Phenotype reversion in fetal human liver epithelial cells identifies the role of an intermediate meso-endodermal stage before hepatic maturation

Journal of Cell Science

Volumn 121, Issue 7, 2008, Pages 1002-1013

  Inada, Mari ^a,b,c   Follenzi, Antonia ^a,b,d   Cheng, Kang ^a,b   Surana, Manju ^a   Joseph, Brigid ^a,b   Benten, Daniel ^a,b   Bandi, Sriram ^a,b   Qian, Hong ^a   Gupta, Sanjeev ^a,b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b MARION BESSIN LIVER RESEARCH CENTER   (United States)

^c CHIBA UNIVERSITY   (Japan)

^d UNIVERSITY OF EASTERN PIEDMONT   (Italy)

Author keywords

Differentiation; Epithelial; Fetal; Liver; Mesenchymal; Stem cells

Indexed keywords

BONE MORPHOGENETIC PROTEIN; FIBROBLAST GROWTH FACTOR; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; LENTIVIRUS VECTOR; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL ISOLATION; CELL LINEAGE; CELL MATURATION; CELL PROLIFERATION; CONTINUOUS CULTURE; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; DEVELOPMENTAL STAGE; ENDODERM; EPITHELIUM CELL; FEMALE; FETUS; FETUS DEVELOPMENT; GENE CONTROL; GENE EXPRESSION; GENETIC MANIPULATION; HEPATOCYTE TRANSPLANTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LIVER CELL; LIVER CELL CULTURE; LIVER DEVELOPMENT; MALE; MESENCHYME CELL; MESODERM; MOUSE; NONHUMAN; PHENOTYPE; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EPITHELIAL CELLS; FETUS; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEPATOCYTES; HUMANS; LIVER; MESENCHYMAL STEM CELLS; MICE; MICE, SCID; MICROSCOPY, ELECTRON, TRANSMISSION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; STEM CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 43149098045     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.019315     Document Type: Article

References (52)

1. Barberi, T., Willis, L. M., Socci, N. D. and Studer, L. (2005). Derivation of multipotent mesenchymal precursors from human embryonic stem cells. PloS Med. 2, e161.
2. Benten, D., Cheng, K. and Gupta, S. (2005a). Identification of transplanted human cells in animal tissues. In In Situ Hybridization Protocols (Methods in Molecular Biology, Vol. 326) (ed. I. A. Derby and T. D. Hewitson), pp. 189-201. Totowa, NJ: Humana Press.
3. Benten, D., Kumaran, V., Joseph, B., Schattenberg, J., Popov, Y., Schuppan, D. and Gupta, S. (2005b). Hepatocyte transplantation activates hepatic stellate cells with beneficial modulation of cell engraftment in the rat. Hepatology 42, 1072-1081.
4. Bolstad, B. M., Irizarry, R. A., Astrand, M. and Speed, T. P. (2003). A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185-193.
5. Boyer, L. A., Lee, T. I., Cole, M. F., Johnstone, S. E., Levine, S. S., Zucker, J. P., Guenther, M. G., Kumar, R. M., Murray, H. L., Jenner, R. G. et al. (2005). Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122, 947-956.
6. Cho, J., Joseph, B., Sappal, B. S., Giri, R. K., Wang, R., Ludlow, J., Susick, R. and Gupta, S. (2004). Analysis of the functional integrity of cryopreserved human liver cells including xenografting in immunodeficient mice to address suitability for clinical applications. Liver Int. 24, 361-370.
7. Cowan, C. A., Atienza, J., Melton, D. A. and Eggan, K. (2005). Nuclear reprogramming of somatic cells after fusion with human embryonic stem cells. Science 309, 1369-1373.
8. D'Amour, K. A., Agulnick, A. D., Eliazer, S., Kelly, O. G., Kroon, E. and Baetge, E. E. (2005). Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat. Biotechnol. 23, 1491-1492.
9. Dan, Y. Y, Riehle, K. J., Lazaro, C., Tcoh, N., Haque, J., Campbell, J. S. and Fausto, N. (2006). Isolation of multipotent progenitor cells from human fetal liver capable of differentiating into liver and mesenchymal lineages. Proc. Nall. Acad. Sci. USA. 103, 9912-9917.
10. Dennis, G., Jr, Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C. and Lempicki, R. A. (2003). DAVID: Database for Annotation, Visualization, and integrated Discovery. Genome Biol. 4, P3.
11. Follenzi, A., Sabatino, G., Lombardo, A., Boccacio, C. and Naldini, L. (2002). Efficient gene delivery and targeted expression to helpatocytes in vivo by improved lentiviral vectors. Hum. Gene Ther. 13, 243-260.
12. Fritzenwanker, J. H., Saina, M. and Technau, U. (2004). Analysis of forkhead and snail expression reveals epithelial-mesenchymal transitions during embryonic and larval development of Nematostella vectensis. Dev. Biol. 15, 389-402.
13. Gershengorn, M. C., Hardikar, A. A. Wei, C., Geras-Raaka, E., Marcus-Samuels, B. and Raaka, B. M. (2004). Epithelial-to-mesenchymal transition generates proliferative human islet precursor cells. Science 306, 2261-2264.
14. Gualdi, R., Bossard, P., Zheng, M., Harnada, Y., Coleman, J. R. and Zaret, K. S. (1996). Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control. Genes Dev. 10, 1670-1682.
15. Hay, E. D. and Zuk, A. (1995). Transformations between epithelium and mesenchyme: normal, pathological, and experimentally induced. Am. J. Kidney Dis. 26, 678-690.
16. Heremans, Y., Van De Casteele, M., in't Veld, P., Gradwohl, G., Serup, P., Madsen, O., Pipeleers, D. and Heimberg, H. (2002). Recapitulation of embryonic neuroendoerme differentiation in adult human pancreatic duct cells expressing neurogenin 3. J. Cell Biol. 159, 303-312.
17. Hugo, H., Ackland, M. L., Blick, T., Lawrence, M. G., Clements, J. A., Williams, E. D. and Thompson, E. W. (2007). Epithelial-mesenchymal and mesenchymal-epithelial transitions in carcinoma progression. J. Cell. Physiol. 213, 374-383.
18. Inada, M., Benten, D., Cheng, K., Joseph, B., Berishvili, E., Badve, S., Logdberg, L., Dabeva, M. and Gupta, S. (2007). Stage-specific regulation of adhesion molecule expression segregates epithehal stem/ progenitor cells in fetal and adult human livers. Hepatol. Int. doi:10.1007/s12072-007-9023-4.
19. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U. and Speed, T. P. (2003). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264.
20. Ishizaka, S., Shiroi, A., Kanda, S., Yoshikawa, M., Rujimme, H., Kuriyama, S., Hasuma, T., Nakatani, K. and Takahashi, K. (2002). Development of hepatocytes from ES cells after transfection with the HNF-3beta gene. FASEV. J. 16, 1444-1446.
21. Lazaro, C. A., Croager, E. J., Mitchell, C., Campbell, J. S., Yu, C., Foraker, J., Rhim, J. A., Yeoh, G. C. and Fausto, N. (2003). Establishment, characterization, and long-term maintenance of cultures of human fetal hepatocytes. Hepatology 38, 1095-1106.
22. Lee, C. S., Friedman, J. R., Fulmer, J. T. and Kaestner, K. H. (2005). The initiation of liver development is dependent on Foxa transcription factors. Nature 435, 944-947.
23. Lemm, I, Lingott, A., Pogge v Strandmann, E., Zoidl, C., Bulman, M. P., Hatterstey, A. T., Schulz, W. A., Ebert, T. and Ryffel, G. U. (1999). Loss of HNF1alpha function in human renal cell carcinoma: frequent mutations in the VHL gene but not the HNF1alpha gene. Mol. Carcinog. 24, 305-314.
24. Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.
25. Malhi, H., Irani, A. N., Gagandeep, S. and Gupta, S. (2002). Isolation of human progenitor liver epithelial cells with extensive replication capacity and differentiation into mature hepatocytes. J. Cell Sci. 115, 2679-2688.
26. Mishra, L., Derynck, R. and Mishra, B. (2005). Transforming growth factor-β signaling in stem cells and cancer. Science 310, 68-71.
27. Morrison, S. J., Perez, S. E., Qiao, Z., Verdi, J. M., Hicks, C., Weinmaster, G. and Anderson, D. J. (2000). Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101, 499-510.
28. Ober, E. A., Verkade, H., Field, H. A. and Stainier, D. Y. R. (2006). Mesodermal wnt2b signaling positively regulates liver specification. Nature 442, 689-691.
29. Okaya, A., Kitanaka, J., Kitanaka, N., Satake, M., Kim, Y., Terada, K., Sugiyama, T., Takemura, M., Fujimoto, J., Terada, N. et al. (2005). Oncostatin M inhibits proliferation of rat oval cells, OC15-5, inducing differentiation into hepatocytes. Am. J. Pathol. 166, 709-719.
30. Olivier, E. N., Rybicki, A. C. and Bouhassira, E. E. (2006). Differentiation of human embryonic stem cells into bipotent mesenchymal stem cells. Stem Cells 24, 1914-1922.
31. Ott, M., Ma, Q., Li, B., Gagandeep, S., Rogler, L. E. and Gupta, S. (1999a). Regulation of hepatitis B virus expression in progenitor and differentiated cell-types: evidence for negative transcriptional control in norpermissive cells. Gene Expr. 8, 175-186.
32. Ott, M., Rajvanshi, P., Sokhl, R., Alpini, G., Aragona, E., Dabeva, M., Shafritz, D. A. and Gupta, S. (1999b). Differentiation-specific regulation of transgene expression in a diploid epithelial cell line derived from the normal F344 rat liver. J. Pathol. 187, 365-373.
33. Pagan, R., Llobera, M. and Vilaro, S. (1995). Epithelial-mesenchymal transition in cultured neonatal hepatocytes. Hepatology 21, 820-831.
34. Qiang, Y. W., Endo, Y., Rubin, J. S. and Rudikoff, S. (2003). Wnt signaling in B-cell neoplasia. Oncogene 22, 1536-1545.
35. Reiner, A., Yekutiell, D. and Benjamini, Y. (2003). Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19, 368-375.
36. Sato, N., Meijer, L., Skaltsounis, L., Greengard, P. and Brivanlou, A. H. (2004). Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat. Med. 10,55-63.
37. Scharenberg, C. W., Harkey, M. A. and Torok-Storb, B. (2002). The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors. Blood 99, 507-512.
38. Schmelzer, E., Wauthier, E. and Reid, L. M. (2006). The phenotypes of pluripotent human hepatic progenitors. Stem Cells 24, 1852-1858.
39. Schwartz, R. E., Reyes, M., Koodie, L., Jiang, Y., Blackstad, M., Lund, T., Lenvik, T., Johnson, S., Hu, W. S. and Verfaillie, C. M. (2002). Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells. J. Clin. Invest. 109, 1291-1302.
40. Shahdadfar, A., Fronsdal, K., Haug, T., Reinholt, F. P. and Brinchmann, J. E. (2005). In vitro expansion of human mesenchymal stem cells: choice of serum is a determinant of cell proliferation, differentiation, gene expression, and transcriptome stability. Stem Cells 23, 1357-1366.
41. Sicklick, J. K., Choi, S. S., Bustamante, M., McCall, S. J., Perez, E. H., Huang, J., Li, Y. X., Rojkind, M. and Diehl, A. M. (2006). Evidence for epithelial-mesenchymal transitions in adult liver cells. Am. J. Physiol. Gastrointest. Liver Physiol. 291, G575-G583.
42. Suand, L., Joseph, B., Formstecher, P. and Laine, B. (1997). mRNA expression of HNF-4 isoforms and of HNF-1alpha/HNF-1beta variants and differentiation of human cell lines that mimic highly specialized phenotypes of intestinal epithelium. Biochem. Biophys. Res. Commun. 235, 920-825.
43. Thiery, J. P. (2002). Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2, 442-454.
44. Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S. and Jones, J. M. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147.
45. Vigna, E., Amendola, M., Benedicenti, F., Simmons, A. D., Follenzi, A. and Naldini, L. (2005). Efficient Tet-dependent expression of human factor IX in vivo by a new self-regulating lentiviral vector. Mol. Ther. 11, 763-775.
46. Walsh, J. and Andrews, P. W. (2003). Expression of Writ and Notch pathway genes in a pluripotent human embryonal carcinoma cell line and embryonic stem cell. APMIS 111, 197-210.
47. Wege, H., Le H. T., Chui, M. S., Liu, L., Wu, J., Giri, R. K., Malhi, H., Sappal, B. S., Kumaran, V., Gupta, S. et al. (2003). Telomerase reconstitution immortalizes human fetal hepatocytes without disrupting their differentiation potential. Gastroenterology 124, 432-444.
48. Winter, M. J, Nagtegaal, I. D., van Krieken, J. H. and Litvinov, S. V. (2003). The epithelial cell adhesion molecule (Ep-CAM) as a morphoregulatory molecule is a tool in surgical pathology. Am. J. Pathol. 163, 2139-2148.
49. Wulbrand, U, Wied, M., Zöfel, P., Göke, B., Arnold, R. and Fehmann, H. (1998). Growth factor receptor expression in human gastroenteropancreatic neuroendocrine tumours. Eur. J. Clin. Invest. 28, 1038-1049.
50. Zalzman, M., Gupta, S., Giri, R. K., Berkovich, I, Sappal, B. S., Karnieli, O., Zern, M. A., Fleischer, N. and Efrat, S. (2003). Reversal of hyperglycerma in mice using human expandable insulin-producing cells differentiated from fetal liver progenitor cells. Proc. Nad. Acad. Sci. USA. 100, 7253-7258.
51. Zavadil, J. and Bottinger, E. P. (2005). TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 24, 5764-5774.
52. Zhou, S., Schuetz, J. D., Bunting, K. D., Colapietro, A. M, Sampath, J., Morris, J. J., Lagutina, I., Grosveld, G. C., Osawa, M., Nakauchi, H. et al. (2001). The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat. Med. 7, 1028-1034.