Isolation, characterization, and differentiation to hepatocyte-like cells of nonparenchymal epithelial cells from adult human liver

Stem Cells

Volumn 25, Issue 7, 2007, Pages 1779-1790

  Duret, Cédric ^a,b   Gerbal Chaloin, Sabine ^a,b   Ramos, Jeanne ^c   Fabre, Jean Michel ^d   Jacquet, Eric ^d   Navarro, Francis ^d   Blanc, Pierre ^d   Sa Cunha, Antonio ^e   Maurel, Patrick ^a,b   Daujat Chavanieu, Martine ^a,b  

^a INSERM   (France)

^b UNIV MONTPELLIER   (France)

^c GUI DE CHAULIAC HOSPITAL   (France)

^d HÔPITAL SAINT ELOI   (France)

^e HAUT LÉVÊQUE HOSPITAL   (France)

Author keywords

Differentiation; Hepatobiliary cell; Human adult hepatic progenitors; Oval cell; Stem cell

Indexed keywords

ALBUMIN; ALPHA 1 ANTITRYPSIN; ALPHA FETOPROTEIN; CD34 ANTIGEN; CYTOCHROME P450 3A4; CYTOCHROME P450 3A7; CYTOKERATIN 18; CYTOKERATIN 19; CYTOKERATIN 7; CYTOKERATIN 8; FIBRINOGEN; GLUTATHIONE TRANSFERASE ALPHA; GLUTATHIONE TRANSFERASE P1; OCTAMER TRANSCRIPTION FACTOR 4; REX PROTEIN; STEM CELL FACTOR; THY 1 ANTIGEN; TRYPTOPHAN 2,3 DIOXYGENASE; TYROSINE AMINOTRANSFERASE;

ADULT; AGED; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER CELL; LIVER FAILURE; LIVER LOBECTOMY; LIVER RESECTION; MALE; PHENOTYPE; PROTEIN EXPRESSION;

ADULT; AGED; BIOLOGICAL MARKERS; BLOOD PROTEINS; CELL DIFFERENTIATION; CELL LINEAGE; CELL SEPARATION; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEPATOCYTE NUCLEAR FACTOR 4; HEPATOCYTES; HUMANS; LIVER; MALE; MIDDLE AGED; PHENOTYPE;

EID: 34547146120     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2006-0664     Document Type: Article

References (63)

1. Selden C, Hodgson H. Cellular therapies for liver replacement. Transpl Immunol 2004;12:273-288.
2. Mazaris EM, Roussos CT, Papalois VE. Hepatocyte transplantation: A review of worldwide clinical developments and experiences. Exp Clin Transplant 2005;3:306-315.
3. Overturf K, al-Dhalimy M, Ou CN et al. Serial transplantation reveals the stem-cell-like regenerative potential of adult mouse hepatocytes. Am J Pathol 1997;151:1273-1280.
4. Sell S. Heterogeneity and plasticity of hepatocyte lineage cells. Hepatology 2001;33:738-750.
5. Newsome PN, Hussain MA, Theise ND. Hepatic oval cells: Helping redefine a paradigm in stem cell biology. Curr Top Dev Biol 2004;61:1-28.
6. Sell S. Comparison of liver progenitor cells in human atypical ductular reactions with those seen in experimental models of liver injury. Hepatology 1998;27:317-331.
7. Crosby HA, Hubscher S, Fabris L et al. Immunolocalization of putative human liver progenitor cells in livers from patients with end-stage primary biliary cirrhosis and sclerosing cholangitis using the monoclonal antibody OV-6. Am J Pathol 1998;152:771-779.
8. Roskams TA, Libbrecht L, Desmet VJ. Progenitor cells in diseased human liver. Semin Liver Dis 2003;23:385-396.
9. Lowes KN, Brennan BA, Yeoh GC et al. Oval cell numbers in human chronic liver diseases are directly related to disease severity. Am J Pathol 1999;154:537-541.
10. Libbrecht L, Desmet V, Van Damme B et al. Deep intralobular extension of human hepatic 'progenitor cells' correlates with parenchymal inflammation in chronic viral hepatitis: Can 'progenitor cells' migrate? J Pathol 2000;192:373-378.
11. Theise ND, Saxena R, Portmann BC et al. The canals of Hering and hepatic stem cells in humans. Hepatology 1999;30:1425-1433.
12. Kim H, Park C, Han KH et al. Primary liver carcinoma of intermediate (hepatocyte-cholangiocyte) phenotype. J Hepatol 2004;40:298-304.
13. Alison MR, Lovell MJ. Liver cancer: The role of stem cells. Cell Prolif 2005;38:407-421.
14. Shafritz DA, Oertel M, Menthena A et al. Liver stem cells and prospects for liver reconstitution by transplanted cells. Hepatology 2006;43(suppl 1):S89-S98.
15. Parent R, Marion MJ, Furio L et al. Origin and characterization of a human bipotent liver progenitor cell line. Gastroenterology 2004;126:1147-1156.
16. Selden C, Chalmers SA, Jones C et al. Epithelial colonies cultured from human explanted liver in subacute hepatic failure exhibit hepatocyte, biliary epithelial, and stem cell phenotypic markers. STEM CELLS 2003;21:624-631.
17. Crosby HA, Kelly DA, Strain AJ. Human hepatic stem-like cells isolated using c-kit or CD34 can differentiate into biliary epithelium. Gastroenterology 2001;120:534-544.
18. Pichard L, Raulet E, Fabre G et al. Human hepatocyte culture. Methods Mol Biol 2006;320:283-293.
19. Ferrini JB, Pichard L, Domergue J et al. Long-term primary cultures of adult human hepatocytes. Chem Biol Interact 1997;107:31-45.
20. Ferrini JB, Ourlin JC, Pichard L et al. Human hepatocyte culture. Methods Mol Biol 1998;107:341-352.
21. Schwartz RE, Reyes M, Koodie L et al. Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells. J Clin Invest 2002;109:1291-1302.
22. Pichard-Garcia L, Gerbal-Chaloin S, Ferrini JB et al. Use of long-term cultures of human hepatocytes to study cytochrome P450 gene expression. Methods Enzymol 2002;357:311-321.
23. Fournier C, Sureau C, Coste J et al. In vitro infection of adult normal human hepatocytes in primary culture by hepatitis C virus. J Gen Virol 1998;79:2367-2374.
24. Sureau C, Fournier-Wirth C, Maurel P. Role of N glycosylation of hepatitis B virus envelope proteins in morphogenesis and infectivity of hepatitis delta virus. J Virol 2003;77:5519-5523.
25. Roskams TA, Theise ND, Balabaud C et al. Nomenclature of the finer branches of the biliary tree: Canals, ductules, and ductular reactions in human livers. Hepatology 2004;39:1739-1745.
26. Duncan SA. Transcriptional regulation of liver development. Dev Dyn 2000;219:131-142.
27. Nagy P, Bisgaard HC, Thorgeirsson SS. Expression of hepatic transcription factors during liver development and oval cell differentiation. J Cell Biol 1994;126:223-233.
28. Xanthopoulos KG, Prezioso VR, Chen WS et al. The different tissue transcription patterns of genes for HNF-1, C/EBP, HNF-3, and HNF-4, protein factors that govern liver-specific transcription. Proc Natl Acad Sci USA 1991;88:3807-3811.
29. Cereghini S. Liver-enriched transcription factors and hepatocyte differentiation. FASEB J 1996;10:267-282.
30. Ishiyama T, Kano J, Minami Y et al. Expression of HNFs and C/EBP alpha is correlated with immunocytochemical differentiation of cell lines derived from human hepatocellular carcinomas, hepatoblastomas and immortalized hepatocytes. Cancer Sci 2003;94:757-763.
31. Kuo CJ, Conley PB, Chen L et al. A transcriptional hierarchy involved in mammalian cell-type specification. Nature 1992;355:457-461.
32. Spath GF, Weiss MC. Hepatocyte nuclear factor 4 provokes expression of epithelial marker genes, acting as a morphogen in dedifferentiated hepatoma cells. J Cell Biol 1998;140:935-946.
33. Parviz F, Matullo C, Garrison WD et al. Hepatocyte nuclear factor 4alpha controls the development of a hepatic epithelium and liver morphogenesis. Nat Genet 2003;34:292-296.
34. Ramji DP, Foka P. CCAAT/enhancer-binding proteins: Structure, function and regulation. Biochem J 2002;365:561-575.
35. Roskams T, De Vos R, Van Eyken P et al. Hepatic OV-6 expression in human liver disease and rat experiments: Evidence for hepatic progenitor cells in man. J Hepatol 1998;29:455-463.
36. Hines RN, McCarver DG. The ontogeny of human drug-metabolizing enzymes: Phase I oxidative enzymes. J Pharmacol Exp Ther 2002;300:355-360.
37. Burchell A, Gibb L, Waddell ID et al. The ontogeny of human hepatic microsomal glucose-6-phosphatase proteins. Clin Chem 1990;36:1633-1637.
38. Oyanagi K, Nakamura K, Sogawa H et al. A study of urea-synthesizing enzymes in prenatal and postnatal human liver. Pediatr Res 1980;14:236-241.
39. Kamiya A, Kojima N, Kinoshita T et al. Maturation of fetal hepatocytes in vitro by extracellular matrices and oncostatin M: Induction of tryptophan oxygenase. Hepatology 2002;35:1351-1359.
40. Ohisalo JJ, Laskowska-Klita T, Andersson SM. Development of tyrosine aminotransferase and para-hydroxyphenylpyruvate dioxygenase activities in fetal and neonatal human liver. J Clin Invest 1982;70:198-200.
41. Henderson CJ, McLaren AW, Moffat GJ et al. Pi-class glutathione S-transferase: Regulation and function. Chem Biol Interact 1998;111-112:69-82.
42. Tew KD, Monks A, Barone L et al. Glutathione-associated enzymes in the human cell lines of the National Cancer Institute Drug Screening Program. Mol Pharmacol 1996;50:149-159.
43. Avital I, Inderbitzin D, Aoki T et al. Isolation, characterization, and transplantation of bone marrow-derived hepatocyte stem cells. Biochem Biophys Res Commun 2001;288:156-164.
44. Minguet S, Cortegano I, Gonzalo P et al. A population of c-Kit-(low)(CD45/TER119)- hepatic cell progenitors of 11-day postcoitus mouse embryo liver reconstitutes cell-depleted liver organoids. J Clin Invest 2003;112:1152-1163.
45. Nava S, Westgren M, Jaksch M et al. Characterization of cells in the developing human liver. Differentiation 2005;73:249-260.
46. Fougere-Deschatrette C, Imaizumi-Scherrer T, Strick-Marchand H et al. Plasticity of hepatic cell differentiation: Bipotential adult mouse liver clonal cell lines competent to differentiate in vitro and in vivo. STEM CELLS 2006;24:2098-2109.
47. Sicklick JK, Li YX, Melhem A et al. Hedgehog signaling maintains resident hepatic progenitors throughout life. Am J Physiol Gastrointest Liver Physiol 2006;290:G859-G870.
48. Schmelzer E, Wauthier E, Reid LM. The phenotypes of pluripotent human hepatic progenitors. STEM CELLS 2006;24:1852-1858.
49. Herrera MB, Bruno S, Buttiglieri S et al. Isolation and characterization of a stem cell population from adult human liver. STEM CELLS 2006;24:2840-2850.
50. Michalopoulos GK, Barua L, Bowen WC. Transdifferentiation of rat hepatocytes into biliary cells after bile duct ligation and toxic biliary injury. Hepatology 2005;41:535-544.
51. Block GD, Locker J, Bowen WC et al. Population expansion, clonal growth, and specific differentiation patterns in primary cultures of hepatocytes induced by HGF/SF, EGF and TGF alpha in a chemically defined (HGM) medium. J Cell Biol 1996;132:1133-1149.
52. Mitaka T, Mizuguchi T, Sato F et al. Growth and maturation of small hepatocytes. J Gastroenterol Hepatol 1998;13(suppl):S70-S77.
53. Liu C, Schreiter T, Dirsch O et al. Presence of markers for liver progenitor cells in human-derived intrahepatic biliary epithelial cells. Liver Int 2004;24:669-678.
54. Ishiki Y, Ohnishi H, Muto Y et al. Direct evidence that hepatocyte growth factor is a hepatotrophic factor for liver regeneration and has a potent antihepatitis effect in vivo. Hepatology 1992;16:1227-1235.
55. Dan YY, Riehle KJ, Lazaro C et al. Isolation of multipotent progenitor cells from human fetal liver capable of differentiating into liver and mesenchymal lineages. Proc Natl Acad Sci USA 2006;103:9912-9917.
56. Hu Z, Evarts RP, Fujio K et al. Expression of hepatocyte growth factor and c-met genes during hepatic differentiation and liver development in the rat. Am J Pathol 1993;142:1823-1830.
57. Kamiya A, Kinoshita T, Miyajima A. Oncostatin M and hepatocyte growth factor induce hepatic maturation via distinct signaling pathways. FEBS Lett 2001;492:90-94.
58. Suzuki A, Iwama A, Miyashita H et al. Role for growth factors and extracellular matrix in controlling differentiation of prospectively isolated hepatic stem cells. Development 2003;130:2513-2524.
59. Jiang Y, Jahagirdar BN, Reinhardt RL et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002;418:41-49.
60. Dravida S, Pal R, Khanna A et al. The transdifferentiation potential of limbal fibroblast-like cells. Brain Res Dev Brain Res 2005;160:239-251.
61. Schwartz RE, Linehan JL, Painschab MS et al. Defined conditions for development of functional hepatic cells from human embryonic stem cells. Stem Cells Dev 2005;14:643-655.
62. Hengstler JG, Brulport M, Schormann W et al. Generation of human hepatocytes by stem cell technology: Definition of the hepatocyte. Expert Opin Drug Metab Toxicol 2005;1:61-74.
63. Lavon N, Benvenisty N. Study of hepatocyte differentiation using embryonic stem cells. J Cell Biochem 2005;96:1193-1202.