Identification of Nrf2-regulated genes induced by chemopreventive isothiocyanate PEITC by oligonucleotide microarray

Life Sciences

Volumn 79, Issue 20, 2006, Pages 1944-1955

  Hu, Rong ^a   Xu, Changjiang ^a   Shen, Guoxiang ^a   Jain, Mohit R ^a   Khor, Tin Oo ^a   Gopalkrishnan, Avantika ^a   Lin, Wen ^a   Reddy, Bandaru ^a   Chan, Jefferson Y ^b   Kong, Ah Ng Tony ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Gene expression profile; Microarray; Nrf2; PEITC, antioxidant response element; Phase II detoxifying genes; Real time PCR

Indexed keywords

ALDEHYDE OXIDASE; ANTINEOPLASTIC AGENT; CYTOCHROME P450; CYTOCHROME P450 2C; CYTOCHROME P450 2C55; CYTOCHROME P450 2U1; HEAT SHOCK PROTEIN; ISOTHIOCYANIC ACID; OXIDIZING AGENT; PHENETHYL ISOTHIOCYANATE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NRF2; UBIQUITIN; UNCLASSIFIED DRUG; XENOBIOTIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CANCER CHEMOTHERAPY; CHEMOPROPHYLAXIS; CONTROLLED STUDY; DETOXIFICATION; DNA MICROARRAY; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; LIPID METABOLISM; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN BINDING; PROTEIN DEFICIENCY; XENOBIOTIC METABOLISM;

ANIMALS; ANTICARCINOGENIC AGENTS; CHEMOPREVENTION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; ISOTHIOCYANATES; LIVER; METABOLIC DETOXICATION, PHASE II; MICE; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS;

EID: 33749263503     PISSN: 00243205     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.lfs.2006.06.019     Document Type: Article

References (69)

1. Alam J., Stewart D., Touchard C., Boinapally S., Choi A.M., and Cook J.L. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. Journal of Biological Chemistry 274 (1999) 26071-26078
2. Aoki Y., Sato H., Nishimura N., Takahashi S., Itoh K., and Yamamoto M. Accelerated DNA adduct formation in the lung of the Nrf2 knockout mouse exposed to diesel exhaust. Toxicology and Applied Pharmacology 173 (2001) 154-160
3. Barecki-Roach M., Wang E.J., and Johnson W.W. Quantitative evaluation of isothiocyanates as substrates and inhibitors of P-glycoprotein. Journal of Pharmacy and Pharmacology 55 (2003) 1251-1257
4. Braun S., Hanselmann C., Gassmann M.G., auf dem Keller U., Born-Berclaz C., Chan K., Kan Y.W., and Werner S. Nrf2 transcription factor, a novel target of keratinocyte growth factor action which regulates gene expression and inflammation in the healing skin wound. Molecular and Cellular Biology 22 (2002) 5492-5505
5. Bueno de Mesquita H.B., Maisonneuve P., Runia S., and Moerman C.J. Intake of foods and nutrients and cancer of the exocrine pancreas: a population-based case-control study in The Netherlands. International Journal of Cancer 48 (1991) 540-549
6. Chan K., and 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 96 (1999) 12731-12736
7. Chan K., Lu R., Chang J.C., and Kan Y.W. NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proceedings of the National Academy of Sciences of the United States of America 93 (1996) 13943-13948
8. Chan K., Han X.D., and Kan Y.W. An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proceedings of the National Academy of Sciences of the United States of America 98 (2001) 4611-4616
9. Chanas S.A., Jiang Q., McMahon M., McWalter G.K., McLellan L.I., Elcombe C.R., Henderson C.J., Wolf C.R., Moffat G.J., Itoh K., Yamamoto M., and Hayes J.D. Loss of the Nrf2 transcription factor causes a marked reduction in constitutive and inducible expression of the glutathione S-transferase Gsta1, Gsta2, Gstm1, Gstm2, Gstm3 and Gstm4 genes in the livers of male and female mice. Biochemical Journal 365 (2002) 405-416
10. Chen C., and Kong A.N. Dietary chemopreventive compounds and ARE/EpRE signaling. Free Radical Biology & Medicine 36 (2004) 1505-1516
11. Chiao J.W., Chung F., Krzeminski J., Amin S., Arshad R., Ahmed T., and Conaway C.C. Modulation of growth of human prostate cancer cells by the N-acetylcysteine conjugate of phenethyl isothiocyanate. International Journal of Oncology 16 (2000) 1215-1219
12. Chung F.L., Conaway C.C., Rao C.V., and Reddy B.S. Chemoprevention of colonic aberrant crypt foci in Fischer rats by sulforaphane and phenethyl isothiocyanate. Carcinogenesis 21 (2000) 2287-2291
13. Duffy S., So A., and Murphy T.H. Activation of endogenous antioxidant defenses in neuronal cells prevents free radical-mediated damage. Journal of Neurochemistry 71 (1998) 69-77
14. Enomoto A., Itoh K., Nagayoshi E., Haruta J., Kimura T., O'Connor T., Harada T., and 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 59 (2001) 169-177
15. Fahey J.W., Haristoy X., Dolan P.M., Kensler T.W., Scholtus I., Stephenson K.K., Talalay P., and Lozniewski A. Sulforaphane inhibits extracellular, intracellular, and antibiotic-resistant strains of Helicobacter pylori and prevents benzo[a]pyrene-induced stomach tumors. Proceedings of the National Academy of Sciences of the United States of America 99 (2002) 7610-7615
16. Forrest G.L., and Gonzalez B. Carbonyl reductase. Chem. Biol. Interact. vol. 129 (2000) 21-40
17. Gabai V.L., Meriin A.B., Mosser D.D., Caron A.W., Rits S., Shifrin V.I., and Sherman M.Y. Hsp70 prevents activation of stress kinases. A novel pathway of cellular thermotolerance. Journal of Biological Chemistry 272 (1997) 18033-18037
18. Gabai V.L., Meriin A.B., Yaglom J.A., Volloch V.Z., and Sherman M.Y. Role of Hsp70 in regulation of stress-kinase JNK: implications in apoptosis and aging. FEBS Letters 438 (1998) 1-4
19. Gamet-Payrastre L., Li P., Lumeau S., Cassar G., Dupont M.A., Chevolleau S., Gasc N., Tulliez J., and Terce F. Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in HT29 human colon cancer cells. Cancer Research 60 (2000) 1426-1433
20. Guo Z., Smith T.J., Wang E., Sadrieh N., Ma Q., Thomas P.E., and Yang C.S. Effects of phenethyl isothiocyanate, a carcinogenesis inhibitor, on xenobiotic-metabolizing enzymes and nitrosamine metabolism in rats. Carcinogenesis 13 (1992) 2205-2210
21. Hara M., Hanaoka T., Kobayashi M., Otani T., Adachi H.Y., Montani A., Natsukawa S., Shaura K., Koizumi Y., Kasuga Y., Matsuzawa T., Ikekawa T., Sasaki S., and Tsugane S. Cruciferous vegetables, mushrooms, and gastrointestinal cancer risks in a multicenter, hospital-based case-control study in Japan. Nutrition and Cancer 46 (2003) 138-147
22. Hayes J.D., Chanas S.A., Henderson C.J., McMahon M., Sun C., Moffat G.J., Wolf C.R., and Yamamoto M. The Nrf2 transcription factor contributes both to the basal expression of glutathione S-transferases in mouse liver and to their induction by the chemopreventive synthetic antioxidants, butylated hydroxyanisole and ethoxyquin. Biochemical Society Transactions 28 (2000) 33-41
23. Hershko A., and Ciechanover A. The ubiquitin system. Annual Review of Biochemistry 67 (1998) 425-479
24. Houry W.A. Chaperone-assisted protein folding in the cell cytoplasm. Curr. Protein Pept. Sci. vol. 2 (2001) 227-244
25. Hu K., and Morris M.E. Effects of benzyl-, phenethyl-, and alpha-naphthyl isothiocyanates on P-glycoprotein-and MRP1-mediated transport. Journal of Pharmaceutical Sciences 93 (2004) 1901-1911
26. Hu R., Kim B.R., Chen C., Hebbar V., and Kong A.N. The roles of JNK and apoptotic signaling pathways in PEITC-mediated responses in human HT-29 colon adenocarcinoma cells. Carcinogenesis 24 (2003) 1361-1367
27. Huang C., Ma W.Y., Li J., Hecht S.S., and Dong Z. Essential role of p53 in phenethyl isothiocyanate-induced apoptosis. Cancer Research 58 (1998) 4102-4106
28. Ishii T., Itoh K., Takahashi S., Sato H., Yanagawa T., Katoh Y., Bannai S., and Yamamoto M. Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. Journal of Biological Chemistry 275 (2000) 16023-16029
29. 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. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochemical and Biophysical Research Communications 236 (1997) 313-322
30. Ji Y., and Morris M.E. Effect of organic isothiocyanates on breast cancer resistance protein (ABCG2)-mediated transport. Pharmaceutical Research 21 (2004) 2261-2269
31. Johnson J.L., and Craig E.A. Protein folding in vivo: unraveling complex pathways. Cell 90 (1997) 201-204
32. Joseph M.A., Moysich K.B., Freudenheim J.L., Shields P.G., Bowman E.D., Zhang Y., Marshall J.R., and Ambrosone C.B. Cruciferous vegetables, genetic polymorphisms in glutathione S-transferases M1 and T1, and prostate cancer risk. Nutrition and Cancer 50 (2004) 206-213
33. Kensler T.W., Groopman J.D., Sutter T.R., Curphey T.J., and Roebuck B.D. Development of cancer chemopreventive agents: oltipraz as a paradigm. Chemical Research in Toxicology 12 (1999) 113-126
34. Keum Y.S., Owuor E.D., Kim B.R., Hu R., and Kong A.-N.T. Involvement of Nrf2 and JNK1 in the Activation of Antioxidant Responsive Element (ARE) by Chemopreventive Agent Phenethyl Isothiocyanate (PEITC). Pharmaceutical Research 20 9 (2003) 1351-1356
35. Kim Y.C., Masutani H., Yamaguchi Y., Itoh K., Yamamoto M., and 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. Journal of Biological Chemistry 276 (2001) 18399-18406
36. Kim B.R., Hu R., Keum Y.S., Hebbar V., and Shen G. Effects of Glutathione on Antioxidant Response Element-mediated Gene Expression and Apoptosis Elicited by Sulforaphane. Cancer Research 63 21 (2003) 7520-7525
37. Knights K.M., and Drogemuller C.J. Xenobiotic-CoA ligases: kinetic and molecular characterization. Current Drug Metabolism 1 (2000) 49-66
38. Kune G.A., Bannerman S., Field B., Watson L.F., Cleland H., Merenstein D., and Vitetta L. Diet, alcohol, smoking, serum beta-carotene, and vitamin A in male nonmelanocytic skin cancer patients and controls. Nutrition and Cancer 18 (1992) 237-244
39. Kwak M.K., Itoh K., Yamamoto M., Sutter T.R., and Kensler T.W. Role of transcription factor Nrf2 in the induction of hepatic phase 2 and antioxidative enzymes in vivo by the cancer chemoprotective agent, 3H-1, 2-dimethiole-3-thione. Molecular Medicine 7 (2001) 135-145
40. Kwak M.K., Wakabayashi N., Itoh K., Motohashi H., Yamamoto M., and 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 278 (2003) 8135-8145
41. Lee J.M., Moehlenkamp J.D., Hanson J.M., and Johnson J.A. Nrf2-dependent activation of the antioxidant responsive element by tert-butylhydroquinone is independent of oxidative stress in IMR-32 human neuroblastoma cells. Biochemical and Biophysical Research Communications 280 (2001) 286-292
42. Lee J.M., Hanson J.M., Chu W.A., and Johnson J.A. Phosphatidylinositol 3-kinase, not extracellular signal-regulated kinase, regulates activation of the antioxidant-responsive element in IMR-32 human neuroblastoma cells. Journal of Biological Chemistry 276 (2001) 20011-20016
43. McMahon M., Itoh K., Yamamoto M., Chanas S.A., Henderson C.J., McLellan L.I., Wolf C.R., Cavin C., and Hayes J.D. The Cap'n'Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes. Cancer Research 61 (2001) 3299-3307
44. Michaud D.S., Spiegelman D., Clinton S.K., Rimm E.B., Willett W.C., and Giovannucci E.L. Fruit and vegetable intake and incidence of bladder cancer in a male prospective cohort. Journal of the National Cancer Institute 91 (1999) 605-613
45. Michaud D.S., Pietinen P., Taylor P.R., Virtanen M., Virtamo J., and Albanes D. Intakes of fruits and vegetables, carotenoids and vitamins A, E, C in relation to the risk of bladder cancer in the ATBC cohort study. British Journal of Cancer 87 (2002) 960-965
46. Morse M.A., Eklind K.I., Hecht S.S., and Chung F.L. Inhibition of tobacco-specific nitrosamine 4-(N-nitrosomethylamino)-1-(3-pyridyl)-1-butanone (NNK) tumorigenesis with aromatic isothiocyanates. IARC Scientific Publications (1991) 529-534
47. Morse M.A., Eklind K.I., Amin S.G., and Chung F.L. Effect of frequency of isothiocyanate administration on inhibition of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone-induced pulmonary adenoma formation in A/J mice. Cancer Letter 62 (1992) 77-81
48. Nguyen T., Huang H.C., and Pickett C.B. Transcriptional regulation of the antioxidant response element. Activation by Nrf2 and repression by MafK. Journal of Biological Chemistry 275 (2000) 15466-15473
49. Oppermann U.C., and Maser E. Molecular and structural aspects of xenobiotic carbonyl metabolizing enzymes. Role of reductases and dehydrogenases in xenobiotic phase I reactions. Toxicology 144 (2000) 71-81
50. Pan S.Y., Ugnat A.M., Mao Y., Wen S.W., and Johnson K.C. A case-control study of diet and the risk of ovarian cancer. Cancer Epidemiology, Biomarkers & Prevention 13 (2004) 1521-1527
51. Ramos-Gomez M., Kwak M.K., Dolan P.M., Itoh K., Yamamoto M., Talalay P., and 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 98 (2001) 3410-3415
52. Rijken P.J., Timmer W.G., van de Kooij A.J., van Benschop I.M., Wiseman S.A., Meijers M., and Tijburg L.B. Effect of vegetable and carotenoid consumption on aberrant crypt multiplicity, a surrogate end-point marker for colorectal cancer in azoxymethane-induced rats. Carcinogenesis 20 (1999) 2267-2272
53. Samali A., and Orrenius S. Heat shock proteins: regulators of stress response and apoptosis. Cell Stress and Chaperones 3 (1998) 228-236
54. Sekhar K.R., Yan X.X., and Freeman M.L. Nrf2 degradation by the ubiquitin proteasome pathway is inhibited by KIAA0132, the human homolog to INrf2. Oncogene 21 (2002) 6829-6834
55. Seow A., Yuan J.M., Sun C.L., Van Den Berg D., Lee H.P., and Yu M.C. Dietary isothiocyanates, glutathione S-transferase polymorphisms and colorectal cancer risk in the Singapore Chinese Health Study. Carcinogenesis 23 (2002) 2055-2061
56. Son H.Y., Nishikawa A., Furukawa F., Lee I.S., Ikeda T., Miyauchi M., Nakamura H., and Hirose M. Modifying effects of 4-phenylbutyl isothiocyanate on N-nitrosobis(2-oxopropyl)amine-induced tumorigenesis in hamsters. Cancer Letter 160 (2000) 141-147
57. Takahashi S., Sakai J., Fujino T., Hattori H., Zenimaru Y., Suzuki J., Miyamori I., and Yamamoto T.T. The very low-density lipoprotein (VLDL) receptor: characterization and functions as a peripheral lipoprotein receptor. Journal of Atherosclerosis and Thrombosis 11 (2004) 200-208
58. Talalay P. Chemoprotection against cancer by induction of phase 2 enzymes. BioFactors 12 (2000) 5-11
59. Tseng E., Kamath A., and Morris M.E. Effect of organic isothiocyanates on the P-glycoprotein-and MRP1-mediated transport of daunomycin and vinblastine. Pharmaceutical Research 19 (2002) 1509-1515
60. Van der Logt E.M., Roelofs H.M., van Lieshout E.M., Nagengast F.M., and Peters W.H. Effects of dietary anticarcinogens and nonsteroidal anti-inflammatory drugs on rat gastrointestinal UDP-glucuronosyltransferases. Anticancer Research 24 (2004) 843-849
61. Verhoeven D.T., Goldbohm R.A., van Poppel G., Verhagen H., and van den Brandt P.A. Epidemiological studies on brassica vegetables and cancer risk. Cancer Epidemiology, Biomarkers & Prevention 5 (1996) 733-748
62. Wang L.I., Giovannucci E.L., Hunter D., Neuberg D., Su L., and Christiani D.C. Dietary intake of Cruciferous vegetables, Glutathione S-transferase (GST) polymorphisms and lung cancer risk in a Caucasian population. Cancer Causes Control 15 (2004) 977-985
63. Watt R., and Piper P.W. UBI4, the polyubiquitin gene of Saccharomyces cerevisiae, is a heat shock gene that is also subject to catabolite derepression control. Molecular & General Genetics 253 (1997) 439-447
64. Wild A.C., Moinova H.R., and Mulcahy R.T. Regulation of gamma-glutamylcysteine synthetase subunit gene expression by the transcription factor Nrf2. Journal of Biological Chemistry 274 (1999) 33627-33636
65. Xu C., Shen G., Chen C., Gelinas C., and Kong A.N. Suppression of NF-kappaB and NF-kappaB-regulated gene expression by sulforaphane and PEITC through IkappaBalpha, IKK pathway in human prostate cancer PC-3 cells. Oncogene 24 28 (2005) 4486-4495
66. Xu C., Li C.Y., and Kong A.N. Induction of phase I, II and III drug metabolism/transport by xenobiotics. Archives of Pharmacal Research 28 (2005) 249-268
67. Yoshihara S., and Ohta S. Involvement of hepatic aldehyde oxidase in conversion of 1-methyl-4-phenyl-2,3-dihydropyridinium (MPDP+) to 1-methyl-4-phenyl-5,6-dihydro-2-pyridone. Archives of Biochemistry and Biophysics 360 (1998) 93-98
68. Yu R., Mandlekar S., Harvey K.J., Ucker D.S., and Kong A.N. Chemopreventive isothiocyanates induce apoptosis and caspase-3-like protease activity. Cancer Research 58 (1998) 402-408
69. Zhu M., and Fahl W.E. Functional characterization of transcription regulators that interact with the electrophile response element. Biochemical and Biophysical Research Communications 289 (2001) 212-219