Renal injury and Nrf2 modulation in mouse kidney following chronic exposure to TiO2 nanoparticles

Journal of Agricultural and Food Chemistry

Volumn 61, Issue 37, 2013, Pages 8959-8968

  Gui, Suxin ^a   Li, Bingyan ^a   Zhao, Xiaoyang ^a   Sheng, Lei ^a   Hong, Jie ^a   Yu, Xiaohong ^a   Sang, Xuezi ^a   Sun, Qingqing ^a   Ze, Yuguan ^a   Wang, Ling ^a   Hong, Fashui ^a,b,c  

^a MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

^b SOOCHOW UNIVERSITY   (China)

^c Key Laboratory of Stem Cell Research   (China)

Author keywords

inflammation; kidney; Nrf2 pathway; oxidative stress; titanium dioxide nanoparticles

Indexed keywords

DETOXIFYING ENZYMES; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE-S-TRANSFERASE; INFLAMMATION; KIDNEY; NRF2 PATHWAY; REACTIVE OXYGEN SPECIES; TITANIUM DIOXIDE NANOPARTICLES;

AMINO ACIDS; BIOLOGICAL ORGANS; CELL DEATH; ENZYME INHIBITION; GENE EXPRESSION; GENE EXPRESSION REGULATION; MAMMALS; NANOPARTICLES; OXIDATIVE STRESS; PATHOLOGY;

TITANIUM DIOXIDE;

NANOPARTICLE; REACTIVE OXYGEN METABOLITE; TITANIUM; TITANIUM DIOXIDE; TRANSCRIPTION FACTOR NRF2;

ANIMAL; ARTICLE; DOWN REGULATION; DRUG EFFECT; GENETICS; INJURY; INSTITUTE FOR CANCER RESEARCH MOUSE; KIDNEY; MALE; METABOLISM; MOUSE; OXIDATIVE STRESS; SIGNAL TRANSDUCTION;

ANIMALS; DOWN-REGULATION; KIDNEY; MALE; MICE; MICE, INBRED ICR; NANOPARTICLES; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TITANIUM;

EID: 84884489334     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf402387e     Document Type: Article

References (98)

1. Powell, J. J.; Faria, N.; Thomas-McKay, E.; Pele, L. C. Origin and fate of dietary nanoparticles and microparticles in the gastrointestinal tract J. Autoimmun. 2010, 34, 226-233
2. Skocaj, M.; Filipic, M.; Petkovic, J.; Novak, S. Titanium dioxide in our everyday life; is it safe? Radiol. Oncol. 2011, 45, 227-247
3. Weir, A.; Westerhoff, P.; Fabricius, L.; Hristovski, K.; von Goetz, N. Titanium dioxide nanoparticles in food and personal care products Environ. Sci. Technol. 2012, 46, 2242-2250
4. Oberdörster, G.; Oberdörster, E.; Oberdörster, J. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles Environ. Health Perspect. 2005, 113 (7) 823-839
5. 2 particles in cultured human lymphoblastoid cells Mutat. Res. 2007, 628, 99-106
6. 2 particles: differential responses related to surface properties Toxicity 2007, 230, 90-104
7. 2 primary particles in mice Environ. Toxicol. Pharmacol. 2007, 24, 239-244
8. 2 to the nematode Caenorhabditis elegans Environ. Pollut. 2009, 157, 1171-1177
9. 2, ZnO and their bulk counterparts on zebrafish: acute toxicity, oxidative stress and oxidative damage Sci. Total Environ. 2011, 409 (8) 1444-1452
10. Linkov, I.; Satterstrom, F. K.; Corey, L. M. Nanotoxicology and nanomedicine: making hard decisions Nanomedicine 2008, 4, 167-171
11. Elsaesser, A.; Howard, C. V. Toxicology of nanoparticles Adv. Drug Delivery Rev. 2012, 64, 129-137
12. IARC. Carbon Black, Titanium Dioxide and Talc; IARC Monographs on the Evaluation of Carcinogenic Risks to Humans 93; International Agency for Research on Cancer: Lyon, France, 2006.
13. Hana, S. G.; Newsomea, B.; Hennig, B. Titanium dioxide nanoparticles increase inflammatory responses in vascular endothelial cells Toxicology 2013, 306, 1-8
14. Afaq, F.; Abidi, P.; Matin, R.; Rahman, Q. Cytotoxicity, pro-oxidant effects and antioxidant depletion in rat lung alveolar macrophages exposed to ultrafine titanium dioxide J. Appl. Toxicol. 1998, 18, 307-312
15. Sun, Q. Q.; Tan, D. L.; Ze, Y. G.; Sang, X. Z.; Liu, X. R.; Gui, S. X.; Cheng, Z.; Cheng, J.; Hu, R. P.; Gao, G. D.; Liu, G.; Zhu, M.; Zhao, X. Y.; Sheng, L.; Wang, L.; Tang, M.; Hong, F. S. Pulmotoxicological effects caused by long-term titanium dioxide nanoparticles exposure in mice J. Hazard. Mater. 2012, 235-236, 47-53
16. Sun, Q. Q.; Tan, D. L.; Zhou, Q. P.; Liu, X. R.; Cheng, Z.; Liu, G.; Zhu, M.; Sang, X. Z.; Gui, S. X.; Cheng, J.; Hu, R. P.; Tang, M.; Hong, F. S. Oxidative damage of lung and its protective mechanism in mice caused by long-term exposure to titanium dioxide nanoparticles J. Biomed. Mater. Res. Part A 2012, 100A (10) 2554-2562
17. Li, B.; Ze, Y. G.; Su, Q. Q.; Zhang, T.; Sang, X. Z.; Cui, Y. L.; Wang, X. C.; Gui, S. X.; Tan, D. L.; Zhu, M.; Zhao, X. Y.; Sheng, L.; Wang, L.; Hong, F. S.; Tang, M. Molecular mechanisms of nanosized titanium dioxide-induced pulmonary injury in mice PLoS One 2013, 8 (2) e55563
18. Federici, G.; Shaw, B. J.; Handy, R. D. Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): gill injury, oxidative stress, and other physiological effects Aquat. Toxicol. 2007, 84, 415-430
19. Wang, J. X.; Zhou, G. Q.; Chen, C. Y.; Yu, H. W.; Wang, T. C.; Ma, Y. M.; Jia, G.; Gao, Y. X.; Li, B.; Sun, J.; Li, Y. F.; Jia, F.; Zhao, Y. L.; Chai, Z. F. Acute toxicity and biodistribution of different sized titanium dioxide particles in mice after oral administration Toxicol. Lett. 2007, 168, 176-185
20. 2 Nanosacle Res. Lett. 2009, 4, 1275-1285
21. Duan, Y. M.; Liu, J.; Ma, L. L.; Li, N.; Liu, H. T.; Wang, J.; Zheng, L.; Liu, C.; Wang, X. F.; Zhang, X. G.; Yan, J. Y.; Wang, H.; Hong, F. S. Toxicological characteristics of nanoparticulate anatase titanium dioxide in mice Biomaterials 2010, 31, 894-899
22. Cui, Y. L.; Gong, X. L.; Duan, Y. M.; Li, N.; Hu, R. P.; Liu, H. T.; Hong, M. M.; Zhou, M.; Wang, L.; Wang, H.; Hong, F. S. Hepatocyte apoptosis and its molecular mechanisms in mice caused by titanium dioxide nanoparticles J. Hazard. Mater. 2010, 183, 874-880
23. 2 nanoparticules J. Biomed. Mater. Res. Part A 2011, 96 (1) 221-229
24. Cui, Y. L.; Liu, H. T.; Ze, Y. G.; Zhang, Z. L.; Hu, Y. Y.; Cheng, Z.; Cheng, J.; Hu, R. P.; Gao, G. D.; Wang, L.; Tang, M.; Hong, F. S. Gene expression in liver injury caused by long-term exposure to titanium dioxide nanoparticles in mice Toxicol. Sci. 2012, 128 (1) 171-185
25. 2 and liver DNA from mice in vivo Nanoscale Res. Lett. 2010, 5, 108-115
26. 2 to mice: liver injury, oxidative stress Toxicol. Environ. Chem. 2010, 92, 175-186
27. Li, N.; Duan, Y. M.; Hong, M. M.; Zheng, L.; Fei, M.; Zhao, X. Y.; Wang, Y.; Cui, Y. L.; Liu, H. T.; Cai, J. W.; Gong, S. J.; Wang, H.; Hong, F. S. Spleen injury and apoptotic pathway in mice caused by titanium dioxide nanoparticles Toxicol. Lett. 2010, 195, 161-168
28. 2 Biol. Trace Elem. Res. 2011, 140, 186-197
29. Sang, X. Z.; Zheng, L.; Sun, Q. Q.; Li, N.; Cui, Y. L.; Hu, R. P.; Gao, G. D.; Cheng, Z.; Cheng, J.; Gui, S. X.; Liu, H. T.; Zhang, Z. L.; Hong, F. S. The chronic spleen injury of mice following long-term exposure to titanium dioxide nanoparticles J. Biomed. Mater. Res. Part A 2012, 100A (4) 894-902
30. Sang, X. Z.; Li, B.; Ze, Y. G.; Hong, J.; Ze, X.; Gui, S. X.; Sun, Q. Q.; Liu, H. T.; Zhao, X. Y.; Sheng, L.; Liu, D.; Yu, X. H.; Hong, F. S. Toxicological effects of nanosized titanium dioxide-induced spleen injury in mice J. Agric. Food Chem. 2013, 61 (23) 5590-5599
31. Yu, Y.; Ren, W.; Ren, B. Nanosize titanium dioxide cause neuronal apoptosis: a potential linkage between nanoparticle exposure and neural disorder Neurol. Res. 2008, 10.1179/17431 3208X 305391
32. 2 nanoparticles in hairless mice and porcine skin after subchronic dermal exposure Toxicol. Lett. 2009, 191, 1-8
33. 2 delivered to the abdominal cavity Biomaterials 2010, 31, 99-105
34. 2 nanoparticles Biomaterials 2010, 31, 8043-8050
35. Hu, R. P.; Zheng, L.; Zhang, T.; Cui, Y. L.; Gao, G. D.; Cheng, Z.; Chen, J.; Tang, M.; Hong, F. S. Molecular mechanism of hippocampal apoptosis of mice following exposure to titanium dioxide nanoparticles J. Hazard. Mater. 2011, 191, 32-40
36. Shin, J. A.; Lee, E. J.; Seo, S. M.; Kim, H. S.; Kang, J. L.; Park, E. M. Nanosized titanium dioxide enhanced inflammatory responses in the septic brain of mouse Neuroscience 2010, 165, 445-454
37. Ze, Y. G.; Zheng, L.; Zhao, X. Y.; Gui, S. X.; Sang, X. Z.; Su, J. J.; Guan, N.; Zhu, L. Y.; Sheng, L.; Hu, R. P.; Cheng, J.; Cheng, Z.; Sun, Q. Q.; Wang, L.; Hong, F. S. Molecular mechanism of titanium dioxide nanoparticles-induced oxidative injury in the brain of mice Chemosphere 2013, 92, 1183-1189
38. Ze, Y. G.; Hu, R. P.; Wang, X. C.; Sang, X. Z.; Ze, X.; Li, B.; Su, J. J.; Wang, Y.; Guan, N.; Zhao, X. Y.; Gui, S. X.; Zhu, L. Y.; Cheng, Z.; Cheng, J.; Sheng, L.; Sun, Q. Q.; Wang, L.; Hong, F. S. Neurotoxicity and gene-expressed profile in brain injured mice caused by exposure to titanium dioxide nanoparticles J. Biomed. Mater. Res. Part A 2013, 10.1002/jbm.a.34705
39. Gao, G. D.; Ze, Y. G.; Li, B.; Zhao, X. Y.; Zhang, T.; Sheng, L.; Hu, R. P.; Gui, S. X.; Sang, X. Z.; Sun, Q. Q.; Cheng, J.; Cheng, Z.; Wang, L.; Tang, M.; Hong, F. S. Ovarian dysfunction and gene-expressed characteristics of female mice caused by long-term exposure to titanium dioxide nanoparticles J. Hazard. Mater. 2012, 243, 19-27
40. 2-induced reproductive system dysfunction and its mechanism in female mice PLoS One 2013, 8 (4) e59378
41. Sheng, L.; Wang, X. C.; Sang, X. Z.; Ze, Y. G.; Zhao, X. Y.; Liu, D.; Gui, S. X.; Sun, Q. Q.; Cheng, J.; Cheng, Z.; Hu, R. P.; Wang, L.; Hong, F. S. Cardiac oxidative damage in mice following exposure to nanoparticlate titanium dioxide J. Biomed. Mater. Res. Part A 2013, 10.1002/jbm.a.34634
42. Scown, T. M.; van Aerle, R. Y.; Johnston, B. D.; Cumberland, S.; Lead, J. R.; Richard, O.; Tyler, C. R. High doses of intravenously administered titanium dioxide nanoparticles accumulate in the kidneys of rainbow trout but with no observable impairment of renal function Toxicol. Sci. 2009, 109, 372-380
43. Chen, J. Y.; Dong, X.; Zhao, J.; Tang, G. P. In vivo acute toxicity of titanium dioxide nanoparticles to mice after intraperitoneal injection J. Appl. Toxicol. 2009, 29, 330-337
44. 2 particles Biol. Trace Elem. Res. 2009, 129, 170-180
45. 2 J. Exp. Nanosci. 2010, 5 (5) 447-462
46. Gui, S. X.; Zhang, Z. L.; Zheng, L.; Sun, Q. Q.; Sang, X. Z.; Liu, X. R.; Gao, G. D.; Cui, Y. L.; Cheng, Z.; Cheng, J.; Tang, M.; Hong, F. S. The molecular mechanism of kidney injury of mice caused by exposure to titanium dioxide nanoparticles J. Hazard. Mater. 2011, 195, 365-370
47. Gui, S. X.; Sang, X. Z.; Zheng, L.; Ze, Y. G.; Zhao, X. Y.; Sheng, L.; Sun, Q. Q.; Cheng, Z.; Cheng, J.; Hu, R. P.; Wang, L.; Hong, F. S.; Tang, M. Intragastric exposure to titanium dioxide nanoparticles induced nephrotoxicity in mice, assessed by physiological and gene expression modifications Particle Fibre Toxicol. 2013, 10, 4
48. Li, W.; Khor, T. O.; Xu, C.; Shen, G.; Jeong, W. S.; Yu, S.; Kong, A. N. Activation of Nrf2-antioxidant signaling attenuates NF-κB-inflammatory response and elicits apoptosis Biochem. Pharmacol. 2008, 76, 1485-1489
49. Sen, C. K.; Packer, L. Antioxidant and redox regulation of gene transcription FASEB J. 1996, 10, 709-720
50. Yang, H.; Magilnick, N.; Lee, C.; Kalmaz, D.; Ou, X.; Chan, J.; Lu, S. Nrf1 and Nrf2 regulate rat glutamate-cysteine ligase catalytic subunit transcription indirectly via NF-κB and AP-1 Mol. Cell. Biol. 2005, 25, 5933-5946
51. Maines, M. D. Heme oxygenase: function, multiplicity, regulatory mechanism, and clinical applications FASEB J. 1988, 2, 2557-2568
52. Cantoni, L.; Rossi, C.; Rizzardini, M.; Gardina, M.; Ghezzi, P. Interleukin-1 and tumor necrosis factor induce hepatic haeme oxygenase Biochem. J. 1991, 279, 891-894
53. Okinaga, S.; Takahashi, K.; Takeda, K.; Yoshizawa, M.; Fujita, H.; Sasaki, H.; Shibahara, S. Regulation of human heme oxygenase-1 gene expression under thermal stress Blood 1996, 87, 5074-5084
54. Maines, M. D. The heme oxygenase system: a regulator of second messenger gases Annu. Rev. Pharmacol. Toxicol. 1997, 37, 517-554
55. Willis, D.; Moore, A. R.; Frederick, R.; Willoughby, D. A. Heme oxygenase: a novel target for the modulation of the inflammatory response Nat. Med. 1996, 2, 87-90
56. Chen, K.; Gunter, K.; Maines, M. D. Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death J. Neurochem. 2002, 75 (1) 304-313
57. Okouchi, M.; Okayama, N.; Alexander, J. S.; Aw, T. Y. Nrf2-dependent glutamate- l -cysteine ligase catalytic subunit expression mediates insulin protection against hyperglycemia-induced brain endothelial cell apoptosis Curr. Neurovasc. Res. 2006, 3, 249-261
58. Itoh, K.; Chiba, T.; Takahashi, S.; Ishii, T.; Igarashi, K.; Katoh, Y.; Oyake, T.; Hayashi, N.; Satoh, K.; Hatayama, I.; Yamamoto, M.; Nabeshima, Y. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements Biochem. Biophys. Res. Commun. 1997, 236, 313-322
59. Yachie, A.; Niida, Y.; Wada, T.; Igarashi, N.; Kaneda, H.; Toma, T.; Ohta, K.; Kasahara, Y.; Koizumi, S. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency Clin. Invest. 1999, 103 (1) 129-135
60. Chan, K.; Han, X. D.; Kan, Y. W. An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 4611-4616
61. Kim, Y. C.; Masutani, H.; Yamaguchi, Y.; Itoh, K.; Yamamoto, M.; Yodoi, J. Hemin induced activation of the thioredoxin gene by Nrf2. A differential regulation of the antioxidant responsive element by a switch of its binding factors J. Biol. Chem. 2010, 276, 18399-18406
62. Kostaropoulos, I.; Papadopoulos, A. I.; Metaxakis, A.; Bouk-ouvala, E.; Papadopoulou-Mourkidou, E. Glutathione S -transferase in the defence against pyrethroids in insects Insect Biochem. Mol. Biol. 2001, 31, 313-319
63. Hemingway, J.; Hawkes, N. J.; McCarroll, L.; Ranson, H. The molecular basis of insecticide resistance in mosquitoes Insect Biochem. Mol. Biol. 2004, 34, 653-665
64. Hurst, R.; Bao, Y.; Jemth, P.; Mannervik, B.; Williamson, G. Phospholipid hydroperoxide glutathione peroxidase activity of human glutathione transferases Biochem. J. 1998, 332, 97-100
65. Sivori, J. L.; Casabe, N.; Zerba, E. N.; Wood, E. J. Induction of glutathione S -transferase activity in Triatoma infestans Mem. Inst. Oswaldo Cruz 1997, 92, 797-802
66. 3+ ions for photocatalysis Mater. Lett. 2002, 57, 794-801
67. Oliveira, C. P.; Lopasso, F. P.; Laurindo, F. R.; Leitao, R. M.; Laudanna, A. A. Protection against liver ischemia-reperfusion injury in rats by silymarin or verapamil Transplant. Proc. 2001, 33, 3010-3014
68. Nourooz-Zadeh, J.; Tajaddini-Sarmadi, J.; Wolff, S. P. Measurement of plasma hydroperoxide concentrations by the ferrous oxidation-xylenol orange assay in conjunction with triphenylphosphine Anal. Biochem. 1994, 220, 403-409
69. Buege, J. A.; Aust, S. D. Microsomal lipid peroxidation Methods Enzymol. 1978, 52, 302-310
70. Fagan, J. M.; Bogdan, G. S.; Sohar, I. Quantitation of oxidative damage to tissue proteins Int. J. Biochem. Cell Biol. 1999, 31, 751-757
71. Hissin, P. J.; Hilf, R. A. Fluorometric method for determination of oxidized and reduced glutathione in tissues Anal. Biochem. 1976, 74, 214-226
72. Ke, L. D.; Chen, Z.; Yung, W. K. A. A reliability test of standard-based quantitative PCR: exogenous vs endogenous standards Mol. Cell Probes 2000, 14, 127-135
73. Livak, K. J.; Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T) (-ΔΔC) method Methods 2001, 25, 402-408
74. Liu, W. H.; Saint, D. A. Validation of a quantitative method for real time PCR kinetics Biochem. Biophys. Res. Commun. 2002, 294, 347-353
75. Benani, A.; Troy, S.; Carmona, M. C.; Fioramonti, X.; Lorsignol, A.; Leloup, C.; Casteilla, L.; Pénicaud, L. Role for mitochondrial reactive oxygen species in brain lipid sensing: redox regulation of food intake Diabetes 2007, 56, 152-160
76. Wolfgang, M. J.; Cha, S. H.; Sidhaye, A.; Chohnan, S.; Cline, G.; Shulman, G. I.; Lane, M. D. Regulation of hypothalamic malonyl-CoA by central glucose and leptin Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 19285-19290
77. Leloup, C.; Magnan, C.; Benani, A.; Bonnet, E.; Alquier, T.; Offer, G.; Carriere, A.; Périquet, A.; Fernandez, Y.; Ktorza, A.; Casteilla, L.; Pénicaud, L. Mitochondrial reactive oxygen species are required for hypothalamic glucose sensing Diabetes 2006, 55, 2084-2090
78. Sardari, R. R. R.; Zarchi, S. R.; Talebi, A.; Nasri, S.; Imani, S.; Khoradmehr, A.; Sheshde, S. A. R. Toxicological effects of silver nanoparticles in rats Afr. J. Microbiol. Res. 2012, 6 (27) 5587-5593
79. Valko, M.; Rhodes, C. J.; Moncol, J.; Izakovic, M.; Mazur, M. Free radicals, metals and antioxidants in oxidative stress-induced cancer Chem. Biol. Interact. 2006, 160, 1-40
80. Yoh, K.; Itoh, K.; Enamoto, A.; Hirayama, A.; Yamaguchi, N.; Kobayashi, M.; Morito, N.; Koyama, A.; Yamamoto, M.; Takahashi, S. Nrf2-deficient female mice develop lupus-like autoimmune nephritis Kidney Int. 2001, 50, 1343-1353
81. Yoh, K.; Hirayama, A.; Ishizaki, K.; Yamada, A.; Takeuchi, M.; Yamagishi, S.; Morito, N.; Nakano, T.; Ojima, M.; Shimohata, H.; Itoh, K.; Takahashi, S.; Yamamoto, M. Hyperglycemia induces oxidative and nitrosative stress and increases renal functional impairment in Nrf2-deficient mice Genes Cells 2008, 13, 1159-1170
82. Morse, D.; Choi, A. M. Heme oxygenase-1: the "emerging molecule" has arrived Am. J. Respir. Cell Mol. Biol. 2002, 27, 8-16
83. Otterbein, L. E.; Soares, M. P.; Yamashita, K.; Bach, F. H. Heme oxygenase-1: unleashing the protective properties of heme Trends Immunol. 2003, 24, 449-455
84. Chen, C. Y.; Jang, J. H.; Li, M. H.; Surh, Y. J. Resveratrol upregulates heme oxygenase-1 expression via activation of NF-E2-related factor 2 in PC12 cells Biochem. Biophys. Res. Commun. 2005, 331, 993-1000
85. Griffith, O. W.; Mulcahy, R. T. The enzymes of glutathione synthesis:γ-glutamylcysteine synthetase Adv. Enzymol. Relat. Areas Mol. Biol. 1999, 73, 209-267
86. Lee, J. S.; Surh, Y. J. Nrf2 as a novel molecular target for chemoprevention Cancer Lett. 2005, 224, 171-184
87. Lim, H. J.; Lee, K. S.; Lee, S.; Park, J. H.; Choi, H. E.; Go, S. H.; Kwak, H. J.; Park, H. Y. 15d-PGJ2 stimulates HO-1 expression through p38 MAP kinase and Nrf-2 pathway in rat vascular smooth muscle cells Toxicol. Appl. Pharmacol. 2007, 223, 20-27
88. Itoh, K.; Wakabayashi, N.; Katoh, Y.; Ishii, T.; O'connor, T.; Yamamoto, M. Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles Genes Cells 2003, 8, 379-391
89. Hayden, M. S.; Ghosh, S. Shared principles in NF-κB signaling Cell 2008, 132, 344-362
90. Karin, M.; Yamamoto, Y.; Wang, Q. M. The IKK NF-κB system: a treasure trove for drug development Nat. Rev. Drug Discov. 2004, 3, 17-26
91. Smith, W. L.; Michael Garavito, R.; DeWit, D. L. Prostaglandin endoperoxide H syntheses (cyclooxygenases)-1 and -2 J. Biol. Chem. 1996, 271 (52) 33157-33160
92. Tanabe, T.; Tohnai, N. Cyclooxygenase isozymes and their gene structures and expression Prostaglandins Other Lipid Mediat. 2002, 68-69, 95-114
93. Park, G. Y.; Christman, J. W. Involvement of cyclooxygenase-2 and prostaglandins in the molecular pathogenesis of inflammatory lung diseases Am. J. Physiol. Lung Cell Mol. Physiol. 2006, 290, L797-L805
94. Rahman, I.; Biswas, S. K.; Kode, A. Oxidant and antioxidant balance in the airways and airway diseases Eur. J. Pharmacol. 2006, 533 (1-3) 222-239
95. Leeand, I. T.; Yang, C. M. Role of NADPH oxidase/ROSin pro-inflammatory mediators-induced airway and pulmonary diseases Biochem. Pharmacol. 2012, 84 (5) 581-590
96. Rieber, N.; Hector, A.; Kuijpers, T.; Roos, D.; Hartl, D. Current concepts of hyperinflammation in chronic granulomatous disease Clin. Dev. Immunol. 2012, 2012, 252460
97. Dworski, R.; Han, W.; Blackwell, T. S.; Hoskins, A.; Freeman, M. L. Vitamin E prevents Nrf2 suppression by allergens in asthmatic alveolar macrophages in vivo Free Radical Biol. Med. 2011, 51, 516-521
98. Yu, M.; Li, H.; Liu, Q.; Liu, F.; Tang, L.; Li, C.; Yuan, Y.; Zhan, Y.; Xu, W.; Li, W.; Chen, H.; Ge, C.; Wang, J.; Yang, X. Nuclear factor p65 interacts with Keap1 to repress the Nrf2-ARE pathway Cell Signal 2011, 23, 883-892