Hepatic differentiation of human embryonic stem cells is promoted by three-dimensional dynamic perfusion culture conditions

Tissue Engineering - Part C: Methods

Volumn 17, Issue 5, 2011, Pages 557-568

  Miki, Toshio ^a,c   Ring, Alexander ^a,b   Gerlach, Jörg ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOREACTORS; CELL GROWTH; FLOW CYTOMETRY; GENE EXPRESSION; METABOLISM; OXYGENATION; PEPTIDES; PHYSIOLOGY; STEM CELLS; THREE DIMENSIONAL;

3D CULTURE; 3D SYSTEMS; AMMONIA METABOLISM; ASIALOGLYCOPROTEIN RECEPTORS; BIOARTIFICIAL LIVER; CYTOCHROME P450 GENES; DEVELOPMENTAL POTENTIAL; DRUG DISCOVERY; FLOW CYTOMETRY ANALYSIS; GROWTH FACTOR; HEPATIC CELLS; HEPATIC DIFFERENTIATION; HEPATIC FUNCTION; HEPATOCYTES; HOLLOW FIBER; HUMAN EMBRYONIC STEM CELLS; HUMAN HEPATOCYTES; IMMUNOHISTOCHEMICAL ANALYSIS; MULTI-STEP; PARALLEL CONTROL; PERFUSION BIOREACTOR; PERFUSION CONDITIONS; PERFUSION CULTURES; PROTEIN EXPRESSIONS; STATIC CONDITIONS; STATIC CULTURE; STRUCTURAL FORMATION; THREE-DIMENSIONAL (3D); THREE-DIMENSIONAL DYNAMICS;

CELL CULTURE;

BIOLOGICAL MARKER; CYP3A4 PROTEIN, HUMAN; CYP3A7 PROTEIN, HUMAN; CYTOCHROME P450 3A; UNSPECIFIC MONOOXYGENASE;

ARTICLE; BIOREACTOR; CELL DIFFERENTIATION; CELL LINE; CULTURE TECHNIQUE; CYTOLOGY; EMBRYONIC STEM CELL; ENDODERM; ENZYMOLOGY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; HUMAN; LIVER; LIVER CELL; METABOLISM; METHODOLOGY; PERFUSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ARYL HYDROCARBON HYDROXYLASES; BIOLOGICAL MARKERS; BIOREACTORS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE; CYTOCHROME P-450 CYP3A; EMBRYONIC STEM CELLS; ENDODERM; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; HEPATOCYTES; HUMANS; LIVER; PERFUSION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 79955462003     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2010.0437     Document Type: Article

References (58)

1. Pillai, A.A., and Levitsky, J. Overview of immunosuppression in liver transplantation. World J Gastroenterol 15, 4225, 2009.
2. Navarro-Alvarez, N., Soto-Gutierrez, A., and Kobayashi, N. Stem cell research and therapy for liver disease. Curr Stem Cell Res Ther 4, 141, 2009.
3. 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, 146, 2002.
4. Yamamoto, H., Quinn, G., Asari, A., Yamanokuchi, H., Teratani, T., Terada, M., and Ochiya, T. Differentiation of embryonic stem cells into hepatocytes: biological functions and therapeutic application. Hepatology 37, 983, 2003.
5. D'Amour, K.A., Agulnick, A.D., Eliazer, S., Kelly, O.G., Kroon, E., and Baetge, E.E. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol 23, 1534, 2005.
6. Cai, J., Zhao, Y., Liu, Y., Ye, F., Song, Z., Qin, H., Meng, S., Chen, Y., Zhou, R., Song, X., Guo, Y., Ding, M., and Deng, H. Directed differentiation of human embryonic stem cells into functional hepatic cells. Hepatology 45, 1229, 2007.
7. Zhou, Q.J., Huang, Y.D., Xiang, L.X., Shao, J.Z., Zhou, G.S., Yao, H., Dai, L.C., and Lu, Y.L. In vitro differentiation of embryonic stem cells into hepatocytes induced by fibroblast growth factors and bone morphological protein-4. Int J Biochem Cell Biol 39, 1714, 2007.
8. Agarwal, S., Holton, K.L., and Lanza, R. Efficient differentiation of functional hepatocytes from human embryonic stem cells. Stem Cells 26, 1117, 2008.
9. Pei, H., Yang, Y., Xi, J., Bai, Z., Yue, W., Nan, X., Bai, C., Wang, Y., and Pei, X. Lineage restriction and differentiation of human embryonic stem cells into hepatic progenitors and zone 1 hepatocytes. Tissue Eng 15, 95, 2009.
10. Schuetz, E.G., Schuetz, J.D., May, B., and Guzelian, P.S. Regulation of cytochrome P-450b/e and P-450p gene expression by growth hormone in adult rat hepatocytes cultured on a reconstituted basement membrane. J Biol Chem 265, 1188, 1990.
11. Wortelboer, H.M., de Kruif, C.A., van Iersel, A.A., Falke, H.E., Noordhoek, J., and Blaauboer, B.J. The isoenzyme pattern of cytochrome P450 in rat hepatocytes in primary culture, comparing different enzyme activities in microsomal incubations and in intact monolayers. Biochem Pharmacol 40, 2525, 1990.
12. Arterburn, L.M., Zurlo, J., Yager, J.D., Overton, R.M., and Heifetz, A.H. A morphological study of differentiated hepatocytes in vitro. Hepatology 22, 175, 1995.
13. Fiegel, H.C., Havers, J., Kneser, U., Smith, M.K., Moeller, T., Kluth, D., Mooney, D.J., Rogiers, X., and Kaufmann, P.M. Influence of flow conditions and matrix coatings on growth and differentiation of three-dimensionally cultured rat hepatocytes. Tissue Eng 10, 165, 2004.
14. Monga, S.P., Hout, M.S., Baun, M.J., Micsenyi, A., Muller, P., Tummalapalli, L., Ranade, A.R., Luo, J.H., Strom, S.C., and Gerlach, J.C. Mouse fetal liver cells in artificial capillary beds in three-dimensional four-compartment bioreactors. Am J Pathol 167, 1279, 2005.
15. Gerlach, J.C. Long-term liver cell cultures in bioreactors and possible application for liver support. Cell Biol Toxicol 13, 349, 1997.
16. Gerlach, J.C., Kloppel, K., Muller, C., Schnoy, N., Smith, M.D., and Neuhaus, P. Hepatocyte aggregate culture technique for bioreactors in hybrid liver support systems. Int J Artif Organs 16, 843, 1993.
17. Ring, A., Gerlach, J., Peters, G., Pazin, B.J., Minervini, C.F., Turner, M.E., Thompson, R.L., Triolo, F., Gridelli, B., and Miki, T. Hepatic maturation of human fetal hepatocytes in four-compartment three-dimensional perfusion culture. Tissue Eng 16, 835, 2010.
18. Gerlach, J.C., Hout, M., Edsbagge, J., Bjorquist, P., Lubberstedt, M., Miki, T., Stachelscheid, H., Schmelzer, E., Schatten, G., and Zeilinger, K. Dynamic 3D culture promotes spontaneous embryonic stem cell differentiation in vitro. Tissue Eng 16, 115, 2010.
19. Gerlach, J.C., Encke, J., Hole, O., Muller, C., Ryan, C.J., and Neuhaus, P. Bioreactor for a larger scale hepatocyte in vitro perfusion. Transplantation 58, 984, 1994.
20. Gerlach, J., Kloppel, K., Stoll, P., Vienken, J., and Muller, C. Gas supply across membranes in bioreactors for hepatocyte culture. Artif Organs 14, 328, 1990.
21. Gerlach, J., Stoll, P., Schnoy, N., and Bucherl, E.S. Membranes as substrates for hepatocyte adhesion in liver support bioreactors. Int J Artif Organs 13, 436, 1990.
22. Gerlach, J., Schnoy, N., Smith, M.D., and Neuhaus, P. Hepatocyte culture between woven capillary networks: a microscopy study. Artif Organs 18, 226, 1994.
23. Heins, N., Englund, M.C., Sjoblom, C., Dahl, U., Tonning, A., Bergh, C., Lindahl, A., Hanson, C., and Semb, H. Derivation, characterization, and differentiation of human embryonic stem cells. Stem Cells 22, 367, 2004.
24. Ellerstrom, C., Strehl, R., Noaksson, K., Hyllner, J., and Semb, H. Facilitated expansion of human embryonic stem cells by single-cell enzymatic dissociation. Stem Cells 25, 1690, 2007.
25. Pfaffl, M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, e45, .2001.
26. Pfaffl, M.W., Horgan, G.W., and Dempfle, L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in realtime PCR. Nucleic Acids Res 30, e36, 2002.
27. Fox, I.J., and Strom, S.C. To be or not to be: generation of hepatocytes from cells outside the liver. Gastroenterology 134, 878, 2008.
28. Li, Y., Huang, G., Diakur, J., and Wiebe, L.I. Targeted delivery of macromolecular drugs: asialoglycoprotein receptor (ASGPR) expression by selected hepatoma cell lines used in antiviral drug development. Curr Drug Deliv 5, 299, 2008.
29. Treichel, U., Meyer zum Buschenfelde, K.H., Dienes, H.P., and Gerken, G. Receptor-mediated entry of hepatitis B virus particles into liver cells. Arch Virol 142, 493, 1997.
30. Treichel, U., Meyer zum Buschenfelde, K.H., Stockert, R.J., Poralla, T., and Gerken, G. The asialoglycoprotein receptor mediates hepatic binding and uptake of natural hepatitis B virus particles derived from viraemic carriers. J Gen Virol 75, 3021, 1994.
31. Treichel, U., Schreiter, T., Meyer zum Buschenfelde, K.H., and Stockert, R.J. High-yield purification and characterization of human asialoglycoprotein receptor. Protein Expr Purif 6, 251, 1995.
32. Bissell, D.M. Primary hepatocyte culture: substratum requirements and production of matrix components. Fed Proc 40, 2469, 1981.
33. Dunn, J.C., Tompkins, R.G., and Yarmush, M.L. Long-term in vitro function of adult hepatocytes in a collagen sandwich configuration. Biotechnol Prog 7, 237, 1991.
34. Elkayam, T., Amitay-Shaprut, S., Dvir-Ginzberg, M., Harel, T., and Cohen, S. Enhancing the drug metabolism activities of C3A - a human hepatocyte cell line-by tissue engineering within alginate scaffolds. Tissue Eng 12, 1357, 2006.
35. Cheng, N., Wauthier, E., and Reid, L.M. Mature human hepatocytes from ex vivo differentiation of alginateencapsulated hepatoblasts. Tissue Eng 14, 1, 2008.
36. Lund, A.W., Yener, B., Stegemann, J.P., and Plopper, G.E. The natural and engineered 3D microenvironment as a regulatory cue during stem cell fate determination. Tissue Eng 15, 371, 2009.
37. Imamura, T., Cui, L., Teng, R., Johkura, K., Okouchi, Y., Asanuma, K., Ogiwara, N., and Sasaki, K. Embryonic stem cell-derived embryoid bodies in three-dimensional culture system form hepatocyte-like cells in vitro and in vivo. Tissue Eng 10, 1716, 2004.
38. Soto-Gutierrez, A., Navarro-Alvarez, N., Rivas-Carrillo, J.D., Chen, Y., Yamatsuji, T., Tanaka, N., and Kobayashi, N. Differentiation of human embryonic stem cells to hepatocytes using deleted variant of HGF and poly-aminourethane- coated nonwoven polytetrafluoroethylene fabric. Cell Transplant 15, 335, 2006.
39. Matsumoto, K., Mizumoto, H., Nakazawa, K., Ijima, H., Funatsu, K., and Kajiwara, T. Hepatic differentiation of mouse embryonic stem cells in a three-dimensional culture system using polyurethane foam. J Biosci Bioeng 105, 350, .2008.
40. Liu, T., Zhang, S., Chen, X., Li, G., and Wang, Y. Hepatic differentiation of mouse embryonic stem cells in threedimensional polymer scaffolds. Tissue Eng 16, 1115, 2010.
41. Jochheim, A., Hillemann, T., Kania, G., Scharf, J., Attaran, M., Manns, M.P., Wobus, A.M., and Ott, M. Quantitative gene expression profiling reveals a fetal hepatic phenotype of murine ES-derived hepatocytes. Int J Dev Biol 48, 23, 2004.
42. Stearns, R.A., Chakravarty, P.K., Chen, R., and Chiu, S.H. Biotransformation of losartan to its active carboxylic acid metabolite in human liver microsomes. Role of cytochrome P4502C and 3A subfamily members. Drug Metab Dispos 23, 207, 1995.
43. Guengerich, F.P. Uncommon P450-catalyzed reactions. Curr Drug Metab 2, 93, 2001.
44. Meunier, B., de Visser, S.P., and Shaik, S. Mechanism of oxidation reactions catalyzed by cytochrome p450 enzymes. Chem Rev 104, 3947, 2004.
45. Lacroix, D., Sonnier, M., Moncion, A., Cheron, G., and Cresteil, T. Expression of CYP3A in the human liver- evidence that the shift between CYP3A7 and CYP3A4 occurs immediately after birth. Eur J Biochem 247, 625, 1997.
46. Ise, H., Nikaido, T., Negishi, N., Sugihara, N., Suzuki, F., Akaike, T., and Ikeda, U. Effective hepatocyte transplantation using rat hepatocytes with low asialoglycoprotein receptor expression. Am J Pathol 165, 501, 2004.
47. Liu, S., Yang, W., Shen, L., Turner, J.R., Coyne, C.B., and Wang, T. Tight junction proteins claudin-1 and occludin control hepatitis C virus entry and are downregulated during infection to prevent superinfection. J Virol 83, 2011, 2009.
48. Boonstra, A., van der Laan, L.J., Vanwolleghem, T., and Janssen, H.L. Experimental models for hepatitis C viral infection. Hepatology 50, 1646, 2009.
49. Brass, V., Moradpour, D., and Blum, H.E. Hepatitis C virus infection: in vivo and in vitro models. J Viral Hepat 14 Suppl 1, 64, 2007.
50. Mavri-Damelin, D., Damelin, L.H., Eaton, S., Rees, M., Selden, C., and Hodgson, H.J. Cells for bioartificial liver devices: the human hepatoma-derived cell line C3A produces urea but does not detoxify ammonia. Biotechnol Bioeng 99, 644, 2008.
51. Hoyes, A.D., Riches, D.J., and Martin, B.G. The fine structure of haemopoiesis in the human fetal liver. I. The haemopoietic precursor cells. J Anat 115, 99, 1973.
52. Antoniou, A., Raynaud, P., Cordi, S., Zong, Y., Tronche, F., Stanger, B.Z., Jacquemin, P., Pierreux, C.E., Clotman, F., and Lemaigre, F.P. Intrahepatic bile ducts develop according to a new mode of tubulogenesis regulated by the transcription factor SOX9. Gastroenterology 136, 2325, 2009.
53. Ohno, M., Motojima, K., Okano, T., and Taniguchi, A. Maturation of the extracellular matrix and cell adhesion molecules in layered co-cultures of HepG2 and endothelial cells. J Biochem 145, 591, 2009.
54. Ng, S., Wu, Y.N., Zhou, Y., Toh, Y.E., Ho, Z.Z., Chia, S.M., Zhu, J.H., Mao, H.Q., and Yu, H. Optimization of 3-D hepatocyte culture by controlling the physical and chemical properties of the extra-cellular matrices. Biomaterials 26, 3153, 2005.
55. Abu-Absi, S.F., Friend, J.R., Hansen, L.K., and Hu, W.S. Structural polarity and functional bile canaliculi in rat hepatocyte spheroids. Exp Cell Res 274, 56, 2002.
56. Gerlach, J.C., Lubberstedt, M., Edsbagge, J., Ring, A., Hout, M., Baun, M., Rossberg, I., Knospel, F., Peters, G., Eckert, K., Wulf-Goldenberg, A., Bjorquist, P., Stachelscheid, H., Urbaniak, T., Schatten, G., Miki, T., Schmelzer, E., and Zeilinger, K. Interwoven four-compartment capillary membrane technology for three-dimensional perfusion with decentralized mass exchange to scale up embryonic stem cell culture. Cells Tissues Organs 192, 39, 2010.
57. Sauer, I.M., Zeilinger, K., Pless, G., Kardassis, D., Theruvath, T., Pascher, A., Goetz, M., Neuhaus, P., and Gerlach, J.C. Extracorporeal liver support based on primary human liver cells and albumin dialysis-treatment of a patient with primary graft non-function. J Hepatol 39, 649, 2003.
58. Sauer, I.M., Kardassis, D., Zeillinger, K., Pascher, A., Gruenwald, A., Pless, G., Irgang, M., Kraemer, M., Puhl, G., Frank, J., Muller, A.R., Steinmuller, T., Denner, J., Neuhaus, P., and Gerlach, J.C. Clinical extracorporeal hybrid liver support-phase I study with primary porcine liver cells. Xenotransplantation 10, 460, 2003.