumar, T. R., Mai, K. H., and Biswal, S. (2003) Acrolein causes transcriptional induction of phase II genes by activation of Nrf2 in human lung type II epithelial (A549) cells Toxicol. Lett. 132 (1) 27-36 (Pubitemid 34655429)
86. Zhang, H. and Forman, H. J. (2007) Acrolein Induces Heme Oxygenase-1 Through PKC-δ and PI3K in Human Bronchial Epithelial Cells Am. J. Respir. Cell Mol. Biol. 38 (4) 483-490
87. Lee, S. E., Jeong, S. I., Kim, G.-D., Yang, H., Park, C.-S., Jin, Y.-H., and Park, Y. S. (2011) Upregulation of heme oxygenase-1 as an adaptive mechanism for protection against crotonaldehyde in human umbilical vein endothelial cells Toxicol. Lett. 201 (3) 240-248
88. Hirakawa, K., Oikawa, S., Hiraku, Y., Hirosawa, I., and Kawanishi, S. (2002) Catechol and Hydroquinone Have Different Redox Properties Responsible for Their Differential DNA-damaging Ability Chem. Res. Toxicol. 15 (1) 76-82 (Pubitemid 34106092)
89. Li, Y. B. and Trush, M. A. (1993) Oxidation of Hydroquinone by Copper: Chemical Mechanism and Biological Effects Arch. Biochem. Biophys. 300 (1) 346-355 (Pubitemid 23225756)
90. Roginsky, V. A., Barsukova, T. K., and Stegmann, H. B. (1999) Kinetics of redox interaction between substituted quinones and ascorbate under aerobic conditions Chem.-Biol. Interact. 121 (2) 177-197 (Pubitemid 29299408)
91. Zang, L. Y., Stone, K., and Pryor, W. A. (1995) Detection of free radicals in aqueous extracts of cigarette tar by electron spin resonance Free Radical Biol. Med. 19 (2) 161-167
92. Seung, S.-A., Lee, J.-Y., Lee, M.-Y., Park, J.-S., and Chung, J.-H. (1998) The relative importance of oxidative stress versus arylation in the mechanism of quinone-induced cytotoxicity to platelets Chem.-Biol. Interact. 113 (2) 133-144
93. Bensasson, R. V., Zoete, V., Dinkova-Kostova, A. T., and Talalay, P. (2008) Two-Step Mechanism of Induction of the Gene Expression of a Prototypic Cancer-Protective Enzyme by Diphenols Chem. Res. Toxicol. 21 (4) 805-812 (Pubitemid 351644558)
94. Wang, X. J., Hayes, J. D., Higgins, L. G., Wolf, C. R., and Dinkova-Kostova, A. T. (2011) Activation of the NRF2 Signaling Pathway by Copper-Mediated Redox Cycling of Para- and Ortho -Hydroquinones Chem. Biol. 17 (1) 75-85
95. Dinkova-Kostova, A. T. and Wang, X. J. (2011) Induction of the Keap1/Nrf2/ARE pathway by oxidizable diphenols Chem.-Biol. Interact. 192 (1-2) 101-106
96. Dorfman, L. M. and Adams, G. E. (1973) Reactivity of the Hydroxyl Radical in Aqueous Solution (Roberts, R. W., Ed.) pp 1-59, U.S. Department of Commerce, National Bureau of Standards, Washington, DC.
97. Holland, R., Navamal, M., Velayutham, M., Zweier, J. L., Kensler, T. W., and Fishbein, J. C. (2009) Hydrogen Peroxide Is a Second Messenger in Phase 2 Enzyme Induction by Cancer Chemopreventive Dithiolethiones Chem. Res. Toxicol. 22 (8) 1427-1434
98. Fourquet, S., Guerois, R., Biard, D., and Toledano, M. B. (2010) Activation of NRF2 by Nitrosative Agents and H2O2 Involves KEAP1 Disulfide Formation J. Biol. Chem. 285 (11) 8463-8471
99. IARC (2008) IRARC, 1,3-Butadiene, Ethylene Oxide, and Vinyl Halides (Vinyl Fluoride, Vinyl Chloride and Vinyl Bromide), International Agency for Research on Cancer, Lyon.
100. Swenberg, J. A., Bordeerat, N. K., Boysen, G., Carro, S., Georgieva, N. I., Nakamura, J., Troutman, J. M., Upton, P. B., Albertini, R. J., Vacek, P. M., Walker, V. E., Sram, R. J., Goggin, M., and Tretyakova, N. (2011) 1,3-Butadiene: Biomarkers and application to risk assessment Chem.-Biol. Interact. 192 (1-2) 150-154
101. Cederbaum, A. I. (2009) Nrf2 and antioxidant defense against CYP2E1 toxicity Expert Opin. Drug Metabol. Toxicol. 5 (10) 1223-1244
102. Ryter, S. W. and Choi, A. M. K. (2010) Autophagy in the Lung Proc. Am. Thorac. Soc. 7 (1) 13-21
103. Walter, P. and Ron, D. (2011) The Unfolded Protein Response: From Stress Pathway to Homeostatic Regulation Science 334 (6059) 1081-1086
104. Cullinan, S. B. and Diehl, J. A. (2004) PERK-dependent Activation of Nrf2 Contributes to Redox Homeostasis and Cell Survival following Endoplasmic Reticulum Stress J. Biol. Chem. 279 (19) 20108-20117 (Pubitemid 38623455)
105. Moi, P., Chan, K., Asunis, I., Cao, A., and Kan, Y. W. (1994) Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region Proc. Natl. Acad. Sci. 91 (21) 9926-9930 (Pubitemid 24311921)
106. Itoh, K., Chiba, T., Takahashi, S., Ishii, T., Igarashi, K., Katoh, Y., Oyake, T., Hayashi, N., Satoh, K., Hatayama, I., Yamamoto, M., and Nabeshima, Y. i. (1997) An Nrf2/Small Maf Heterodimer Mediates the Induction of Phase II Detoxifying Enzyme Genes through Antioxidant Response Elements Biochem. Biophys. Res. Commun. 236 (2) 313-322 (Pubitemid 27373291)
107. 1 gene Proc. Natl. Acad. Sci. 93 (25) 14960-14965 (Pubitemid 26419078)
108. Gebel, S., Gerstmayer, B., Bosio, A., Haussmann, H. J., Miert, E. V., and Müller, T. (2004) Gene expression profiling in respiratory tissues from rats exposed to mainstream cigarette smoke Carcinogenesis 25 (2) 169-178 (Pubitemid 38239800)
109. Spira, A., Beane, J., Shah, V., Liu, G., Schembri, F., Yang, X., Palma, J., and Brody, J. S. (2004) Effects of cigarette smoke on the human airway epithelial cell transcriptome Proc. Natl. Acad. Sci. 101 (27) 10143-10148 (Pubitemid 38891209)
110. Rangasamy, T., Cho, C. Y., Thimmulappa, R. K., Zhen, L., Srisuma, S. S., Kensler, T. W., Yamamoto, M., Petrache, I., Tuder, R. M., and Biswal, S. (2004) Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice J. Clin. Invest. 114 (9) 1248-1259 (Pubitemid 40385296)
111. Iizuka, T., Ishii, Y., Itoh, K., Kiwamoto, T., Kimura, T., Matsuno, Y., Morishima, Y., Hegab, A. E., Homma, S., Nomura, A., Sakamoto, T., Shimura, M., Yoshida, A., Yamamoto, M., and Sekizawa, K. (2005) Nrf2-deficient mice are highly susceptible to cigarette smoke-induced emphysema Genes Cells 10 (12) 1113-1125 (Pubitemid 41830071)
112. Biswal, S., Rangasamy, T., and Tuder, R. M. (2006) Modifier Role of Nrf2 in Cigarette Smoke-induced Emphysema Proc. Am. Thorac. Soc. 3 (6) 543a
113. Singh, A., Rangasamy, T., Thimmulappa, R. K., Lee, H., Osburn, W. O., Brigelius-Flohé, R., Kensler, T. W., Yamamoto, M., and Biswal, S. (2006) Glutathione Peroxidase 2, the Major Cigarette Smoke-inducible Isoform of GPX in Lungs is Regulated by Nrf2 Am. J. Respir. Cell Mol. Biol. 35 (6) 639-650 (Pubitemid 44901853)
114. Singh, A., Ling, G., Suhasini, A. N., Zhang, P., Yamamoto, M., Navas-Acien, A., Cosgrove, G., Tuder, R. M., Kensler, T. W., Watson, W. H., and Biswal, S. (2008) Nrf2-dependent sulfiredoxin-1 expression protects against cigarette smoke-induced oxidative stress in lungs Free Radical Biol. Med. 46 (3) 376-386
115. -/- Mice Provides Evidence for Impaired Cell Cycle Progression in the Development of Cigarette Smoke-Induced Emphysematous Changes Toxicol. Sci. 115 (1) 238-252
116. Ishii, Y., Itoh, K., Morishima, Y., Kimura, T., Kiwamoto, T., Iizuka, T., Hegab, A. E., Hosoya, T., Nomura, A., Sakamoto, T., Yamamoto, M., and Sekizawa, K. (2005) Transcription Factor Nrf2 Plays a Pivotal Role in Protection against Elastase-Induced Pulmonary Inflammation and Emphysema J. Immunol. 175 (10) 6968-6975 (Pubitemid 41598943)
117. Botelho, F. M., Gaschler, G. J., Kianpour, S., Zavitz, C. C. J., Trimble, N. J., Nikota, J. K., Bauer, C. M. T., and Stampfli, M. R. (2010) Innate Immune Processes Are Sufficient for Driving Cigarette Smoke-Induced Inflammation in Mice Am. J. Respir. Cell Mol. Biol. 42 (4) 394-403
118. Cavarra, E., Fardin, P., Fineschi, S., Ricciardi, A., De Cunto, G., Sallustio, F., Zorzetto, M., Luisetti, M., Pfeffer, U., Lungarella, G., and Varesio, L. (2009) Early response of gene clusters is associated with mouse lung resistance or sensitivity to cigarette smoke Am. J. Physiol. Lung Cell. Mol. Physiol. 296 (3) L418-L429
119. Vecchio, D., Arezzini, B., Pecorelli, A., Valacchi, G., Martorana, P. A., and Gardi, C. (2010) Reactivity of mouse alveolar macrophages to cigarette smoke is strain dependent Am. J. Physiol. Lung Cell. Mol. Physiol. 298 (5) L704-L713
120. Barnes, P. J. (2004) Mediators of Chronic Obstructive Pulmonary Disease Pharmacol. Rev. 56 (4) 515-548 (Pubitemid 39658462)
121. 1-Antitrypsin Deficiency Proc. Am. Thorac. Soc. 7 (6) 381-386
122. Reddy, N. M., Kleeberger, S. R., Bream, J. H., Fallon, P. G., Kensler, T. W., Yamamoto, M., and Reddy, S. P. (2008) Genetic disruption of the Nrf2 compromises cell-cycle progression by impairing GSH-induced redox signaling Oncogene 27 (44) 5821-5832
123. Goven, D., Boutten, A., Lecon-Malas, V., Marchal-Somme, J., Amara, N., Crestani, B., Fournier, M., Leseche, G., Soler, P., Boczkowski, J., and Bonay, M. (2008) Altered Nrf2/Keap1-Bach1 equilibrium in pulmonary emphysema Thorax 63 (10) 916-924
124. Wakabayashi, N., Itoh, K., Wakabayashi, J., Motohashi, H., Noda, S., Takahashi, S., Imakado, S., Kotsuji, T., Otsuka, F., Roop, D. R., Harada, T., Engel, J. D., and Yamamoto, M. (2003) Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation Nat. Genet. 35 (3) 238-245 (Pubitemid 37363177)
125. Blake, D. J., Singh, A., Kombairaju, P., Malhotra, D., Mariani, T. J., Tuder, R. M., Gabrielson, E., and Biswal, S. (2010) Deletion of Keap1 in the Lung Attenuates Acute Cigarette Smoke-induced Oxidative Stress and Inflammation Am. J. Respir. Cell Mol. Biol. 42 (5) 524-536
126. Adair-Kirk, T. L., Atkinson, J. J., Griffin, G. L., Watson, M. A., Kelley, D. G., DeMello, D., Senior, R. M., and Betsuyaku, T. (2008) Distal Airways in Mice Exposed to Cigarette Smoke: Nrf2-regulated Genes are Increased in Clara Cells Am. J. Respir. Cell Mol. Biol. 39 (4) 400-411
127. Taguchi, K., Maher, J. M., Suzuki, T., Kawatani, Y., Motohashi, H., and Yamamoto, M. (2010) Genetic Analysis of Cytoprotective Functions Supported by Graded Expression of Keap1 Mol. Cell. Biol. 30 (12) 3016-3026
128. Comandini, A., Marzano, V., Curradi, G., Federici, G., Urbani, A., and Saltini, C. (2010) Markers of anti-oxidant response in tobacco smoke exposed subjects: A data-mining review Pulm. Pharmacol. Ther. 23 (6) 482-492
129. Hübner, R. H., Schwartz, J. D., De, B. P., Ferris, B., Omberg, L., Mezey, J. G., Hackett, N. R., and Crystal, R. G. (2009) Coordinate Control of Expression of Nrf2-Modulated Genes in the Human Small Airway Epithelium Is Highly Responsive to Cigarette Smoking Mol. Med. 15 (7-8) 203-219
130. Malhotra, D., Thimmulappa, R., Navas-Acien, A., Sandford, A., Elliott, M., Singh, A., Chen, L., Zhuang, X., Hogg, J., Pare, P., Tuder, R. M., and Biswal, S. (2008) Decline in NRF2 Regulated Antioxidants in COPD Lungs due to Loss of its Positive Regulator DJ-1 Am. J. Respir. Crit Care Med. 178, 592-603
131. Clements, C. M., McNally, R. S., Conti, B. J., Mak, T. W., and Ting, J. P. Y. (2006) DJ-1, a cancer- and Parkinson's disease-associated protein, stabilizes the antioxidant transcriptional master regulator Nrf2 Proc. Natl. Acad. Sci. 103 (41) 15091-15096 (Pubitemid 44583169)
132. Malhotra, D., Thimmulappa, R. K., Mercado, N., Ito, K., Kombairaju, P., Kumar, S., Ma, J., Feller-Kopman, D., Wise, R., Barnes, P., and Biswal, S. (2011) Denitrosylation of HDAC2 by targeting Nrf2 restores glucocorticosteroid sensitivity in macrophages from COPD patients J. Clin. Invest. 121 (11) 4289-4302
133. Ito, K., Ito, M., Elliott, W. M., Cosio, B., Caramori, G., Kon, O. M., Barczyk, A., Hayashi, S., Adcock, I. M., Hogg, J. C., and Barnes, P. J. (2005) Decreased Histone Deacetylase Activity in Chronic Obstructive Pulmonary Disease N. Engl. J. Med. 352 (19) 1967-1976 (Pubitemid 40638367)
134. Barnes, P. J. (2009) Histone deacetylase-2 and airway disease Ther. Adv. Respir. Dis. 3 (5) 235-243
135. Mercado, N., Thimmulappa, R., Thomas, C. M. R., Fenwick, P. S., Chana, K. K., Donnelly, L. E., Biswal, S., Ito, K., and Barnes, P. (2011) Decreased histone deacetylase 2 impairs Nrf2 activation by oxidative stress Biochem. Biophys. Res. Commun. 406 (2) 292-298
136. Sun, Z., Chin, Y. E., and Zhang, D. D. (2009) Acetylation of Nrf2 by p300/CBP Augments Promoter-Specific DNA Binding of Nrf2 during the Antioxidant Response Mol. Cell. Biol. 29 (10) 2658-2672
137. Adenuga, D., Caito, S., Yao, H., Sundar, I. K., Hwang, J.-W., Chung, S., and Rahman, I. (2010) Nrf2 deficiency influences susceptibility to steroid resistance via HDAC2 reduction Biochem. Biophys. Res. Commun. 403 (3-4) 452-456
138. Chen, Z. H., Kim, H. P., Sciurba, F. C., Lee, S. J., Feghali-Bostwick, C., Stolz, D. B., Dhir, R., Landreneau, R. J., Schuchert, M. J., Yousem, S. A.,
139. Kim, H. P., Wang, X., Lee, S. J., Huang, M. H., Wang, Y., Ryter, S., and Choi, A. M. K. (2008) Autophagic proteins regulate cigarette smoke induced apoptosis: Protective role of heme oxygenase-1 Autophagy 4 (7) 887-895
140. Mizushima, N. and Komatsu, D. (2011) Autophagy: Renovation of Cells and Tissues Cell 147 (4) 728-741
141. Rusten, T. E. and Stenmark, H. (2010) p62, an autophagy hero or culprit? Nat. Cell Biol. 12 (3) 207-209
142. Ryter, S., Lee, S.-J., and Choi, A. M. K. (2010) Autophagy in cigarette smoke-induced chronic obstructive pulmonary disease Exp. Rev. Respir. Med. 4 (5) 573-584
143. Stepkowski, T. M. and Kruszewski, M. K. (2011) Molecular cross-talk between the NRF2/KEAP1 signaling pathway, autophagy, and apoptosis Free Radical Biol. Med. 50 (9) 1186-1195
144. Lamark, T., Kirkin, V., Dikic, I., and Johansen, T. (2009) NBR1 and p62 as cargo receptors for selective autophagy of ubiquitinated targets Cell Cycle 8 (13) 1986-1990
145. Komatsu, M., Kurokawa, H., Waguri, S., Taguchi, K., Kobayashi, A., Ichimura, Y., Sou, Y. S., Ueno, I., Sakamoto, A., Tong, K. I., Kim, M., Nishito, Y., Iemura, S. i., Natsume, T., Ueno, T., Kominami, E., Motohashi, H., Tanaka, K., and Yamamoto, M. (2010) The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1 Nat. Cell Biol. 12 (3) 213-223
146. Hengstermann, A. and Müller, T. (2008) Endoplasmic Reticulum stress induced by aqueous extracts of cigarette smoke in 3T3 cells activates the unfolded protein response-dependent PERK pathway of cell survival Free Radical Biol. Med. 44 (6) 1097-1107
147. Jorgensen, E. D., Stinson, A., Shan, L., Yang, J., Gietl, D., and Albino, A. P. (2008) Cigarette Smoke Induces Endoplasmic Reticulum Stress and the Unfolded Protein Response in Normal and Malignant Human Lung Cells BMC Cancer 8, 229
148. Kelsen, S. G., Duan, X., Ji, R., Perez, O., Liu, C., and Merali, S. (2007) Cigarette Smoke Induces an Unfolded Protein Response in the Human Lung: A Proteomic Approach Am. J. Respir. Cell Mol. Biol. 38 (5) 541-550 (Pubitemid 351758672)
149. Padmanabhan, B., Tong, K. I., Ohta, T., Nakamura, Y., Scharlock, M., Ohtsuji, M., Kang, M. I., Kobayashi, A., Yokoyama, S., and Yamamoto, M. (2006) Structural Basis for Defects of Keap1 Activity Provoked by Its Point Mutations in Lung Cancer Mol. Cell 21 (5) 689-700 (Pubitemid 43290735)
150. Li, Q. K., Singh, A., Biswal, S., Askin, F., and Gabrielson, E. (2011) KEAP1 gene mutations and NRF2 activation are common in pulmonary papillary adenocarcinoma J. Hum. Genet. 56 (3) 230-234
151. Ohta, T., Iijima, K., Miyamoto, M., Nakahara, I., Tanaka, H., Ohtsuji, M., Suzuki, T., Kobayashi, A., Yokota, J., Sakiyama, T., Shibata, T., Yamamoto, M., and Hirohashi, S. (2008) Loss of Keap1 Function Activates Nrf2 and Provides Advantages for Lung Cancer Cell Growth Cancer Res. 68 (5) 1303-1309 (Pubitemid 351346836)
152. Shibata, T., Ohta, T., Tong, K. I., Kokubu, A., Odogawa, R., Tsuta, K., Asamura, H., Yamamoto, M., and Hirohashi, S. (2008) Cancer related mutations in NRF2 impair its recognition by Keap1-Cul3 E3 ligase and promote malignancy Proc. Natl. Acad. Sci. 105 (36) 13568-13573
153. Singh, A., Misra, V., Thimmulappa, R. K., Lee, H., Ames, S., Hoque, M. O., Herman, J. G., Baylin, S. B., Sidransky, D., Gabrielson, E., Brock, M. V., and Biswal, S. (2006) Dysfunctional KEAP1-NRF2 Interaction in Non-Small-Cell Lung Cancer PLoS. Med. 3 (10) e420
154. Homma, S., Ishii, Y., Morishima, Y., Yamadori, T., Matsuno, Y., Haraguchi, N., Kikuchi, N., Satoh, H., Sakamoto, T., Hizawa, N., Itoh, K., and Yamamoto, M. (2009) Nrf2 Enhances Cell Proliferation and Resistance to Anticancer Drugs in Human Lung Cancer Clin. Cancer Res. 15 (10) 3423-3432
155. Solis, L. M., Behrens, C., Dong, W., Suraokar, M., Ozburn, N. C., Moran, C. A., Corvalan, A. H., Biswal, S., Swisher, S. G., Bekele, B. N., Minna, J. D., Stewart, D. J., and Wistuba, I. I. (2010) Nrf2 and Keap1 Abnormalities in Non-Small Cell Lung Carcinoma and Association with Clinicopathologic Features Clin. Cancer Res. 16 (14) 3743-3753
156. Herbst, R. S., Heymach, J. V., and Lippman, S. M. (2008) Lung Cancer N. Engl. J. Med. 359 (13) 1367-1380
157. DeNicola, G. M., Karreth, F. A., Humpton, T. J., Gopinathan, A., Wei, C., Frese, K., Mangal, D., Yu, K. H., Yeo, C. J., Calhoun, E. S., Scrimieri, F., Winter, J. M., Hruban, R. H., Iacobuzio-Donahue, C., Kern, S. E., Blair, I. A., and Tuveson, D. A. (2011) Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis Nature 475 (7354) 106-109
158. Niture, S. K. and Jaiswal, A. K. (2012) Nrf2 Protein Up-regulates Antiapoptotic Protein Bcl-2 and Prevents Cellular Apoptosis J. Biol. Chem. 287 (13) 9873-9886
159. Wang, R., An, J., Ji, F., Jiao, H., Sun, H., and Zhou, D. (2008) Hypermethylation of the Keap1 gene in human lung cancer cell lines and lung cancer tissues Biochem. Biophys. Res. Commun. 373 (1) 151-154
160. Perera, R. M. and Bardeesy, N. (2011) Cancer: When antioxidants are bad Nature 475 (7354) 43-44
161. Ren, D., Villeneuve, N. F., Jiang, T., Wu, T., Lau, A., Toppin, H. A., and Zhang, D. D. (2011) Brusatol enhances the efficacy of chemotherapy by inhibiting the Nrf2-mediated defense mechanism Proc. Natl. Acad. Sci. 108 (4) 1433-1438
162. Kensler, T. W. and Wakabayashi, N. (2010) Nrf2: Friend or Foe for Chemoprevention? Carcinogenesis 31 (1) 90-99
163. Kwak, M.-K. and Kensler, T. W. (2010) Targeting NRF2 signaling for cancer chemoprevention Toxicol. Appl. Pharmacol. 244 (1) 66-76
164. Kwak, M. K., Wakabayashi, N., and Kensler, T. W. (2007) Chemoprevention through the Keap1-Nrf2 signaling pathway by phase 2 enzyme inducers Mutat. Res., Fundam. Mol. Mech. Mutagen. 555 (1-2) 133-148
165. Slocum, S. L. and Kensler, T. W. (2011) Nrf2: Control of sensitivity to carcinogens Arch. Toxicol. 85 (4) 273-284
166. Lam, T. K., Rotunno, M., Lubin, J. H., Wacholder, S., Consonni, D., Pesatori, A. C., Bertazzi, P. A., Chanock, S. J., Burdette, L., Goldstein, A. M., Tucker, M. A., Caporaso, N. E., Subar, A. F., and Landi, M. T. (2010) Dietary quercetin, quercetin-gene interaction, metabolic gene expression in lung tissue and lung cancer risk Carcinogenesis 31 (4) 634-642
167. Landi, M. T., Consonni, D., Rotunno, M., Bergen, A., Goldstein, A., Lubin, J., Goldin, L., Alavanja, M., Morgan, G., Subar, A., Linnoila, I., Previdi, F., Corno, M., Rubagotti, M., Marinelli, B., Albetti, B., Colombi, A., Tucker, M., Wacholder, S., Pesatori, A., Caporaso, N., and Bertazzi, P. A. (2008) Environment And Genetics in Lung cancer Etiology (EAGLE) study: An integrative population-based case-control study of lung cancer BMC Pub. Health 8 (1) 203
168. Tanigawa, S., Fujii, M., and Hou, D. X. (2007) Action of Nrf2 and Keap1 in ARE-mediated NQO1 expression by quercetin Free Radical Biol. Med. 42 (11) 1690-1703 (Pubitemid 46617147)
169. Dinkova-Kostova, A. T., Liby, K. T., Stephenson, K. K., Holtzclaw, W. D., Gao, X., Suh, N., Williams, C., Risingsong, R., Honda, T., Gribble, G. W., Sporn, M. B., and Talalay, P. (2005) Extremely potent triterpenoid inducers of the phase 2 response: Correlations of protection against oxidant and inflammatory stress Proc. Natl. Acad. Sci. 102 (12) 4584-4589 (Pubitemid 40397155)
170. Yates, M. S., Tauchi, M., Katsuoka, F., Flanders, K. C., Liby, K. T., Honda, T., Gribble, G. W., Johnson, D. A., Johnson, J. A., Burton, N. C., Guilarte, T. R., Yamamoto, M., Sporn, M. B., and Kensler, T. W. (2007) Pharmacodynamic characterization of chemopreventive triterpenoids as exceptionally potent inducers of Nrf2-regulated genes Mol. Cancer Ther. 6 (1) 154-162 (Pubitemid 46206678)
171. Sussan, T. E., Rangasamy, T., Blake, D. J., Malhotra, D., El-Haddad, H., Bedja, D., Yates, M. S., Kombairaju, P., Yamamoto, M., Liby, K. T., Sporn, M. B., Gabrielson, K. L., Champion, H. C., Tuder, R. M., Kensler, T. W., and Biswal, S. (2009) Targeting Nrf2 with the triterpenoid CDDO-imidazolide attenuates cigarette smoke-induced emphysema and cardiac dysfunction in mice Proc. Natl. Acad. Sci. 106 (1) 250-255
172. Gebel, S., Gerstmayer, B., Kuhl, P., Borlak, J., Meurrens, K., and Müller, T. (2006) The Kinetics of Transcriptomic Changes Induced by Cigarette Smoke in Rat Lungs Reveals a Specific Program of Defense, Inflammation, and Circadian Clock Gene Expression Toxicol. Sci. 93 (2) 422-431 (Pubitemid 44400459)
173. Churg, A., Sin, D. D., and Wright, J. L. (2011) Everything Prevents Emphysema: Are Animal Models of Cigarette Smoke-Induced COPD Any Use? Am. J. Respir. Cell Mol. Biol. 45 (6) 1111-1115
174. Wright, J. L. and Churg, A. (2010) Animal models of cigarette smoke-induced chronic obstructive pulmonary disease Expert Rev. Respir. Med. 4 (6) 723-734
175. Grivennikov, S. I., Greten, F. R., and Karin, M. (2010) Immunity, Inflammation, and Cancer Cell 140 (6) 883-899
176. Nathan, C. and Ding, A. (2010) Nonresolving Inflammation Cell 140 (6) 871-882
177. Reuter, S., Gupta, S. C., Chaturvedi, M. M., and Aggarwal, B. B. (2010) Oxidative stress, inflammation, and cancer: How are they linked? Free Radical Biol. Med. 49 (11) 1603-1616
178. Hanahan, D. and Weinberg, R. A. (2011) Hallmarks of Cancer: The Next Generation Cell 144 (5) 646-674
179. Mantovani, A., Allavena, P., Sica, A., and Balkwill, F. (2008) Cancer-related inflammation Nature 454 (7203) 436-444