Physiologically based biokinetic (PBBK) model for safrole bioactivation and detoxification in rats

Chemical Research in Toxicology

Volumn 24, Issue 6, 2011, Pages 818-834

  Martati, E ^a,b   Boersma, M G ^a   Spenkelink, A ^a   Khadka, D B ^a   Punt, A ^a   Vervoort, J ^a   Van Bladeren, P J ^a,c   Rietjens, I M C M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b BRAWIJAYA UNIVERSITY   (Indonesia)

^c NESTLÉ RESEARCH CENTER   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ALKENYL GROUP; ALLYL COMPOUND; BENZENE DERIVATIVE; CARCINOGEN; CYTOCHROME P450; DNA; GLUCURONIDE; METHYLEUGENOL; SAFROLE;

ARTICLE; BIOTRANSFORMATION; CARCINOGENICITY; DETOXIFICATION; DNA BINDING; FRACTIONATION; IN VITRO STUDY; IN VIVO STUDY; KINETICS; MALE; METABOLIC PARAMETERS; METABOLITE; NONHUMAN; OXIDATION; PHYSIOLOGICALLY BASED BIOKINETICS; PREDICTION; RAT;

ALLYL COMPOUNDS; ANIMALS; ANISOLES; BENZENE DERIVATIVES; CYTOCHROME P-450 ENZYME SYSTEM; EUGENOL; FOOD ADDITIVES; GLUCURONIDES; KINETICS; MALE; MODELS, BIOLOGICAL; MUTAGENS; OXIDATION-REDUCTION; RATS; RATS, SPRAGUE-DAWLEY; SAFROLE;

RATTUS;

EID: 79959452603     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx200032m     Document Type: Article

References (51)

1. Miller, J. A. and Miller, E. C. (1983) The metabolic activation and nucleic acid adducts of naturally-occurring carcinogens: recent results with ethyl carbamate and the spice flavors safrole and estragole Br. J. Cancer 48, 1-15 (Pubitemid 13067940)
2. 6 atom of adenine residues as sites for covalent binding of metabolically activated 1′-hydroxysafrole to mouse liver DNA in vivo Cancer Res. 41, 2664-2671 (Pubitemid 11071793)
3. Borchert, P., Miller, J. A., Miller, E. C., and Shires, T. K. (1973) 1′-Hydroxysafrole a proximate carcinogenic metabolite of safrole in the rat and mouse Cancer Res. 33, 590-600
4. Siano, F., Ghizzoni, C., Gionfriddo, F., Colombo, E., Servillo, L., and Castaldo, D. (2003) Determination of estragole, safrole and eugenol methyl ether in food products Food Chem. 81, 469-475 (Pubitemid 36349479)
5. Hwang, L. S., Wang, C. K., Shen, M. J., and Kao, L. S. (1992) Phenolic Compounds of Piper betle Flower As Flavoring and Neuronal Activity Modulating Agents, in Phenolic Compounds in Food and Their Effects on Health. I: Analysis, Occurrence and Chemistry (Ho, C. T., Lee, C. Y., and Huang, M. T., Eds.) pp 200 - 213, American Chemical Society, Washington, DC.
6. SCF (2002) Opinion of the Scientific Committee on Food on the safety of the presence of safrole (1-allyl-3,4- methylene dioxy benzene) in flavourings and other food ingredients with flavouring properties, http://ec.europa.eu/food/ fs/sc/scf/out116-en.pdf.
7. JECFA (2008) Evaluation of certain food additives. Sixty-ninth report of Joint FAO/WHO Expert Committe on Food Additives WHO Technical Report Series 952, http://whqlibdoc.who.int/trs/WHO-TRS-952-eng.pdf.
8. Wislocki, P. G., Borchert, P., Miller, J. A., and Miller, E. C. (1976) The metabolic activation of the carcinogen 1′-hydroxysafrole in vivo and in vitro and the electrophilic reactivities of possible ultimate carcinogens Cancer Res. 36, 1686-1695
9. 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 (Pubitemid 8095207)
10. Bolton, J. L., Acay, N. M., and Vukomanovic, V. (1994) Evidence that 4-allyl-o-quinones spontaneously rearrange to their more electrophilic quinone methides: potential bioactivation mechanism for the hepatocarcinogen safrole Chem. Res. Toxicol. 7, 443-450 (Pubitemid 24150107)
11. Ueng, Y.-F., Hsieh, C.-H., Don, M.-J., Chi, C.-W., and Ho, L.-K. (2004) Identification of the main human cytochrome P450 enzymes involved in safrole 1′-hydroxylation Chem. Res. Toxicol. 17, 1151-1156 (Pubitemid 39108682)
12. Jeurissen, S. M. F., Bogaards, J. J. P., Awad, H. M., Boersma, M. G., Brand, W., Fiamegos, Y. C., van Beek, T. A., Alink, G. M., Sudholter, E. J. R., Cnubben, N. H. P., and Rietjens, I. M. C. M. (2004) Human cytochrome P450 enzyme specificity for bioactivation of safrole to the proximate carcinogen 1-hydroxysafrole Chem. Res. Toxicol. 17, 1245-1250 (Pubitemid 39265880)
13. Liu, T.-Y., Chung, Y.-T., Wang, P.-F., Chi, C.-W., and Hsieh, L.-L. (2004) Safrole-DNA adducts in human peripheral blood an association with areca quid chewing and CYP2E1 polymorphisms Mutat. Res. 559, 59-66 (Pubitemid 38452918)
14. Ioannides, C., Delaforge, M., and Parke, D. V. (1981) Safrole: Its metabolism, carcinogenicity and interactions with cytochrome P-450 Food Cosmet. Toxicol. 19, 657-666 (Pubitemid 12205792)
15. Stillwell, W. G., Carman, M. J., Bell, L., and Horning, M. G. (1974) The metabolism of safrole and 2′,3′-epoxysafrole in the rat and guinea pig Drug Metab. Dispos. 2, 489-498
16. Benedetti, M. S., Malnoë, A., and Broillet, A. L. (1977) Absorption, metabolism and excretion of safrole in the rat and man Toxicology 7, 69-83 (Pubitemid 8041334)
17. Punt, A., Paini, A., Boersma, M. G., Freidig, A. P., Delatour, T., Scholz, G., Schilter, B., Bladeren, P. J. v., 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
18. 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
19. Borchert, P., Wislocki, P. G., Miller, J. A., and Miller, E. C. (1973) The metabolism of the naturally occurring hepatocarcinogen safrole to 1′-hydroxysafrole and the electrophilic reactivity of 1′- acetoxysafrole Cancer Res. 33, 575-589
20. Boberg, E. W., Miller, E. C., and Miller, J. A. (1986) The metabolic sulfonation and side-chain oxidation of 3′-hydroxyisosafrole in the mouse and its inactivity as a hepatocarcinogen relative to 1′-hydroxysafrole Chem.-Biol. Interact. 59, 73-97 (Pubitemid 16030993)
21. Chang, M. J. W., Ko, C. Y., Lin, R. F., and Hsieh, L. L. (2002) Biological monitoring of environment exposure to safrole and the Taiwanese betel quid chewing Arch. Environ. Contam. Toxicol. 43, 432-437 (Pubitemid 35215748)
22. Klungsøyr, J. and Scheline, R. R. (1982) Metabolism of isosafrole and dihydrosafrole in the rat Biomed. Mass Spectrom. 9, 323-329 (Pubitemid 13254193)
23. Lee-Chen, S.-F., Chen, C.-L., Ho, L.-Y., Hsu, P.-C., Chang, J.-T., Sun, C.-M., Chi, C.-W., and Liu, T.-Y. (1996) Role of oxidative DNA damage in hydroxychavicol-induced genotoxicity Mutagenesis 11, 519-523 (Pubitemid 26306169)
24. Nakagawa, Y., Suzuki, T., Nakajima, K., Ishii, H., and Ogata, A. (2009) Biotransformation and cytotoxic effects of hydroxychavicol, an intermediate of safrole metabolism, in isolated rat hepatocytes Chem.Biol. Interact. 180, 89-97
25. Klungsøyr, J. and Scheline, R. R. (1983) Metabolism of safrole in the rat Acta Pharmacol. Toxicol. 52, 211-216 (Pubitemid 13152378)
26. Angle, S. R., Choi, I., and Tham, F. S. (2008) Stereoselective synthesis of 3-alkyl-2-aryltetrahydrofuran-4-ols: total synthesis of (±)-Paulownin J. Org. Chem. 73, 6268-6278
27. Fisher, M. B., Campanale, K., Ackermann, B. L., VandenBranden, M., and Wrighton, S. A. (2000) In vitro glucuronidation using human liver microsomes and the pore-forming peptide alamethicin Drug Metab. Dispos. 28, 560-566 (Pubitemid 30238515)
28. Al-Subeihi, A. A. A., Spenkelink, B., Rachmawati, N., Boersma, M. G., Punt, A., Vervoort, J., van Bladeren, P. J., and Rietjens, I. M. C. M. (2011) Physiologically based biokinetic model of bioactivation and detoxification of the alkenylbenzene methyleugenol in rat Toxicol. in Vitro 25, 267-285
29. 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 (Pubitemid 18017569)
30. Medinsky, M. A., Leavens, T. L., Csanady, G. A., Gargas, M. L., and Bond, J. A. (1994) In vivo metabolism of butadiene by mice and rats: a comparison of physiological model predictions and experimental data Carcinogenesis 15, 1329-1340 (Pubitemid 24217683)
31. Beierschmitt, W. P. and Weiner, M. (1986) Age-related changes in renal metabolism of acetaminophen in male fischer 344 rats Age 9, 7-13 (Pubitemid 16169569)
32. Brown, R. P., Delp, M. D., Lindstedt, S. L., Rhomberg, L. R., and Beliles, R. P. (1997) Physiological parameter values for physiologically based pharmacokinetic models Toxicol. Ind. Health 13, 407-484 (Pubitemid 27314117)
33. DeJongh, J., Verhaar, H. J. M., and Hermens, J. L. M. (1997) A quantitative property-property relationship (QPPR) approach to estimate in vitro tissue-blood partition coefficients of organic chemicals in rats and humans Arch. Toxicol. 72, 17-25 (Pubitemid 28062388)
34. DeWoskin, R. S. (2007) PBPK models in risk assessment: A focus on chloroprene Chem.-Biol. Interact. 166, 352-359
35. Tardif, R., Droz, P.-O., Charest-Tardif, G., Pierrehumbert, G., and Truchon, G. (2002) Impact of human variability on the biological monitoring of exposure to toluene: I. Physiologically based toxicokinetic modelling Toxicol. Lett. 134, 155-163 (Pubitemid 35007299)
36. 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 (Pubitemid 30152457)
37. Garg, A. and Balthasar, J. (2007) Physiologically-based pharmacokinetic (PBPK) model to predict IgG tissue kinetics in wild-type and FcRn-knockout mice J. Pharmacokinet. Pharmacodyn. 34, 687-709 (Pubitemid 47477039)
38. Delaforge, M., Janiaud, P., Levi, P., and Morizot, J. P. (1980) Biotransformation of allylbenzene analogues in vivo and in vitro through the epoxide-diol pathway Xenobiotica 10, 737-744 (Pubitemid 11251356)
39. 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
40. 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 (Pubitemid 32200463)
41. Kishida, T., Muto, S., Hayashi, M., Tsutsui, M., Tanaka, S., Murakami, M., and Kuroda, J. (2008) Strain differences in hepatic cytochrome P450 1A and 3A expression between Sprague-Dawley and Wistar rats J. Toxicol. Sci. 33, 447-457
42. Boberg, E. W., Miller, E. C., Miller, J. A., Poland, A., and Liem, A. (1983) 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. 43, 5163-5173 (Pubitemid 14227494)
43. Miller, E. C., Swanson, A. B., Phillips, D. H., Fletcher, 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 (Pubitemid 13160033)
44. Swanson, A. B., Miller, E. C., and Miller, J. A. (1981) The side-chain epoxidation and hydroxylation of the hepatocarcinogens safrole and estragole and some related compounds by rat and mouse liver microsomes Biochim. Biophys. Acta 673, 504-516 (Pubitemid 11103749)
45. 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 (Pubitemid 8009095)
46. Phillips, D. H., Reddy, M. V., and Randerath, K. (1984) 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 (Pubitemid 15127028)
47. 32P-Postlabelling 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 (Pubitemid 15127027)
48. Daimon, H., Sawada, S., Asakura, S., and Sagami, F. (1998) In vivo genotoxicity and DNA adduct levels in the liver of rats treated with safrole Carcinogenesis 19, 141-146 (Pubitemid 28376836)
49. Zhou, G. D., Moorthy, B., Bi, J., Donnelly, K. C., and Randerath, K. (2007) DNA adducts from alkoxyallylbenzene herb and spice constituents in cultured human (HepG2) cells Environ. Mol. Mutagen. 48, 715-721 (Pubitemid 350305007)
50. Rietjens, I. M. C. M., Slob, W., Galli, C., and Silano, V. (2008) Risk assessment of botanicals and botanical preparations intended for use in food and food supplements: Emerging issues Toxicol. Lett. 180, 131-136
51. Rietjens, I. M. C. M., Punt, A., Schilter, B., Scholz, G., Delatour, T., and Bladeren, P. J. v. (2010) In silico methods for physiologically based biokinetic models describing bioactivation and detoxification of coumarin and estragole: Implications for risk assessment Mol. Nutr. Food Res. 54, 195-207