Evaluation of human embryonic stem cell-derived hepatocyte-like cells for detection of CYP1A inducers

Drug Metabolism and Pharmacokinetics

Volumn 27, Issue 6, 2012, Pages 598-604

  Tsuchiya, Hiroyuki ^a   Matsunaga, Tamihide ^b   Aikawa, Kaori ^a   Kamada, Noboru ^c   Nakamura, Katsunori ^a   Ichikawa, Hinako ^d   Sasaki, Katsunori ^d   Ohmori, Shigeru ^a  

^a SHINSHU UNIVERSITY HOSPITAL   (Japan)

^b NAGOYA CITY UNIVERSITY   (Japan)

^c KISSEI PHARMACEUTICAL CO LTD   (Japan)

^d SHINSHU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

CYP1A; Differentiation; HESC derived hepatocyte like cells; HESCs; Induction

Indexed keywords

3 METHYLCHOLANTHRENE; ALBUMIN; ALPHA FETOPROTEIN; CYTOCHROME P450 1A; CYTOCHROME P450 1A2; CYTOCHROME P450 3A4; CYTOCHROME P450 3A7; GLUCURONOSYLTRANSFERASE 1A1; MESSENGER RNA; OMEPRAZOLE;

ADULT; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG MECHANISM; DRUG SCREENING; EMBRYO; EMBRYONIC STEM CELL; ENZYME ACTIVITY; ENZYME INDUCTION; FETUS; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; LIVER CELL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION;

EID: 84871673923     PISSN: 13474367     EISSN: 18800920     Source Type: Journal    
DOI: 10.2133/dmpk.DMPK-12-RG-017     Document Type: Article

References (35)

1. Rodríguez-Antona, C., Donato, M. T., Boobis, A., Edwards, R. J., Watts, P. S., Castell, J. V. and Gómez-Lechón, M. J.: Cytochrome P450 expression in human hepatocytes and hepatoma cell lines: molecular mechanisms that determine lower expression in cultured cells. Xenobiotica, 32: 505-520 (2002).
2. Jensen, J., Hyllner, J. and Bj'rquist, P.: Human embryonic stem cell technologies and drug discovery. J. Cell. Physiol., 219: 513-519 (2009).
3. Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S. and Jones, J. M.: Embryonic stem cell lines derived from human blastocysts. Science, 282: 1145-1147 (1998).
4. Murry, C. E. and Keller, G.: Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell, 132: 661-680 (2008).
5. Shimada, T. and Fujii-Kuriyama, Y.: Metabolic activation of polycyclic aromatic hydrocarbons to carcinogens by cytochromes P450 1A1 and 1B1. Cancer Sci., 95: 1-6 (2004).
6. Sugimura, T., Wakabayashi, K., Nakagama, H. and Nagao, M.: Heterocyclic amines: Mutagens/carcinogens produced during cooking of meat and fish. Cancer Sci., 95: 290-299 (2004).
7. Wood, A. W., Chang, R. L., Levin, W., Thomas, P. E., Ryan, D., Stoming, T. A., Thakker, D. R., Jerina, D. M. and Conney, A. H.: Metabolic activation of 3-methylcholanthrene and its metabolites to products mutagenic to bacterial and mammalian cells. Cancer Res., 38: 3398-3404 (1978).
8. Suemori, H., Yasuchika, K., Hasegawa, K., Fujioka, T., Tsuneyoshi, N. and Nakatsuji, N.: Efficient establishment of human embryonic stem cell lines and long-term maintenance with stable karyotype by enzymatic bulk passage. Biochem. Biophys. Res. Commun., 345: 926-932 (2006).
9. Kubo, A., Shinozaki, K., Shannon, J. M., Kouskoff, V., Kennedy, M., Woo, S., Fehling, H. J. and Keller, G.: Development of definitive endoderm from embryonic stem cells in culture. Development, 131: 1651-1662 (2004).
10. D'Amour, K. A., Agulnick, A. D., Eliazer, S., Kelly, O. G., Kroon, E. and Baetge, E. E.: Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat. Biotechnol., 23: 1534-1541 (2005).
11. Cai, J., Zhao, Y., Liu, Y., Ye, F., Song, Z., Qin, H., Meng, S., Chen, Y., Zhou, R., Song, X., Guo, Y., Ding, M. and Deng, H.: Directed differentiation of human embryonic stem cells into functional hepatic cells. Hepatology, 45: 1229-1239 (2007).
12. Hay, D. C., Fletcher, J., Payne, C., Terrace, J. D., Gallagher, R. C., Snoeys, J., Black, J. R., Wojtacha, D., Samuel, K., Hannoun, Z., Pryde, A., Filippi, C., Currie, I. S., Forbes, S. J., Ross, J. A., Newsome, P. N. and Iredale, J. P.: Highly efficient differentiation of hESCs to functional hepatic endoderm requires ActivinA and Wnt3a signaling. Proc. Natl. Acad. Sci. USA, 105: 12301-12306 (2008).
13. Watanabe, K., Ueno, M., Kamiya, D., Nishiyama, A., Matsumura, M., Wataya, T., Takahashi, J. B., Nishikawa, S., Nishikawa, S., Muguruma, K. and Sasai, Y.: A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat. Biotechnol., 25: 681-686 (2007).
14. Takehara, T., Teramura, T., Onodera, Y., Kakegawa, R., Fukunaga, N., Takenoshita, M., Sagawa, N., Fukuda, K. and Hosoi, Y.: Rho-associated kinase inhibitor Y-27632 promotes survival of cynomolgus monkey embryonic stem cells. Mol. Hum. Reprod., 14: 627-634 (2008).
15. Jones, E. A., Clement-Jones, M., James, O. F. and Wilson, D. I.: Differences between human and mouse alpha-fetoprotein expression during early development. J. Anat., 198: 555-559 (2001).
16. Ek, M., S'derdahl, T., Küppers-Munther, B., Edsbagge, J., Andersson, T. B., Bj'rquist, P., Cotgreave, I., Jernstr'm, B., Ingelman-Sundberg, M. and Johansson, I.: Expression of drug metabolizing enzymes in hepatocyte-like cells derived from human embryonic stem cells. Biochem. Pharmacol., 74: 496-503 (2007).
17. Hay, D. C., Zhao, D., Fletcher, J., Hewitt, Z. A., McLean, D., Urruticoechea-Uriguen, A., Black, J. R., Elcombe, C., Ross, J. A., Wolf, R. and Cui, W.: Efficient differentiation of hepatocytes from human embryonic stem cells exhibiting markers recapitulating liver development in vivo. Stem Cells, 26: 894-902 (2008).
18. Agarwal, S., Holton, K. L. and Lanza, R.: Efficient differentiation of functional hepatocytes from human embryonic stem cells. Stem Cells, 26: 1117-1127 (2008).
19. Duan, Y., Ma, X., Zou, W., Wang, C., Bahbahan, I. S., Ahuja, T. P., Tolstikov, V. and Zern, M. A.: Differentiation and characterization of metabolically functioning hepatocytes from human embryonic stem cells. Stem Cells, 28: 674-686 (2010).
20. Baharvand, H., Hashemi, S. M., Kazemi Ashtiani, S. and Farrokhi, A.: Differentiation of human embryonic stem cells into hepatocytes in 2D and 3D culture systems in vitro. Int. J. Dev. Biol., 50: 645-652 (2006).
21. Elkayam, T., Amitay-Shaprut, S., Dvir-Ginzberg, M., Harel, T. and Cohen, S.: Enhancing the drug metabolism activities of C3A-a human hepatocyte cell line-by tissue engineering within alginate scaffolds. Tissue Eng., 12: 1357-1368 (2006).
22. Sasaki, K., Ichikawa, H., Takei, S., No, H. S., Tomotsune, D., Kano, Y., Yokoyama, T., Sirasawa, S., Mogi, A., Yoshie, S., Sasaki, S., Yamada, S., Matsumoto, K., Mizuguchi, M., Yue, F. and Tanaka, Y.: Hepatocyte differentiation from human ES cells using the simple embryoid body formation method and the stagedadditional cocktail. ScientificWorldJournal, 9: 884-890 (2009).
23. Takayama, K., Inamura, M., Kawabata, K., Katayama, K., Higuchi, M., Tashiro, K., Nonaka, A., Sakurai, F., Hayakawa, T., Kusuda Furue, M. and Mizuguchi, H.: Efficient generation of functional hepatocytes from human embryonic stem cells and induced pluripotent stem cells by HNF4α transduction. Mol. Ther., 20: 127-137 (2012).
24. Whitlock, J. P., Jr.: Induction of cytochrome P4501A1. Annu. Rev. Pharmacol. Toxicol., 39: 103-125 (1999).
25. Denison, M. S. and Nagy, S. R.: Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu. Rev. Pharmacol. Toxicol., 43: 309-334 (2003).
26. Nebert, D. W., Dalton, T. P., Okey, A. B. and Gonzalez, F. J.: Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J. Biol. Chem., 279: 23847-23850 (2004).
27. Daujat, M., Peryt, B., Lesca, P., Fourtanier, G., Domergue, J. and Maurel, P.: Omeprazole, an inducer of human CYP1A1 and 1A2, is not a ligand for the Ah receptor. Biochem. Biophys. Res. Commun., 188: 820-825 (1992).
28. Quattrochi, L. C. and Tukey, R. H.: Nuclear uptake of the Ah (dioxin) receptor in response to omeprazole: transcriptional activation of the human CYP1A1 gene. Mol. Pharmacol., 43: 504-508 (1993).
29. Lesca, P., Peryt, B., Larrieu, G., Alvinerie, M., Galtier, P., Daujat, M., Maurel, P. and Hoogenboom, L.: Evidence for the ligand-independent activation of the AH receptor. Biochem. Biophys. Res. Commun., 209: 474-482 (1995).
30. Daujat, M., Charrasse, S., Fabre, I., Lesca, P., Jounaïdi, Y., Larroque, C., Poellinger, L. and Maurel, P.: Induction of CYP1A1 gene by benzimidazole derivatives during Caco-2 cell differentiation. Evidence for an aryl-hydrocarbon receptor-mediated mechanism. Eur. J. Biochem., 237: 642-652 (1996).
31. Kalthoff, S., Ehmer, U., Freiberg, N., Manns, M. P. and Strassburg, C. P.: Coffee induces expression of glucuronosyltransferases by the aryl hydrocarbon receptor and Nrf2 in liver and stomach. Gastroenterology, 139: 1699-1710 (2010).
32. Ueda, R., Iketaki, H., Nagata, K., Kimura, S., Gonzalez, F. J., Kusano, K., Yoshimura, T. and Yamazoe, Y.: A common regulatory region functions bidirectionally in transcriptional activation of the human CYP1A1 and CYP1A2 genes. Mol. Pharmacol., 69: 1924-1930 (2006).
33. Matsunaga, T., Maruyama, M., Harada, E., Katsuyama, Y., Sugihara, N., Ise, H., Negishi, N., Ikeda, U. and Ohmori, S.: Expression and induction of CYP3As in human fetal hepatocytes. Biochem. Biophys. Res. Commun., 318: 428-434 (2004).
34. Takezawa, T., Matsunaga, T., Aikawa, K., Nakamura, K. and Ohmori, S.: Lower expression of HNF4α and PGC1α might impair rifampicin-mediated CYP3A4 induction under conditions where PXR overexpressed in human fetal liver cells. Drug Metab. Pharmacokinet., 27: 430-438 (2012).
35. Duan, Y., Catana, A., Meng, Y., Yamamoto, N., He, S., Gupta, S., Gambhir, S. S. and Zern, M. A.: Differentiation and enrichment of hepatocyte-like cells from human embryonic stem cells in vitro and in vivo. Stem Cells, 25: 3058-3068 (2007).