Impact of Eugenol and Isoeugenol on AhR Translocation, Target Gene Expression, and Proliferation in Human HaCaT Keratinocytes

REFERENCES

• Akintobi , A. M. , Villano , C. M. and White , L. A. 2007 . 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) exposure of normal human dermal fibroblasts results in AhR-dependent and -independent changes in gene expression . Toxicol. Appl. Pharmacol. , 220 : 9 – 17 .
   PubMed Web of Science ®Google Scholar
• Al Masaoudi , T. , Sieben , S. , Callahan , C.P. , Merk , H.F. and Blömeke , B. 2001 . Eugenol but not isoeugenol induces CYPIA1 mRNA in human keratinocytes . Int. Arch. Allergy Immunol. , 124 : 309 – 11 .
   Web of Science ®Google Scholar
• Bonifas , J. , Scheitza , S. , Clemens , J. and Blomeke , B. 2010 . Characterization of N-acetyltransferase 1 activity in human keratinocytes and modulation by para-phenylenediamine . J. Pharmacol. Exp. Ther. , 334 : 318 – 26 .
   PubMed Web of Science ®Google Scholar
• Casper , R. F. , Quesne , M. , Rogers , I. M. , Shirota , T. , Jolivet , A. , Milgrom , E. and Savouret , J. F. 1999 . Resveratrol has antagonist activity on the aryl hydrocarbon receptor: Implications for prevention of dioxin toxicity . Mol. Pharmacol. , 56 : 784 – 90 .
   PubMed Web of Science ®Google Scholar
• Chang , M. C. , Uang , B. J. , Wu , H. L. , Lee , J. J. , Hahn , L. J. and Jeng , J. H. 2002 . Inducing the cell cycle arrest and apoptosis of oral KB carcinoma cells by hydroxychavicol: roles of glutathione and reactive oxygen species . Br. J. Pharmacol. , 135 : 619 – 30 .
   PubMed Web of Science ®Google Scholar
• Denison , M. S. and Heath-Pagliuso , S. 1998 . The Ah receptor: a regulator of the biochemical and toxicological actions of structurally diverse chemicals . Bull. Environ. Contam. Toxicol. , 61 : 557 – 68 .
   PubMed Web of Science ®Google Scholar
• Denison , M. S. and Nagy , S. R. 2003 . Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals . Annu. Rev. Pharmacol. Toxicol. , 43 : 309 – 34 .
   PubMed Web of Science ®Google Scholar
• Elbi , C. , Misteli , T. and Hager , G. L. 2002 . Recruitment of dioxin receptor to active transcription sites . Mol. Biol. Cell , 13 : 2001 – 15 .
   PubMed Web of Science ®Google Scholar
• Elferink , C. J. 2003 . Aryl hydrocarbon receptor-mediated cell cycle control . Prog. Cell Cycle Res. , 5 : 261 – 67 .
   PubMedGoogle Scholar
• Elferink , C. J. , Ge , N. L. and Levine , A. 2001 . Maximal aryl hydrocarbon receptor activity depends on an interaction with the retinoblastoma protein . Mol. Pharmacol. , 59 : 664 – 73 .
   PubMed Web of Science ®Google Scholar
• Ge , N. L. and Elferink , C. J. 1998 . A direct interaction between the aryl hydrocarbon receptor and retinoblastoma protein. Linking dioxin signaling to the cell cycle . J. Biol. Chem. , 273 : 22708 – 13 .
   PubMed Web of Science ®Google Scholar
• Ghosh , R. , Nadiminty , N. , Fitzpatrick , J. E. , Alworth , W. L. , Slaga , T. J. and Kumar , A. P. 2005 . Eugenol causes melanoma growth suppression through inhibition of E2F1 transcriptional activity . J. Biol. Chem. , 280 : 5812 – 19 .
   PubMed Web of Science ®Google Scholar
• Han , E. H. , Hwang , Y. P. , Jeong , T. C. , Lee , S. S. , Shin , J. G. and Jeong , H. G. 2007 . Eugenol inhibit 7,12-dimethylbenz[a]anthracene-induced genotoxicity in MCF-7 cells: Bifunctional effects on CYP1 and NAD(P)H:quinone oxidoreductase . FEBS Lett. , 581 : 749 – 56 .
   PubMed Web of Science ®Google Scholar
• Hankinson , O. 1995 . The aryl hydrocarbon receptor complex . Annu. Rev. Pharmacol. Toxicol. , 35 : 307 – 40 .
   PubMed Web of Science ®Google Scholar
• Hennen , J. , Aeby , P , Goebel , C. , Schettgen , T. , Oberli , O. , Kalmes , M. and Blömeke , B. 2011 . Cross talk between keratinocytes and dendritic cells: Impact on the prediction of sensitization . Toxicol. Sci. , 123 : 501 – 10 .
   PubMed Web of Science ®Google Scholar
• Huang , G. and Elferink , C. J. 2005 . Multiple mechanisms are involved in Ah receptor-mediated cell cycle arrest . Mol. Pharmacol. , 67 : 88 – 96 .
   PubMed Web of Science ®Google Scholar
• Ikuta , T. , Kobayashi , Y. and Kawajiri , K. 2004 . Cell density regulates intracellular localization of aryl hydrocarbon receptor . J. Biol. Chem. , 279 : 19209 – 16 .
   PubMed Web of Science ®Google Scholar
• Ikuta , T. , Namiki , T. , Fujii-Kuriyama , Y. and Kawajiri , K. 2008 . AhR protein trafficking and function in the skin . Biochem. Pharmacol. , 77 : 588 – 96 .
   PubMed Web of Science ®Google Scholar
• Kalmes , M. , Neumeyer , A. , Rio , P. , Hanenberg , H. , Fritsche , E. and Blömeke , B. 2006 . Impact of the arylhydrocarbon receptor on eugenol- and isoeugenol-induced cell cycle arrest in human immortalized keratinocytes (HaCaT) . Biol. Chem. , 387 : 1201 – 7 .
   PubMed Web of Science ®Google Scholar
• Kaur , G. , Athar , M. and Alam , M. S. 2010 . Eugenol precludes cutaneous chemical carcinogenesis in mouse by preventing oxidative stress and inflammation and by inducing apoptosis . Mol. Carcinogen. , 49 : 290 – 301 .
   PubMed Web of Science ®Google Scholar
• Knockaert , M. , Blondel , M. , Bach , S. , Leost , M. , Elbi , C. , Hager , G. L. , Nagy , S. R. , Han , D. , Denison, Ffrench , M. , Ryan , X. P. , Magiatis , P. , Polychronopoulos , P. , Greengard , P. , Skaltsounis , L. and Meijer , L. 2004 . Independent actions on cyclin-dependent kinases and aryl hydrocarbon receptor mediate the antiproliferative effects of indirubins . Oncogene , 23 : 4400 – 12 .
   PubMed Web of Science ®Google Scholar
• Kolluri , S. K. , Weiss , C. , Koff , A. and Göttlicher , M. 1999 . p27(Kip1) induction and inhibition of proliferation by the intracellular Ah receptor in developing thymus and hepatoma cells . Genes Dev , 13 : 1742 – 53 .
   PubMed Web of Science ®Google Scholar
• Kruse , C. , Bodo , E. , Petschnik , A. E. , Danner , S. , Tiede , S. and Paus , R. 2006 . Towards the development of a pragmatic technique for isolating and differentiating nestin-positive cells from human scalp skin into neuronal and glial cell populations: Generating neurons from human skin? . Exp. Dermatol. , 15 : 794 – 800 .
   PubMed Web of Science ®Google Scholar
• Ledirac , N. , Delescluse , C. , de Sousa , G. , Pralavorio , M. , Lesca , P. , Amichot , M. , Berge , J. B. and Rahmani , R. 1997 . Carbaryl induces CYP1A1 gene expression in HepG2 and HaCaT cells but is not a ligand of the human hepatic Ah receptor . Toxicol. Appl. Pharmacol. , 144 : 177 – 82 .
   PubMed Web of Science ®Google Scholar
• Ma , Q. 2001 . Induction of CYP1A1. The AhR/DRE paradigm: Transcription, receptor regulation, and expanding biological roles . Curr. Drug Metab. , 2 : 149 – 64 .
   PubMed Web of Science ®Google Scholar
• Mace , K. , Bowman , E. D. , Vautravers , P. , Shields , P. G. , Harris , C. C. and Pfeifer , A. M. 1998 . Characterisation of xenobiotic-metabolising enzyme expression in human bronchial mucosa and peripheral lung tissues . Eur. J. Cancer , 34 : 914 – 20 .
   PubMed Web of Science ®Google Scholar
• Manikandan , P. , Vinothini , G. , Vidya Priyadarsini , R. , Prathiba , D. and Nagini , S. 2011 . Eugenol inhibits cell proliferation via NF-kappaB suppression in a rat model of gastric carcinogenesis induced by MNNG . Invest. New Drugs , 29 : 110 – 17 .
   PubMed Web of Science ®Google Scholar
• Marlowe , J. L. , Fan , Y. , Chang , X. , Peng , L. , Knudsen , E. S. , Xia , Y. and Puga , A. 2008 . The aryl hydrocarbon receptor binds to E2F1 and inhibits E2F1-induced apoptosis . Mol. Biol. Cell , 19 : 3263 – 71 .
   PubMed Web of Science ®Google Scholar
• Marlowe , J. L. , Knudsen , E. S. , Schwemberger , S. and Puga , A. 2004 . The aryl hydrocarbon receptor displaces p300 from E2F-dependent promoters and represses S phase-specific gene expression . J. Biol. Chem. , 279 : 29013 – 22 .
   PubMed Web of Science ®Google Scholar
• Medjakovic , S. and Jungbauer , A. 2008 . Red clover isoflavones biochanin A and formononetin are potent ligands of the human aryl hydrocarbon receptor . J. Steroid Biochem. Mol. Biol. , 108 : 171 – 77 .
   PubMed Web of Science ®Google Scholar
• Mitchell , K. A. and Elferink , C. J. 2008 . Timing is everything: Consequences of transient and sustained AhR activity . Biochem. Pharmacol. , 77 : 947 – 56 .
   PubMed Web of Science ®Google Scholar
• Nguyen , L. P. and Bradfield , C. A. 2008 . The search for endogenous activators of the aryl hydrocarbon receptor . Chem. Res. Toxicol. , 21 : 102 – 16 .
   PubMed Web of Science ®Google Scholar
• Okada , N. , Hirata , A. , Murakami , Y. , Shoji , M. , Sakagami , H. and Fujisawa , S. 2005 . Induction of cytotoxicity and apoptosis and inhibition of cyclooxygenase-2 gene expression by eugenol-related compounds . Anticancer Res. , 25 : 3263 – 69 .
   PubMed Web of Science ®Google Scholar
• Park , B. S. , Song , Y. S. , Yee , S. B. , Lee , B. G. , Seo , S. Y. , Park , Y. C. , Kim , J. M. , Kim , H. M. and Yoo , Y. H. 2005 . Phospho-ser 15-p53 translocates into mitochondria and interacts with Bcl-2 and Bcl-xL in eugenol-induced apoptosis . Apoptosis , 10 : 193 – 200 .
   PubMed Web of Science ®Google Scholar
• Pisano , M. , Pagnan , G. , Loi , M. , Mura , M. E. , Tilocca , M. G. , Palmieri , G. , Fabbri , D. , Dettori , M. A. , Delogu , G. , Ponzoni , M. and Rozzo , C. 2007 . Antiproliferative and pro-apoptotic activity of eugenol-related biphenyls on malignant melanoma cells . Mol. Cancer 6: 8. ,
   Google Scholar
• Puga , A. , Barnes , S. J. , Dalton , T. P. , Chang , C. , Knudsen , E. S. and Maier , M. A. 2000 . Aromatic hydrocarbon receptor interaction with the retinoblastoma protein potentiates repression of E2F-dependent transcription and cell cycle arrest . J. Biol. Chem. , 275 : 2943 – 50 .
   PubMed Web of Science ®Google Scholar
• Puga , A. , Xia , Y. and Elferink , C. 2002 . Role of the aryl hydrocarbon receptor in cell cycle regulation . Chem. Biol. Interact. , 141 : 117 – 30 .
   PubMed Web of Science ®Google Scholar
• Ray , S. S. and Swanson , H. I. 2003 . Alteration of keratinocyte differentiation and senescence by the tumor promoter dioxin . Toxicol. Appl. Pharmacol. , 192 : 131 – 45 .
   PubMed Web of Science ®Google Scholar
• Ray , S. S. and Swanson , H. I. 2004 . Dioxin-induced immortalization of normal human keratinocytes and silencing of p53 and p16INK4a . J. Biol. Chem. , 279 : 27187 – 93 .
   PubMed Web of Science ®Google Scholar
• Rinaldi , A. L. , Morse , M. A. , Fields , H. W. , Rothas , D. A. , Pei , P. , Rodrigo , K. A. , Renner , R. J. and Mallery , S. R. 2002 . Curcumin activates the aryl hydrocarbon receptor yet significantly inhibits (-)-benzo(a)pyrene-7R-trans-7,8-dihydrodiol bioactivation in oral squamous cell carcinoma cells and oral mucosa . Cancer Res. , 62 : 5451 – 56 .
   PubMed Web of Science ®Google Scholar
• Santini , R. P. , Myrand , S. , Elferink , C. and Reiners , J. J. Jr . 2001 . Regulation of Cyp1a1 induction by dioxin as a function of cell cycle phase . J. Pharmacol. Exp. Ther. , 299 : 718 – 28 .
   PubMed Web of Science ®Google Scholar
• Sieben , S. , Hertl , M. , Al Masaoudi , T. , Merk , H. F. and Blomeke , B. 2001 . Characterization of T cell responses to fragrances . Toxicol. Appl. Pharmacol. , 172 : 172 – 78 .
   PubMed Web of Science ®Google Scholar
• Strobeck , M. W. , Fribourg , A. F. , Puga , A. and Knudsen , E. S. 2000 . Restoration of retinoblastoma mediated signaling to Cdk2 results in cell cycle arrest . Oncogene , 19 : 1857 – 67 .
   PubMed Web of Science ®Google Scholar
• Trapani , V. , Patel , V. , Leong , C. O. , Ciolino , H. P. , Yeh , G. C. , Hose , C. , Trepel , J. B. , Stevens , M. F. , Sausville , E. A. and Loaiza-Perez , A. I. 2003 . DNA damage and cell cycle arrest induced by 2-(4-amino-3-methylphenyl)-5-fluorobenzothiazole (5F 203, NSC 703786) is attenuated in aryl hydrocarbon receptor deficient MCF-7 cells . Br. J. Cancer , 88 : 599 – 605 .
   PubMed Web of Science ®Google Scholar
• Trimarchi , J. M. and Lees , J. A. 2002 . Sibling rivalry in the E2F family . Nat. Rev. Mol. Cell Biol. , 3 : 11 – 20 .
   PubMed Web of Science ®Google Scholar
• Tuschl , H. and Kovac , J. A. 2001 . Langerhans cells and immature dendritic cells as model systems for screening of skin sensitizers . Toxicol. In Vitro , 15 : 327 – 31 .
   PubMed Web of Science ®Google Scholar
• Van Och , F. M. , Van Loveren , H. , Van Wolfswinkel , J. C. , Machielsen , A. J. and Vandebriel , R. J. 2005 . Assessment of potency of allergenic activity of low molecular weight compounds based on IL-1 alpha and IL-18 production by a murine and human keratinocyte cell line . Toxicology , 210 : 95 – 109 .
   PubMed Web of Science ®Google Scholar
• Vanden Heuvel , J. P. , Clark , G. C. , Kohn , M. C. , Tritscher , A. M. , Greenlee , W. F. , Lucier , G. W. and Bell , D. A. 1994 . Dioxin-responsive genes: Examination of dose-response relationships using quantitative reverse transcriptase-polymerase chain reaction . Cancer Res. , 54 : 62 – 68 .
   PubMed Web of Science ®Google Scholar
• Verrier , A. C. , Schmitt , D. and Staquet , M. J. 1999 . Fragrance and contact allergens in vitro modulate the HLA-DR and E- cadherin expression on human epidermal Langerhans cells . Int. Arch. Allergy Immunol. , 120 : 56 – 62 .
   PubMed Web of Science ®Google Scholar
• Yamamoto , J. , Ihara , K. , Nakayama , H. , Hikino , S. , Satoh , K. , Kubo , N. , Iida , T. , Fujii , Y. and Hara , T. 2004 . Characteristic expression of aryl hydrocarbon receptor repressor gene in human tissues: Organ-specific distribution and variable induction patterns in mononuclear cells . Life Sci. , 74 : 1039 – 49 .
   PubMed Web of Science ®Google Scholar