Improved hepatic differentiation strategies for human induced pluripotent stem cells

Current Molecular Medicine

Volumn 13, Issue 5, 2013, Pages 842-855

  Sgodda, M ^a   Mobus S ^a   Hoepfner, J ^a   Sharma, A D ^a   Schambach, A ^a   Greber, B ^b   Ott, M ^a,c   Cantz, T ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^c INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

Author keywords

Hepatic differentiation; Human ES cells; Human iPS cells; Lentiviral selection constructs; Metabolic functions

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ACTIVIN A; ALKALINE PHOSPHATASE; ALPHA FETOPROTEIN; ANTIBIOTIC G 418; CYTOCHROME P450 1A1; HEPATOCYTE NUCLEAR FACTOR 4; KRUPPEL LIKE FACTOR 4; LENTIVIRUS VECTOR; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX1; TRANSCRIPTION FACTOR SOX2;

ALBUMIN BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROBLAST CULTURE; FLOW CYTOMETRY; GENE EXPRESSION; GENE TRANSFER; GENETIC TRANSDUCTION; HISTOLOGY; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; ANTIGENS, DIFFERENTIATION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; FIBROBLASTS; GENE EXPRESSION; HEPATOCYTES; HOMEODOMAIN PROTEINS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; LIVER; MICE; NUCLEAR REPROGRAMMING; OCTAMER TRANSCRIPTION FACTOR-3; SOXB1 TRANSCRIPTION FACTORS;

EID: 84881341670     PISSN: 15665240     EISSN: 18755666     Source Type: Journal    
DOI: 10.2174/1566524011313050015     Document Type: Article

References (68)

1. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126(4): 663-676.
2. Okita K, Ichisaka T, Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature 2007; 448(7151): 313-317.
3. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of Pluripotent Stem Cells from Adult Human Fibroblasts by Defined Factors. Cell 2007; 131(5): 861-872.
4. Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced Pluripotent Stem Cell Lines Derived from Human Somatic Cells. Science 2007; 318(5858): 1917-1920.
5. Okita K, Nakagawa M, Hyenjong H, Ichisaka T, Yamanaka S. Generation of mouse induced pluripotent stem cells without viral vectors. Science 2008; 322(5903): 949-953.
6. Stadtfeld M, Nagaya M, Utikal J, Weir G, Hochedlinger K. Induced pluripotent stem cells generated without viral integration. Science 2008; 322(5903): 945-949.
7. Fusaki N, Ban H, Nishiyama A, Saeki K, Hasegawa M. Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proc Jpn Acad Ser B Phys Biol Sci 2009; 85(8): 348-362.
8. Yu J, Hu K, Smuga-Otto K, et al. Human induced pluripotent stem cells free of vector and transgene sequences. Science 2009; 324(5928): 797-801.
9. Kim D, Kim CH, Moon JI, et al. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 2009; 4(6): 472-476.
10. Utikal J, Polo JM, Stadtfeld M, et al. Immortalization eliminates a roadblock during cellular reprogramming into iPS cells. Nature 2009; 460(7259): 1145-1148.
11. Warren L, Manos PD, Ahfeldt T, et al. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 2010; 7(5): 618-630.
12. Mayshar Y, Ben-David U, Lavon N, et al. Identification and classification of chromosomal aberrations in human induced pluripotent stem cells. Cell Stem Cell 2010; 7(4): 521-531.
13. Hussein SM, Batada NN, Vuoristo S, et al. Copy number variation and selection during reprogramming to pluripotency. Nature 2011; 471(7336): 58-62.
14. Gore A, Li Z, Fung HL, et al. Somatic coding mutations in human induced pluripotent stem cells. Nature 2011; 471(7336): 63-67.
15. Lister R, Pelizzola M, Kida YS, et al. Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 2011; 471(7336): 68-73.
16. Judson RL, Babiarz JE, Venere M, Blelloch R. Embryonic stem cell-specific microRNAs promote induced pluripotency. Nat Biotechnol 2009; 27(5): 459-4561.
17. Pfaff N, Moritz T, Thum T, Cantz T. miRNAs involved in the generation, maintencance, and differentiation of pluripotent stem cells. J Mol Med 2012; 90(7): 747-752.
18. Pfaff N, Fiedler J, Holzmann A, et al. miRNA screening reveals a new miRNA family stimulating iPS cell generation via regulation of Meox2. EMBO Rep 2011; 12(11): 1153-1159.
19. Sommer CA, Stadtfeld M, Murphy GJ, Hochedlinger K, Kotton DN, Mostoslavsky G. Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells 2009; 27(3): 543-549.
20. Warlich E, Kühle J, Cantz T, et al. Lentiviral Vector Design and Imaging Approaches to Visualize the Early Stages of Cellular Reprogramming. Mol Ther 2011; 19(4): 782-789.
21. Voelkel C, Galla M, Maetzig T, et al. Protein transduction from retroviral Gag precursors. Proc Natl Acad Sci USA 2010; 107(17): 7805-7810.
22. Papapetrou EP, Tomishima MJ, Chambers SM, et al. Stoichiometric and temporal requirements of Oct4, Sox2, Klf4, and c-Myc expression for efficient human iPSC induction and differentiation. Proc Natl Acad Sci USA 2009; 106(31): 12759-12764.
23. Tiemann U, Sgodda M, Warlich E, et al. Optimal Reprogramming Factor Stoichiometry Increases Colony Numbers and Affects Molecular Characteristics of Murine Induced Pluripotent Stem Cells. Cytometry Part A 2011; 79A: 426-435.
24. Dhawan A, Mitry RR, Hughes RD. Hepatocyte transplantation for liver-based metabolic disorders. J Inherit Metab Dis 2006; 29(2-3): 431-435.
25. Meyburg J, Das AM, Hoerster F, et al. One liver for four children: first clinical series of liver cell transplantation for severe neonatal urea cycle defects. Transplantation 2009; 87(5): 636-641.
26. Puppi J, Strom SC, Hughes RD, et al. Improving the Techniques for Human Hepatocyte Transplantation: Report from a Consensus Meeting in London. Cell Transplant 2012; 21(1): 1-10.
27. Cantz T, Zuckerman DM, Burda MR, et al. Quantitative gene expression analysis reveals transition of fetal liver progenitor cells to mature hepatocytes after transplantation in uPA/RAG-2 mice. Am J Pathol 2003; 162(1): 37-45.
28. Sharma AD, Cantz T, Vogel A, et al. Murine embryonic stem cell-derived hepatic progenitor cells engraft in recipient livers with limited capacity of liver tissue formation. Cell Transplant 2008; 17(3): 313-323.
29. Haridass D, Yuan Q, Becker PD, et al. Repopulation Efficiencies of Adult Hepatocytes, Fetal Liver Progenitor Cells, and Embryonic Stem Cell-Derived Hepatic Cells in Albumin-Promoter-Enhancer Urokinase-Type Plasminogen Activator Mice. Am J Pathol 2009; 175(4): 1483-1492.
30. Miyashita H, Suzuki A, Fukao K, Nakauchi H, Taniguchi H. Evidence for hepatocyte differentiation from embryonic stem cells in vitro. Cell Transplant 2002; 11(5): 429-434.
31. Kania G, Blyszczuk P, Jochheim A, Ott M, Wobus AM. Generation of glycogen- and albumin-producing hepatocyte-like cells from embryonic stem cells. Biol Chem 2004; 385(10): 943-953.
32. Zaret KS, Grompe M. Generation and regeneration of cells of the liver and pancreas. Science 2008; 322(5907): 1490-1494.
33. McLean AB, D'Amour KA, Jones KL, et al. Activin a efficiently specifies definitive endoderm from human embryonic stem cells only when phosphatidylinositol 3-kinase signaling is suppressed. Stem Cells 2007; 25(1): 29-38.
34. Gouon-Evans V, Boussemart L, Gadue P, et al. BMP-4 is required for hepatic specification of mouse embryonic stem cell-derived definitive endoderm. Nat Biotechnol 2006; 24(11): 1402-1411.
35. Heo J, Factor VM, Uren T, et al. Hepatic precursors derived from murine embryonic stem cells contribute to regeneration of injured liver. Hepatology 2006; 44(6): 1478-1486.
36. Loya K, Eggenschwiler R, Ko K, et al. Hepatic differentiation of pluripotent stem cells. Biol Chem 2009; 390(10): 1047-1055.
37. Eggenschwiler R, Loya K, Sgodda M, Andre F, Cantz T. Hepatic differentiation of murine disease-specific induced pluripotent stem cells allows disease modelling in vitro. Stem Cells Int 2011; 2011: 924782.
38. Cai J, Zhao Y, Liu Y, et al. Directed differentiation of human embryonic stem cells into functional hepatic cells. Hepatology 2007; 45(5): 1229-1239.
39. Si-Tayeb K, Noto FK, Nagaoka M, et al. Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 2010; 51(1): 297-305.
40. Sullivan GJ, Hay DC, Park IH, et al. Generation of functional human hepatic endoderm from human induced pluripotent stem cells. Hepatology 2010; 51(1): 329-335.
41. Touboul T, Hannan NR, Corbineau S, et al. Generation of functional hepatocytes from human embryonic stem cells under chemically defined conditions that recapitulate liver development. Hepatology 2010; 51(5): 1754-1765.
42. Zaehres H, Kogler G, Arauzo-Bravo MJ, et al. Induction of pluripotency in human cord blood unrestricted somatic stem cells. Exp Hematol 2010; 38(9): 809-818.
43. Dull T, Zufferey R, Kelly M, et al. A third-generation lentivirus vector with a conditional packaging system. J Virol 1998; 72(11): 8463-8471.
44. Zimmer V, Lammert F. Genetics in liver disease: new concepts. Curr Opin Gastroenterol 2011; 27(3): 231-239.
45. Estep JM, Birerdinc A, Younossi Z. Non-invasive diagnostic tests for non-alcoholic fatty liver disease. Curr Mol Med 2010; 10(2): 166-172.
46. Polyzos SA, Kountouras J, Deretzi G, Zavos C, Mantzoros CS. The emerging role of endocrine disruptors in pathogenesis of insulin resistance: a concept implicating nonalcoholic fatty liver disease. Curr Mol Med 2012; 12(1): 68-82.
47. Gonzalez-Gallego J, Garcia-Mediavilla MV, Sanchez-Campos S. Hepatitis C virus, oxidative stress and steatosis: current status and perspectives. Curr Mol Med 2011; 11(5): 373-390.
48. Park IH, Arora N, Huo H, et al. Disease-specific induced pluripotent stem cells. Cell 2008; 134(5): 877-886.
49. Ye ZH, Zhan HC, Mali P, et al. Human-induced pluripotent stem cells from blood cells of healthy donors and patients with acquired blood disorders. Blood 2009; 114(27): 5473-5480.
50. Wang YX, Jiang YH, Liu S, Sun XF, Gao SR. Generation of induced pluripotent stem cells from human beta-thalassemia fibroblast cells. Cell Res 2009; 19(9): 1120-1123.
51. Dimos JT, Rodolfa KT, Niakan KK, et al. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 2008; 321(5893): 1218-1221.
52. Ebert AD, Yu J, Rose FF, Jr., et al. Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 2009; 457(7227): 277-280.
53. Soldner F, Hockemeyer D, Beard C, et al. Parkinson's Disease Patient-Derived Induced Pluripotent Stem Cells Free of Viral Reprogramming Factors. Cell 2009; 136(5): 964-977.
54. Lee G, Papapetrou EP, Kim H, et al. Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature 2009; 461(7262): U402-U500.
55. Maehr R, Chen SB, Snitow M, et al. Generation of pluripotent stem cells from patients with type 1 diabetes. Proc Natl Acad Sci USA 2009; 106(37): 15768-15773.
56. Moretti A, Bellin M, Welling A, et al. Patient-specific induced pluripotent stem-cell models for long-QT syndrome. N Engl J Med 2010; 363(15): 1397-1409.
57. Carvajal-Vergara X, Sevilla A, D'Souza SL, et al. Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome. Nature 2010; 465(7299): 808-812.
58. Jin ZB, Okamoto S, Osakada F, et al. Modeling retinal degeneration using patient-specific induced pluripotent stem cells. PLoS One 2011; 6(2): e17084.
59. Ghodsizadeh A, Taei A, Totonchi M, et al. Generation of liver disease-specific induced pluripotent stem cells along with efficient differentiation to functional hepatocyte-like cells. Stem Cell Rev 2010; 6(4): 622-632.
60. Rashid ST, Corbineau S, Hannan N, et al. Modeling inherited metabolic disorders of the liver using human induced pluripotent stem cells. J Clin Invest 2010; 120(9): 3127-3136.
61. Hay DC, Zhao D, Ross A, Mandalam R, Lebkowski J, Cui W. Direct differentiation of human embryonic stem cells to hepatocyte-like cells exhibiting functional activities. Cloning Stem Cells 2007; 9(1): 51-62.
62. Zhao XY, Li W, Lv Z, et al. iPS cells produce viable mice through tetraploid complementation. Nature 2009; 461(7260): 86-90.
63. Kang L, Wang J, Zhang Y, Kou Z, Gao S. iPS cells can support full-term development of tetraploid blastocyst-complemented embryos. Cell Stem Cell 2009; 5(2): 135-138.
64. Boland MJ, Hazen JL, Nazor KL, et al. Adult mice generated from induced pluripotent stem cells. Nature 2009; 461(7260): 91-94.
65. Muller FJ, Schuldt BM, Williams R, et al. A bioinformatic assay for pluripotency in human cells. Nat Methods 2011; 8(4): 315-317.
66. Modlich U, Navarro S, Zychlinski D, et al. Insertional transformation of hematopoietic cells by self-inactivating lentiviral and gammaretroviral vectors. Mol Ther 2009; 17(11): 1919-1928.
67. Wu G, Liu N, Rittelmeyer I, et al. Generation of Healthy Mice from Gene-Corrected Disease-Specific Induced Pluripotent Stem Cells. PLoS Biol 2011; 9(7): e1001099.
68. Raya A, Rodriguez-Piza I, Guenechea G, et al. Disease-corrected haematopoietic progenitors from Fanconi anaemia induced pluripotent stem cells. Nature 2009; 460(7251): 53-59.