Isolation and Characterization of Mouse Hepatic Stem Cells in Vitro

Seminars in Liver Disease

Volumn 23, Issue 4, 2003, Pages 313-324

  Weiss, Mary C ^a,b   Strick Marchand, Hélène ^b  

^a CNRS   (France)

^b INSTITUT PASTEUR   (France)

Author keywords

Cholangiocytes; Hepatoblasts; Hepatocytes; Oval cells

Indexed keywords

ANIMAL CELL; CELL DIFFERENTIATION; CELL IMMORTALIZATION; CELL ISOLATION; CELL PROLIFERATION; CELL TRANSFORMATION; CELL TYPE; COLONY FORMING UNIT C; EMBRYO DEVELOPMENT; GENE MUTATION; LIVER CELL; LIVER CELL CULTURE; LIVER DEVELOPMENT; LIVER STEM CELL; MESENCHYME CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVIEW; STEM CELL; TISSUE REPAIR; TRANSGENIC MOUSE;

ANIMALS; BILE DUCTS; CELL CULTURE TECHNIQUES; CELL LINE; GENE EXPRESSION PROFILING; HEPATOCYTES; LIVER; MICE; STEM CELLS;

EID: 0345731277     PISSN: 02728087     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-2004-815558     Document Type: Review

References (69)

1. Ott MO, Rey-Campos J, Cereghini S, Yaniv M. vHNF1 is expressed in epithelial cells of distinct embryonic origin during development and precedes HNF1 expression. Mech Dev 1991;36:47-58
2. 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
3. Ang SL, Wierda A, Wong D, et al. The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of HNF3/forkhead proteins. Development 1993;119:1301-1315
4. Bisgaard HC, Nagy P, Santoni-Rugiu E, Thorgeirsson SS. Proliferation, apoptosis, and induction of hepatic transcription factors are characteristics of the early response of biliary, epithelial (oval) cells to chemical carcinogens. Hepatology 1996;23:62-70
5. Rausa F, Samadani U, Ye H, et al. The cut-homeodomain transcriptional activator HNF-6 is coexpressed with its target gene HNF-3 beta in the developing murine liver and pancreas. Dev Biol 1997;192:228-246
6. Rausa FM, Galarneau L, Belanger L, Costa RH. The nuclear receptor fetoprotein transcription factor is coexpressed with its target gene HNF-3beta in the developing murine liver, intestine and pancreas. Mech Dev 1999;89:185-188
7. Duncan SA, Manova K, Chen WS, et al. Expression of transcription factor HNF-4 in the extraembryonic endoderm, gut, and nephrogenic tissue of the developing mouse embryo: HNF-4 is a marker for primary endoderm in the implanting blastocyst. Proc Natl Acad Sci USA 1994;91:7598-7602
8. Kuo CF, Xanthopoulos KG, Darnell JE. Fetal and adult localization of C/EBP: evidence for combinatorial action of transcription factors in cell-specific gene expression. Development 1990;109:473-481
9. Barbacci E, Reber M, Ott MO, et al. Variant hepatocyte nuclear factor 1 is required for visceral endoderm specification. Development 1999;126:4795-4805
10. Coffinier C, Thépot D, Babinet C, Yaniv M, Barra J. Essential role for the homeoprotein vHNF1/HNF1B in visceral endoderm differentiation. Development 1999;126:4785-4794
11. Coffinier C, Gresh L, Fiette L, et al. Bile system morphogenesis defects and liver dysfunction upon targeted deletion of HNF1β. Development 2002;129:1829-1838
12. Landry C, Clotman F, Hioki T, et al. HNF-6 is expressed in endoderm derivatives and nervous system of the mouse embryo and participates to the cross-regulatory network of liver-enriched transcription factors. Dev Biol 1997;192:247-257
13. Clotman F, Lannoy VJ, Reber M, et al. The onecut transcription factor HNF6 is required for normal development of the biliary tract. Development 2002;129:1819-1828
14. Germain L, Blouin MJ, Marceau N. Biliary epithelial and hepatocytic cell lineage relationships in embryonic rat liver as determined by the differential expression of cytokeratins, a-fetoprotein, albumin, and cell surface-exposed components. Cancer Res 1988;48:4909-4918
15. Shiojiri N, Lemire JM, Fausto N. Cell lineages and oval cell progenitors in rat liver development. Cancer Res 1991;51:2611-2620
16. Petersen BE, Goff JP, Greenberger JS, Michalopoulos GK. Hepatic oval cells express the hematopoietic stem cell marker Thy-1 in the rat. Hepatology 1998;27:433-445
17. Omori N, Omori M, Evarts RP, et al. Partial cloning of rat CD34 cDNA and expression during stem cell-dependent liver regeneration in the adult rat. Hepatology 1997;26:720-727
18. Fujio K, Hu Z, Evarts RP, et al. Coexpression of stem cell factor and c-kit in embryonic and adult liver. Exp Cell Res 1996;224:243-250
19. Zhang M, Thorgeirsson SS. Modulation of connexins during differentiation of oval cells into hepatocytes. Exp Cell Res 1994;213:37-42
20. Volpes R, van den Oord JJ, Desmet VJ. Integrins as differential cell lineage markers of primary liver tumors. Am J Pathol 1993;142:1483-1492
21. Couvelard A, Bringuier AF, Dauge MC, et al. Expression of integrins during liver organogenesis in humans. Hepatology 1998;27:839-847
22. Rogler LE. Selective bipotential differentiation of mouse embryonic hepatoblasts in vitro. Am J Pathol 1997;150:591-602
23. Glickman RM, Sabesin SM. Lipoprotein metabolism. In: Arias IM, Boyer JL, Jakoby WB, et al, eds. The Liver Biology and Pathobiology. New York: Raven Press; 1994:391-415
24. Holic N, Suzuki T, Corlu A, et al. Differential expression of the rat gamma-glutamyl transpeptidase gene promoters along with differentiation of hepatoblasts into biliary or hepatocytic lineage. Am J Pathol 2000;157:537-548
25. Tietjen TG, Mjaatvedt CH, Yang VW. Expression of class I alcohol dehydrogenase gene in developing rat fetuses. J Histochem Cytochem 1994;42:745-753
26. Vonesch JL, Nakshatri H, Philippe M, Chambon P, Dolle P. Stage and tissue-specific expression of the alcohol dehydrogenase 1 (Adh-1) gene during mouse development. Dev Dyn 1994;199:199-213
27. Guillouzo A, Weber A, Le Provost E, Rissel M, Schapira F. Cell types involved in the expression of foetal aldolases during rat azo-dye hepatocarcinogenesis. J Cell Sci 1981;49:249-260
28. Numazaki M, Tsutsumi K, Tsutsumi R, Ishikawa K. Expression of aldolase isozyme mRNAs in fetal rat liver. Eur J Biochem 1984;142:165-170
29. Petersen BE, Bowen WC, Patrene KD, et al. Bone marrow as a potential source of hepatic oval cells. Science 1999;284:1168-1170
30. Theise ND, Nimmakayalu M, Gardner R, et al. Liver from bone marrow in humans. Hepatology 2000;32:11-16
31. Lagasse E, Connors H, Al-Dhalimy M, et al. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 2000;6:1229-1234
32. Wang X, Al-Dhalimy M, Lagasse E, Finegold M, Grompe M. Liver repopulation and correction of metabolic liver disease by transplanted adult mouse pancreatic cells. Am J Pathol 2001;158:571-579
33. 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
34. Jiang Y, Jahagirdar BN, Reinhardt RL, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002;418:41-49
35. Wang X, Willenbring H, Akkari Y, et al. Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 2003;422:897-901
36. Vassilopoulos G, Wang PR, Russell DW. Transplanted bone marrow regenerates liver by cell fusion. Nature 2003;422:901-904
37. Zheng Y-W, Suzuki A, Taniguchi H. Diversity of hepatic stem cells in the fetal and adult liver. Semin Liver Dis 2003;23:xxx-xxx
38. Nitou M, Sugiyama Y, Ishikawa K, Shiojiri N. Purification of fetal mouse hepatoblasts by magnetic beads coated with monoclonal anti-E-cadherin antibodies and their in vitro culture. Exp Cell Res 2002;279:330-343
39. Suzuki A, Zheng YW, Kondo R, et al. Flow-cytometric separation and enrichment of hepatic progenitor cells in the developing mouse liver. Hepatology 2000;32:1230-1239
40. Suzuki A, Zheng YW, Kaneko S, et al. Clonal identification and characterization of self-renewing pluripotent stem cells in the developing liver. J Cell Biol 2002;156:173-184
41. Amicone L, Spagnoli FM, Späth G, et al. Transgenic expression in the liver of truncated Met blocks apoptosis and permits immortalization of hepatocytes. EMBO J 1997;16:495-503
42. Spagnoli FM, Amicone L, Tripodi M, Weiss MC. Identification of a bipotential precursor cell in hepatic cell lines derived from transgenic mice expressing cyto-Met in the liver. J Cell Biol 1998;143:1101-1112
43. Spagnoli FM, Cicchini C, Tripodi M, Weiss MC. Inhibition of MMH (Met murine hepatocyte) cell differentiation by TGF(beta) is abrogated by pre-treatment with the heritable differentiation effector FGF1. J Cell Sci 2000;113:3639-3647
44. Aiuti A, Cicchini C, Bernardini S, et al. Hematopoietic support and cytokine expression of murine-stable hepatocyte cell lines (MMH). Hepatology 1998;28:1645-1654
45. Chagraoui J, Lepage-Noll A, Anjo A, Uzan G, Charbord P. Fetal liver stroma consists of cells in epithelial-to-mesenchymal transition. Blood 2003;101:2973-2982
46. Strick-Marchand H, Weiss MC. Inducible differentiation and morphogenesis of bipotential liver cell lines from wild-type mouse embryos. Hepatology 2002;36:794-805
47. Mennone A, Alvaro D, Cho W, Boyer JL. Isolation of small polarized bile duct units. Proc Natl Acad Sci USA 1995;92:6527-6531
48. Cho WK, Mennone A, Boyer JL. Isolation of functional polarized bile duct units from mouse liver. Am J Physiol Gastrointest Liver Physiol 2001;280:G241-G246
49. Strick-Marchand H, Weiss MC. Embryonic liver cells and permanent lines as models for hepatocyte and bile duct cell differentiation. Mech Dev 2003;120:89-99
50. Coleman WB, Grisham JW. Epithelial stem-like cells of the rodent liver. In: Strain AJ, Diehl AM, eds. Liver Growth and Repair. London: Chapman & Hall; 1998:50-99
51. Fausto N, Campbell JS. The role of hepatocytes and oval cells in liver regeneration and repopulation. Mechanisms of Development 2003;120:117-130
52. Richards WG, Yoder BK, Isfort RJ, et al. Isolation and characterization of liver epithelial cell lines from wild-type and mutant TgN737Rpw mice. Am J Pathol 1997;150:1189-1197
53. Richards WG, Yoder BK, Isfort RJ, et al. Oval cell proliferation associated with the murine insertional mutation TgN737Rpw. Am J Pathol 1996;149:1919-1930
54. Dumble ML, Croager EJ, Yeoh GCT, Quail EA. Generation and characterization of p53 null transformed hepatic progenitor cells: oval cells give rise to hepatocellular carcinoma. Carcinogenesis 2002;23:435-445
55. Petersen BE, Grossbard B, Hatch H, Pi L, Deng J, Scott EW. Mouse A6-positive hepatic oval cells also express several hematopoietic stem cell markers. Hepatology 2003;37:632-640
56. Hamazaki T, Iiboshi Y, Oka M, et al. Hepatic maturation in differentiating embryonic stem cells in vitro. FEBS Lett 2001;497:15-19
57. Miyashita H, Suzuki A, Fukao K, Nakauchi H, Taniguchi H. Evidence for hepatocyte differentiation from embryonic stem cells in vitro. Cell Transplant 2002;11:429-434
58. Chinzei R, Tanaka Y, Shimizu-Saito K, et al. Embryoid-body cells derived from a mouse embryonic stem cell lines show differentiation into functional hepatocytes. Hepatology 2002;36:22-29
59. Ishizaka S, Shiori A, Kanda S, et al. Development of hepatocytes from embryonic stem cells after transfection with the HNF3beta gene. FASEB J 2002;16:1444-1454
60. Reyes M, Lund T, Lenvik T, et al. Purification and ex vivo expansion of post-natal human marrow mesodermal progenitor cells. Blood 2001;98:2615-2625
61. Ivanova NB, Dimos JT, Schaniel C, et al. A stem cell molecular signature. Science 2002;298:601-604
62. Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC, Melton DA. "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 2002;298:597-600
63. Plescia C, Rogler C, Rogler L. Genomic expression analysis implicates Wnt signaling pathway and extracellular matrix alterations in hepatic specification and differentiation of murine hepatic stem cells. Differentiation 2001;68:254-269
64. Wu JC, Merlino G, Cveklova K, Mosinger B Jr, Fausto N. Autonomous growth in serum-free medium and production of hepatocellular carcinomas by differentiated hepatocyte lines that overexpress transforming growth factor alpha 1. Cancer Res 1994;54:5964-5973
65. Wu JC, Merlino G, Fausto N. Establishment and characterization of differentiated, nontransformed hepatocyte cell lines derived from mice transgenic for transforming growth factor α. Proc Natl Acad Sci USA 1994;91:674-678
66. Matise MP, Auerbach W, Joyner AL. Production of targeted embryonic stem cell clones. In: Joyner AL, ed. Gene Targeting: a Practical Approach. Oxford: Oxford University Press; 1999:101-131
67. Tang DG, Tokumoto YM, Apperly JA, Lloyd AC, Raff MC. Lack of replicative senescence in cultured rat oligodendrocyte precursor cells. Science 2001;291:868-871
68. Mathon NF, Malcolm DS, Harrisingh MC, Cheng L, Lloyd AC. Lack of replicative senescence in normal rodent glia. Science 2001;291:868-875
69. Ramirez RD, Morales CP, Herbert BS, et al. Putative telomere-independent mechanisms of replicative aging reflect inadequate growth conditions. Genes Dev 2001;15:398-403