Generation of functional hepatocyte-like cells from human pluripotent stem cells in a scalable suspension culture

Stem Cells and Development

Volumn 22, Issue 20, 2013, Pages 2693-2705

  Vosough, Massoud ^a,b   Omidinia, Eskandar ^a   Kadivar, Mehdi ^a   Shokrgozar, Mohammad Ali ^a   Pournasr, Behshad ^b   Aghdami, Nasser ^b   Baharvand, Hossein ^b,c  

^a AVICENNA RESEARCH INSTITUTE   (Iran)

^b ROYAN INSTITUTE FOR REPRODUCTIVE BIOMEDICINE   (Iran)

^c UNIVERSITY OF SCIENCE AND CULTURE   (Iran)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL LOW DENSITY LIPOPROTEIN; ALBUMIN; CARBON TETRACHLORIDE; COLLAGEN; CYTOCHROME P450; INDOCYANINE GREEN; UREA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL SELECTION; COLLAGEN SYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVITY; FLOW CYTOMETRY; GENE EXPRESSION; GENETIC MANIPULATION; HUMAN; HUMAN CELL; LIVER CELL; LIVER INJURY; MARKER GENE; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; STIRRED REACTOR; SURVIVAL RATE; SUSPENSION CELL CULTURE; UREA CYCLE;

ANIMALIA; MUS;

ACTIVINS; ALBUMINS; ANIMALS; BIOLOGICAL TRANSPORT; BIOREACTORS; CARBOCYANINES; CARBON TETRACHLORIDE; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL- AND TISSUE-BASED THERAPY; COLLAGEN; DRUG-INDUCED LIVER INJURY; ENDODERM; HEPATOCYTES; LIPOPROTEINS, LDL; LIVER; MALE; MICE; PLURIPOTENT STEM CELLS; SIROLIMUS; SPLEEN; TRANSPLANTATION, HETEROTOPIC;

EID: 84885108863     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2013.0088     Document Type: Article

References (50)

1. Hughes RD, RR Mitry and A Dhawan. (2012). Current status of hepatocyte transplantation. Transplantation 93:342-347
2. Dhawan A, RR Mitry and RD Hughes. (2006). Hepatocyte transplantation for liver-based metabolic disorders. J Inherit Metab Dis 29:431-435
3. Dhawan A, J Puppi, RD Hughes and RR Mitry. (2010). Human hepatocyte transplantation: Current experience and future challenges. Nat Rev Gastroenterol Hepatol 7:288-298
4. Vosough M, M Moslem, B Pournasr and H Baharvand. (2011). Cell-based therapeutics for liver disorders. Br Med Bull 100:157-172
5. Duan Y, A Catana, Y Meng, N Yamamoto, S He, S Gupta, SS Gambhir and MA Zern. (2007). Differentiation and enrichment of hepatocyte-like cells from human embryonic stem cells in vitro and in vivo. Stem Cells 25:3058-3068
6. Cai J, Y Zhao, Y Liu, F Ye, Z Song, H Qin, S Meng, Y Chen, R Zhou, et al. (2007). Directed differentiation of human embryonic stem cells into functional hepatic cells. Hepatology 45:1229-1239
7. Hay DC, D Zhao, J Fletcher, ZA Hewitt, D McLean, A Urruticoechea-Uriguen, JR Black, C Elcombe, JA Ross, R Wolf and W Cui. (2008). Efficient differentiation of hepatocytes from human embryonic stem cells exhibiting markers recapitulating liver development in vivo. Stem Cells 26:894-902
8. Basma H, A Soto-Gutierrez, GR Yannam, L Liu, R Ito, T Yamamoto, E Ellis, SD Carson, S Sato, et al. (2009). Differentiation and transplantation of human embryonic stem cellderived hepatocytes. Gastroenterology 136:990-999
9. Duan Y, X Ma, W Zou, C Wang, IS Bahbahan, TP Ahuja, V Tolstikov and MA Zern. (2010). Differentiation and characterization of metabolically functioning hepatocytes from human embryonic stem cells. Stem Cells 28:674-686
10. Si-Tayeb K, FK Noto, M Nagaoka, J Li, MA Battle, C Duris, PE North, S Dalton and SA Duncan. (2010). Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 51:297-305
11. Asgari S, M Moslem, K Bagheri-Lankarani, B Pournasr, M Miryounesi and H Baharvand. (2011). Differentiation and transplantation of human induced pluripotent stem cellderived hepatocyte-like cells. Stem Cell Rev [Epub ahead of print]; DOI: 10.1007/s12015-011-9330-y.
12. Sullivan GJ, DC Hay, IH Park, J Fletcher, Z Hannoun, CM Payne, D Dalgetty, JR Black, JA Ross, et al. (2010). Generation of functional human hepatic endoderm from human induced pluripotent stem cells. Hepatology 51:329-335
13. Touboul T, NR Hannan, S Corbineau, A Martinez, C Martinet, S Branchereau, S Mainot, H Strick-Marchand, R Pedersen, et al. (2010). Generation of functional hepatocytes from human embryonic stem cells under chemically defined conditions that recapitulate liver development. Hepatology 51:1754-1765
14. Chen YF, CY Tseng, HW Wang, HC Kuo, VW Yang and OK Lee. (2012). Rapid generation of mature hepatocyte-like cells from human induced pluripotent stem cells by an efficient three-step protocol. Hepatology 55:1193-1203
15. Song Z, J Cai, Y Liu, D Zhao, J Yong, S Duo, X Song, Y Guo, Y Zhao, et al. (2009). Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells. Cell Res 19:1233-1242
16. Hay DC, J Fletcher, C Payne, JD Terrace, RC Gallagher, J Snoeys, JR Black, D Wojtacha, K Samuel, et al. (2008). Highly efficient differentiation of hESCs to functional hepatic endoderm requires ActivinA and Wnt3a signaling. Proc Natl Acad Sci U S A 105:12301-12306
17. Hay DC, S Pernagallo, JJ Diaz-Mochon, CN Medine, S Greenhough, Z Hannoun, J Schrader, JR Black, J Fletcher, et al. (2011). Unbiased screening of polymer libraries to define novel substrates for functional hepatocytes with inducible drug metabolism. Stem Cell Res 6:92-102
18. Totonchi M, A Taei, A Seifinejad, M Tabebordbar, H Rassouli, A Farrokhi, H Gourabi, N Aghdami, G Hosseini- Salekdeh and H Baharvand. (2010). Feeder- and serum-free establishment and expansion of human induced pluripotent stem cells. Int J Dev Biol 54:877-886
19. Baharvand H, SK Ashtiani, A Taee, M Massumi, MR Valojerdi, PE Yazdi, SZ Moradi and A Farrokhi. (2006). Generation of new human embryonic stem cell lines with diploid and triploid karyotypes. Dev Growth Differ 48:117-128
20. Dixit V, N Hariparsad, F Li, P Desai, KE Thummel and JD Unadkat. (2007). Cytochrome P450 enzymes and transporters induced by anti-human immunodeficiency virus protease inhibitors in human hepatocytes: Implications for predicting clinical drug interactions. Drug Metab Dispos 35:1853-1859
21. Abbasalizadeh S, MR Larijani, A Samadian and H Baharvand. (2012). Bioprocess development for mass production of size-controlled human pluripotent stem cell aggregates in stirred suspension bioreactor. Tissue Eng Part C Methods 18:831-851
22. Larijani MR, A Seifinejad, B Pournasr, V Hajihoseini, SN Hassani, M Totonchi, M Yousefi, F Shamsi, GH Salekdeh and H Baharvand. (2011). Long-term maintenance of undifferentiated human embryonic and induced pluripotent stem cells in suspension. Stem Cells Dev 20:1911-1923
23. Kanai-Azuma M, Y Kanai, JM Gad, Y Tajima, C Taya, M Kurohmaru, Y Sanai, H Yonekawa, K Yazaki, PP Tam and Y Hayashi. (2002). Depletion of definitive gut endoderm in Sox17-null mutant mice. Development 129:2367-2379
24. Bauwens CL, R Peerani, S Niebruegge, KA Woodhouse, E Kumacheva, M Husain and PW Zandstra. (2008). Control of human embryonic stem cell colony and aggregate size heterogeneity influences differentiation trajectories. Stem Cells 26:2300-2310
25. Tahamtani Y, M Azarnia, A Farrokhi, A Sharifi-Zarchi, N Aghdami and H Baharvand. (2013). Treatment of human embryonic stem cells with different combinations of priming and inducing factors toward definitive endoderm. Stem Cells Dev 22:1419-1432
26. Mfopou JK and L Bouwens. (2008). Hedgehog signals in pancreatic differentiation from embryonic stem cells: Revisiting the neglected. Differentiation 76:107-117
27. Zhou W, Z Hannoun, E Jaffray, CN Medine, JR Black, S Greenhough, L Zhu, JA Ross, S Forbes, et al. (2012). SUMOylation of HNF4alpha regulates protein stability and hepatocyte function. J Cell Sci 125:3630-3635
28. Miki T, A Ring and J Gerlach. (2011). Hepatic differentiation of human embryonic stem cells is promoted by three-dimensional dynamic perfusion culture conditions. Tissue Eng Part C Methods 17:557-568
29. Dvir-Ginzberg M, I Gamlieli-Bonshtein, R Agbaria and S Cohen. (2003). Liver tissue engineering within alginate scaffolds: Effects of cell-seeding density on hepatocyte viability, morphology, and function. Tissue Eng 9:757-766
30. Behbahan IS, Y Duan, A Lam, S Khoobyari, X Ma, TP Ahuja and MA Zern. (2011). New approaches in the differentiation of human embryonic stem cells and induced pluripotent stem cells toward hepatocytes. Stem Cell Rev 7:748-759
31. Asgari S, B Pournasr, GH Salekdeh, A Ghodsizadeh, M Ott and H Baharvand. (2010). Induced pluripotent stem cells: A new era for hepatology. J Hepatol 53:738-751
32. Chistiakov DA and PA Chistiakov. (2012). Strategies to produce hepatocytes and hepatocyte-like cells from pluripotent stem cells. Hepatol Res 42:111-119
33. Ungrin MD, G Clarke, T Yin, S Niebrugge, MC Nostro, F Sarangi, G Wood, G Keller and PW Zandstra. (2012). Rational bioprocess design for human pluripotent stem cell expansion and endoderm differentiation based on cellular dynamics. Biotechnol Bioeng 109:853-866
34. Lock LT and ES Tzanakakis. (2009). Expansion and differentiation of human embryonic stem cells to endoderm progeny in a microcarrier stirred-suspension culture. Tissue Eng Part A 15:2051-2063
35. Schulz TC,HYYoung,ADAgulnick,MJ Babin, EE Baetge,AG Bang, A Bhoumik, I Cepa, RMCesario, et al. (2012). A scalable system for production of functional pancreatic progenitors from human embryonic stem cells. PLoS One 7:e37004
36. Tong JZ, S Sarrazin, D Cassio, F Gauthier and F Alvarez. (1994). Application of spheroid culture to human hepatocytes and maintenance of their differentiation. Biol Cell 81:77-81
37. Ramasamy TS, JS Yu, C Selden, H Hodgson and W Cui. (2012). Application of three-dimensional culture conditions to human embryonic stem cell-derived definitive endoderm cells enhances hepatocyte differentiation and functionality. Tissue Eng Part A 19:360-367
38. Baharvand H, SM Hashemi, S Kazemi Ashtiani and A Farrokhi. (2006). Differentiation of human embryonic stem cells into hepatocytes in 2D and 3D culture systems in vitro. Int J Dev Biol 50:645-652
39. Schmelzer E, F Triolo, ME Turner, RL Thompson, K Zeilinger, LM Reid, B Gridelli and JC Gerlach. (2010). Threedimensional perfusion bioreactor culture supports differentiation of human fetal liver cells. Tissue Eng Part A 16:2007-2016
40. Miranda JP, SB Leite, U Muller-Vieira, A Rodrigues, MJ Carrondo and PM Alves. (2009). Towards an extended functional hepatocyte in vitro culture. Tissue Eng Part C Methods 15:157-167
41. Gabriel E, S Schievenbusch, E Kolossov, JG Hengstler, T Rotshteyn, H Bohlen, D Nierhoff, J Hescheler and I Drobinskaya. (2012). Differentiation and selection of hepatocyte precursors in suspension spheroid culture of transgenic murine embryonic stem cells. PLoS One 7:e44912
42. Takayama K, K Kawabata, Y Nagamoto, K Kishimoto, K Tashiro, F Sakurai, M Tachibana, K Kanda, T Hayakawa, MK Furue and H Mizuguchi. (2012). 3D spheroid culture of hESC/hiPSC-derived hepatocyte-like cells for drug toxicity testing. Biomaterials 34:1781-1789
43. Sherar MD, MB Noss and FS Foster. (1987). Ultrasound backscatter microscopy images the internal structure of living tumour spheroids. Nature 330:493-495
44. Glicklis R, JC Merchuk and S Cohen. (2004). Modeling mass transfer in hepatocyte spheroids via cell viability, spheroid size, and hepatocellular functions. Biotechnol Bioeng 86:672-680
45. ten Berge D, W Koole, C Fuerer, M Fish, E Eroglu and R Nusse. (2008). Wnt signaling mediates self-organization and axis formation in embryoid bodies. Cell Stem Cell 3:508-518
46. Jeon SO, HJ Hwang, DH Oh, JE Seo, KH Chun, SM Hong, MJ Kim, WC Kim, MS Park, et al. (2012). Enhanced percutaneous delivery of recombinant human epidermal growth factor employing nano-liposome system. J Microencapsul 29:234-241
47. Hu J and PX Ma. (2011). Nano-fibrous tissue engineering scaffolds capable of growth factor delivery. Pharm Res 28:1273-1281
48. Yu J, NF Huang, KDWilson, JB Velotta,MHuang, Z Li,ALee, RC Robbins, JP Cooke and JC Wu. (2009). nAChRs mediate human embryonic stem cell-derived endothelial cells: proliferation, apoptosis, and angiogenesis. PLoS One 4:e7040
49. Takayama K, M Inamura, K Kawabata, K Katayama, M Higuchi, K Tashiro, A Nonaka, F Sakurai, T Hayakawa, MK Furue and H Mizuguchi. (2012). Efficient generation of functional hepatocytes from human embryonic stem cells and induced pluripotent stem cells by HNF4alpha transduction. Mol Ther 20:127-137
50. Woo DH, SK Kim, HJ Lim, J Heo, HS Park, GY Kang, SE Kim, HJ You, DJ Hoeppner, et al. (2012). Direct and indirect contribution of human embryonic stem cell-derived hepatocytelike cells to liver repair in mice. Gastroenterology 142:602-611