In vivo validation and physiologically based biokinetic modeling of the inhibition of SULT-mediated estragole DNA adduct formation in the liver of male sprague-dawley rats by the basil flavonoid nevadensin

Molecular Nutrition and Food Research

Volumn 57, Issue 11, 2013, Pages 1969-1978

  Alhusainy, Wasma ^a,b,c,d   Paini, Alicia ^a,d   van den Berg, Johannes H J ^a   Punt, Ans ^a   Scholz, Gabriele ^d   Schilter, Benoit ^d   van Bladeren, Peter J ^a,d   Taylor, Sean ^c   Adams, Timothy B ^b   Rietjens, Ivonne M C M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b Flavor and Extract Manufacturers Association   (United States)

^c International Organization of the Flavor Industry   (Switzerland)

^d NESTLÉ RESEARCH CENTER   (Switzerland)

Author keywords

Bioactivation; Estragole; Nevadensin; Physiologically based biokinetic (PBBK) modeling; Sulfotransferase (SULT)

Indexed keywords

ANISOLE DERIVATIVE; ESTRAGOLE; FLAVONE DERIVATIVE; NEVADENSIN; SULFOTRANSFERASE;

ANIMAL; ARTICLE; BASIL; BIOACTIVATION; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; DNA ADDUCT; DRUG EFFECT; HUMAN; INTESTINE; LIVER; LIVER CELL; MALE; METABOLISM; PHYSIOLOGICALLY BASED BIOKINETIC (PBBK) MODELING; RAT; SENSITIVITY AND SPECIFICITY; SPRAGUE DAWLEY RAT; SULFOTRANSFERASE (SULT); VALIDATION STUDY;

BIOACTIVATION; ESTRAGOLE; NEVADENSIN; PHYSIOLOGICALLY BASED BIOKINETIC (PBBK) MODELING; SULFOTRANSFERASE (SULT);

ANIMALS; ANISOLES; DNA ADDUCTS; FLAVONES; HEPATOCYTES; HUMANS; INTESTINES; LIVER; MALE; MODELS, MOLECULAR; OCIMUM BASILICUM; RATS; RATS, SPRAGUE-DAWLEY; SENSITIVITY AND SPECIFICITY; SULFOTRANSFERASES;

EID: 84886785652     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201300144     Document Type: Article

References (36)

1. Smith, R. L., Adams, T. B., Doull, J., Feron, V. J. et al., Safety assessment of allylalkoxybenzene derivatives used as flavouring substances - methyl eugenol and estragole. Food Chem. Toxicol. 2002, 40, 851-870.
2. 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 1984, 5, 1623-1628.
3. 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 1984, 5, 1613-1622.
4. Boberg, E. W., Miller, E. C., Miller, J. A., Strong evidence from studies with brachymorphic mice and pentachlorophenol that 1'-sulfooxysafrole is the major ultimate electrophilic and carcinogenic metabolite of 1'-hydroxysafrole in mouse liver. Cancer Res. 1983, 43, 5163-5173.
5. European Commission (EC), 2008. Regulation (EC) no 1334/2008 of the European Parliament and of the Council of 16 December 2008 on Flavourings and Certain Food Ingredients with Flavouring Properties for Use in and on Foods and Amending Council Regulation (EEC) No 1601/91, Regulations (EC) No 2232/96 and (EC) No 110/2008 and Directive 2000/13/EC.
6. Alhusainy, W., Paini, A., Punt, A., Louisse, J. et al., Identification of nevadensin as an important herb-based constituent inhibiting estragole bioactivation and physiology-based biokinetic modeling of its possible in vivo effect. Toxicol. Appl. Pharmacol. 2010, 245, 179-190.
7. Jeurissen, S. M. F., Punt, A., Delatour, T., Rietjens, I. M. C. M., 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. 2008, 46, 2296-2302.
8. Alhusainy, W., van den Berg, S. J. P. L., Paini, A., Campana, A. et al., Matrix modulation of the bioactivation of estragole by constituents of different alkenylbenzene-containing herbs and spices and physiologically based biokinetic modeling of possible in vivo effects. Toxicol. Sci. 2012, 129, 174-187.
9. Punt, A., Freidig, A. P., Delatour, T., Scholz, G. et al., A physiologically based biokinetic (PBBK) model for estragole bioactivation and detoxification in rat. Toxicol. Appl. Pharmacol. 2008, 231, 248-259.
10. Punt, A., Paini, A., Boersma, M. G., Freidig, A. P. et al., Use of physiologically based biokinetic (PBBK) modeling to study estragole bioactivation and detoxification in humans as compared with male rats. Toxicol. Sci. 2009, 110, 255-269.
11. Paini, A., Punt, A., Scholz, G., Gremaud, E. et al., In vivo validation of DNA adduct formation by estragole in rats predicted by physiologically based biodynamic modelling. Mutagenesis 2012, 27, 653-663.
12. Wiseman, R. W., Miller, E. C., Miller, J. A., Liem, A., Structure-activity studies of the hepatocarcinogenicities of alkenylbenzene derivatives related to estragole and safrole on administration to preweanling male C57BL/6J x C3H/HeJ F1 mice. Cancer Res. 1987, 47, 2275-2283.
13. Paini, A., Punt, A., Viton, F., Scholz, G. et al., A physiologically based biodynamic (PBBD) model for estragole DNA binding in rat liver based on in vitro kinetic data and estragole DNA adduct formation in primary hepatocytes. Toxicol. Appl. Pharmacol. 2010, 245, 57-66.
14. Fisher, M. B., Campanale, K., Ackermann, B. L., Vandenbranden, M. et al., In vitro glucuronidation using human liver microsomes and the pore-forming peptide alamethicin. Drug Metab. Dispos. 2000, 28, 560-566.
15. Li, H., Zhao, X., Ma, Y., Zhai, G. et al., Enhancement of gastrointestinal absorption of quercetin by solid lipid nanoparticles. J. Control. Release 2009, 133, 238-244.
16. Singh, S. P., Wahajuddin, Tewari, D., Patel, K. et al., Permeability determination and pharmacokinetic study of nobiletin in rat plasma and brain by validated high-performance liquid chromatography method. Fitoterapia 2011, 82, 1206-1214.
17. Medinsky, M. A., Leavens, T. L., Csanády, G. A., Gargas, M. L. et al., In vivo metabolism of butadiene by mice and rats: a comparison of physiological model predictions and experimental data. Carcinogenesis 1994, 15, 1329-1340.
18. van de Kerkhof, E. G., de Graaf, I. A. M., Groothuis, G. M. M., In vitro methods to study intestinal drug metabolism. Curr. Drug Metab. 2007, 8, 658-675.
19. Paini, A., Scholz, G., Boersma, M. G., Spenkelink, A. et al., Generation of in vitro data to model dose dependent in vivo DNA binding of genotoxic carcinogens and its consequences: the case of estragole. 2012, pp. 70-85. http://library.wur.nl/WebQuery/clc/1984285
20. Evans, M. V., Andersen, M. E., 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. 2000, 54, 71-80.
21. Koster, H., Scholtens, E., Mulder, G. J., Inhibition of sulfation of phenols in vivo by 2, 6-dichloro-4-nitrophenol: selectivity of its action in relation to other conjugations in the rat in vivo. Med. Biol. 1979, 57, 340-344.
22. Bamforth, K. J., Jones, A. L., Roberts, R. C., Coughtrie, M. W. H., Common food additives are potent inhibitors of human liver 17α-ethinyloestradiol and dopamine sulphotransferases. Biochem. Pharmacol. 1993, 46, 1713-1720.
23. Morimitsu, Y., Sugihara, N., Furuno, K., Inhibitory effect of flavonoids on sulfo- and glucurono-conjugation of acetaminophen in rat cultured hepatocytes and liver subcellular preparations. Biol. Pharm. Bull. 2004, 27, 714-717.
24. Gooderham, M. J., Adlercreutz, H., Ojala, S. T., Wähälä, K. et al., A soy protein isolate rich in genistein and daidzein and its effects on plasma isoflavone concentrations, platelet aggregation, blood lipids and fatty acid composition of plasma phospholipid in normal men. J. Nutr. 1996, 126, 2000-2006.
25. Walle, T., Methylation of dietary flavones greatly improves their hepatic metabolic stability and intestinal absorption. Mol. Pharmaceut. 2007, 4, 826-832.
26. Wen, X., Walle, T., Methylated flavonoids have greatly improved intestinal absorption and metabolic stability. Drug Metab. Dispos. 2006, 34, 1786-1792.
27. Phillips, D. H., Miller, J. A., Miller, E. C., Adams, B., Structures of the DNA adducts formed in mouse liver after administration of the proximate hepatocarcinogen 1'-hydroxyestragole. Cancer Res. 1981, 41, 176-186.
28. Punt, A., Delatour, T., Scholz, G., Schilter, B. et al., Tandem mass spectrometry analysis of N-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. 2007, 20, 991-998.
29. Wiseman, R. W., Fennell, T. R., Miller, J. A., Miller, E. C., 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. 1985, 45, 3096-3105.
30. Herrmann, K., Engst, W., Appel, K. E., Monien, B. H. et al., Identification of human and murine sulfotransferases able to activate hydroxylated metabolites of methyleugenol to mutagens in Salmonella typhimurium and detection of associated DNA adducts using UPLC-MS/MS methods. Mutagenesis 2012, 27, 453-462.
31. Herrmann, K., Schumacher, F., Engst, W., Appel, K. E. et al., Abundance of DNA adducts of methyleugenol, a rodent hepatocarcinogen, in human: Liver samples. Carcinogenesis 2013, 34, 1025-1030.
32. Ishii, Y., Suzuki, Y., Hibi, D., Jin, M. et al., Detection and quantification of specific DNA adducts by liquid chromatography-tandem mass spectrometry in the livers of rats given estragole at the carcinogenic dose. Chem. Res. Toxicol. 2011, 24, 532-541.
33. Suzuki, Y., Umemura, T., Ishii, Y., Hibi, D. et al., Possible involvement of sulfotransferase 1A1 in estragole-induced DNA modification and carcinogenesis in the livers of female mice. Mutat. Res. 2012, 749, 23-28.
34. EFSA, Opinion of the scientific committee on a request from EFSA related to a harmonised approach for risk assessment of substances which are both genotoxic and carcinogenic. EFSA J. 2005, 282, 1-31.
35. Miller, E. C., Swanson, A. B., Phillips, D. H., Fetcher, T. L. et al., Structure-activity studies of the carcinogenicities in the mouse and rat of some naturally occuring and synthetic alkenylbenzene derivatives related to safrole and estragole. Cancer Res. 1983, 43, 1124-1134.
36. van den Berg, S. J. P. L., Restani, P., Boersma, M. G., Delmulle, L. et al., Levels of genotoxic and carcinogenic compounds in plant food supplements and associated risk assessment. Food Nutr. Sci. 2011, 2, 989-1010.