Evaluation of human interindividual variation in bioactivation of estragole using physiologically based biokinetic modeling

Toxicological Sciences

Volumn 113, Issue 2, 2009, Pages 337-348

  Punt, Ans ^a   Jeurissen, Suzanne M ^a   Boersma, Marelle G ^a   Delatour, Thierry ^b   Scholz, Gabriele ^b   Schilter, Benoît ^b   Van Bladeren, Peter J ^a,b   Rietjens, Ivonne M C M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b NESTLÉ RESEARCH CENTER   (Switzerland)

Author keywords

Estragole; In vitro; Interindividual differences; Metabolism; Monte Carlo simulation; PBBK or PBPK

Indexed keywords

CYTOCHROME P450 1A2; CYTOCHROME P450 2A6; CYTOCHROME P450 2E1; ESTRAGOLE; TESTOSTERONE 17BETA DEHYDROGENASE;

AREA UNDER THE CURVE; ARTICLE; CARCINOGENICITY; CHEMICAL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME METABOLISM; FEMALE; GENETIC VARIABILITY; HUMAN; HUMAN TISSUE; LIVER MICROSOME; MALE; MATHEMATICAL ANALYSIS; MONTE CARLO METHOD; PREDICTION; PROCESS MODEL; TOXICOKINETICS;

ANISOLES; CARCINOGENS; CYTOCHROME P-450 ENZYME SYSTEM; FLAVORING AGENTS; HUMANS; LIVER; MICROSOMES, LIVER; MODELS, CHEMICAL; MONTE CARLO METHOD; OXIDATION-REDUCTION;

EID: 75249103572     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfp272     Document Type: Article

References (42)

1. Anthony, A., Caldwell, J., Hutt, A.J., and Smith, R.L. (1987). Metabolism of estragole in rat and mouse and influence of dose size on excretion of the proximate carcinogen 1'-hydroxyestragole. Food Chem. Toxicol. 25, 799-806.
2. Barter, Z.E., Bayliss, M.K., Beaune, P.H., Boobis, A.R., Carlile, D.J., Edwards, R.J., Houston, J.B., Lake, B.G., Lipscomb, J.C., Pelkonen, O.R., et al. (2007). Scaling factors for the extrapolation of in vivo metabolic drug clearance from in vitro data: Reaching a consensus on values of human microsomal protein and hepatocellularity per gram of liver. Curr. Drug Metab. 8, 33-45.
3. Bogaards, J.J.P., Hissink, E.M., Briggs, M., Weaver, R., Jochemsen, R., Jackson, P., Bertrand, M., and van Bladeren, P.J. (2000). Prediction of interindividual variation in drug plasma levels in vivo from individual enzyme kinetic data and physiologically based pharmacokinetic modeling. Eur. J. Pharm. Sci. 12, 117-124.
4. Drinkwater, N.R., Miller, E.C., Miller, J.A., and Pitot, H.C. (1976). Hepatocarcinogenicity of estragole (1-allyl-4-methoxybenzene) and 1'-hydroxyestragole in the mouse and mutagenicity of 1'-acetoxyestragole in bacteria. J. Natl. Cancer Inst. 57, 1323-1331.
5. Evans, M.V., and Andersen, M.E. (2000). Sensitivity analysis of a physiological model for 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD): Assessing the impact of specific model parameters on sequestration in liver and fat in the rat. Toxicol. Sci. 54, 71-80.
6. Fennell, T.R., Miller, J.A., and Miller, E.C. (1984). Characterization of the biliary and urinary glutathione and N-acetylcysteine metabolites of the hepatic carcinogen 1'-hydroxysafrole and its 1'-oxo metabolite in rats and mice. Cancer Res. 44, 3231-3240.
7. Gentry, P.R., Hack, C.E., Haber, L., Maier, A., and Clewell, H.J., III. (2002). An approach for the quantitative consideration of genetic polymorphism data in chemical risk assessment: Examples with warfarin and parathion. Toxicol. Sci. 70, 120-139.
8. Glatt, H. (2000). Sulfotransferases in the bioactivation of xenobiotics. Chem. Biol. Interact. 129, 141-170.
9. Guenthner, T.M., and Luo, G. (2001). Investigation of the role of the 2',3'-epoxidation pathway in the bioactivation and genotoxicity of dietary allylbenzene analogs. Toxicology 160, 47-58.
10. Ingelman-Sundberg, M., Oscarson, M., and McLellan, R.A. (1999). Polymorphic human cytochrome P450 enzymes: An opportunity for individualized drug treatment. Trends Pharmacol. Sci. 20, 342-349.
11. International Programme on Chemical Safety (IPCS). (2005). Chemical-specific adjustment factors for interspecies differences and human variability: Guidance document for use of data in dose/concentration-response assessment. Available at: http://whqlibdoc.who.int/publications/2005/9241546786_eng.pdf. Accessed November 28, 2009.
12. Jeurissen, S.M., Punt, A., Boersma, M.G., Bogaards, J.J.P., Fiamegos, Y.C., Schilter, B., van Bladeren, P.J., Cnubben, N.H.P., and Rietjens, I.M.C. M. (2007). Human cytochrome p450 enzyme specificity for the bioactivation of estragole and related alkenylbenzenes. Chem. Res. Toxicol. 20, 798-806.
13. Jeurissen, S.M., Punt, A., Delatour, T., and Rietjens, I.M.C. M. (2008). Basil extract inhibits the sulfotransferase mediated formation of DNA adducts of the procarcinogen 1'-hydroxyestragole by rat and human liver S9 homogenates and in HepG2 human hepatoma cells. Food Chem. Toxicol. 46, 2296-2302.
14. Jiang, Z., Dragin, N., Jorge-Nebert, L.F., Martin, M.V., Guengerich, F.P., Aklillu, E., Ingelman-Sundberg, M., Hammons, G.J., Lyn-Cook, B.D., Kadlubar, F.F., et al. (2006). Search for an association between the human CYP1A2 genotype and CYP1A2 metabolic phenotype. Pharmacogenet. Genomics 16, 359-367.
15. Lipscomb, J.C., and Poet, T.S. (2008). In vitro measurements of metabolism for application in pharmacokinetic modeling. Pharmacol. Ther. 118, 82-103.
16. Luo, G., Qato, M.K., and Guenthner, T.M. (1992). Hydrolysis of the 2',3'-allylic epoxides of allylbenzene, estragole, eugenol, and safrole by both microsomal and cytosolic epoxide hydrolases. Drug Metab. Dispos. 20, 440-445.
17. Miller, E.C., Swanson, A.B., Phillips, D.H., Fletcher, T.L., Liem, A., and Miller, J.A. (1983). Structure-activity studies of the carcinogenicities in the mouse and rat of some naturally occurring and synthetic alkenylbenzene derivatives related to safrole and estragole. Cancer Res. 43, 1124-1134.
18. Moisan, A.M., Ricketts, M.L., Tardy, V., Desrochers, M., Mebarki, F., Chaussain, J.L., Cabrol, S., Raux-Demay, M.C., Forest, M.G., Sippell, W.G., et al. (1999). New insight into the molecular basis of 3beta-hydroxysteroid dehydrogenase deficiency: Identification of eight mutations in the HSD3B2 gene in eleven patients from seven new families and comparison of the functional properties of twenty-five mutant enzymes. J. Clin. Endocrinol. Metab. 84, 4410-4425.
19. Nagar, S., Walther, S., and Blanchard, R.L. (2006). Sulfotransferase (SULT) 1A1 polymorphic variants *1, *2, and *3 are associated with altered enzymatic activity, cellular phenotype, and protein degradation. Mol. Pharmacol. 69, 2084-2092.
20. Peltoketo, H., Luu-The, V., Simard, J., and Adamski, J. (1999). 17Beta-hydroxysteroid dehydrogenase (HSD)/17-ketosteroid reductase (KSR) family; nomenclature and main characteristics of the 17HSD/KSR enzymes. J. Mol. Endocrinol. 23, 1-11.
21. Phillips, D.H., Miller, J.A., Miller, E.C., and Adams, B. (1981). Structures of the DNA adducts formed in mouse liver after administration of the proximate hepatocarcinogen 1'-hydroxyestragole. Cancer Res. 41, 176-186.
22. 32P-post-labelling analysis of DNA adducts formed in the livers of animals treated with safrole, estragole and other naturally-occurring alkenylbenzenes. II. Newborn male B6C3F1 mice. Carcinogenesis 5, 1623-1628.
23. Plourde, M., Manhes, C., Leblanc, G., Durocher, F., Dumont, M., Sinilnikova, O., and Simard, J. (2008). Mutation analysis and characterization of HSD17B2 sequence variants in breast cancer cases from French Canadian families with high risk of breast and ovarian cancer. J. Mol. Endocrinol. 40, 161-172.
24. Poirier, D., Bydal, P., Tremblay, M.R., Sam, K.M., and Luu-The, V. (2001). Inhibitors of type II 17beta-hydroxysteroid dehydrogenase. Mol. Cell Endocrinol. 171, 119-128.
25. 2-(trans-isoestragol-3'-yl)-2'-deoxyguanosine as a strategy to study species differences in sulfotransferase conversion of the proximate carcinogen 1'-hydroxyestragole. Chem. Res. Toxicol. 20, 991-998.
26. Punt, A., Freidig, A.P., Delatour, T., Scholz, G., Boersma, M.G., Schilter, B., Van Bladeren, P.J., and Rietjens, I.M.C. M. (2008). A physiologically based biokinetic (PBBK) model for estragole bioactivation and detoxification in rat. Toxicol. Appl. Pharmacol. 231, 248-259.
27. Punt, A., Paini, A., Boersma, M.G., Freidig, A.P., Delatour, T., Scholz, G., Schilter, B., Van Bladeren, P.J., and Rietjens, I.M.C. M. (2009). Use of physiologically based biokinetic (PBBK) modeling to study estragole bioactivation and detoxification in humans as compared with male rats. Toxicol. Sci. 110, 255-269.
28. 32P-post-labelling analysis of DNA adducts formed in the livers of animals treated with safrole, estragole and other naturally-occurring alkenylbenzenes. I. Adult female CD-1 mice. Carcinogenesis 5, 1613-1622.
29. Rostami-Hodjegan, A., and Tucker, G.T. (2007). Simulation and prediction of in vivo drug metabolism in human populations from in vitro data. Nat. Rev. Drug Discov. 6, 140-148.
30. Sangster, S.A., Caldwell, J., Hutt, A.J., Anthony, A., and Smith, R.L. (1987). The metabolic disposition of [methoxy-14C]-labelled trans-anethole, estragole and p-propylanisole in human volunteers. Xenobiotica 17, 1223-1232.
31. Scientific Committee on Food (SCF). (2001). Opinion of the Scientific Committee on Food on Estragole (1-allyl-4-methyxybenzene) Available at: http://ec.europa.eu/food/fs/sc/scf/out104_en.pdf. Accessed November 28, 2009.
32. Schuster, D., Nashev, L.G., Kirchmair, J., Laggner, C., Wolber, G., Langer, T., and Odermatt, A. (2008). Discovery of nonsteroidal 17beta-hydroxysteroid dehydrogenase 1 inhibitors by pharmacophore-based screening of virtual compound libraries. J. Med. Chem. 51, 4188-4199.
33. Simard, J., Ricketts, M.L., Gingras, S., Soucy, P., Feltus, F.A., and Melner, M.H. (2005). Molecular biology of the 3beta-hydroxysteroid dehydrogenase/delta5-delta4 isomerase gene family. Endocr. Rev. 26, 525-582.
34. Smith, R.L., Adams, T.B., Doull, J., Feron, V.J., Goodman, J.I., Marnett, L.J., Portoghese, P.S., Waddell, W.J., Wagner, B.M., Rogers, A.E., et al. (2002). Safety assessment of allylalkoxybenzene derivatives used as flavouring substances - methyl eugenol and estragole. Food Chem. Toxicol. 40, 851-870.
35. Solheim, E., and Scheline, R.R. (1973). Metabolism of alkenebenzene derivatives in the rat. I. p-Methoxyallylbenzene (estragole) and p-methoxypropenylbenzene (anethole). Xenobiotica 3, 493-510.
36. Stupans, I., Stretch, G., and Hayball, P. (2000). Olive oil phenols inhibit human hepatic microsomal activity. J. Nutr. 130, 2367-2370.
37. Thomae, B.A., Eckloff, B.W., Freimuth, R.R., Wieben, E.D., and Weinshilboum, R.M. (2002). Human sulfotransferase SULT2A1 pharmacogenetics: Genotype to-phenotype studies. Pharmacogenomics J2, 48-56.
38. Wenker, M.A., Kezic, S., Monster, A.C., and De Wolff, F.A. (2001). Metabolism of styrene in the human liver in vitro: Interindividual variation and enantioselectivity. Xenobiotica 31, 61-72.
39. Wiseman, R.W., Fennell, T.R., Miller, J.A., and Miller, E.C. (1985). Further characterization of the DNA adducts formed by electrophilic esters of the hepatocarcinogens 1'-hydroxysafrole and 1'-hydroxyestragole in vitro and in mouse liver in vivo, including new adducts at C-8 and N-7 of guanine residues. Cancer Res. 45, 3096-3105.
40. 1mice. Cancer Res. 47, 2275-2283.
41. Wislocki, P.G., Miller, E.C., Miller, J.A., McCoy, E.C., and Rosenkranz, H.S. (1977). Carcinogenic and mutagenic activities of safrole, 1'-hydroxysafrole, and some known or possible metabolites. Cancer Res. 37, 1883-1891.
42. Zhang, X., Tsang, A.M., Okino, M.S., Power, F.W., Knaak, J.B., Harrison, L.S., and Dary, C.C. (2007). A physiologically based pharmacokinetic/pharmacodynamic model for carbofuran in Sprague-Dawley rats using the exposure-related dose estimating model. Toxicol. Sci. 100, 345-359.