Small-molecule-driven hepatocyte differentiation of human pluripotent stem cells

Stem Cell Reports

Volumn 4, Issue 5, 2015, Pages 939-952

  Siller, Richard ^a   Greenhough, Sebastian ^a   Naumovska, Elena ^a   Sullivan, Gareth J ^a,b,c  

^a UNIVERSITY OF OSLO   (Norway)

^b Norwegian Center for Stem Cell Research   (Norway)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

DEXAMETHASONE; DIMETHYL SULFOXIDE; GLUCOCORTICOID; GLYCOGEN SYNTHASE KINASE 3; GROWTH FACTOR; HYDROCORTISONE SODIUM SUCCINATE; INDOCYANINE GREEN; INSULIN; N HEXANOIC TRYSOSYLISOLEUCYL AMINOHEXANOC AMIDE; OMEPRAZOLE; RIFAMPICIN; STEM CELL FACTOR RECEPTOR; STEM CELL FACTOR RECEPTOR AGONIST; UNCLASSIFIED DRUG; GLYCOGEN; MOLECULAR LIBRARY; N-HEXANOIC-TYR-ILE-(6) AMINOHEXANOIC AMIDE; OLIGOPEPTIDE; PLASMA PROTEIN; SCATTER FACTOR RECEPTOR;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENDODERM; ENZYME INHIBITION; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; HUMAN; HUMAN CELL; LIVER CELL; LIVER FUNCTION; MORPHOLOGY; PHASE CONTRAST MICROSCOPY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; AGONISTS; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; METABOLISM; MOLECULAR LIBRARY; PHARMACOLOGY;

BLOOD PROTEINS; CELL DIFFERENTIATION; CELLS, CULTURED; DEXAMETHASONE; DIMETHYL SULFOXIDE; GLYCOGEN; GLYCOGEN SYNTHASE KINASE 3; HEPATOCYTES; HUMANS; MICROSCOPY, FLUORESCENCE; OLIGOPEPTIDES; PLURIPOTENT STEM CELLS; PROTO-ONCOGENE PROTEINS C-MET; SMALL MOLECULE LIBRARIES;

EID: 84929291312     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2015.04.001     Document Type: Article

References (47)

1. S. Agarwal, K.L. Holton, and R. Lanza Efficient differentiation of functional hepatocytes from human embryonic stem cells Stem Cells 26 2008 1117 1127
2. S.L. Ang, A. Wierda, D. Wong, K.A. Stevens, S. Cascio, J. Rossant, and K.S. Zaret The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of HNF3/forkhead proteins Development 119 1993 1301 1315
3. K. Asahina, H. Fujimori, K. Shimizu-Saito, Y. Kumashiro, K. Okamura, Y. Tanaka, K. Teramoto, S. Arii, and H. Teraoka Expression of the liver-specific gene Cyp7a1 reveals hepatic differentiation in embryoid bodies derived from mouse embryonic stem cells Genes Cells 9 2004 1297 1308
4. H. Baharvand, S.M. Hashemi, S. Kazemi Ashtiani, and A. Farrokhi Differentiation of human embryonic stem cells into hepatocytes in 2D and 3D culture systems in vitro Int. J. Dev. Biol. 50 2006 645 652
5. H. Basma, A. Soto-Gutiérrez, G.R. Yannam, L. Liu, R. Ito, T. Yamamoto, E. Ellis, S.D. Carson, S. Sato, and Y. Chen Differentiation and transplantation of human embryonic stem cell-derived hepatocytes Gastroenterology 136 2009 990 999
6. M. Blum, S.J. Gaunt, K.W. Cho, H. Steinbeisser, B. Blumberg, D. Bittner, and E.M. De Robertis Gastrulation in the mouse: the role of the homeobox gene goosecoid Cell 69 1992 1097 1106
7. M. Borowiak, R. Maehr, S. Chen, A.E. Chen, W. Tang, J.L. Fox, S.L. Schreiber, and D.A. Melton Small molecules efficiently direct endodermal differentiation of mouse and human embryonic stem cells Cell Stem Cell 4 2009 348 358
8. G. Brolén, L. Sivertsson, P. Björquist, G. Eriksson, M. Ek, H. Semb, I. Johansson, T.B. Andersson, M. Ingelman-Sundberg, and N. Heins Hepatocyte-like cells derived from human embryonic stem cells specifically via definitive endoderm and a progenitor stage J. Biotechnol. 145 2010 284 294
9. J. Cai, Y. Zhao, Y. Liu, F. Ye, Z. Song, H. Qin, S. Meng, Y. Chen, R. Zhou, and X. Song Directed differentiation of human embryonic stem cells into functional hepatic cells Hepatology 45 2007 1229 1239
10. S.M. Chambers, Y. Qi, Y. Mica, G. Lee, X.-J. Zhang, L. Niu, J. Bilsland, L. Cao, E. Stevens, and P. Whiting Combined small-molecule inhibition accelerates developmental timing and converts human pluripotent stem cells into nociceptors Nat. Biotechnol. 30 2012 715 720
11. Y.-F. Chen, C.-Y. Tseng, H.-W. Wang, H.-C. Kuo, V.W. Yang, and O.K. Lee Rapid generation of mature hepatocyte-like cells from human induced pluripotent stem cells by an efficient three-step protocol Hepatology 55 2012 1193 1203
12. K.A. D'Amour, A.D. Agulnick, S. Eliazer, O.G. Kelly, E. Kroon, and E.E. Baetge Efficient differentiation of human embryonic stem cells to definitive endoderm Nat. Biotechnol. 23 2005 1534 1541
13. S. Engert, I. Burtscher, W.P. Liao, S. Dulev, G. Schotta, and H. Lickert Wnt/β-catenin signalling regulates Sox17 expression and is essential for organizer and endoderm formation in the mouse Development 140 2013 3128 3138
14. M.C. Garcia, C. Thangavel, and B.H. Shapiro Epidermal growth factor regulation of female-dependent CYP2A1 and CYP2C12 in primary rat hepatocyte culture Drug Metab. Dispos. 29 2001 111 120
15. S. Han, A. Bourdon, W. Hamou, N. Dziedzic, O. Goldman, and V. Gouon-Evans Generation of functional hepatic cells from pluripotent stem cells J. Stem Cell Res. Ther. Suppl 10 2012 1 7
16. N.R.F. Hannan, C.-P. Segeritz, T. Touboul, and L. Vallier Production of hepatocyte-like cells from human pluripotent stem cells Nat. Protoc. 8 2013 430 437
17. D.C. Hay, J. Fletcher, C. Payne, J.D. Terrace, R.C.J. Gallagher, J. Snoeys, J.R. Black, D. Wojtacha, K. Samuel, and Z. Hannoun Highly efficient differentiation of hESCs to functional hepatic endoderm requires ActivinA and Wnt3a signaling Proc. Natl. Acad. Sci. USA 105 2008 12301 12306
18. T. Imamura, L. Cui, R. Teng, K. Johkura, Y. Okouchi, K. Asanuma, N. Ogiwara, and K. Sasaki Embryonic stem cell-derived embryoid bodies in three-dimensional culture system form hepatocyte-like cells in vitro and in vivo Tissue Eng. 10 2004 1716 1724
19. J. Itskovitz-Eldor, M. Schuldiner, D. Karsenti, A. Eden, O. Yanuka, M. Amit, H. Soreq, and N. Benvenisty Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers Mol. Med. 6 2000 88 95
20. K.H. Kaestner The making of the liver: developmental competence in foregut endoderm and induction of the hepatogenic program Cell Cycle 4 2005 1146 1148
21. M. Kanai-Azuma, Y. Kanai, J.M. Gad, Y. Tajima, C. Taya, M. Kurohmaru, Y. Sanai, H. Yonekawa, K. Yazaki, P.P.L. Tam, and Y. Hayashi Depletion of definitive gut endoderm in Sox17-null mutant mice Development 129 2002 2367 2379
22. Y. Kunisada, N. Tsubooka-Yamazoe, M. Shoji, and M. Hosoya Small molecules induce efficient differentiation into insulin-producing cells from human induced pluripotent stem cells Stem Cell Res. (Amst.) 8 2012 274 284
23. X. Lian, C. Hsiao, G. Wilson, K. Zhu, L.B. Hazeltine, S.M. Azarin, K.K. Raval, J. Zhang, T.J. Kamp, and S.P. Palecek Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling Proc. Natl. Acad. Sci. USA 109 2012 E1848 E1857
24. H. Liu, Z. Ye, Y. Kim, S. Sharkis, and Y.-Y. Jang Generation of endoderm-derived human induced pluripotent stem cells from primary hepatocytes Hepatology 51 2010 1810 1819
25. C.C. Lu, J. Brennan, and E.J. Robertson From fertilization to gastrulation: axis formation in the mouse embryo Curr. Opin. Genet. Dev. 11 2001 384 392
26. T.H.-W. Lüdtke, V.M. Christoffels, M. Petry, and A. Kispert Tbx3 promotes liver bud expansion during mouse development by suppression of cholangiocyte differentiation Hepatology 49 2009 969 978
27. A.T. McCoy, C.C. Benoist, J.W. Wright, L.H. Kawas, J.M. Bule-Ghogare, M. Zhu, S.M. Appleyard, G.A. Wayman, and J.W. Harding Evaluation of metabolically stabilized angiotensin IV analogs as procognitive/antidementia agents J. Pharmacol. Exp. Ther. 344 2013 141 154
28. A.P. Monaghan, K.H. Kaestner, E. Grau, and G. Schütz Postimplantation expression patterns indicate a role for the mouse forkhead/HNF-3 alpha, beta and gamma genes in determination of the definitive endoderm, chordamesoderm and neuroectoderm Development 119 1993 567 578
29. M. Nakanishi, A. Kurisaki, Y. Hayashi, M. Warashina, S. Ishiura, M. Kusuda-Furue, and M. Asashima Directed induction of anterior and posterior primitive streak by Wnt from embryonic stem cells cultured in a chemically defined serum-free medium FASEB J. 23 2009 114 122
30. L. Rambhatla, C.-P. Chiu, P. Kundu, Y. Peng, and M.K. Carpenter Generation of hepatocyte-like cells from human embryonic stem cells Cell Transplant. 12 2003 1 11
31. H. Sasaki, and B.L. Hogan Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo Development 118 1993 47 59
32. N. Sato, L. Meijer, L. Skaltsounis, P. Greengard, and A.H. Brivanlou Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor Nat. Med. 10 2004 55 63
33. S.D. Schwartz, J.-P. Hubschman, G. Heilwell, V. Franco-Cardenas, C.K. Pan, R.M. Ostrick, E. Mickunas, R. Gay, I. Klimanskaya, and R. Lanza Embryonic stem cell trials for macular degeneration: a preliminary report Lancet 379 2012 713 720
34. K. Si-Tayeb, F.P. Lemaigre, and S.A. Duncan Organogenesis and development of the liver Dev. Cell 18 2010 175 189
35. K. Si-Tayeb, F.K. Noto, M. Nagaoka, J. Li, M.A. Battle, C. Duris, P.E. North, S. Dalton, and S.A. Duncan Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells Hepatology 51 2010 297 305
36. G.S. Sineva, and V.A. Pospelov Inhibition of GSK3beta enhances both adhesive and signalling activities of beta-catenin in mouse embryonic stem cells Biol. Cell 102 2010 549 560
37. Z. Song, J. Cai, Y. Liu, D. Zhao, J. Yong, S. Duo, X. Song, Y. Guo, Y. Zhao, and H. Qin Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells Cell Res. 19 2009 1233 1242
38. B. Sosa-Pineda, J.T. Wigle, and G. Oliver Hepatocyte migration during liver development requires Prox1 Nat. Genet. 25 2000 254 255
39. A. Soto-Gutierrez, N. Navarro-Alvarez, J.D. Rivas-Carrillo, Y. Chen, T. Yamatsuji, N. Tanaka, and N. Kobayashi Differentiation of human embryonic stem cells to hepatocytes using deleted variant of HGF and poly-amino-urethane-coated nonwoven polytetrafluoroethylene fabric Cell Transplant. 15 2006 335 341
40. A. Soto-Gutiérrez, N. Navarro-Alvarez, D. Zhao, J.D. Rivas-Carrillo, J. Lebkowski, N. Tanaka, I.J. Fox, and N. Kobayashi Differentiation of mouse embryonic stem cells to hepatocyte-like cells by co-culture with human liver nonparenchymal cell lines Nat. Protoc. 2 2007 347 356
41. S. Ström, F. Holm, R. Bergström, A.-M. Strömberg, and O. Hovatta Derivation of 30 human embryonic stem cell lines - improving the quality In Vitro Cell. Dev. Biol. Anim. 46 2010 337 344
42. G.J. Sullivan, D.C. Hay, I.-H. Park, J. Fletcher, Z. Hannoun, C.M. Payne, D. Dalgetty, J.R. Black, J.A. Ross, and K. Samuel Generation of functional human hepatic endoderm from human induced pluripotent stem cells Hepatology 51 2010 329 335
43. D. Szkolnicka, S.L. Farnworth, B. Lucendo-Villarin, C. Storck, W. Zhou, J.P. Iredale, O. Flint, and D.C. Hay Accurate prediction of drug-induced liver injury using stem cell-derived populations Stem Cells Transl. Med. 3 2014 141 148
44. Y. Tahamtani, M. Azarnia, A. Farrokhi, A. Sharifi-Zarchi, N. Aghdami, and H. Baharvand Treatment of human embryonic stem cells with different combinations of priming and inducing factors toward definitive endoderm Stem Cells Dev. 22 2013 1419 1432
45. J.Y. Tan, G. Sriram, A.J. Rufaihah, K.G. Neoh, and T. Cao Efficient derivation of lateral plate and paraxial mesoderm subtypes from human embryonic stem cells through GSKi-mediated differentiation Stem Cells Dev. 22 2013 1893 1906
46. J. Taylor, I. Wilmut, and G. Sullivan What are the limits to cell plasticity? Cell Res. 20 2010 502 503
47. T. Touboul, N.R.F. Hannan, S. Corbineau, A. Martinez, C. Martinet, S. Branchereau, S. Mainot, H. Strick-Marchand, R. Pedersen, and J. Di Santo Generation of functional hepatocytes from human embryonic stem cells under chemically defined conditions that recapitulate liver development Hepatology 51 2010 1754 1765