Functional hepatocyte-like cells derived from mouse embryonic stem cells: A novel in vitro hepatotoxicity model for drug screening

Toxicology in Vitro

Volumn 20, Issue 6, 2006, Pages 1014-1022

  Kulkarni, J S ^a   Khanna, A ^a  

^a RELIANCE LIFE SCIENCES PVT LTD   (India)

Author keywords

Carbon tetrachloride; Cell culture models; Drug screening; Embryonic stem cells; Hepatotoxicity; In vitro toxicity models

Indexed keywords

ACETYLCYSTEINE; ALANINE AMINOTRANSFERASE; ANTIOXIDANT; ASPARTATE AMINOTRANSFERASE; CARBON TETRACHLORIDE; LACTATE DEHYDROGENASE; LIVER ENZYME;

ANIMAL CELL; ANTIBODY DETECTION; ARTICLE; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; DRUG SCREENING; EMBRYO; EMBRYONIC STEM CELL; GENE EXPRESSION; LIVER CELL; LIVER INJURY; LIVER TOXICITY; MOUSE; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ALANINE TRANSAMINASE; ANIMALS; ASPARTATE AMINOTRANSFERASES; CARBON TETRACHLORIDE; CELL DIFFERENTIATION; CELLS, CULTURED; DRUG EVALUATION, PRECLINICAL; EMBRYO; FLUORESCENT ANTIBODY TECHNIQUE; HEPATOCYTES; HUMANS; L-LACTATE DEHYDROGENASE; MICE; RNA, MESSENGER; STEM CELLS;

EID: 33745484751     PISSN: 08872333     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tiv.2005.12.011     Document Type: Article

References (40)

1. Abe K., Niwa H., Iwase K., Takiguchi M., Mori M., Abe S.I., Abe K., and Yamamura K.I. Endoderm-specific gene expression in embryonic stem cells differentiated to embryoid bodies. Experimental Cell Research 229 (1996) 27-34
2. Bradley D.W., and Tappel A.L. Automated multiple enzyme analysis systems. Analytical Biochemistry 33 (1970) 400-413
3. Brandon E.F.A., Raap C.D., Meijerman I., Beijnen J.H., and Schellens J.H.M. An update on in vitro test methods in human hepatic drug biotransformation research: pros and cons. Toxicology and Applied Pharmacology 189 (2003) 233-246
4. 4-induced hydroperoxide generation and cytotoxicity possibly through C1b receptor in rat hepatocytes. Biochemical Biophyical Research Communication 218 (1996) 865-871
5. Chinzei R., Tanaka Y., Shimizu-Saito K., Hara Y., Kakinuma S., Watanabe M., Teramoto K., Arii S., Takase K., Sato C., Terada N., and Teraoka H. Embryoid-body cells derived from a mouse embryonic stem cell line show differentiation into functional hepatocytes. Hepatology 36 (2002) 22-29
6. Choi D., Oh H.J., Chang U.J., Koo S.K., Jiang J.X., Hwang S.Y., Lee J.D., Yeoh G.C., Shin H.S., Lee J.S., and Oh B. In vivo differentiation of mouse embryonic stem cells into hepatocytes. Cell Transplantation 11 (2002) 359-368
7. Cross D.M., and Bayliss M.K. A commentary on the use of hepatocytes in drug metabolism studies during drug discovery and development. Drug Metabolism Reviews 32 (2000) 219-240
8. Davila J.C., Cezar G.G., Thiede M., Strom S., Miki T., and Trosko J. Use and application of stem cells in toxicology. Toxicological Sciences 79 (2004) 214-223
9. Doetschman T.C., Eistetter H., Katz M., Schmidt W., and Kemler R. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. Journal of Embryology Experimental Morphology 87 (1985) 27-45
10. Dvorak Z., Kosina P., Walterova D., Simanek V., Bachleda P., and Ulrichova J. Primary cultures of human hepatocytes as a tool in cytotoxicity studies: cell protection against model toxins by flavonolignans obtained from Silybum marianum. Toxicological Letters 137 (2003) 201-212
11. Fardel O., Morel F., Ratanasavanh D., Fautrel A., Beaume P., and Guillouzo A. Expression of drug metabolizing enzymes in human HepG2 hepatoma cells. Cellular and Molecular Aspects in Cirrhosis 216 (1992) 327-330
12. Ha K.T., Yoon S.J., Choi D.Y., Kim D.W., Kim J.K., and Kim C.H. Protective effect of Lycium chinense fruit on carbon tetrachloride-induced hepatotoxicity. Journal of Ethnopharmacology 96 (2005) 529-535
13. Hall T.J., James P.R., and Cambridge G. Development of an in vitro hepatotoxicity assay for assessing the effects of chronic drug exposure. Research Communications in Chemical Pathology and Pharmacology 79 (1993) 249-256
14. Hamazaki T., Iiboshi Y., Oka M., Papst P.J., Meacham A.M., Zon L.I., and Terada N. Hepatic maturation in differentiating embryonic stem cells in vitro. FEBS Letters 497 (2001) 15-19
15. Janakat S., and Al-Merie H. Optimization of the dose and route of injection, and characterisation of the time course of carbon tetrachloride-induced hepatotoxicity in the rat. Journal of Pharmacological and Toxicological Methods 48 (2002) 41-44
16. Jones E.A., Tosh D., Wilson D.I., Lindsay S., and Forrester L.M. Hepatic differentiation of murine embryonic stem cells. Experimental Cell Research 272 (2002) 15-22
17. Keller G.M. In vitro differentiation of embryonic stem cells. Current Opinion in Cell Biology 7 (1995) 862-869
18. Kim J.A., Kang Y.S., Park S.H., Kim H.W., Cho S.Y., and Lee Y.S. Role of reactive oxygen species in apoptosis induced by N-ethylmaleimide in HepG2 human hepatoblastoma cells. European Journal of Pharmacology 433 (2001) 1-6
19. Lagasse E., Connors H., Al-Dhalimy M., Reitsma M., Dohse M., Osborne L., Wang X., Finegold M., Weissman I.L., and Grompe M. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nature Medicine 6 (2000) 1229-1234
20. LeCluyse E.L., Alexandre E., Hamilton G.A., Viollon-Abadie C., Coon D.J., and Richert L. Isolation and culture of primary human hepatocytes. Methods in Molecular Biology 290 (2004) 207-230
21. Lee K.D., Kuo T.K., Whang-Peng J., Chung Y.F., Lin C.T., Chou S.H., Chen J.R., Chen Y.P., and Lee OK. In vitro hepatic differentiation of human mesenchymal stem cells. Hepatology 40 (2004) 275-284
22. McNeish J. Embryonic stem cells in drug discovery. Nature Reviews Drug Discovery 3 (2004) 70-80
23. Miyashita H., Suzuki A., Fukao K., Nakauchi H., and Taniguchi H. Evidence for hepatocyte differentiation from embryonic stem cells in vitro. Cell Transplantation 11 (2002) 429-434
24. Morrisey E.E., Tang Z., Sigrist K., Lu M.M., Jiang F., Ip H.S., and Parmacek M.S. GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes and Development 12 (1998) 3579-3590
25. Neuman M.G., Koren G., and Tiribelli C. In vitro assessment of the ethanol-induced hepatotoxicity on HepG2 cell line. Biochemical Biophysical Research Communication 197 (1993) 932-941
26. O'Brien P.J., Chan K., and Silber P.M. Human and animal hepatocytes in vitro with extrapolation in vivo. Chemical-Biological Interactions 150 (2004) 97-114
27. Oh S.H., and Lim S.C. A rapid and transient ROS generation by cadmium triggers apoptosis via caspase-dependent pathway in HepG2 cells and this is inhibited through N-acetylcysteine-mediated catalase upregulation. Toxicology and Applied Pharmacology (2005) [Epub ahead of print; doi:10.1016/j.taap.2005.07.018]
28. Pal R., and Khanna A. Role of hepatocytes in differentiation of cardiomyocytes from mouse embryonic stem cells. Stem Cells and Development 14 2 (2005) 153-161
29. Park J.H., Kim S.J., Lee J.B., Song J.M., Kim C.G., Roh S., and Yoon H.S. Establishment of a human embryonic germ cell line and comparison with mouse and human embryonic stem cells. Molecular Cell 30 (2004) 309-315
30. Parrish A.R., Gandolfi A.J., and Brendel K. Precision-cut liver slices: applications in pharmacology and toxicology. Life Sciences 57 (1995) 1887-1901
31. Pavanato A., Tunon M.J., Sanchez-Campos S., Marroni C.A., Llesuy S., Gonzalez-Gallego J., and Marroni N. Effects of quercetin on liver damage in rats with carbon tetrachloride-induced cirrhosis. Diagnostic and Discovery Sciences 48 (2003) 824-829
32. Ritter C., Reinke A., Andrades M., Martins M.R., Rocha J., Menna-Barreto S., Quevedo J., Moreira J.C., and Dal-Pizzol F. Protective effect of N-acetylcysteine and deferoxamine on carbon tetrachloride-induced acute hepatic failure in rats. Critical Care Medicine 32 (2004) 2079-2083
33. Schwartz R.E., Reyes M., Koodie L., Jiang Y., Blackstad M., Lund T., Lenvik T., Johnson S., Hu W.S., and Verfaillie C.M. Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocytes. Journal of Clinical Investigation 109 (2002) 1291-1302
34. Simko V., Michael S., Katz J., Oberstein E., and Popescu A. Protective effect of oral acetylcysteine against the hepatorenal toxicity of carbon tetrachloride potentiated by ethyl alcohol. Alcohol Clinical Experimental Research 16 (1992) 795-799
35. Strom S.C., Pisarov L.A., Dorko K., Thompson M.T., Schuetz J.D., and Schuetz E.G. Use of human hepatocytes to study P450 gene induction. Methods in Enzymology 272 (1996) 340-388
36. Suzuki A., Zheng Y.W., Kaneko S., Onodera M., Fukao K., Nakauchi H., and Taniguchi H. Clonal identification and characterization of self-renewing pluripotent stem cells in the developing liver. Journal of Cell Biology 156 (2002) 173-184
37. Yamada T., Yoshikawa M., Kanda S., Kato Y., Nakajima Y., Ishizaka S., and Tsunoda Y. In vitro differentiation of embryonic stem cells into hepatocyte-like cells identified by cellular uptake of indocyanine green. Stem Cells 20 (2002) 146-154
38. Yin Y., Lim Y.K., Salto-Tellez M., Ng S.C., Lin C.S., and Lim S.K. AFP(+), ESC-derived cells engraft and differentiate into hepatocytes in vivo. Stem Cells 20 (2002) 338-346
39. Young H.E., Duplaa C., Young T.M., Floyd J.A., Reeves M.L., Davis K.H., Mancini G.J., Eaton M.E., Hill J.D., Thomas K., Austin T., Edwards C., Cuzzourt J., Parikh A., Groom J., Hudson J., and Black Jr. A.C. Clonogenic analysis reveals reserve stem cells in postnatal mammals: I. Pluripotent mesenchymal stem cells. Anatomical Record 263 (2001) 350-360
40. Zurlo J., and Arterburn L.M. Characterization of a primary hepatocyte culture system for toxicological studies. In Vitro Cellular and Developmental Biology Animal 32 (1996) 211-220