Carnosic acid induces the NAD(P)H: Quinone oxidoreductase 1 expression in rat clone 9 cells through the p38/nuclear factor erythroid-2 related factor 2 pathway

Journal of Nutrition

Volumn 141, Issue 12, 2011, Pages 2119-2125

  Tsai, Chia Wen ^a   Lin, Chia Yuan ^a   Wang, Yu Jung ^a  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CARNOSIC ACID; CARNOSOL; LUCIFERASE; MESSENGER RNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE) 1; ROSMARINUS OFFICINALIS EXTRACT; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE SILENCING; LIVER CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; RAT;

ANIMALS; ANTICARCINOGENIC AGENTS; ANTIOXIDANTS; BLOTTING, WESTERN; CELL NUCLEUS; CELLS, CULTURED; DITERPENES, ABIETANE; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE SILENCING; LIVER; LUCIFERASES; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PLANT EXTRACTS; PLASMIDS; RATS; RESPONSE ELEMENTS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSFECTION; UP-REGULATION;

RATTUS; ROSMARINUS OFFICINALIS;

EID: 84862908099     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.111.146779     Document Type: Article

References (55)

1. Guengerich FP, Shimada T. Oxidation of toxic and carcinogenic chemicals by human cytochrome P-450 enzymes. Chem Res Toxicol. 1991;4:391-407.
2. Ikeda H, Nishi S, Sakai M. Transcription factor Nrf2/MafK regulates rat placental glutathione S-transferase gene during hepatocarcinogenesis. Biochem J. 2004;380:515-21.
3. Martin D, Rojo AI, Salinas M, Diaz R, Gallardo G, Alam J, De Galarreta CM, Cuadrado A. Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol. J Biol Chem. 2004;279:8919-29.
4. Nioi P, Hayes JD. Contribution of NAD(P)H:quinone oxidoreductase 1 to protection against carcinogenesis, and regulation of its gene by the Nrf2 basic-region leucine zipper and the arylhydrocarbon receptor basic helix-loop-helix transcription factors. Mutat Res. 2004;555:149-71.
5. Girolami F, Abbadessa G, Racca S, Spaccamiglio A, Piccione F, Dacasto M, Carletti M, Gardini G, Di Carlo F, Nebbia C. Time-dependent acetylsalicylic acid effects on liver CYP1A and antioxidant enzymes in a rat model of 7,12-dimethylbenzanthracene (DMBA)-induced mammary carcinogenesis. Toxicol Lett. 2008;181:87-92.
6. Begleiter A, Sivananthan K, Lefas GM, Maksymiuk AW, Bird RP. Inhibition of colon carcinogenesis by post-initiation induction of NQO1 in Sprague-Dawley rats. Oncol Rep. 2009;21:1559-65.
7. Iskander K, Gaikwad A, Paquet M, Long DJ II, Brayton C, Barrios R, Jaiswal AK. Lower induction of p53 and decreased apoptosis in NQO1-null mice lead to increased sensitivity to chemical-induced skin carcinogenesis. Cancer Res. 2005;65:2054-8.
8. Dinkova-Kostova AT, Talalay P. NAD(P)H:quinone acceptor oxidoreductase 1 (NQO1), a multifunctional antioxidant enzyme and exceptionally versatile cytoprotector. Arch Biochem Biophys. 2010;501:116-23.
9. Jaiswal AK. Regulation of genes encoding NAD(P)H:quinone oxidoreductases. Free Radic Biol Med. 2000;29:254-62.
10. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 1999;13:76-86.
11. Hayes JD, McMahon M. Molecular basis for the contribution of the antioxidant responsive element to cancer chemoprevention. Cancer Lett. 2001;174:103-13.
12. Ramos-Gomez M, Kwak MK, Dolan PM, Itoh K, Yamamoto M, Talalay P, Kensler TW. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc Natl Acad Sci USA. 2001;98:3410-5.
13. Lee JS, Surh YJ. Nrf2 as a novel molecular target for chemoprevention. Cancer Lett. 2005;224:171-84.
14. Aruoma OI, Halliwell B, Aeschbach R, Loligers J. Antioxidant and prooxidant properties of active rosemary constituents: carnosol and carnosic acid. Xenobiotica. 1992;22:257-68.
15. Debersac P, Heydel JM, Amiot MJ, Goudonnet H, Artur Y, Suschetet M, Siess MH. Induction of cytochrome P450 and/or detoxication enzymes by various extracts of rosemary: description of specific patterns. Food Chem Toxicol. 2001;39:907-18.
16. Singletary KW. Rosemary extract and carnosol stimulate rat liver glutathione-S-transferase and quinone reductase activities. Cancer Lett. 1996;100:139-44.
17. Tamaki Y, Tabuchi T, Takahashi T, Kosaka K, Satoh T. Activated glutathione metabolism participates in protective effects of carnosic acid against oxidative stress in neuronal HT22 cells. Planta Med. 2010;76:683-8.
18. Sancheti G, Goyal PK. Effect of Rosmarinus officinalis in modulating 7,12-dimethylbenz(a)anthracene induced skin tumorigenesis in mice. Phytother Res. 2006;20:981-6.
19. Singletary K, MacDonald C, Wallig M. Inhibition by rosemary and carnosol of 7,12-dimethylbenz[a]anthracene (DMBA)-induced rat mammary tumorigenesis and in vivo DMBA-DNA adduct formation. Cancer Lett. 1996;104:43-8.
20. Offord EA, Mace K, Ruffieux C, Malnoe A, Pfeifer AM. Rosemary components inhibit benzo[a]pyrene-induced genotoxicity in human bronchial cells. Carcinogenesis. 1995;16:2057-62.
21. Manoharan S, Vasanthaselvan M, Silvan S, Baskaran N, Kumar Singh A, Vinoth Kumar V. Carnosic acid: a potent chemopreventive agent against oral carcinogenesis. Chem Biol Interact. 2010;188:616-22.
22. Lii CK, Liu KL, Cheng YP, Lin AH, Chen HW, Tsai CW. Sulforaphane and alpha-lipoic acid upregulate the expression of the pi class of glutathione S-transferase through c-jun and Nrf2 activation. J Nutr. 2010;140:885-92.
23. Tsai CW, Lin AH, Wang TS, Liu KL, Chen HW, Lii CK. Methionine restriction up-regulates the expression of the pi class of glutathione S-transferase partially via the extracellular signal-regulated kinaseactivator protein-1 signaling pathway initiated by glutathione depletion. Mol Nutr Food Res. 2010;54:841-50.
24. Jamieson D, Wilson K, Pridgeon S, Margetts JP, Edmondson RJ, Leung HY, Knox R, Boddy AV. NAD(P)H:quinone oxidoreductase 1 and nrh: quinone oxidoreductase 2 activity and expression in bladder and ovarian cancer and lower NRH:quinone oxidoreductase 2 activity associated with an NQO2 exon 3 single-nucleotide polymorphism. Clin Cancer Res. 2007;13:1584-90.
25. Kataoka K, Handa H, Nishizawa M. Induction of cellular antioxidative stress genes through heterodimeric transcription factor Nrf2/small Maf by antirheumatic gold(I) compounds. J Biol Chem. 2001;276:34074-81.
26. Hwang YP, Jeong HG. The coffee diterpene kahweol induces heme oxygenase-1 via the PI3K and p38/Nrf2 pathway to protect human dopaminergic neurons from 6-hydroxydopamine-derived oxidative stress. FEBS Lett. 2008;582:2655-62.
27. Jia Z, Zhu H, Misra HP, Li Y. Potent induction of total cellular GSH and NQO1 as well as mitochondrial GSH by 3H-1,2-dithiole-3-thione in SH-SY5Y neuroblastoma cells and primary human neurons: protection against neurocytotoxicity elicited by dopamine, 6-hydroxydopamine, 4-hydroxy-2-nonenal, or hydrogen peroxide. Brain Res. 2008;1197:159-69.
28. Jia Z, Zhu H, Li Y, Misra HP. Cruciferous nutraceutical 3H-1,2-dithiole-3-thione protects human primary astrocytes against neurocytotoxicity elicited by MPTP, MPP(+), 6-OHDA, HNE and acrolein. Neurochem Res. 2009;34:1924-34.
29. Long DJ II, Waikel RL, Wang XJ, Roop DR, Jaiswal AK. NAD(P)H: quinone oxidoreductase 1 deficiency and increased susceptibility to 7,12-dimethylbenz[a]-anthracene-induced carcinogenesis in mouse skin. J Natl Cancer Inst. 2001;93:1166-70.
30. Patrick BA, Gong X, Jaiswal AK. Disruption of NAD(P)H:quinone oxidoreductase 1 gene in mice leads to 20S proteasomal degradation of p63 resulting in thinning of epithelium and chemical-induced skin cancer. Oncogene. 2011; 30:1098-107.
31. Lu F, Zahid M, Wang C, Saeed M, Cavalieri EL, Rogan EG. Resveratrol prevents estrogen-DNA adduct formation and neoplastic transformation in MCF-10F cells. Cancer Prev Res (Phila). 2008;1:135-45.
32. Montano MM, Chaplin LJ, Deng H, Mesia-Vela S, Gaikwad N, Zahid M, Rogan E. Protective roles of quinone reductase and tamoxifen against estrogen-induced mammary tumorigenesis. Oncogene. 2007;26:3587-90.
33. Garg R, Gupta S, Maru GB. Dietary curcumin modulates transcriptional regulators of phase I and phase II enzymes in benzo[a]pyrenetreated mice: mechanism of its anti-initiating action. Carcinogenesis. 2008;29:1022-32.
34. Soyalan B, Minn J, Schmitz HJ, Schrenk D, Will F, Dietrich H, Baum M, Eisenbrand G, Janzowski C. Apple juice intervention modulates expression of ARE-dependent genes in rat colon and liver. Eur J Nutr. 2011;50:135-43.
35. Jones SB, Brooks JD. Modest induction of phase 2 enzyme activity in the F-344 rat prostate. BMC Cancer. 2006;6:62.
36. Johnson JJ, Syed DN, Heren CR, Suh Y, Adhami VM, Mukhtar H. Carnosol, a dietary diterpene, displays growth inhibitory effects in human prostate cancer PC3 cells leading to G2-phase cell cycle arrest and targets the 59-AMP-activated protein kinase (AMPK) pathway. Pharm Res. 2008;25:2125-34.
37. Aruoma OI, Spencer JP, Rossi R, Aeschbach R, Khan A, Mahmood N, Munoz A, Murcia A, Butler J, Halliwell B. An evaluation of the antioxidant and antiviral action of extracts of rosemary and Provencal herbs. Food Chem Toxicol. 1996;34:449-56.
38. Cheng AC, Lee MF, Tsai ML, Lai CS, Lee JH, Ho CT, Pan MH. Rosmanol potently induces apoptosis through both the mitochondrial apoptotic pathway and death receptor pathway in human colon adenocarcinoma COLO 205 cells. Food Chem Toxicol. 2011;49:485-93.
39. Posadas SJ, Caz V, Largo C, De la Gandara B, Matallanas B, Reglero G, De Miguel E. Protective effect of supercritical fluid rosemary extract, Rosmarinus officinalis, on antioxidants of major organs of aged rats. Exp Gerontol. 2009;44:383-9.
40. Soler-Rivas C, Marin FR, Santoyo S, Garcia-Risco MR, Senorans FJ, Reglero G. Testing and enhancing the in vitro bioaccessibility and bioavailability of Rosmarinus officinalis extracts with a high level of antioxidant abietanes. J Agric Food Chem. 2010;58:1144-52.
41. Yan H, Wang L, Li X, Yu C, Zhang K, Jiang Y, Wu L, Lu W, Tu P. Highperformance liquid chromatography method for determination of carnosic acid in rat plasma and its application to pharmacokinetic study. Biomed Chromatogr. 2009;23:776-81.
42. Chang CH, Chyau CC, Hsieh CL, Wu YY, Ker YB, Tsen HY, Peng RY. Relevance of phenolic diterpene constituents to antioxidant activity of supercritical CO(2) extract from the leaves of rosemary. Nat Prod Res. 2008;22:76-90.
43. Satoh T, Kosaka K, Itoh K, Kobayashi A, Yamamoto M, Shimojo Y, Kitajima C, Cui J, Kamins J, Okamoto S, et al. Carnosic acid, a catecholtype electrophilic compound, protects neurons both in vitro and in vivo through activation of the Keap1/Nrf2 pathway via S-alkylation of targeted cysteines on Keap1. J Neurochem. 2008;104:1116-31.
44. Satoh T, Izumi M, Inukai Y, Tsutsumi Y, Nakayama N, Kosaka K, Shimojo Y, Kitajima C, Itoh K, Yokoi T, et al. Carnosic acid protects neuronal HT22 Cells through activation of the antioxidant-responsive element in free carboxylic acid- and catechol hydroxyl moietiesdependent manners. Neurosci Lett. 2008;434:260-5.
45. Elangovan S, Hsieh TC. Control of cellular redox status and upregulation of quinone reductase NQO1 via Nrf2 activation by alpha-lipoic acid in human leukemia HL-60 cells. Int J Oncol. 2008;33:833-8.
46. Morimitsu Y, Nakagawa Y, Hayashi K, Fujii H, Kumagai T, Nakamura Y, Osawa T, Horio F, Itoh K, Iida K, et al. A sulforaphane analogue that potently activates the Nrf2-dependent detoxification pathway. J Biol Chem. 2002;277:3456-63.
47. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, Oyake T, Hayashi N, Satoh K, Hatayama I, et al. An Nrf2/smallMaf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun. 1997;236:313-22.
48. Chen CC, Chen HL, Hsieh CW, Yang YL, Wung BS. Upregulation of NF-E2-related factor-2-dependent glutathione by carnosol provokes a cytoprotective response and enhances cell survival. Acta Pharmacol Sin. 2011;32:62-9.
49. Manandhar S, Cho JM, Kim JA, Kensler TW, Kwak MK. Induction of Nrf2-regulated genes by 3H-1, 2-dithiole-3-thione through the ERK signaling pathway in murine keratinocytes. Eur J Pharmacol. 2007; 577:17-27.
50. Yuan X, Xu C, Pan Z, Keum YS, Kim JH, Shen G, Yu S, Oo KT, Ma J, Kong AN. Butylated hydroxyanisole regulates ARE-mediated gene expression via Nrf2 coupled with ERK and JNK signaling pathway in HepG2 cells. Mol Carcinog. 2006;45:841-50.
51. Yu R, Mandlekar S, Lei W, Fahl WE, Tan TH, Kong AN. p38 mitogenactivated protein kinase negatively regulates the induction of phase II drug-metabolizing enzymes that detoxify carcinogens. J Biol Chem. 2000;275:2322-7.
52. Lai CS, Lee JH, Ho CT, Liu CB, Wang JM, Wang YJ, Pan MH. Rosmanol potently inhibits lipopolysaccharide-induced iNOS and COX-2 expression through downregulating MAPK, NF-kappaB, STAT3 and C/EBP signaling pathways. J Agric Food Chem. 2009;57:10990-8.
53. Yoshida H, Mimura J, Imaizumi T, Matsumiya T, Ishikawa A, Metoki N, Tanji K, Ota K, Hayakari R, Kosaka K, et al. Edaravone and carnosic acid synergistically enhance the expression of nerve growth factor in human astrocytes under hypoxia/reoxygenation. Neurosci Res. 2011;69:291-8.
54. El Omri A, Han J, Yamada P, Kawada K, Ben Abdrabbah M, Isoda H. Rosmarinus officinalis polyphenols activate cholinergic activities in PC12 cells through phosphorylation of ERK1/2. J Ethnopharmacol. 2010;131:451-8.
55. Park JA, Kim S, Lee SY, Kim CS, Kim do K, Kim SJ, Chun HS. Beneficial effects of carnosic acid on dieldrin-induced dopaminergic neuronal cell death. Neuroreport. 2008;19:1301-4.