Identification of aldo-keto reductases as NRF2-target marker genes in human cells

Toxicology Letters

Volumn 218, Issue 1, 2013, Pages 39-49

  Jung, Kyeong Ah ^a   Choi, Bo hyun ^a   Nam, Chang Won ^b   Song, Mingu ^b   Kim, Sang Tae ^a   Lee, Joo Young ^a   Kwak, Mi Kyoung ^a  

^a The Catholic University of Korea   (South Korea)

^b Yeungnam University   (South Korea)

Author keywords

Aldo keto reductases; Human monocytic cells; Human renal epithelial cells; Inducers; KEAP1; NRF2

Indexed keywords

ALDEHYDE KETONE REDUCTASE; ALDEHYDE REDUCTASE; ALDOKETOREDUCTASE 1A1; ALDOKETOREDUCTASE 1B1; ALDOKETOREDUCTASE 1B10; ALDOKETOREDUCTASE 1C1; ALDOKETOREDUCTASE 1C2; ALDOKETOREDUCTASE 1C3; CD14 ANTIGEN; CINNAMALDEHYDE; HYDROGEN PEROXIDE; KELCH LIKE ECH ASSOCIATED PROTEIN 1; OXIDOREDUCTASE; SULFORAPHANE; TERT BUTYLHYDROQUINONE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ARTICLE; BLOOD CELL; CELL LINE; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; EPITHELIUM CELL; GENE EXPRESSION; GENE IDENTIFICATION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; KIDNEY EPITHELIAL CELL; KIDNEY EPITHELIUM; LEUKEMIA CELL LINE; MONOCYTIC LEUKEMIA; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STABILITY;

20-HYDROXYSTEROID DEHYDROGENASES; ACROLEIN; ALDEHYDE REDUCTASE; BIOLOGICAL MARKERS; ENZYME INDUCTION; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; GENETIC MARKERS; HUMANS; HYDROGEN PEROXIDE; HYDROQUINONES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KIDNEY TUBULES, PROXIMAL; LEUKEMIA, MONOCYTIC, ACUTE; MONOCYTES; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; THIOCYANATES; U937 CELLS;

EID: 84873443918     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2012.12.026     Document Type: Article

References (56)

1. Agyeman A.S., Chaerkady R., Shaw P.G., Davidson N.E., Visvanathan K., Pandey A., Kensler T.W. Transcriptomic and proteomic profiling of KEAP1 disrupted and sulforaphane-treated human breast epithelial cells reveals common expression profiles. Breast Cancer Research and Treatment 2012, 132:175-187.
2. Aoki Y., Sato H., Nishimura N., Takahashi S., Itoh K., Yamamoto M. Accelerated DNA adduct formation in the lung of the Nrf2 knockout mouse exposed to diesel exhaust. Toxicology and Applied Pharmacology 2001, 173:154-160.
3. Arisawa T., Tahara T., Shibata T., Nagasaka M., Nakamura M., Kamiya Y., Fujita H., Yoshioka D., Okubo M., Sakata M., Wang F.Y., Hirata I., Nakano H. Nrf2 gene promoter polymorphism is associated with ulcerative colitis in a Japanese population. Hepato-Gastroenterology 2008, 55:394-397.
4. Bains J.S., Shaw C.A. Neurodegenerative disorders in humans: the role of glutathione in oxidative stress-mediated neuronal death. Brain Research. Brain Research Reviews 1997, 25:335-358.
5. Bains O.S., Grigliatti T.A., Reid R.E., Riggs K.W. Naturally occurring variants of human aldo-keto reductases with reduced in vitro metabolism of daunorubicin and doxorubicin. Journal of Pharmacology and Experimental Therapeutics 2010, 335:533-545.
6. Barski O.A., Tipparaju S.M., Bhatnagar A. The aldo-keto reductase superfamily and its role in drug metabolism and detoxification. Drug Metabolism Reviews 2008, 40:553-624.
7. Becks L., Prince M., Burson H., Christophe C., Broadway M., Itoh K., Yamamoto M., Mathis M., Orchard E., Shi R., McLarty J., Pruitt K., Zhang S., Kleiner-Hancock H.E. Aggressive mammary carcinoma progression in Nrf2 knockout mice treated with 7,12-dimethylbenz[a]anthracene. BMC Cancer 2010, 10:540.
8. Bonnesen C., Eggleston I.M., Hayes J.D. Dietary indoles and isothiocyanates that are generated from cruciferous vegetables can both stimulate apoptosis and confer protection against DNA damage in human colon cell lines. Cancer Research 2001, 61:6120-6130.
9. Burczynski M.E., Lin H.K., Penning T.M. Isoform-specific induction of a human aldo-keto reductase by polycyclic aromatic hydrocarbons (PAHs), electrophiles, and oxidative stress: implications for the alternative pathway of PAH activation catalyzed by human dihydrodiol dehydrogenase. Cancer Research 1999, 59:607-614.
10. Chan K., Kan Y.W. Nrf2 is essential for protection against acute pulmonary injury in mice. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:12731-12736.
11. Chen J., Emara N., Solomides C., Parekh H., Simpkins H. Resistance to platinum-based chemotherapy in lung cancer cell lines. Cancer Chemotherapy and Pharmacology 2010, 66:1103-1111.
12. Cho H.Y., Jedlicka A.E., Reddy S.P., Kensler T.W., Yamamoto M., Zhang L.Y., Kleeberger S.R. Role of NRF2 in protection against hyperoxic lung injury in mice. American Journal of Respiratory Cell and Molecular Biology 2002, 26:175-182.
13. Cordova E.J., Velazquez-Cruz R., Centeno F., Baca V., Orozco L. The NRF2 gene variant, -653G/A, is associated with nephritis in childhood-onset systemic lupus erythematosus. Lupus 2010, 19:1237-1242.
14. Devling T.W., Lindsay C.D., McLellan L.I., McMahon M., Hayes J.D. Utility of siRNA against Keap1 as a strategy to stimulate a cancer chemopreventive phenotype. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:7280-7285A.
15. Enomoto A., Itoh K., Nagayoshi E., Haruta J., Kimura T., O'Connor T., Harada T., Yamamoto M. High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicological Sciences 2001, 59:169-177.
16. Fourquet S., Guerois R., Biard D., Toledano M.B. Activation of NRF2 by nitrosative agents and H2O2 involves KEAP1 disulfide formation. Journal of Biological Chemistry 2010, 285:8463-8471.
17. Hayes J.D., McMahon M., Chowdhry S., Dinkova-Kostova A.T. Cancer chemoprevention mechanisms mediated through the Keap1-Nrf2 pathway. Antioxidants and Redox Signalling 2010, 13:1713-1748.
18. Herrling T., Fuchs J., Rehberg J., Groth N. UV-induced free radicals in the skin detected by ESR spectroscopy and imaging using nitroxides. Free Radical Biology and Medicine 2003, 35:59-67.
19. Hiura T.S., Kaszubowski M.P., Li N., Nel A.E. Chemicals in diesel exhaust particles generate reactive oxygen radicals and induce apoptosis in macrophages. Journal of Immunology 1999, 163:5582-5591.
20. Hong F., Sekhar K.R., Freeman M.L., Liebler D.C. Specific patterns of electrophile adduction trigger Keap1 ubiquitination and Nrf2 activation. Journal of Biological Chemistry 2005, 280:31768-31775.
21. 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. Biochemical and Biophysical Research Communications 1997, 236:313-322.
22. Itoh K., Mimura J., Yamamoto M. Discovery of the negative regulator of Nrf2, Keap1: a historical overview. Antioxidants and Redox Signalling 2010, 13:1665-1678.
23. Jung K.A., Kwak M.K. The Nrf2 system as a potential target for the development of indirect antioxidants. Molecules 2010, 15:7266-7291.
24. Khor T.O., Huang M.T., Kwon K.H., Chan J.Y., Reddy B.S., Kong A.N. Nrf2-deficient mice have an increased susceptibility to dextran sulfate sodium-induced colitis. Cancer Research 2006, 66:11580-11584.
25. Kim T.H., Hur E.G., Kang S.J., Kim J.A., Thapa D., Lee Y.M., Ku S.K., Jung Y., Kwak M.K. NRF2 blockade suppresses colon tumor angiogenesis by inhibiting hypoxia-induced activation of HIF-1alpha. Cancer Research 2011, 71:2260-2275.
26. Kitamura Y., Umemura T., Kanki K., Kodama Y., Kitamoto S., Saito K., Itoh K., Yamamoto M., Masegi T., Nishikawa A., Hirose M. Increased susceptibility to hepatocarcinogenicity of Nrf2-deficient mice exposed to 2-amino-3-methylimidazo[4,5-f]quinoline. Cancer Science 2007, 98:19-24.
27. Klaunig J.E., Xu Y., Bachowski S., Ketcham C.A., Isenberg J.S., Kolaja K.L., Baker T.K., Walborg E.F., Stevenson D.E. Oxidative stress in nongenotoxic carcinogenesis. Toxicology Letters 1995, 82-83:683-691.
28. Kobayashi M., Yamamoto M. Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxidants and Redox Signalling 2005, 7:385-394.
29. Kraft A.D., Johnson D.A., Johnson J.A. Nuclear factor E2-related factor 2-dependent antioxidant response element activation by tert-butylhydroquinone and sulforaphane occurring preferentially in astrocytes conditions neurons against oxidative insult. Journal of Neuroscience 2004, 24:1101-1112.
30. Kwak M.K., Wakabayashi N., Itoh K., Motohashi H., Yamamoto M., Kensler T.W. Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway. Identification of novel gene clusters for cell survival. Journal of Biological Chemistry 2003, 278:8135-8145.
31. Kwak M.K., Wakabayashi N., Kensler T.W. Chemoprevention through the Keap1-Nrf2 signaling pathway by phase 2 enzyme inducers. Mutation Research 2004, 555:133-148.
32. Li J., Lee J.M., Johnson J.A. Microarray analysis reveals an antioxidant responsive element-driven gene set involved in conferring protection from an oxidative stress-induced apoptosis in IMR-32 cells. Journal of Biological Chemistry 2002, 277:388-394.
33. Li W., Kong A.N. Molecular mechanisms of Nrf2-mediated antioxidant response. Molecular Carcinogenesis 2009, 48:91-104.
34. Lou H., Du S., Ji Q., Stolz A. Induction of AKR1C2 by phase II inducers: identification of a distal consensus antioxidant response element regulated by NRF2. Molecular Pharmacology 2006, 69:1662-1672.
35. MacLeod A.K., McMahon M., Plummer S.M., Higgins L.G., Penning T.M., Igarashi K., Hayes J.D. Characterization of the cancer chemopreventive NRF2-dependent gene battery in human keratinocytes: demonstration that the KEAP1-NRF2 pathway, and not the BACH1-NRF2 pathway, controls cytoprotection against electrophiles as well as redox-cycling compounds. Carcinogenesis 2009, 30:1571-1580.
36. Marnett L.J., Riggins J.N., West J.D. Endogenous generation of reactive oxidants and electrophiles and their reactions with DNA and protein. Journal of Clinical Investigation 2003, 111:583-593.
37. Marzec J.M., Christie J.D., Reddy S.P., Jedlicka A.E., Vuong H., Lanken P.N., Aplenc R., Yamamoto T., Yamamoto M., Cho H.Y., Kleeberger S.R. Functional polymorphisms in the transcription factor NRF2 in humans increase the risk of acute lung injury. FASEB Journal 2007, 21:2237-2246.
38. McMahon M., Lamont D.J., Beattie K.A., Hayes J.D. Keap1 perceives stress via three sensors for the endogenous signaling molecules nitric oxide, zinc, and alkenals. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:18838-18843.
39. Mindnich R.D., Penning T.M. Aldo-keto reductase (AKR) superfamily: genomics and annotation. Human Genomics 2009, 3:362-370.
40. Okawa H., Motohashi H., Kobayashi A., Aburatani H., Kensler T.W., Yamamoto M. Hepatocyte-specific deletion of the keap1 gene activates Nrf2 and confers potent resistance against acute drug toxicity. Biochemical and Biophysical Research Communications 2006, 339:79-88.
41. Osburn W.O., Karim B., Dolan P.M., Liu G., Yamamoto M., Huso D.L., Kensler T.W. Increased colonic inflammatory injury and formation of aberrant crypt foci in Nrf2-deficient mice upon dextran sulfate treatment. International Journal of Cancer 2007, 121:1883-1891.
42. Penning T.M., Byrns M.C. Steroid hormone transforming aldo-keto reductases and cancer. Annals of the New York Academy of Sciences 2009, 1155:33-42.
43. Penning T.M., Drury J.E. Human aldo-keto reductases: Function, gene regulation, and single nucleotide polymorphisms. Archives of Biochemistry and Biophysics 2007, 464:241-250.
44. Rahman I., MacNee W. Lung glutathione and oxidative stress: implications in cigarette smoke-induced airway disease. American Journal of Physiology 1999, 277:L1067-L1088.
45. Ramos-Gomez M., Kwak M.K., Dolan P.M., Itoh K., Yamamoto M., Talalay P., Kensler T.W. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:3410-3415.
46. Rangasamy T., Misra V., Zhen L., Tankersley C.G., Tuder R.M., Biswal S. Cigarette smoke-induced emphysema in A/J mice is associated with pulmonary oxidative stress, apoptosis of lung cells, and global alterations in gene expression. American Journal of Physiology. Lung Cellular and Molecular Physiology 2009, 296:L888-L900.
47. Reisman S.A., Yeager R.L., Yamamoto M., Klaassen C.D. Increased Nrf2 activation in livers from Keap1-knockdown mice increases expression of cytoprotective genes that detoxify electrophiles more than those that detoxify reactive oxygen species. Toxicological Sciences 2009, 108:35-47.
48. Ryan M.J., Johnson G., Kirk J., Fuerstenberg S.M., Zager R.A., Torok-Storb B. HK-2: an immortalized proximal tubule epithelial cell line from normal adult human kidney. Kidney International 1994, 45:48-57.
49. Tan X.L., Spivack S.D. Dietary chemoprevention strategies for induction of phase II xenobiotic-metabolizing enzymes in lung carcinogenesis: a review. Lung Cancer 2009, 65:129-137.
50. Thimmulappa R.K., Mai K.H., Srisuma S., Kensler T.W., Yamamoto M., Biswal S. Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Research 2002, 62:5196-5203.
51. Vondracek J., Krcmar P., Prochazkova J., Trilecova L., Gavelova M., Skalova L., Szotakova B., Buncek M., Radilova H., Kozubik A., Machala M. The role of aryl hydrocarbon receptor in regulation of enzymes involved in metabolic activation of polycyclic aromatic hydrocarbons in a model of rat liver progenitor cells. Chemico-Biological Interactions 2009, 180:226-237.
52. Wakabayashi N., Dinkova-Kostova A.T., Holtzclaw W.D., Kang M.L., Kobayashi A., Yamamoto M., Kensler T.W., Talalay P. Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:2040-2045.
53. Wakabayashi N., Slocum S.L., Skoko J.J., Shin S., Kensler T.W. When NRF2 talks, who's listening?. Antioxidants and Redox Signalling 2010, 13:1649-1663.
54. Wondrak G.T., Villeneuve N.F., Lamore S.D., Bause A.S., Jiang T., Zhang D.D. The cinnamon-derived dietary factor cinnamic aldehyde activates the Nrf2-dependent antioxidant response in human epithelial colon cells. Molecules 2010, 15:3338-3355.
55. Xu C., Huang M.T., Shen G., Yuan X., Lin W., Khor T.O., Conney A.H., Kong A.N. Inhibition of 7,12-dimethylbenz(a)anthracene-induced skin tumorigenesis in C57BL/6 mice by sulforaphane is mediated by nuclear factor E2-related factor 2. Cancer Research 2006, 66:8293-8296.
56. Yeh C.T., Yen G.C. Effect of sulforaphane on metallothionein expression and induction of apoptosis in human hepatoma HepG2 cells. Carcinogenesis 2005, 26:2138-2148.