Engraftment potential of spheroid-forming hepatic endoderm derived from human embryonic stem cells

Stem Cells and Development

Volumn 22, Issue 12, 2013, Pages 1818-1829

  Kim, Sung Eun ^a   An, Su Yeon ^a   Woo, Dong Hun ^a   Han, Jiyou ^a   Kim, Jong Hyun ^a   Jang, Yu Jin ^a   Son, Jeong Sang ^a   Yang, Hyunwon ^b   Cheon, Yong Pil ^c   Kim, Jong Hoon ^a  

^a Korea University   (South Korea)

^b Seoul Women University   (South Korea)

^c Sungshin Women's University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; ALPHA FETOPROTEIN; AMYLASE; BETA CATENIN; BETA TUBULIN; BIOLOGICAL MARKER; BONE MORPHOGENETIC PROTEIN 4; CCAAT ENHANCER BINDING PROTEIN BETA; CD34 ANTIGEN; CYTOKERATIN 18; CYTOKERATIN 19; DEXAMETHASONE; GAMMA GLUTAMYLTRANSFERASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOGEN; HEPATOCYTE NUCLEAR FACTOR 3BETA; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; INDOCYANINE GREEN; NESTIN; OCTAMER TRANSCRIPTION FACTOR 4; ONCOSTATIN M; PERIODIC ACID; SCATTER FACTOR; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR PDX 1; TRANSCRIPTION FACTOR SOX17; UNINDEXED DRUG; UVOMORULIN; WNT3A PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CELL AGGREGATION; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENDODERM; ENGRAFTMENT; ENRICHMENT CULTURE; GENE EXPRESSION; HOMEOBOX; HUMAN; HUMAN CELL; LIVER CELL; LIVER INJURY; MALE; MARKER GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SPHEROID CELL; STEM CELL TRANSPLANTATION; UREA CYCLE;

ALBUMINS; ANIMALS; BIOLOGICAL MARKERS; BONE MORPHOGENETIC PROTEIN 4; CARBON TETRACHLORIDE; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; DEXAMETHASONE; DRUG-INDUCED LIVER INJURY; EMBRYONIC STEM CELLS; ENDODERM; GLYCOGEN; GRAFT SURVIVAL; HEPATOCYTE GROWTH FACTOR; HEPATOCYTES; HUMANS; MICE; MICE, NUDE; ONCOSTATIN M; SPHEROIDS, CELLULAR; TRANSPLANTATION, HETEROLOGOUS; UREA; WNT3A PROTEIN;

EID: 84881094106     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2012.0401     Document Type: Article

References (52)

1. Thomson JA, J Itskovitz-Eldor, SS Shapiro, MA Waknitz, JJ Swiergiel, VS Marshall and JM Jones. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282:1145-1147.
2. Biswas A and R Hutchins. (2007). Embryonic stem cells. Stem Cells Dev 16:213-222.
3. Kim JH, JM Auerbach, JA Rodriguez-Gomez, I Velasco, D Gavin, N Lumelsky, SH Lee, J Nguyen, R Sanchez-Pernaute, K Bankiewicz and R McKay. (2002). Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 418:50-56.
4. Shim JH, SE Kim, DH Woo, SK Kim, CH Oh, R McKay and JH Kim. (2007). Directed differentiation of human embryonic stem cells towards a pancreatic cell fate. Diabetologia 50: 1228-1238.
5. Kelly OG, KI Pinson and WC Skarnes. (2004). The Wnt co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice. Development 131:2803-2815.
6. Sherwood RI, R Maehr, EO Mazzoni and DA Melton. (2011). Wnt signaling specifies and patterns intestinal endoderm. Mech Dev 128:387-400.
7. Zaret KS. (2002). Regulatory phases of early liver development: paradigms of organogenesis. Nat Rev Genet 3:499-512.
8. Agarwal S, KL Holton and R Lanza. (2008). Efficient differentiation of functional hepatocytes from human embryonic stem cells. Stem Cells 26:1117-1127.
9. Basma H, A Soto-Gutierrez, GR Yannam, L Liu, R Ito, T Yamamoto, E Ellis, SD Carson, S Sato, et al. (2009). Differentiation and transplantation of human embryonic stem cell-derived hepatocytes. Gastroenterology 136:990-999.
10. Hay DC, D Zhao, J Fletcher, ZA Hewitt, D McLean, A Urruticoechea-Uriguen, JR Black, C Elcombe, JA Ross, R Wolf and W Cui. (2008). Efficient differentiation of hepato-cytes from human embryonic stem cells exhibiting markers recapitulating liver development in vivo. Stem Cells 26: 894-902.
11. Touboul T, NR Hannan, S Corbineau, A Martinez, C Martinet, S Branchereau, S Mainot, H Strick-Marchand, R Pedersen, et al. (2010). Generation of functional hepatocytes from human embryonic stem cells under chemically defined conditions that recapitulate liver development. Hepatology 51:1754-1765.
12. Bukong TN, T Lo, G Szabo and A Dolganiuc. (2012). Novel developmental biology-based protocol of embryonic stem cell differentiation to morphologically sound and functional yet immature hepatocytes. Liver Int 32:732-741.
13. Duan Y, A Catana, Y Meng, N Yamamoto, S He, S Gupta, SS Gambhir and MA Zern. (2007). Differentiation and enrichment of hepatocyte-like cells from human embryonic stem cells in vitro and in vivo. Stem Cells 25:3058-3068.
14. Tsuchiya A, T Heike, H Fujino, M Shiota, K Umeda, M Yoshimoto, Y Matsuda, T Ichida, Y Aoyagi and T Nakahata. (2005). Long-term extensive expansion of mouse hepatic stem/progenitor cells in a novel serum-free culture system. Gastroenterology 128:2089-2104.
15. Moliner A, P Enfors, CF Ibanez and M Andang. (2008). Mouse embryonic stem cell-derived spheres with distinct neurogenic potentials. Stem Cells Dev 17:233-243.
16. Zhang Q, AL Nguyen, S Shi, C Hill, P Wilder-Smith, TB Krasieva and AD Le. (2012). Three-dimensional spheroid culture of human gingiva-derived mesenchymal stem cells enhances mitigation of chemotherapy-induced oral mucosi-tis. Stem Cells Dev 21:937-947.
17. Palmer TD, EA Markakis, AR Willhoite, F Safar and FH Gage. (1999). Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci 19:8487-8497.
18. Reynolds BA and S Weiss. (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710.
19. Takeichi M. (1988). The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development 102: 639-655.
20. MatsushitaT, KNakano, YNishikura, KHiguchi, AKiyota and R Ueoka. (2003). Spheroid formation and functional restoration of human fetal hepatocytes on poly-amino acid-coated dishes after serial proliferation. Cytotechnology 42:57-66.
21. Tong JZ, S Sarrazin, D Cassio, F Gauthier and F Alvarez. (1994). Application of spheroid culture to human hepato-cytes and maintenance of their differentiation. Biol Cell 81:77-81.
22. Gil JE, DH Woo, JH Shim, SE Kim, HJ You, SH Park, SH Paek, SK Kim and JH Kim. (2009). Vitronectin promotes oligodendrocyte differentiation during neurogenesis of human embryonic stem cells. FEBS Lett 583:561-567.
23. Rutenburg AM, H Kim, JW Fischbein, JS Hanker, HL Wasserkrug and AM Seligman. (1969). Histochemical and ultrastructural demonstration of gamma-glutamyl transpeptidase activity. J Histochem Cytochem 17:517-526.
24. Gouon-Evans V, L Boussemart, P Gadue, D Nierhoff, CI Koehler, A Kubo, DA Shafritz and G Keller. (2006). BMP-4 is required for hepatic specification of mouse embryonic stem cell-derived definitive endoderm. Nat Biotechnol24:1402- 1411.
25. Rossi JM, NR Dunn, BL Hogan and KS Zaret. (2001). Distinct mesodermal signals, including BMPs from the septum transversum mesenchyme, are required in combination for hepatogenesis from the endoderm. Genes Dev 15:1998-2009.
26. Tada S, T Era, C Furusawa, H Sakurai, S Nishikawa, M Kinoshita, K Nakao and T Chiba. (2005). Characterization of mesendoderm: a diverging point of the definitive endoderm and mesoderm in embryonic stem cell differentiation culture. Development 132:4363-4374.
27. Lickert H, CDomon, G Huls, C Wehrle, I Duluc, HClevers, BI Meyer, JN Freund and R Kemler. (2000). Wnt/(beta)-catenin signaling regulates the expression of the homeobox gene Cdx1 in embryonic intestine. Development 127:3805-3813.
28. Hussain SZ, T Sneddon, X Tan, A Micsenyi, GK Michalo-poulos and SP Monga. (2004) Wnt impacts growth and differentiation in ex vivo liver development. Exp Cell Res 292: 157-169.
29. Izumi N, T Era, H Akimaru, M Yasunaga and S Nishikawa. (2007). Dissecting the molecular hierarchy for mesendoderm differentiation through a combination of embryonic stem cell culture and RNA interference. Stem Cells 25:1664-1674.
30. Nakanishi M, A Kurisaki, Y Hayashi, M Warashina, S Ish-iura, M Kusuda-Furue and M Asashima. (2009). Directed induction of anterior and posterior primitive streak by Wnt from embryonic stem cells cultured in a chemically defined serum-free medium. FASEB J 23:114-122.
31. Li L, F Li, H Qi, G Feng, K Yuan, H Deng and H Zhou. (2008). Coexpression of Pdx1 and betacellulin in mesenchy-mal stem cells could promote the differentiation of nestin-positive epithelium-like progenitors and pancreatic islet-like spheroids. Stem Cells Dev 17:815-823.
32. Moll R, WW Franke, DL Schiller, B Geiger and R Krepler. (1982). The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells. Cell 31:11-24.
33. Shiojiri N, JM Lemire and N Fausto. (1991). Cell lineages and oval cell progenitors in rat liver development. Cancer Res 51:2611-2620.
34. Germain L, MJ Blouin and N Marceau. (1988). Biliary epithelial and hepatocytic cell lineage relationships in embryonic rat liver as determined by the differential expression of cytokeratins, alpha-fetoprotein, albumin, and cell surface-exposed components. Cancer Res 48:4909-4918.
35. Shiojiri N. (1981). Enzymo-and immunocytochemical analyses of the differentiation of liver cells in the prenatal mouse. J Embryol Exp Morphol 62:139-152.
36. Hunter MP, CM Wilson, X Jiang, R Cong, H Vasavada, KH Kaestner and CW Bogue. (2007). The homeobox gene Hhex is essential for proper hepatoblast differentiation and bile duct morphogenesis. Dev Biol 308:355-367.
37. Belanger L, M Frain, P Baril, MC Gingras, J Bartkowiak and JM Sala-Trepat. (1981). Glucocorticosteroid suppression of alpha1-fetoprotein synthesis in developing rat liver. Evidence for selective gene repression at the transcriptional level. Biochemistry 20:6665-6672.
38. Kamiya A, T Kinoshita and A Miyajima. (2001). Oncostatin M and hepatocyte growth factor induce hepatic maturation via distinct signaling pathways. FEBS Lett 492:90-94.
39. Michalopoulos GK, WC Bowen, K Mule and J Luo. (2003). HGF-, EGF-, and dexamethasone-induced gene expression patterns during formation of tissue in hepatic organoid cultures. Gene Expr 11:55-75.
40. Schmidt C, F Bladt, S Goedecke, V Brinkmann, W Zschiesche, M Sharpe, E Gherardi and C Birchmeier. (1995). Scatter factor/hepatocyte growth factor is essential for liver development. Nature 373:699-702.
41. Houssaint E. (1980). Differentiation of the mouse hepatic primordium. I. An analysis of tissue interactions in hepato-cyte differentiation. Cell Differ 9:269-279.
42. Shelley HJ. (1964). Carbohydrate reserves in the newborn infant. Br Med J 1:273-275.
43. Farrar WE, Jr. and LM Corwin. (1966). The essential role of the liver in detoxification of endotoxin. Ann N Y Acad Sci 133:668-684.
44. Chiao E, M Elazar, Y Xing, A Xiong, M Kmet, MT Millan, JS Glenn, WH Wong and J Baker. (2008). Isolation and transcriptional profiling of purified hepatic cells derived from human embryonic stem cells. Stem Cells 26:2032-2041.
45. Hynes RO and AD Lander. (1992). Contact and adhesive specificities in the associations, migrations, and targeting of cells and axons. Cell 68:303-322.
46. De Bruijne J, HJ Jongsma and AC van Ginneken. (1984). The passive electrical properties of spheroidal aggregates cultured from neonatal rat heart cells. J Physiol 355:281-293.
47. Sansone P, G Storci, S Tavolari, T Guarnieri, C Giovannini, M Taffurelli, C Ceccarelli, D Santini, et al. (2007). IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J Clin Invest 117:3988-4002.
48. Moscona A. (1961). Rotation-mediated histogenetic aggregation of dissociated cells. A quantifiable approach to cell interactions in vitro. Exp Cell Res 22:455-475.
49. Steinberg MS and SF Gilbert. (2004). Townes and Holtfreter (1955): directed movements and selective adhesion of embryonic amphibian cells. J Exp Zool A Comp Exp Biol 301:701-706.
50. Sharma AD, T Cantz, A Vogel, A Schambach, D Haridass, M Iken, M Bleidissel, MP Manns, HR Scholer and M Ott. (2008). Murine embryonic stem cell-derived hepatic progenitor cells engraft in recipient livers with limited capacity of liver tissue formation. Cell Transplant 17:313-323.
51. Song Z, J Cai, Y Liu, D Zhao, J Yong, S Duo, X Song, Y Guo, Y Zhao, et al. (2009). Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells. Cell Res 19:1233-1242.
52. Takayama K, M Inamura, K Kawabata, M Sugawara, K Kikuchi, M Higuchi, Y Nagamoto, H Watanabe, K Tashiro, et al. (2012). Generation of metabolically functioning hepa-tocytes from human pluripotent stem cells by FOXA2 and HNF1alpha transduction. J Hepatol 57:628-636.