Recombinant Laminins Drive the Differentiation and Self-Organization of hESC-Derived Hepatocytes

Stem Cell Reports

Volumn 5, Issue 6, 2015, Pages 1250-1262

  Cameron, Kate ^a   Tan, Rosanne ^a   Schmidt Heck, Wolfgang ^b   Campos, Gisela ^c   Lyall, Marcus J ^a   Wang, Yu ^a   Lucendo Villarin, Baltasar ^a   Szkolnicka, Dagmara ^a   Bates, Nicola ^d   Kimber, Susan J ^d   Hengstler, Jan G ^c   Godoy, Patricio ^c   Forbes, Stuart J ^a   Hay, David C ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b HANS KNÖLL INSTITUTE   (Germany)

^c TU DORTMUND UNIVERSITY   (Germany)

^d Faculty of Life Sciences   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LAMININ; RECOMBINANT PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; FIBROBLAST; GENE REGULATORY NETWORK; HUMAN; HUMAN CELL; LIVER CELL; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SELF CONCEPT; STEM CELL; CELL CULTURE TECHNIQUE; CELL LINE; CYTOLOGY; HUMAN GENOME; METABOLISM;

CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; EMBRYONIC STEM CELLS; GENE REGULATORY NETWORKS; GENOME, HUMAN; HEPATOCYTES; HUMANS; LAMININ; RECOMBINANT PROTEINS;

EID: 84949534577     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2015.10.016     Document Type: Article

References (55)

1. H. Basma, A. Soto-Gutiérrez, G.R. Yannam, L. Liu, R. Ito, T. Yamamoto, E. Ellis, S.D. Carson, S. Sato, Y. Chen, and et al. Differentiation and transplantation of human embryonic stem cell-derived hepatocytes Gastroenterology 136 2009 990 999
2. P. Cahan, H. Li, S.A. Morris, E. Lummertz da Rocha, G.Q. Daley, and J.J. Collins CellNet: network biology applied to stem cell engineering Cell 158 2014 903 915
3. J. Cai, Y. Zhao, Y. Liu, F. Ye, Z. Song, H. Qin, S. Meng, Y. Chen, R. Zhou, X. Song, and et al. Directed differentiation of human embryonic stem cells into functional hepatic cells Hepatology 45 2007 1229 1239
4. K. Cameron, B.L. Villarin, D. Szkolnicka, and D.C. Hay Serum-free directed differentiation of human embryonic stem cells to hepatocytes M. Vinken, V. Rogiers, Protocols in In Vitro Hepatocyte Research 2015 Humana Press 105 111
5. R. Carlsson, E. Engvall, A. Freeman, and E. Ruoslahti Laminin and fibronectin in cell adhesion: enhanced adhesion of cells from regenerating liver to laminin Proc. Natl. Acad. Sci. USA 78 1981 2403 2406
6. A. Carpentier, A. Tesfaye, V. Chu, I. Nimgaonkar, F. Zhang, S.B. Lee, S.S. Thorgeirsson, S.M. Feinstone, and T.J. Liang Engrafted human stem cell-derived hepatocytes establish an infectious HCV murine model J. Clin. Invest. 124 2014 4953 4964
7. A. Domogatskaya, S. Rodin, and K. Tryggvason Functional diversity of laminins Annu. Rev. Cell Dev. Biol. 28 2012 523 553
8. Y. Duan, A. Catana, Y. Meng, N. Yamamoto, S. He, S. Gupta, S.S. Gambhir, and M.A. Zern Differentiation and enrichment of hepatocyte-like cells from human embryonic stem cells in vitro and in vivo Stem Cells 25 2007 3058 3068
9. S.J. Forbes, S. Gupta, and A. Dhawan Cell therapy for liver disease: From liver transplantation to cell factory J. Hepatol. 62 1, Suppl 2015 S157 S169
10. J. Gadi, S.H. Jung, M.J. Lee, A. Jami, K. Ruthala, K.M. Kim, N.H. Cho, H.S. Jung, C.H. Kim, and S.K. Lim The transcription factor protein Sox11 enhances early osteoblast differentiation by facilitating proliferation and the survival of mesenchymal and osteoblast progenitors J. Biol. Chem. 288 2013 25400 25413
11. P. Godoy, J.G. Hengstler, I. Ilkavets, C. Meyer, A. Bachmann, A. Müller, G. Tuschl, S.O. Mueller, and S. Dooley Extracellular matrix modulates sensitivity of hepatocytes to fibroblastoid dedifferentiation and transforming growth factor beta-induced apoptosis Hepatology 49 2009 2031 2043
12. P. Godoy, S. Lakkapamu, M. Schug, A. Bauer, J.D. Stewart, E. Bedawi, S. Hammad, J. Amin, R. Marchan, W. Schormann, and et al. Dexamethasone-dependent versus -independent markers of epithelial to mesenchymal transition in primary hepatocytes Biol. Chem. 391 2010 73 83
13. P. Godoy, W. Schmidt-Heck, K. Natarajan, B. Lucendo-Villarin, D. Szkolnicka, A. Asplund, P. Björquist, A. Widera, R. Stöber, G. Campos, and et al. Gene networks and transcription factor motifs defining the differentiation of stem cells into hepatocyte-like cells J. Hepatol. 63 2015 934 942
14. D.C. Hay, D. Zhao, A. Ross, R. Mandalam, J. Lebkowski, and W. Cui Direct differentiation of human embryonic stem cells to hepatocyte-like cells exhibiting functional activities Cloning Stem Cells 9 2007 51 62
15. D.C. Hay, J. Fletcher, C. Payne, J.D. Terrace, R.C. Gallagher, J. Snoeys, J.R. Black, D. Wojtacha, K. Samuel, Z. Hannoun, and et al. Highly efficient differentiation of hESCs to functional hepatic endoderm requires ActivinA and Wnt3a signaling Proc. Natl. Acad. Sci. USA 105 2008 12301 12306
16. D.C. Hay, S. Pernagallo, J.J. Diaz-Mochon, C.N. Medine, S. Greenhough, Z. Hannoun, J. Schrader, J.R. Black, J. Fletcher, D. Dalgetty, and et al. Unbiased screening of polymer libraries to define novel substrates for functional hepatocytes with inducible drug metabolism Stem Cell Res. (Amst.) 6 2011 92 102
17. D. Holl, P. Kuckenberg, T. Woynecki, A. Egert, A. Becker, S. Huss, D. Stabenow, A. Zimmer, P. Knolle, R. Tolba, and et al. Transgenic overexpression of Tcfap2c/AP-2gamma results in liver failure and intestinal dysplasia PLoS ONE 6 2011 e22034
18. G. Holmgren, A.K. Sjögren, I. Barragan, A. Sabirsh, P. Sartipy, J. Synnergren, P. Björquist, M. Ingelman-Sundberg, T.B. Andersson, and J. Edsbagge Long-term chronic toxicity testing using human pluripotent stem cell-derived hepatocytes Drug Metab. Dispos. 42 2014 1401 1406
19. S. Jitraruch, A. Dhawan, R.D. Hughes, C. Filippi, D. Soong, C. Philippeos, S.C. Lehec, N.D. Heaton, M.S. Longhi, and R.R. Mitry Alginate microencapsulated hepatocytes optimised for transplantation in acute liver failure PLoS ONE 9 2014 e113609
20. S.J. Karpen, and F.J. Suchy Structural and functional development of the liver F.J. Suchy, R.J. Sokol, W.F. Balistreri, Liver Disease in Children 2001 Lippincott Williams & Wilkins
21. N. Lavon, O. Yanuka, and N. Benvenisty Differentiation and isolation of hepatic-like cells from human embryonic stem cells Differentiation 72 2004 230 238
22. S.Y. Lee, G.R. Lee, D.H. Woo, N.H. Park, H.J. Cha, Y.H. Moon, and I.S. Han Depletion of Aurora A leads to upregulation of FoxO1 to induce cell cycle arrest in hepatocellular carcinoma cells Cell Cycle 12 2013 67 75
23. S. Lorenzini, T.G. Bird, L. Boulter, C. Bellamy, K. Samuel, R. Aucott, E. Clayton, P. Andreone, M. Bernardi, M. Golding, and et al. Characterisation of a stereotypical cellular and extracellular adult liver progenitor cell niche in rodents and diseased human liver Gut 59 2010 645 654
24. A. Martinez-Hernandez, and P.S. Amenta The hepatic extracellular matrix. I. Components and distribution in normal liver Virchows Arch. A Pathol. Anat. Histopathol. 423 1993 1 11
25. A. Martinez-Hernandez, and P.S. Amenta The hepatic extracellular matrix. II. Ontogenesis, regeneration and cirrhosis Virchows Arch. A Pathol. Anat. Histopathol. 423 1993 77 84
26. A. Martinez-Hernandez, and P.S. Amenta The extracellular matrix in hepatic regeneration FASEB J. 9 1995 1401 1410
27. C.N. Medine, B. Lucendo-Villarin, C. Storck, F. Wang, D. Szkolnicka, F. Khan, S. Pernagallo, J.R. Black, H.M. Marriage, J.A. Ross, and et al. Developing high-fidelity hepatotoxicity models from pluripotent stem cells Stem Cells Transl. Med. 2 2013 505 509
28. J.H. Miner, C. Li, J.L. Mudd, G. Go, and A.E. Sutherland Compositional and structural requirements for laminin and basement membranes during mouse embryo implantation and gastrulation Development 131 2004 2247 2256
29. S.A. Morris, P. Cahan, H. Li, A.M. Zhao, A.K. San Roman, R.A. Shivdasani, J.J. Collins, and G.Q. Daley Dissecting engineered cell types and enhancing cell fate conversion via CellNet Cell 158 2014 889 902
30. S. Ng, R.E. Schwartz, S. March, A. Galstian, N. Gural, J. Shan, M. Prabhu, M.M. Mota, and S.N. Bhatia Human iPSC-derived hepatocyte-like cells support Plasmodium liver-stage infection in vitro Stem Cell Reports 4 2015 348 359
31. C.M. Payne, K. Samuel, A. Pryde, J. King, D. Brownstein, J. Schrader, C.N. Medine, S.J. Forbes, J.P. Iredale, P.N. Newsome, and D.C. Hay Persistence of functional hepatocyte-like cells in immune-compromised mice Liver Int. 31 2011 254 262
32. S.T. Rashid, S. Corbineau, N. Hannan, S.J. Marciniak, E. Miranda, G. Alexander, I. Huang-Doran, J. Griffin, L. Ahrlund-Richter, J. Skepper, and et al. Modeling inherited metabolic disorders of the liver using human induced pluripotent stem cells J. Clin. Invest. 120 2010 3127 3136
33. S. Rodin, A. Domogatskaya, S. Ström, E.M. Hansson, K.R. Chien, J. Inzunza, O. Hovatta, and K. Tryggvason Long-term self-renewal of human pluripotent stem cells on human recombinant laminin-511 Nat. Biotechnol. 28 2010 611 615
34. P. Roelandt, S. Obeid, J. Paeshuyse, J. Vanhove, A. Van Lommel, Y. Nahmias, F. Nevens, J. Neyts, and C.M. Verfaillie Human pluripotent stem cell-derived hepatocytes support complete replication of hepatitis C virus J. Hepatol. 57 2012 246 251
35. R.E. Schwartz, H.E. Fleming, S.R. Khetani, and S.N. Bhatia Pluripotent stem cell-derived hepatocyte-like cells Biotechnol. Adv. 32 2014 504 513
36. K. Si-Tayeb, F.K. Noto, M. Nagaoka, J. Li, M.A. Battle, C. Duris, P.E. North, S. Dalton, and S.A. Duncan Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells Hepatology 51 2010 297 305
37. R. Siller, S. Greenhough, E. Naumovska, and G.J. Sullivan Small-molecule-driven hepatocyte differentiation of human pluripotent stem cells Stem Cell Reports 4 2015 939 952
38. H. Sirma, M. Kumar, J.K. Meena, B. Witt, J.M. Weise, A. Lechel, S. Ande, V. Sakk, C. Guguen-Guillouzo, L. Zender, and et al. The promoter of human telomerase reverse transcriptase is activated during liver regeneration and hepatocyte proliferation Gastroenterology 141 2011 326-337, 337.e1-337.e3
39. S.C. Stamatoglou, C. Enrich, M.M. Manson, and R.C. Hughes Temporal changes in the expression and distribution of adhesion molecules during liver development and regeneration J. Cell Biol. 116 1992 1507 1515
40. G.J. Sullivan, D.C. Hay, I.H. Park, J. Fletcher, Z. Hannoun, C.M. Payne, D. Dalgetty, J.R. Black, J.A. Ross, K. Samuel, and et al. Generation of functional human hepatic endoderm from human induced pluripotent stem cells Hepatology 51 2010 329 335
41. P. Sun, X. Zhou, S.L. Farnworth, A.H. Patel, and D.C. Hay Modeling human liver biology using stem cell-derived hepatocytes Int. J. Mol. Sci. 14 2013 22011 22021
42. D. Szkolnicka, W. Zhou, B. Lucendo-Villarin, and D.C. Hay Pluripotent stem cell-derived hepatocytes: potential and challenges in pharmacology Annu. Rev. Pharmacol. Toxicol. 53 2013 147 159
43. D. Szkolnicka, S.L. Farnworth, B. Lucendo-Villarin, and D.C. Hay Deriving functional hepatocytes from pluripotent stem cells Curr. Protoc. Stem Cell Biol. 30 2014 1 12, 12
44. D. Szkolnicka, S.L. Farnworth, B. Lucendo-Villarin, C. Storck, W. Zhou, J.P. Iredale, O. Flint, and D.C. Hay Accurate prediction of drug-induced liver injury using stem cell-derived populations Stem Cells Transl. Med. 3 2014 141 148
45. K. Takayama, Y. Nagamoto, N. Mimura, K. Tashiro, F. Sakurai, M. Tachibana, T. Hayakawa, K. Kawabata, and H. Mizuguchi Long-term self-renewal of human ES/iPS-derived hepatoblast-like cells on human laminin 111-coated dishes Stem Cell Reports 1 2013 322 335
46. K. Takayama, K. Kawabata, Y. Nagamoto, K. Kishimoto, K. Tashiro, F. Sakurai, M. Tachibana, K. Kanda, T. Hayakawa, M.K. Furue, and H. Mizuguchi 3D spheroid culture of hESC/hiPSC-derived hepatocyte-like cells for drug toxicity testing Biomaterials 34 2013 1781 1789
47. N. Tanimizu, Y. Kikkawa, T. Mitaka, and A. Miyajima α1- and α5-containing laminins regulate the development of bile ducts via β1 integrin signals J. Biol. Chem. 287 2012 28586 28597
48. H. Taylor-Weiner, J.E. Schwarzbauer, and A.J. Engler Defined extracellular matrix components are necessary for definitive endoderm induction Stem Cells 31 2013 2084 2094
49. T. Touboul, N.R. Hannan, S. Corbineau, A. Martinez, C. Martinet, S. Branchereau, S. Mainot, H. Strick-Marchand, R. Pedersen, J. Di Santo, and et al. Generation of functional hepatocytes from human embryonic stem cells under chemically defined conditions that recapitulate liver development Hepatology 51 2010 1754 1765
50. A. Treyer, and A. Müsch Hepatocyte polarity Compr. Physiol. 3 2013 243 287
51. B.L. Villarin, K. Cameron, D. Szkolnicka, H. Rashidi, N. Bates, S.J. Kimber, O. Flint, S.J. Forbes, J.P. Iredale, M. Bradley, and D.C. Hay Polymer Supported Directed Differentiation Reveals a Unique Gene Signature Predicting Stable Hepatocyte Performance Adv. Healthc. Mater. 4 2015 1820 1825
52. B.R. Ware, D.R. Berger, and S.R. Khetani Prediction of drug-induced liver injury in micropatterned co-cultures containing iPSC-derived human hepatocytes Toxicol. Sci. 145 2015 252 262 10.1093/toxsci/kfv048
53. X. Wu, J.M. Robotham, E. Lee, S. Dalton, N.M. Kneteman, D.M. Gilbert, and H. Tang Productive hepatitis C virus infection of stem cell-derived hepatocytes reveals a critical transition to viral permissiveness during differentiation PLoS Pathog. 8 2012 e1002617
54. W. Zhou, Z. Hannoun, E. Jaffray, C.N. Medine, J.R. Black, S. Greenhough, L. Zhu, J.A. Ross, S. Forbes, I. Wilmut, and et al. SUMOylation of HNF4α regulates protein stability and hepatocyte function J. Cell Sci. 125 2012 3630 3635
55. X. Zhou, P. Sun, B. Lucendo-Villarin, A.G.N. Angus, D. Szkolnicka, K. Cameron, S.L. Farnworth, A.H. Patel, and D.C. Hay Modulating innate immunity improves hepatitis C virus infection and replication in stem cell-derived hepatocytes Stem Cell Reports 3 2014 204 214