Derivation of high-purity definitive endoderm from human parthenogenetic stem cells using an in vitro analog of the primitive streak

Cell Transplantation

Volumn 21, Issue 1, 2012, Pages 217-234

  Turovets, Nikolay ^a   Fair, Jeffrey ^b   West, Richard ^c   Ostrowska, Alina ^a   Semechkin, Ruslan ^a   Janus, Jeffrey ^a   Cui, Li ^d   Agapov, Vladimir ^a   Turovets, Irina ^a   Semechkin, Andrey ^a   Csete, Marie ^d   Agapova, Larissa ^a  

^a INTERNATIONAL STEM CELL CORPORATION   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

^c West Labs Scientific   (United States)

^d Organovo   (United States)

Author keywords

Definitive endoderm (DE); Differentiation; Extracellular matrix (ECM); Hepatocytes; Human embryonic stem cells (hESCs); Human parthenogenetic stem cells (hpSCs)

Indexed keywords

CYTOCHROME P450; INDOCYANINE GREEN; OCTAMER TRANSCRIPTION FACTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL STRUCTURE; CONFORMATIONAL TRANSITION; EMBRYO; EMBRYO DEVELOPMENT; ENDODERM; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN PARTHENOGENETIC STEM CELL; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; LIVER CELL; MOUSE; NONHUMAN; PARTHENOGENESIS; PRIMITIVE STREAK; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL;

ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; ENDODERM; EPITHELIAL-MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEPATOCYTES; HUMANS; MICE; OCTAMER TRANSCRIPTION FACTOR-3; PARTHENOGENESIS; PLURIPOTENT STEM CELLS; PRIMITIVE STREAK;

MUS;

EID: 84858141898     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368911X582723     Document Type: Article

References (60)

1. Baharvand, H.; Hashemi, S. M.; Kazemi Ashtiani, S.; Farrokhi, A. Differentiation of human embryonic stem cells into hepatocytes in 2D and 3D culture systems in vitro. Int. J. Dev. Biol. 50:645-652; 2006.
2. Barrallo-Gimeno, A.; Nieto, M. A. The Snail genes as inducers of cell movement and survival: Implications in development and cancer. Development 132:3151-3161; 2005.
3. Basma, H.; Soto-Gutierrez, A.; Yannam, G. R.; Liu, L.; Ito, R.; Yamamoto, T.; Ellis, E.; Carson, S. D.; Sato, S.; Chen, Y.; Muirhead, D.; Navarro-Alvarez, N.; Wong, R. J.; Roy-Chowdhury, J.; Platt, J. L.; Mercer, D. F.; Miller, J. D.; Strom, S. C.; Kobayashi, N.; Fox, I. J. Differentiation and transplantation of human embryonic stem cell-derived hepatocytes. Gastroenterology 136:990-999; 2009.
4. Bonora-Centelles, A.; Jover, R.; Mirabet, V.; Lahoz, A.; Carbonell, F.; Castell, J. V.; Gomez-Lechon, M. J. Sequential hepatogenic transdifferentiation of adipose tissuederived stem cells: Relevance of different extracellular signaling molecules, transcription factors involved, and expression of new key marker genes. Cell Transplant. 18: 1319-1340; 2009.
5. Brolen, G.; Sivertsson, L.; Bjorquist, P.; Eriksson, G.; Ek, M.; Semb, H.; Johansson, I.; Andersson, T. B.; Ingelman-Sundberg, M.; Heins, N. Hepatocyte-like cells derived from human embryonic stem cells specifically via definitive endoderm and a progenitor stage. J. Biotechnol. 145: 284-294; 2010.
6. Campbell, A.; Wicha, M. S.; Long, M. Extracellular matrix promotes the growth and differentiation of murine hematopoietic cells in vitro. J. Clin. Invest. 75:2085-2090; 1985.
7. Chea, H. K.; Wright, C. V.; Swalla, B. J. Nodal signaling and the evolution of deuterostome gastrulation. Dev. Dyn. 234:269-278; 2005.
8. Chen, S. S.; Fitzgerald, W.; Zimmerberg, J.; Kleinman, H. K.; Margolis, L. Cell-cell and cell-extracellular matrix interactions regulate embryonic stem cell differentiation. Stem Cells 25:553-561; 2007.
9. Chen, Y.; Soto-Gutierrez, A.; Navarro-Alvarez, N.; Rivas-Carrillo, J. D.; Yamatsuji, T.; Shirakawa, Y.; Tanaka, N.; Basma, H.; Fox, I. J.; Kobayashi, N. Instant hepatic differentiation of human embryonic stem cells using activin A and a deleted variant of HGF. Cell Transplant. 15:865-871; 2006.
10. Chen, Z.; Liu, Z.; Huang, J.; Amano, T.; Li, C.; Cao, S.; Wu, C.; Liu, B.; Zhou, L.; Carter, M. G.; Keefe, D. L.; Yang, X.; Liu, L. Birth of parthenote mice directly from parthenogenetic embryonic stem cells. Stem Cells 27: 2136-2145; 2009.
11. D'Amour, K. A.; Agulnick, A. D.; Eliazer, S.; Kelly, O. G.; Kroon, E.; Baetge, E. E. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat. Biotechnol. 23:1534-1541; 2005.
12. D'Amour, K. A.; Bang, A. G.; Eliazer, S.; Kelly, O. G.; Agulnick, A. D.; Smart, N. G.; Moorman, M. A.; Kroon, E.; Carpenter, M. K.; Baetge, E. E. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat. Biotechnol. 24:1392-1401; 2006.
13. Eakin, G. S.; Behringer, R. R. Gastrulation in other mammals and humans. In: Stern, C. D., ed. Gastrulation. From cells to embryo. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2004:275-287.
14. Evans, N. D.; Minelli, C.; Gentleman, E.; LaPointe, V.; Patankar, S. N.; Kallivretaki, M.; Chen, X.; Roberts, C. J.; Stevens, M. M. Substrate stiffness affects early differentiation events in embryonic stem cells. Eur. Cell. Mater. 18: 1-13; 2009.
15. Fischbach, C.; Kong, H. J.; Hsiong, S. X.; Evangelista, M. B.; Yuen, W.; Mooney, D. J. Cancer cell angiogenic capability is regulated by 3D culture and integrin engagement. Proc. Natl. Acad. Sci. USA 106:399-404; 2009.
16. Flaim, C. J.; Chien, S.; Bhatia, S. N. An extracellular matrix microarray for probing cellular differentiation. Nat. Methods 2:119-125; 2005.
17. Harness, J. V.; Turovets, N. A.; Seiler, M. J.; Nistor, G.; Altun, G.; Agapova, L. S.; Ferguson, D.; Laurent, L. C.; Loring, J. F.; Keirstead, H. S. Equivalence of conventionally-derived and parthenote-derived human embryonic stem cells. PLoS One 6(1):e14499; 2011.
18. Hay, D. C.; Fletcher, J.; Payne, C.; Terrace, J. D.; Gallagher, R. C.; Snoeys, J.; Black, J. R.; Wojtacha, D.; Samuel, K.; Hannoun, Z.; Pryde, A.; Filippi, C.; Currie, I. S.; Forbes, S. J.; Ross, J. A.; Newsome, P. N.; Iredale, J. P. Highly efficient differentiation of hESC to functional hepatic endoderm requires ActivinA and Wnt3a signaling. Proc. Natl. Acad. Sci. USA 105:12301-12306; 2008.
19. Hay, E. D. The mesenchymal cell, its role in the embryo, and the remarkable signaling mechanisms that create it. Dev. Dyn. 233:706-720; 2005.
20. Iwamuro, M.; Komaki, T.; Kubota, Y.; Seita, M.; Kawamoto, H.; Yuasa, T.; Shahid, J. M.; Hassan, R. A.; Hassan, W. A.; Nakaji, S.; Nishikawa, Y.; Kondo, E.; Yamamoto, K.; Kobayashi, N. Comparative analysis of endoderm formation efficiency between mouse ES cells and iPS cells. Cell Transplant. 19:831-839; 2010.
21. Jung, J.; Zheng, M.; Goldfarb, M.; Zaret, K. S. Initiation of mammalian liver development from endoderm by fibroblast growth factors. Science 284:1998-2003; 1999.
22. Kihara, T.; Hirose, M.; Oshima, A.; Ohgushi, H. Exogenous type I collagen facilitates osteogenic differentiation and acts as a substrate for mineralization of rat marrow mesenchymal stem cells in vitro. Biochem. Biophys. Res. Commun. 341:1029-1035; 2006.
23. Kroon, E.; Martinson, L. A.; Kadoya, K.; Bang, A. G.; Kelly, O. G.; Eliazer, S.; Young, H.; Richardson, M.; Smart, N. G.; Cunningham, J.; Agulnick, A. D.; D'Amour, K. A.; Carpenter, M. K.; Baetge, E. E. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat. Biotechnol. 26:443-452; 2008.
24. Lee, K. D.; Kuo, T. K.; Whang-Peng, J.; Chung, Y. F.; Lin, C. T.; Chou, S. H.; Chen, J. R.; Chen, Y. P.; Lee, O. K. In vitro hepatic differentiation of human mesenchymal stem cells. Hepatology 40:1275-1284; 2004.
25. Lin, G.; Ou Yang, Q.; Zhou, X.; Gu, Y.; Yuan, D.; Li, W.; Liu, G.; Liu, T.; Lu, G. A highly homozygous and parthenogenetic human embryonic stem cell line derived from a one-pronuclear oocyte following in vitro fertilization procedure. Cell Res. 17:999-1007; 2007.
26. Liu, P.; Wakamiya, M.; Shea, M. J.; Albrecht, U.; Behringer, R. R.; Bradley, A. Requirement for Wnt3 in vertebrate axis formation. Nat. Genet. 22:361-365; 1999.
27. Lu, C. C.; Brennan, J.; Robertson, E. J. From fertilization to gastrulation: Axis formation in the mouse embryo. Curr. Opin. Genet. Dev. 11:384-392; 2001.
28. Mai, Q.; Yu, Y.; Li, T.; Wang, L.; Chen, M. J.; Huang, S. Z.; Zhou, C.; Zhou, Q. Derivation of human embryonic stem cell lines from parthenogenetic blastocysts. Cell Res. 17:1008-1019; 2007.
29. Martin, A. C.; Kaschube, M.; Wieschaus, E. F. Pulsed actin-myosin network contractions drive apical constriction. Nature 457:495-499; 2009.
30. McLean, A. B.; D'Amour, K. A.; Jones, K. L.; Krishnamoorthy, M.; Kulik, M. J.; Reynolds, D. M.; Sheppard, A. M.; Liu, H.; Xu, Y.; Baetge, E. E.; Dalton, S. Activin a efficiently specifies definitive endoderm from human embryonic stem cells only when phosphatidylinositol 3-kinase signaling is suppressed. Stem Cells 25:29-38; 2007.
31. Moreno-Bueno, G.; Portillo, F.; Cano, A. Transcriptional regulation of cell polarity in EMT and cancer. Oncogene 27:6958-6969; 2008.
32. Nakaya, Y.; Sukowati, E. W.; Wu, Y.; Sheng, G. RhoA and microtubule dynamics control cell-basement membrane interaction in EMT during gastrulation. Nat. Cell Biol. 10:765-775; 2008.
33. Naugle, J. E.; Olson, E. R.; Zhang, X.; Mase, S. E.; Pilati, C. F.; Maron, M. B.; Folkesson, H. G.; Horne, W. I.; Doane, K. J.; Meszaros, J. G. Type VI collagen induces cardiac myofibroblast differentiation: Implications for postinfarction remodeling. Am. J. Physiol. Heart Circ. Physiol. 290:H323-H330; 2006.
34. Ostrowska, A.; Bode, D.; Pruss, J.; Bilir, B.; Smith, G.; Zeisloft, S. Investigation of functional and morphological integrity of freshly isolated and cryopreserved human hepatocytes. Cell Tissue Bank. 1:55-68; 2000.
35. Ostrowska, A.; Karrer, F. M.; Bilir, B. Histological identification of purified and cryopreserved allogeneic hepatocytes following transplantation in a murine model without immunosuppression. Transpl. Int. 12:188-194; 1999.
36. Park, I. H.; Zhao, R.; West, J. A.; Yabuuchi, A.; Huo, H.; Ince, T. A.; Lerou, P. H.; Lensch, M. W.; Daley, G. Q. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451:141-146; 2008.
37. Peinado, H.; Olmeda, D.; Cano, A. Snail, Zeb and bHLH factors in tumor progression: An alliance against the epithelial phenotype? Nat. Rev. Cancer 7:415-428; 2007.
38. Popperl, H.; Schmidt, C.; Wilson, V.; Hume, C. R.; Dodd, J.; Krumlauf, R.; Beddington, R. S. Misexpression of Cwnt8C in the mouse induces an ectopic embryonic axis and causes a truncation of the anterior neuroectoderm. Development 124:2997-3005; 1997.
39. Reubinoff, B. E.; Pera, M. F.; Fong, C. Y.; Trounson, A.; Bongso, A. Embryonic stem cell lines from human blastocysts: Somatic differentiation in vitro. Nat. Biotechnol. 18: 399-404; 2000.
40. Revazova, E. S.; Turovets, N. A.; Kochetkova, O. D.; Agapova, L. S.; Sebastian, J. L.; Pryzhkova, M. V.; Smolnikova, V. I.; Kuzmichev, L. N.; Janus, J. D. HLA homozygous stem cell lines derived from human parthenogenetic blastocysts. Cloning Stem Cells 10:11-24; 2008.
41. Revazova, E. S.; Turovets, N. A.; Kochetkova, O. D.; Kindarova, L. B.; Kuzmichev, L. N.; Janus, J. D.; Pryzhkova, M. V. Patient-specific stem cell lines derived from human parthenogenetic blastocysts. Cloning Stem Cells 9:432-449; 2007.
42. Robb, L.; Tam, P. P. Gastrula organiser and embryonic patterning in the mouse. Semin. Cell Dev. Biol. 15:543-554; 2004.
43. Sanchez-Pernaute, R.; Lee, H.; Patterson, M.; Reske-Nielsen, C.; Yoshizaki, T.; Sonntag, K. C.; Studer, L.; Isacson, O. Parthenogenetic dopamine neurons from primate embryonic stem cells restore function in experimental Parkinson's disease. Brain 131:2127-2139; 2008.
44. Si-Tayeb, K.; Noto, F. K.; Nagaoka, M.; Li, J.; Battle, M. A.; Duris, C.; North, P. E.; Dalton, S.; Duncan, S. A. Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 51:297-305; 2010.
45. Skromne, I.; Stern, C. D. Interactions between Wnt and Vg1 signalling pathways initiate primitive streak formation in the chick embryo. Development 128:2915-2927; 2001.
46. Souza, B. S.; Nogueira, R. C.; de Oliveira, S. A.; de Freitas, L. A.; Lyra, L. G.; Ribeiro dos Santos, R.; Lyra, A. C.; Soares, M. B. Current status of stem cell therapy for liver diseases. Cell Transplant. 18:1261-1279; 2009.
47. Sullivan, G. J.; Hay, D. C.; Park, I. H.; Fletcher, J.; Hannoun, Z.; Payne, C. M.; Dalgetty, D.; Black, J. R.; Ross, J. A.; Samuel, K.; Wang, G.; Daley, G. Q.; Lee, J. H.; Church, G. M.; Forbes, S. J.; Iredale, J. P.; Wilmut, I. Generation of functional human hepatic endoderm from human induced pluripotent stem cells. Hepatology 51: 329-335; 2010.
48. Suzuki, A.; Iwama, A.; Miyashita, H.; Nakauchi, H.; Taniguchi, H. Role for growth factors and extracellular matrix in controlling differentiation of prospectively isolated hepatic stem cells. Development 130:2513-2524; 2003.
49. Takahashi, K.; Tanabe, K.; Ohnuki, M.; Narita, M.; Ichisaka, T.; Tomoda, K.; Yamanaka, S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861-872; 2007.
50. Tam, P. P. L.; Gad, J. M. Gastrulation in the mouse embryo. In: Stern, C. D., ed. Gastrulation. From cells to embryo. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2004:233-262.
51. Taylor, C. J.; Bolton, E. M.; Pocock, S.; Sharples, L. D.; Pedersen, R. A.; Bradley, J. A. Banking on human embryonic stem cells: Estimating the number of donor cell lines needed for HLA matching. Lancet 366:2019-2025; 2005.
52. Teratani, T.; Yamamoto, H.; Aoyagi, K.; Sasaki, H.; Asari, A.; Quinn, G.; Sasaki, H.; Terada, M.; Ochiya, T. Direct hepatic fate specification from mouse embryonic stem cells. Hepatology 41:836-846; 2005.
53. Thomson, J. A.; Itskovitz-Eldor, J.; Shapiro, S. S.; Waknitz, M. A.; Swiergiel, J. J.; Marshall, V. S.; Jones, J. M. Embryonic stem cell lines derived from human blastocysts. Science 282:1145-1147; 1998.
54. Touboul, T.; Hannan, N. R.; Corbineau, S.; Martinez, A.; Martinet, C.; Branchereau, S.; Mainot, S.; Strick-Marchand, H.; Pedersen, R.; Di Santo, J.; Weber, A.; Vallier, L. Generation of functional hepatocytes from human embryonic stem cells under chemically defined conditions that recapitulate liver development. Hepatology 51:1754-1765; 2010.
55. Turovets, N.; D'Amour, K. A.; Agapov, V.; Turovets, I.; Kochetkova, O.; Janus, J.; Semechkin, A.; Moorman, M. A.; Agapova, L. Human parthenogenetic stem cells produce enriched populations of definitive endoderm cells after trichostatin A pretreatment. Differentiation 81(5): 292-298; 2011.
56. Viebahn, C. Gastrulation in the rabbit. In: Stern, C. D., ed. Gastrulation. From cells to embryo. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2004:263-274.
57. Wilkinson, D. G.; Bhatt, S.; Herrmann, B. G. Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 343:657-659; 1990.
58. Yamada, T.; Yoshikawa, M.; Kanda, S.; Kato, Y.; Nakajima, Y.; Ishizaka, S.; Tsunoda, Y. In vitro differentiation of embryonic stem cells into hepatocyte-like cells identified by cellular uptake of indocyanine green. Stem Cells 20: 146-154; 2002.
59. Yu, J.; Hu, K.; Smuga-Otto, K.; Tian, S.; Stewart, R.; Slukvin, I. I.; Thomson, J. A. Human induced pluripotent stem cells free of vector and transgene sequences. Science 318:1917-1920; 2007.
60. Zaret, K. S. Regulatory phases of early liver development: Paradigms of organogenesis. Nat. Rev. Genet. 3:499-512; 2002.