Concentration dependent effects of tobacco particulates from different types of cigarettes on expression of drug metabolizing proteins, and benzo(a)pyrene metabolism in primary normal human oral epithelial cells

Food and Chemical Toxicology

Volumn 49, Issue 9, 2011, Pages 2348-2355

  Sacks, Peter G ^a   Zhao, Zhong Lin ^a   Kosinska, Wieslawa ^a   Fleisher, Kenneth E ^a   Gordon, Terry ^b   Guttenplan, Joseph B ^a,b  

^a NEW YORK UNIVERSITY COLLEGE OF DENTISTRY   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ah receptor; Benzo(a)pyrene; DNA adducts; Estrogen; Gene; Tobacco

Indexed keywords

BENZO[A]PYRENE; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; DRUG METABOLIZING ENZYME; GLUTATHIONE TRANSFERASE; HYDROXYSTEROID 17BETA DEHYDROGENASE 2; MICROSOMAL GLUTATHIONE S TRANSFERASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE) 1; TESTOSTERONE 17BETA DEHYDROGENASE; TOBACCO SMOKE; UNCLASSIFIED DRUG;

ARTICLE; CARBON METABOLISM; CARCINOGENICITY; CELL METABOLISM; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DETOXIFICATION; EPITHELIUM CELL; GENE EXPRESSION; GENE INDUCTION; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUTH MUCOSA; PARTICULATE MATTER; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOKING;

BENZO(A)PYRENE; CELLS, CULTURED; DNA ADDUCTS; GENE EXPRESSION REGULATION; HUMANS; MOUTH MUCOSA; POLYMERASE CHAIN REACTION; TOBACCO;

NICOTIANA TABACUM;

EID: 79960838954     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2011.06.037     Document Type: Article

References (46)

1. Alexandrov K., Rojas M., Geneste O., Castegnaro M., Camus A.M., Petruzzelli S., Giuntini C., Bartsch H. An improved fluorometric assay for dosimetry of benzo(a)pyrene diol-epoxide-DNA adducts in smokers' lung: comparisons with total bulky adducts and aryl hydrocarbon hydroxylase activity. Cancer Res. 1992, 52:6248-6253.
2. Baird W.M., Hooven L.A., Mahadevan B. Carcinogenic polycyclic aromatic hydrocarbon-DNA adducts and mechanism of action. Environ. Mol. Mutagen. 2005, 45:106-114.
3. Bock K.W., Kohle C. Ah receptor: dioxin-mediated toxic responses as hints to deregulated physiologic functions. Biochem. Pharmacol. 2006, 72:393-404.
4. Boyle J.O., Gumus Z.H., Kacker A., Choksi V.L., Bocker J.M., Zhou X.K., Yantiss R.K., Hughes D.B., Du B., Judson B.L., Subbaramaiah K., Dannenberg A.J. Effects of cigarette smoke on the human oral mucosal transcriptome. Cancer Prev. Res. (Phila Pa) 2010, 3:266-278.
5. Chlebowski R.T., Schwartz A.G., Wakelee H., Anderson G.L., Stefanick M.L., Manson J.E., Rodabough R.J., Chien J.W., Wactawski-Wende J., Gass M., Kotchen J.M., Johnson K.C., O'Sullivan M.J., Ockene J.K., Chen C., Hubbell F.A. Oestrogen plus progestin and lung cancer in postmenopausal women (Women's Health Initiative trial): a post-hoc analysis of a randomised controlled trial. Lancet 2009, 374:1243-1251.
6. Church T.R., Anderson K.E., Caporaso N.E., Geisser M.S., Le C.T., Zhang Y., Benoit A.R., Carmella S.G., Hecht S.S. A prospectively measured serum biomarker for a tobacco-specific carcinogen and lung cancer in smokers. Cancer Epidemiol. Biomarkers Prev. 2009, 18:260-266.
7. Culp S.J., Gaylor D.W., Sheldon W.G., Goldstein L.S., Beland F.A. A comparison of the tumors induced by coal tar and benzo[a]pyrene in a 2-year bioassay. Carcinogenesis 1998, 19:117-124.
8. Ding Y.S., Yan X.J., Jain R.B., Lopp E., Tavakoli A., Polzin G.M., Stanfill S.B., Ashley D.L., Watson C.H. Determination of 14 polycyclic aromatic hydrocarbons in mainstream smoke from US Brand and non-US brand cigarettes. Environ. Sci. Technol. 2006, 40:1133-1138.
9. Dinkova-Kostova A.T., Fahey J.W., Wade K.L., Jenkins S.N., Shapiro T.A., Fuchs E.J., Kerns M.L., Talalay P. Induction of the phase 2 response in mouse and human skin by sulforaphane-containing broccoli sprout extracts. Cancer Epidemiol. Biomarkers Prev. 2007, 16:847-851.
10. Fields W.R., Leonard R.M., Odom P.S., Nordskog B.K., Ogden M.W., Doolittle D.J. Gene expression in normal human bronchial epithelial (NHBE) cells following in vitro exposure to cigarette smoke condensate. Toxicol. Sci. 2005, 86:84-91.
11. Foy J.W., Bombick B.R., Bombick D.W., Doolittle D.J., Mosberg A.T., Swauger J.E. A comparison of in vitro toxicities of cigarette smoke condensate from Eclipse cigarettes and four commercially available ultra low-" tar" cigarettes. Food Chem. Toxicol. 2004, 42:237-243.
12. Fukano Y., Oishi M., Chibana F., Numazawa S., Yoshida T. Analysis of the expression of heme oxygenase-1 gene in human alveolar epithelial cells exposed to cigarette smoke condensate. J. Toxicol. Sci. 2006, 31:99-109.
13. Guengerich F.P. Metabolism of chemical carcinogens. Carcinogenesis 2000, 21:345-351.
14. Guengerich F.P. Cytochrome P450: what have we learned and what are the future issues?. Drug Metab. Rev. 2004, 36:159-197.
15. Gumus Z.H., Du B., Kacker A., Boyle J.O., Bocker J.M., Mukherjee P., Subbaramaiah K., Dannenberg A.J., Weinstein H. Effects of tobacco smoke on gene expression and cellular pathways in a cellular model of oral leukoplakia. Cancer Prev. Res. (Phila) 2008, 1:100-111.
16. Guttenplan J.B., Spratt T.E., Khmelnitsky M., Kosinska W., Desai D., El-Bayoumy K. Effects of 3H-1,2-dithiole-3-thione,1,4-phenylenebis(methylene)selenocyanate, and selenium-enriched yeast individually and in combination on benzo[a]pyrene-induced mutagenesis in oral tissue and esophagus in lacZ mice. Mutat. Res. 2004, 559:199-210.
17. Hecht S.S. Tobacco carcinogens, their biomarkers and tobacco-induced cancer. Nat. Rev. Cancer 2003, 3:733-744.
18. Hoffmann D., Djordjevic M.V., Hoffmann I. The changing cigarette. Prev. Med. 1997, 26:427-434.
19. Hoffmann D., Hoffmann I., El-Bayoumy K. The less harmful cigarette: a controversial issue. A tribute to Ernst L. Wynder. Chem. Res. Toxicol. 2001, 14:767-790.
20. Hughes D., Guttenplan J.B., Marcus C.B., Subbaramaiah K., Dannenberg A.J. Heat shock protein 90 inhibitors suppress aryl hydrocarbon receptor-mediated activation of CYP1A1 and CYP1B1 transcription and DNA adduct formation. Cancer Prev. Res. (Phila Pa) 2008, 1:485-493.
21. RC I.A. Tobacco smoke and involuntary smoking. IARC Monogr. Eval. Carcinog. Risks Hum. 2004, 83:1-1438.
22. Johnson M.D., Schilz J., Djordjevic M.V., Rice J.R., Shields P.G. Evaluation of in vitro assays for assessing the toxicity of cigarette smoke and smokeless tobacco. Cancer Epidemiol. Biomarkers Prev. 2009, 18:3263-3304.
23. Kasai A., Hiramatsu N., Hayakawa K., Yao J., Maeda S., Kitamura M. High levels of dioxin-like potential in cigarette smoke evidenced by in vitro and in vivo biosensing. Cancer Res. 2006, 66:7143-7150.
24. Knight T.R., Choudhuri S., Klaassen C.D. Induction of hepatic glutathione S-transferases in male mice by prototypes of various classes of microsomal enzyme inducers. Toxicol. Sci. 2008, 106:329-338.
25. Kwak M.K., Itoh K., Yamamoto M., Sutter T.R., 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. Mol. Med. 2001, 7:135-145.
26. Meek M.D., Finch G.L. Diluted mainstream cigarette smoke condensates activate estrogen receptor and aryl hydrocarbon receptor-mediated gene transcription. Environ. Res. 1999, 80:9-17.
27. Muscat J.E., Richie J.P., Thompson S., Wynder E.L. Gender differences in smoking and risk for oral cancer. Cancer Res. 1996, 56:5192-5197.
28. Nagaraj N.S., Beckers S., Mensah J.K., Waigel S., Vigneswaran N., Zacharias W. Cigarette smoke condensate induces cytochromes P450 and aldo-keto reductases in oral cancer cells. Toxicol. Lett. 2006, 165:182-194.
29. Nair S., Kekatpure V.D., Judson B.L., Rifkind A.B., Granstein R.D., Boyle J.O., Subbaramaiah K., Guttenplan J.B., Dannenberg A.J. UVR exposure sensitizes keratinocytes to DNA adduct formation. Cancer Prev. Res. (Phila Pa) 2009, 2:895-902.
30. Nebert D.W., Roe A.L., Dieter M.Z., Solis W.A., Yang Y., Dalton T.P. Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem. Pharmacol. 2000, 59:65-85.
31. Phillips D.H., Grover P.L. Polycyclic hydrocarbon activation: bay regions and beyond. Drug Metab. Rev. 1994, 26:443-467.
32. Putnam K.P., Bombick D.W., Doolittle D.J. Evaluation of eight in vitro assays for assessing the cytotoxicity of cigarette smoke condensate. Toxicol. In Vitro 2002, 16:599-607.
33. Rickert W.S., Trivedi A.H., Momin R.A., Wright W.G., Lauterbach J.H. Effect of smoking conditions and methods of collection on the mutagenicity and cytotoxicity of cigarette mainstream smoke. Toxicol. Sci. 2007, 92:285-293.
34. Rinaldi A.L., Morse M.A., Fields H.W., Rothas D.A., Pei P., Rodrigo K.A., Renner R.J., Mallery S.R. 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. 2002, 62:5451-5456.
35. Rojas M., Alexandrov K., van Schooten F.J., Hillebrand M., Kriek E., Bartsch H. Validation of a new fluorometric assay for benzo[a]pyrene diolepoxide-DNA adducts in human white blood cells: comparisons with 32P-postlabeling and ELISA. Carcinogenesis 1994, 15:557-560.
36. Rotinen M., Celay J., Alonso M.M., Arrazola A., Encio I., Villar J. Estradiol induces type 8 17beta-hydroxysteroid dehydrogenase expression: crosstalk between estrogen receptor alpha and C/EBPbeta. J. Endocrinol. 2009, 200:85-92.
37. Rubin H. Synergistic mechanisms in carcinogenesis by polycyclic aromatic hydrocarbons and by tobacco smoke: a bio-historical perspective with updates. Carcinogenesis 2001, 22:1903-1930.
38. Shugart L., Holland J.M., Rahn R.O. Dosimetry of PAH skin carcinogenesis: covalent binding of benzo[a]pyrene to mouse epidermal DNA. Carcinogenesis 1983, 4:195-198.
39. Stepanov I., Hecht S.S., Lindgren B., Jacob P., Wilson M., Benowitz N.L. Relationship of human toenail nicotine, cotinine, and 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol to levels of these biomarkers in plasma and urine. Cancer Epidemiol. Biomarkers Prev. 2007, 16:1382-1386.
40. Talalay P. Chemoprotection against cancer by induction of phase 2 enzymes. BioFactors 2000, 12:5-11.
41. Todorovic R., Ariese F., Devanesan P., Jankowiak R., Small G.J., Rogan E., Cavalieri E. Determination of benzo[a]pyrene- and 7, 12-dimethylbenz[a]anthracene-DNA adducts formed in rat mammary glands. Chem. Res. Toxicol. 1997, 10:941-947.
42. Tsuchiya Y., Nakajima M., Itoh S., Iwanari M., Yokoi T. Expression of aryl hydrocarbon receptor repressor in normal human tissues and inducibility by polycyclic aromatic hydrocarbons in human tumor-derived cell lines. Toxicol. Sci. 2003, 72:253-259.
43. Wilhelmsson A., Whitelaw M.L., Gustafsson J.A., Poellinger L. Agonistic and antagonistic effects of alpha-naphthoflavone on dioxin receptor function. Role of the basic region helix-loop-helix dioxin receptor partner factor Arnt. J. Biol. Chem. 1994, 269:19028-19033.
44. Xu L., Schantz S.P., Edelstein D., Sacks P.G. A simplified method for the routine culture of normal oral epithelial (NOE) cells from upper aerodigestive tract mucosa. Methods Cell Sci. 1996, 18:31-39.
45. Xue W., Warshawsky D. Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review. Toxicol. Appl. Pharmacol. 2005, 206:73-93.
46. Zhang Y., Talalay P., Cho C.G., Posner G.H. A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure. Proc. Natl. Acad. Sci. USA 1992, 89:2399-2403.