Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2015, Article ID 647437, 10 pages
http://dx.doi.org/10.1155/2015/647437
Research Article

Neural Progenitor Cells Derived from Human Embryonic Stem Cells as an Origin of Dopaminergic Neurons

1School of Biotechnology, Institute of Agricultural Technology, Suranaree University of Technology, Nakhon Ratchasima 30000, Thailand
2Institute of Biomedicine, Department of Physiology, University of Helsinki, 00290 Helsinki, Finland
3Children’s Hospital, Helsinki University Central Hospital, 00290 Helsinki, Finland
4Institute of Reproductive and Developmental Biology, Department of Surgery and Cancer, Faculty of Medicine, Imperial College London, Hammersmith Campus, London W12 0NN, UK

Received 27 January 2015; Revised 11 April 2015; Accepted 14 April 2015

Academic Editor: Boon Chin Heng

Copyright © 2015 Parinya Noisa et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. A. Thomson, J. Itskovitz-Eldor, S. S. Shapiro et al., “Embryonic stem cell lines derived from human blastocysts,” Science, vol. 282, no. 5391, pp. 1145–1147, 1998. View at Publisher · View at Google Scholar · View at Scopus
  2. D. C. Hay, D. Zhao, J. Fletcher et al., “Efficient differentiation of hepatocytes from human embryonic stem cells exhibiting markers recapitulating liver development in vivo,” Stem Cells, vol. 26, no. 4, pp. 894–902, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. O. Lindvall and A. Björklund, “Cell therapy in Parkinson's disease,” NeuroRx, vol. 1, no. 4, pp. 382–393, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. T. Ben-Hur, M. Idelson, H. Khaner et al., “Transplantation of human embryonic stem cell-derived neural progenitors improves behavioral deficit in Parkinsonian rats,” Stem Cells, vol. 22, no. 7, pp. 1246–1255, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. L. Gerrard, L. Rodgers, and W. Cui, “Differentiation of human embryonic stem cells to neural lineages in adherent culture by blocking bone morphogenetic protein signaling,” Stem Cells, vol. 23, no. 9, pp. 1234–1241, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. S. M. Chambers, C. A. Fasano, E. P. Papapetrou, M. Tomishima, M. Sadelain, and L. Studer, “Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling,” Nature Biotechnology, vol. 27, no. 3, pp. 275–280, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Q. Wu, L. Habegger, P. Noisa et al., “Dynamic transcriptomes during neural differentiation of human embryonic stem cells revealed by short, long, and paired-end sequencing,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 11, pp. 5254–5259, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. I. Muñoz-Sanjuán and A. H. Brivanlou, “Neural induction, the default model and embryonic stem cells,” Nature Reviews Neuroscience, vol. 3, no. 4, pp. 271–280, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Hollnagel, V. Oehlmann, J. Heymer, U. Rüther, and A. Nordheim, “Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells,” The Journal of Biological Chemistry, vol. 274, no. 28, pp. 19838–19845, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. T. Takizawa, W. Ochiai, K. Nakashima, and T. Taga, “Enhanced gene activation by Notch and BMP signaling cross-talk,” Nucleic Acids Research, vol. 31, no. 19, pp. 5723–5731, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. Y. Yokota, “Id and development,” Oncogene, vol. 20, no. 58, pp. 8290–8298, 2001. View at Publisher · View at Google Scholar · View at Scopus
  12. D.-S. Kim, J. S. Lee, J. W. Leem et al., “Robust enhancement of neural differentiation from human ES and iPS cells regardless of their innate difference in differentiation propensity,” Stem Cell Reviews and Reports, vol. 6, no. 2, pp. 270–281, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Temple, “The development of neural stem cells,” Nature, vol. 414, no. 6859, pp. 112–117, 2001. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Wolpert, “Positional information and pattern formation in development,” Developmental Genetics, vol. 15, no. 6, pp. 485–490, 1994. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Sánchez-Danés, A. Consiglio, Y. Richaud et al., “Efficient generation of A9 midbrain dopaminergic neurons by lentiviral delivery of LMX1A in human embryonic stem cells and induced pluripotent stem cells,” Human Gene Therapy, vol. 23, no. 1, pp. 56–69, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Sagal, X. Zhan, J. Xu et al., “Proneural transcription factor Atoh1 drives highly efficient differentiation of human pluripotent stem cells into dopaminergic neurons,” Stem Cells Translational Medicine, vol. 3, no. 8, pp. 888–898, 2014. View at Publisher · View at Google Scholar
  17. O. Cooper, G. Hargus, M. Deleidi et al., “Differentiation of human ES and Parkinson's disease iPS cells into ventral midbrain dopaminergic neurons requires a high activity form of SHH, FGF8a and specific regionalization by retinoic acid,” Molecular and Cellular Neuroscience, vol. 45, no. 3, pp. 258–266, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. E. Andersson, J. B. Jensen, M. Parmar, F. Guillemot, and A. Björklund, “Development of the mesencephalic dopaminergic neuron system is compromised in the absence of neurogenin 2,” Development, vol. 133, no. 3, pp. 507–516, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. A. L. M. Ferri, W. Lin, Y. E. Mavromatakis et al., “Foxa1 and Foxa2 regulate multiple phases of midbrain dopaminergic neuron development in a dosage-dependent manner,” Development, vol. 134, no. 15, pp. 2761–2769, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Martinat, J.-J. Bacci, T. Leete et al., “Cooperative transcription activation by Nurr1 and Pitx3 induces embryonic stem cell maturation to the midbrain dopamine neuron phenotype,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 8, pp. 2874–2879, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Vogt, R. Traynor, and G. P. Sapkota, “The specificities of small molecule inhibitors of the TGFß and BMP pathways,” Cellular Signalling, vol. 23, no. 11, pp. 1831–1842, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Boutin, B. Schmitz, H. Cremer, and S. Diestel, “NCAM expression induces neurogenesis in vivo,” European Journal of Neuroscience, vol. 30, no. 7, pp. 1209–1218, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. F. T. Merkle and A. Alvarez-Buylla, “Neural stem cells in mammalian development,” Current Opinion in Cell Biology, vol. 18, no. 6, pp. 704–709, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Itsykson, N. Ilouz, T. Turetsky et al., “Derivation of neural precursors from human embryonic stem cells in the presence of noggin,” Molecular and Cellular Neuroscience, vol. 30, no. 1, pp. 24–36, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. S.-C. Zhang, B. Ge, and I. D. Duncan, “Tracing human oligodendroglial development in vitro,” Journal of Neuroscience Research, vol. 59, no. 3, pp. 421–429, 2000. View at Publisher · View at Google Scholar · View at Scopus
  26. V. Baladrón, M. J. Ruiz-Hidalgo, M. L. Nueda et al., “Dlk acts as a negative regulator of Notch1 activation through interactions with specific EGF-like repeats,” Experimental Cell Research, vol. 303, no. 2, pp. 343–359, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Iso, L. Kedes, and Y. Hamamori, “HES and HERP families: multiple effectors of the Notch signaling pathway,” Journal of Cellular Physiology, vol. 194, no. 3, pp. 237–255, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. K.-I. Mizutani, K. Yoon, L. Dang, A. Tokunaga, and N. Gaiano, “Differential Notch signalling distinguishes neural stem cells from intermediate progenitors,” Nature, vol. 449, no. 7160, pp. 351–355, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. X. Qian, A. A. Davis, S. K. Goderie, and S. Temple, “FGF2 concentration regulates the generation of neurons and glia from multipotent cortical stem cells,” Neuron, vol. 18, no. 1, pp. 81–93, 1997. View at Publisher · View at Google Scholar · View at Scopus
  30. R. C. Burrows, D. Wancio, P. Levitt, and L. Lillien, “Response diversity and the timing of progenitor cell maturation are regulated by developmental changes in EGFR expression in the cortex,” Neuron, vol. 19, no. 2, pp. 251–267, 1997. View at Publisher · View at Google Scholar · View at Scopus
  31. S. M. Wu, K. S. Tan, H. Chen et al., “Enhanced production of neuroprogenitors, dopaminergic neurons, and identification of target genes by overexpression of sonic hedgehog in human embryonic stem cells,” Stem Cells and Development, vol. 21, no. 5, pp. 729–741, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. K. Yamauchi, S. Mizushima, A. Tamada, N. Yamamoto, S. Takashima, and F. Murakami, “FGF8 signaling regulates growth of midbrain dopaminergic axons by inducing semaphorin 3F,” Journal of Neuroscience, vol. 29, no. 13, pp. 4044–4055, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. S.-H. Lee, N. Lumelsky, L. Studer, J. M. Auerbach, and R. D. McKay, “Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells,” Nature Biotechnology, vol. 18, no. 6, pp. 675–679, 2000. View at Publisher · View at Google Scholar · View at Scopus
  34. B. E. Reubinoff, P. Itsykson, T. Turetsky et al., “Neural progenitors from human embryonic stem cells,” Nature Biotechnology, vol. 19, no. 12, pp. 1134–1140, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. M. A. Cohen, P. Itsykson, and B. E. Reubinoff, “Unit 23.7 neural differentiation of human ES cells,” in Current Protocols in Cell Biology, chapter 23, 2007. View at Publisher · View at Google Scholar
  36. M. Götz and Y.-A. Barde, “Radial glial cells defined and major intermediates between embryonic stem cells and CNS neurons,” Neuron, vol. 46, no. 3, pp. 369–372, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Bibel, J. Richter, K. Schrenk et al., “Differentiation of mouse embryonic stem cells into a defined neuronal lineage,” Nature Neuroscience, vol. 7, no. 9, pp. 1003–1009, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Conti, S. M. Pollard, T. Gorba et al., “Niche-independent symmetrical self-renewal of a mammalian tissue stem cell,” PLoS Biology, vol. 3, no. 9, p. e283, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. A. M. Arias, V. Zecchini, and K. Brennan, “CSL-independent Notch signalling: a checkpoint in cell fate decisions during development?” Current Opinion in Genetics and Development, vol. 12, no. 5, pp. 524–533, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. B. Surmacz, H. Fox, A. Gutteridge, P. Fish, S. Lubitz, and P. Whiting, “Directing differentiation of human embryonic stem cells toward anterior neural ectoderm using small molecules,” Stem Cells, vol. 30, pp. 1875–1884, 2012. View at Google Scholar
  41. J. Zhou, P. Su, D. Li, S. Tsang, E. Duan, and F. Wang, “High-efficiency induction of neural conversion in human ESCs and human induced pluripotent stem cells with a single chemical inhibitor of transforming growth factor beta superfamily receptors,” Stem Cells, vol. 28, no. 10, pp. 1741–1750, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. L. B. Zimmerman, J. M. De Jesús-Escobar, and R. M. Harland, “The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4,” Cell, vol. 86, no. 4, pp. 599–606, 1996. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Krieglstein, B. Reuss, D. Maysinger, and K. Unsicker, “Transforming growth factor-β mediates the neurotrophic effect of fibroblast growth factor-2 on midbrain dopaminergic neurons,” European Journal of Neuroscience, vol. 10, no. 8, pp. 2746–2750, 1998. View at Publisher · View at Google Scholar · View at Scopus
  44. H.-G. König, D. Kögel, A. Rami, and J. H. M. Prehn, “TGF-β1 activates two distinct type I receptors in neurons: implications for neuronal NF-κB signaling,” The Journal of Cell Biology, vol. 168, no. 7, pp. 1077–1086, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Ramalingam and S. J. Kim, “Mechanisms of action of brain insulin against neurodegenerative diseases,” Journal of Neural Transmission, vol. 121, no. 6, pp. 611–626, 2014. View at Publisher · View at Google Scholar · View at Scopus
  46. C. R. Giordano, L. J. Terlecky, A. Bollig-Fischer, P. A. Walton, and S. R. Terlecky, “Amyloid-beta neuroprotection mediated by a targeted antioxidant,” Scientific Reports, vol. 4, article 4983, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Fathi, H. Rasouli, M. Yeganeh, G. H. Salekdeh, and H. Baharvand, “Efficient differentiation of human embryonic stem cells toward dopaminergic neurons using recombinant LMX1A factor,” Molecular Biotechnology, vol. 57, no. 2, pp. 184–194, 2015. View at Publisher · View at Google Scholar
  48. T. Vazin, R. S. Ashton, A. Conway et al., “The effect of multivalent Sonic hedgehog on differentiation of human embryonic stem cells into dopaminergic and GABAergic neurons,” Biomaterials, vol. 35, no. 3, pp. 941–948, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. N. Zavazava, “Progress toward establishing embryonic stem or induced pluripotent stem cell-based clinical translation,” Current Opinion in Organ Transplantation, vol. 19, no. 6, pp. 598–602, 2014. View at Publisher · View at Google Scholar