An efficient method for differentiation of human induced pluripotent stem cells into hepatocyte-like cells retaining drug metabolizing activity

Drug Metabolism and Pharmacokinetics

Volumn 29, Issue 3, 2014, Pages 237-243

  Kondo, Yuki ^a   Iwao, Takahiro ^a   Nakamura, Katsunori ^a   Sasaki, Takamitsu ^b   Takahashi, Shogo ^b   Kamada, Noboru ^c   Matsubara, Tsutomu ^d,e   Gonzalez, Frank J ^d   Akutsu, Hidenori ^f   Miyagawa, Yoshitaka ^f   Okita, Hajime ^f   Kiyokawa, Nobutaka ^f   Toyoda, Masashi ^f   Umezawa, Akihiro ^f   Nagata, Kiyoshi ^b   Matsunaga, Tamihide ^a   Ohmori, Shigeru ^g  

^a NAGOYA CITY UNIVERSITY   (Japan)

^b TOHOKU PHARMACEUTICAL UNIVERSITY   (Japan)

^c KISSEI PHARMACEUTICAL CO LTD   (Japan)

^d NATIONAL CANCER INSTITUTE   (United States)

^e OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f NATIONAL RESEARCH INSTITUTE FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^g SHINSHU UNIVERSITY HOSPITAL   (Japan)

Author keywords

CYP; Differentiation; Drug metabolizing enzyme; Hepatocyte; IPS

Indexed keywords

ACTIVIN A; ALBUMIN; CYTOCHROME P450 3A4; DEXAMETHASONE; DIMETHYL SULFOXIDE; DRUG METABOLIZING ENZYME; GLUCURONOSYLTRANSFERASE 1A1; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; ONCOSTATIN M; SCATTER FACTOR; ACTIVIN; CYP3A4 PROTEIN, HUMAN; CYTOCHROME P450 3A; GLUCURONOSYLTRANSFERASE; MESSENGER RNA; STEROID HORMONE 6-BETA-HYDROXYLASE; STEROID MONOOXYGENASE; UGT1A1 ENZYME;

ADULT; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; DRUG METABOLISM; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER CELL; MALE; MICROARRAY ANALYSIS; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; CELL LINE; DRUG INACTIVATION; GENETICS; METABOLISM; PHYSIOLOGY;

ACTIVINS; CELL DIFFERENTIATION; CELL LINE; CYTOCHROME P-450 CYP3A; DEXAMETHASONE; DIMETHYL SULFOXIDE; GLUCURONOSYLTRANSFERASE; HEPATOCYTE GROWTH FACTOR; HEPATOCYTES; HUMANS; INACTIVATION, METABOLIC; INDUCED PLURIPOTENT STEM CELLS; ONCOSTATIN M; RNA, MESSENGER; STEROID HYDROXYLASES;

EID: 84903593865     PISSN: 13474367     EISSN: 18800920     Source Type: Journal    
DOI: 10.2133/dmpk.DMPK-13-RG-104     Document Type: Article

References (46)

1. Park, I. H., Zhao, R., West, J. A., Yabuuchi, A., Huo, H., Ince, T. A., Lerou, P. H., Lensch, M. W. and Daley, G. Q.: Reprogramming of human somatic cells to pluripotency with defined factors. Nature, 451: 141-146 (2008).
2. Lowry, W. E., Richter, L., Yachechko, R., Pyle, A. D., Tchieu, J., Sridharan, R., Clark, A. T. and Plath, K.: Generation of human induced pluripotent stem cells from dermal fibroblasts. Proc. Natl. Acad. Sci. USA, 105: 2883-2888 (2008).
3. Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K. and Yamanaka, S.: Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 131: 861-872 (2007).
4. Takahashi, K. and Yamanaka, S.: Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126: 663-676 (2006).
5. Ochiya, T., Yamamoto, Y. and Banas, A.: Commitment of stem cells into functional hepatocytes. Differentiation, 79: 65-73 (2010).
6. Hannoun, Z., Filippi, C., Sullivan, G., Hay, D. C. and Iredale, J. P.: Hepatic endoderm differentiation from human embryonic stem cells. Curr. Stem Cell Res. Ther., 5: 233-244 (2010).
7. Lacroix, D., Sonnier, M., Moncion, A., Cheron, G. and Cresteil, T.: Expression of CYP3A in the human liver-Evidence that the shift between CYP3A7 and CYP3A4 occurs immediately after birth. Eur. J. Biochem., 247: 625-634 (1997).
8. Stevens, J. C., Hines, R. N., Gu, C., Koukouritaki, S. B., Manro, J. R., Tandler, P. J. and Zaya, M. J.: Developmental Expression of the Major Human Hepatic CYP3A Enzymes. J. Pharmacol. Exp. Ther., 307: 573-582 (2003).
9. Shimada, T., Yamazaki, H., Mimura, M., Inui, Y. and Guengerich, F. P.: Interindividual variations in human liver cytochrome P-450 enzymes involved in the oxidation of drugs, carcinogens and toxic chemicals: studies with liver microsomes of 30 Japanese and 30 Caucasians. J. Pharmacol. Exp. Ther., 270: 414-423 (1994).
10. Wienkers, L. C. and Health, T. G.: Predicting in vivo drug interactions from in vitro drug discovery data. Nat. Rev. Drug Discov., 4: 825-833 (2005).
11. Li, A. P., Rasmussen, A., Xu, L. and Kaminski, D. L.: Rifampicin induction of lidocaine metabolism in cultured human hepatocytes. J. Pharmacol. Exp. Ther., 274: 673-677 (1995).
12. Kocarek, T. A., Schuetz, E. G., Strom, S. C., Fisher, R. A. and Guzelian, P. S.: Comparative analysis of cytochrome P4503A induction in primary cultures of rat, rabbit, and human hepatocytes. Drug Metab. Dispos., 23: 415-421 (1995).
13. Silva, J. M., Morin, P. E., Day, S. H., Kennedy, B. P., Payette, P., Rushmore, T., Yergey, J. A. and Nicoll-Griffith, D. A.: Refinement of an in vitro cell model for cytochrome P450 induction. Drug Metab. Dispos., 26: 490-496 (1998).
14. Cai, J., Zhao, Y., Liu, Y., Ye, F., Song, Z., Qin, H., Meng, S., Chen, Y., Zhou, R., et al.: Directed differentiation of human embryonic stem cells into functional hepatic cells. Hepatology, 45: 1229-1239 (2007).
15. Si-Tayeb, K., Noto, F. K., Nagaoka, M., Li, J., Battle, M. A., Duris, C., North, P. E., Dalton, S. and Duncan, S. A.: Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology, 51: 297-305 (2010).
16. Touboul, T., Hannan, N. R., Corbineau, S., Martinez, A., Martinet, C., Branchereau, S., Mainot, S., Strick-Marchand, H., Pedersen, R., et al.: Generation of functional hepatocytes from human embryonic stem cells under chemically defined conditions that recapitulate liver development. Hepatology, 51: 1754-1765 (2010).
17. Song, Z., Cai, J., Liu, Y., Zhao, D., Yong, J., Duo, S., Song, X., Guo, Y., Zhao, Y., et al.: Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells. Cell Res., 19: 1233-1242 (2009).
18. Takayama, K., Inamura, M., Kawabata, K., Katayama, K., Higuchi, M., Tashiro, K., Nonaka, A., Sakurai, F., Hayakawa, T., et al.: Efficient generation of functional hepatocytes from human embryonic stem cells and induced pluripotent stem cells by HNF4α transduction. Mol. Ther., 20: 127-137 (2012).
19. Takayama, K., Inamura, M., Kawabata, K., Sugawara, M., Kikuchi, K., Higuchi, M., Nagamoto, Y., Watanabe, H., Tashiro, K., et al.: Generation of metabolically functioning hepatocytes from human pluripotent stem cells by FOXA2 and HNF1α transduction. J. Hepatol., 57: 628-636 (2012).
20. Nagamoto, Y., Tashiro, K., Takayama, K., Ohashi, K., Kawabata, K., Sakurai, F., Tachibana, M., Hayakawa, T., Furue, M. K., et al.: The promotion of hepatic maturation of human pluripotent stem cells in 3D co-culture using type I collagen and Swiss 3T3 cell sheets. Biomaterials, 33: 4526-4534 (2012).
21. Amimoto, N., Mizumoto, H., Nakazawa, K., Ijima, H., Funatsu, K. and Kajiwara, T.: Hepatic differentiation of mouse embryonic stem cells and induced pluripotent stem cells during organoid formation in hollow fibers. Tissue Eng. Part A, 2011(17): 2071-2078 (2011).
22. Tsuchiya, H., Matsunaga, T., Aikawa, K., Kamada, N., Nakamura, K., Ichikawa, H., Sasaki, K. and Ohmori, S.: Evaluation of human embryonic stem cell-derived hepatocyte-like cells for detection of CYP1A inducers. Drug Metab. Pharmacokinet., 27: 598-604 (2012).
23. Momose, Y., Matsunaga, T., Murai, K., Takezawa, T. and Ohmori, S.: Differentiation of monkey embryonic stem cells into hepatocytes and mRNA expression of cytochrome P450 enzymes responsible for drug metabolism: comparison of embryoid body formation conditions and matrices. Biol. Pharm. Bull., 32: 619-626 (2009).
24. Maruyama, M., Matsunaga, T., Harada, E. and Ohmori, S.: Comparison of basal gene expression and induction of CYP3As in HepG2 and human fetal liver cells. Biol. Pharm. Bull., 30: 2091-2097 (2007).
25. Nishimura, M., Koeda, A., Suganuma, Y., Suzuki, E., Shimizu, T., Nakayama, M., Satoh, T., Narimatsu, S. and Naito, S.: Comparison of inducibility of CYP1A and CYP3A mRNAs by prototypical inducers in primary cultures of human, cynomolgus monkey, and rat hepatocytes. Drug Metab. Pharmacokinet., 22: 178-186 (2007).
26. Maezawa, K., Matsunaga, T., Takezawa, T., Kanai, M., Ohira, S. and Ohmori, S.: Cytochrome P450 3As gene expression and testosterone 6- hydroxylase activity in human fetal membranes and placenta at full term. Biol. Pharm. Bull., 33: 249-254 (2010).
27. 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).
28. Hay, D. C., Zhao, D., Fletcher, J., Hewitt, Z. A., McLean, D., Urruticoechea-Uriguen, A., Black, J. R., Elcombe, C., Ross, J. A., et al.: Efficient differentiation of hepatocytes from human embryonic stem cells exhibiting markers recapitulating liver development in vivo. Stem Cells, 26: 894-902 (2008).
29. Kamiya, A., Kinoshita, T., Ito, Y., Matsui, T., Morikawa, Y., Senba, E., Nakashima, K., Taga, T., Yoshida, K., et al.: Fetal liver development requires a paracrine action of oncostatin M through the gp130 signal transducer. EMBO J., 18: 2127-2136 (1999).
30. Kamiya, A., Kinoshita, T. and Miyajima, A.: Oncostatin M and hepatocyte growth factor induce hepatic maturation via distinct signaling pathways. FEBS Lett., 492: 90-94 (2001).
31. Suzuki, A., Iwama, A., Miyashita, H., Nakauchi, H. and Taniguchi, H.: Role for growth factors and extracellular matrix in controlling differentiation of prospectively isolated hepatic stem cells. Development, 130: 2513-2524 (2003).
32. Chou, J. Y.: Regulators of fetal liver differentiation in vitro. Arch. Biochem. Biophys., 263: 378-386 (1988).
33. Jochheim, A., Hillemann, T., Kania, G., Scharf, J., Attaran, M., Manns, M. P., Wobus, A. M. and Ott, M.: Quantitative gene expression profiling reveals a fetal hepatic phenotype of murine ES-derived hepatocytes. Int. J. Dev. Biol., 48: 23-29 (2004).
34. Kondraganti, S. R., Jiang, W. and Moorthy, B.: Differential regulation of expression of hepatic and pulmonary cytochrome P4501A enzymes by 3- methylcholanthrene in mice lacking the CYP1A2 gene. J. Pharmacol. Exp. Ther., 303: 945-951 (2002).
35. Bock, K. W.: Functions and transcriptional regulation of adult human hepatic UDP-glucuronosyl-transferases (UGTs): mechanisms responsible for interindividual variation of UGT levels. Biochem. Pharmacol., 80: 771-777 (2010).
36. 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).
37. Kamiya, A., Kojima, N., Kinoshita, T., Sakai, Y. and Miyaijma, A.: Maturation of fetal hepatocytes in vitro by extracellular matrices and oncostatin M: induction of tryptophan oxygenase. Hepatology, 35: 1351-1359 (2002).
38. Cerec, V., Glaise, D., Garnier, D., Morosan, S., Turlin, B., Drenou, B., Gripon, P., Kremsdorf, D., Guguen-Guillouzo, C., et al.: Transdifferentiation of hepatocyte-like cells from the human hepatoma HepaRG cell line through bipotent progenitor. Hepatology, 45: 957-967 (2007).
39. Oda, H., Nozawa, K., Hitomi, Y. and Kakinuma, A.: Laminin-rich extracellular matrix maintains high level of hepatocyte nuclear factor 4 in rat hepatocyte culture. Biochem. Biophys. Res. Commun., 212: 800-805 (1995).
40. Caron, J. M.: Induction of albumin gene transcription in hepatocytes by extracellular matrix proteins. Mol. Cell. Biol., 10: 1239-1243 (1990).
41. Gibson, G. G., Plant, N. J., Swales, K. E., Ayrton, A. and El-Sankary, W.: Receptor-dependent transcriptional activation of cytochrome P4503A genes: induction mechanisms, species differences and interindividual variation in man. Xenobiotica, 32: 165-206 (2002).
42. Sinz, M., Wallace, G. and Sahi, J.: Current industrial practices in assessing CYP450 enzyme induction: preclinical and clinical. AAPS J., 10: 391-400 (2008).
43. Krusekopf, S., Roots, I. and Kleeberg, U.: Differential drug-induced mRNA expression of human CYP3A4 compared to CYP3A5, CYP3A7 and CYP3A43. Eur. J. Pharmacol., 466: 7-12 (2003).
44. Ring, J. A., Ghabrial, H., Ching, M. S., Smallwood, R. A. and Morgan, D. J.: Fetal hepatic drug elimination. Pharmacol. Ther., 84: 429-445 (1999).
45. Osafune, K., Caron, L., Borowiak, M., Martinez, R. J., Fitz-Gerald, C. S., Sato, Y., Cowan, C. A., Chien, K. R. and Melton, D. A.: Marked differences in differentiation propensity among human embryonic stem cell lines. Nat. Biotechnol., 26: 313-315 (2008).
46. Kajiwara, M., Aoi, T., Okita, K., Takahashi, R., Inoue, H., Takayama, N., Endo, H., Eto, K., Toguchida, J., et al.: Donor-dependent variations in hepatic differentiation from human-induced pluripotent stem cells. Proc. Natl. Acad. Sci. USA, 109: 12538-12543 (2012).