Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2012 (2012), Article ID 140427, 12 pages
http://dx.doi.org/10.1155/2012/140427
Research Article

Small Molecules Greatly Improve Conversion of Human-Induced Pluripotent Stem Cells to the Neuronal Lineage

Basic Research Department, The Parkinson’s Institute, 675 Almanor Ave, Sunnyvale, CA 94085, USA

Received 15 October 2011; Accepted 16 January 2012

Academic Editor: Mahendra Rao

Copyright © 2012 Sally K. Mak 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. L. E. Allan, G. H. Petit, and P. Brundin, “Cell transplantation in Parkinson's disease: problems and perspectives,” Current Opinion in Neurology, vol. 23, no. 4, pp. 426–432, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. R. SoRelle, “Two-thirds of Bush-approved stem-cell lines too immature for research, Thompson says; NIH access to some assured,” Circulation, vol. 104, no. 12, pp. E9027–9028, 2001. View at Google Scholar · View at Scopus
  3. E. A. Zerhouni and J. F. Battey, “National Institutes of Health (NIH)—progress on stem cell research,” Stem Cell Reviews, vol. 1, no. 2, pp. 83–85, 2005. View at Google Scholar · View at Scopus
  4. A. D. Ebert, J. Yu, F. F. Rose et al., “Induced pluripotent stem cells from a spinal muscular atrophy patient,” Nature, vol. 457, no. 7227, pp. 277–280, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Urbach, O. Bar-Nur, G. Q. Daley, and N. Benvenisty, “Differential modeling of fragile X syndrome by human embryonic stem cells and induced pluripotent stem cells,” Cell Stem Cell, vol. 6, no. 5, pp. 407–411, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. J. Zhang, Q. Lian, G. Zhu et al., “A Human iPSC model of Hutchinson Gilford progeria reveals vascular smooth muscle and mesenchymal stem cell defects,” Cell Stem Cell, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. H. N. Nguyen, B. Byers, B. Cord et al., “LRRK2 mutant iPSC-derived da neurons demonstrate increased susceptibility to oxidative stress,” Cell Stem Cell, vol. 8, no. 3, pp. 267–280, 2011. View at Publisher · View at Google Scholar
  8. P. Seibler, J. Graziotto, H. Jeong, F. Simunovic, C. Klein, and D. Krainc, “Mitochondrial parkin recruitment is impaired in neurons derived from mutant PINK1 induced pluripotent stem cells,” Journal of Neuroscience, vol. 31, no. 16, pp. 5970–5976, 2011. View at Publisher · View at Google Scholar
  9. M. J. Devine, M. Ryten, P. Vodicka et al., “Parkinson's disease induced pluripotent stem cells with triplication of the α-synuclein locus,” Nature Communications, vol. 2, no. 1, article 440, 2011. View at Publisher · View at Google Scholar
  10. J. R. Mazzulli, Y. -H. Xu, Y. Sun et al., “Gaucher disease glucocerebrosidase and α-synuclein form a bidirectional pathogenic loop in synucleinopathies,” Cell, vol. 146, no. 1, pp. 37–52, 2011. View at Publisher · View at Google Scholar
  11. A. D. Ebert and C. N. Svendsen, “Human stem cells and drug screening: opportunities and challenges,” Nature Reviews Drug Discovery, vol. 9, no. 5, pp. 367–372, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. B. Schüle, R. A. R. Pera, and J. W. Langston, “Can cellular models revolutionize drug discovery in Parkinson's disease?” Biochimica et Biophysica Acta, vol. 1792, no. 11, pp. 1043–1051, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. A. L. Perrier and L. Studer, “Making and repairing the mammalian brain—in vitro production of dopaminergic neurons,” Seminars in Cell and Developmental Biology, vol. 14, no. 3, pp. 181–189, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Kriks and L. Studer, “Protocols for generating ES cell-derived dopamine neurons,” Advances in Experimental Medicine and Biology, vol. 651, pp. 101–111, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. 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
  16. H. Kawasaki, K. Mizuseki, S. Nishikawa et al., “Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity,” Neuron, vol. 28, no. 1, pp. 31–40, 2000. View at Google Scholar · View at Scopus
  17. T. Vazin, J. Chen, C. T. Lee, R. Amable, and W. J. Freed, “Assessment of stromal-derived inducing activity in the generation of dopaminergic neurons from human embryonic stem cells,” Stem Cells, vol. 26, no. 6, pp. 1517–1525, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. 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
  19. S. C. Zhang, M. Wernig, I. D. Duncan, O. Brüstle, and J. A. Thomson, “In vitro differentiation of transplantable neural precursors from human embryonic stem cells,” Nature Biotechnology, vol. 19, no. 12, pp. 1129–1133, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Kriks, J. -W. Shim, J. Piao et al., “Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease,” Nature, vol. 480, no. 7378, pp. 547–551, 2011. View at Publisher · View at Google Scholar
  21. T. J. Zuber, “Punch biopsy of the skin,” American Family Physician, vol. 65, no. 6, pp. 1155–1167, 2002. View at Google Scholar · View at Scopus
  22. K. Takahashi, K. Tanabe, M. Ohnuki et al., “Induction of pluripotent stem cells from adult human fibroblasts by defined factors,” Cell, vol. 131, no. 5, pp. 861–872, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. I. H. Park, P. H. Lerou, R. Zhao, H. Huo, and G. Q. Daley, “Generation of human-induced pluripotent stem cells,” Nature Protocols, vol. 3, no. 7, pp. 1180–1186, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. M. J. West, L. Slomianka, and H. J. Gundersen, “Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator,” The Anatomical Record, vol. 231, pp. 482–497, 1991. View at Google Scholar
  25. H. J. Gundersen and E. B. Jensen, “The efficiency of systematic sampling in stereology and its prediction,” Journal of Microscopy, vol. 147, pp. 229–263, 1987. View at Google Scholar
  26. X. Zeng, J. Cai, J. Chen et al., “Dopaminergic differentiation of human embryonic stem cells,” Stem Cells, vol. 22, no. 6, pp. 925–940, 2004. View at Google Scholar
  27. A. Swistowski, J. Peng, Q. Liu et al., “Efficient generation of functional dopaminergic neurons from human induced pluripotent stem cells under defined conditions,” Stem Cells, vol. 28, no. 10, pp. 1893–1904, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Swistowski, J. Peng, Y. Han, A. M. Swistowska, M. S. Rao, and X. Zeng, “Xeno-free defined conditions for culture of human embryonic stem cells, neural stem cells and dopaminergic neurons derived from them,” PLoS One, vol. 4, no. 7, Article ID e6233, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Colleoni, C. Galli, S. G. Giannelli et al., “Long-term culture and differentiation of CNS precursors derived from anterior human neural rosettes following exposure to ventralizing factors,” Experimental Cell Research, vol. 316, no. 7, pp. 1148–1158, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. H. Kim, G. Lee, Y. Ganat et al., “miR-371-3 expression predicts neural differentiation propensity in human pluripotent stem cells,” Cell Stem Cell, vol. 8, no. 6, pp. 695–706, 2011. View at Publisher · View at Google Scholar
  31. S. Chung, B. S. Shin, M. Hwang et al., “Neural precursors derived from embryonic stem cells, but not those from fetal ventral mesencephalon, maintain the potential to differentiate into dopaminergic neurons after expansion in vitro,” Stem Cells, vol. 24, no. 6, pp. 1583–1593, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. 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
  33. A. Morizane, D. Doi, T. Kikuchi, K. Nishimura, and J. Takahashi, “Small-molecule inhibitors of bone morphogenic protein and activin/nodal signals promote highly efficient neural induction from human pluripotent stem cells,” Journal of Neuroscience Research, vol. 89, no. 2, pp. 117–126, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. S. M. Chambers, Y. Mica, L. Studer, and M. J. Tomishima, “Converting human pluripotent stem cells to neural tissue and neurons to model neurodegeneration,” Methods in Molecular Biology, vol. 793, pp. 87–97, 2011. View at Publisher · View at Google Scholar
  35. P. B. Yu, C. C. Hong, C. Sachidanandan et al., “Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism,” Nature Chemical Biology, vol. 4, no. 1, pp. 33–41, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. G. J. Inman, F. J. Nicolás, J. F. Callahan et al., “SB-431542 is a potent and specific inhibitor of transforming growth factor-β superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7,” Molecular Pharmacology, vol. 62, no. 1, pp. 65–74, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. G. S. Belinsky, A. R. Moore, S. M. Short, M. T. Rich, and S. D. Antic, “Physiological properties of neurons derived from human embryonic stem cells using a dibutyryl cyclic AMP-based protocol,” Stem Cells and Development, vol. 20, no. 10, pp. 1733–1746, 2011. View at Publisher · View at Google Scholar
  38. G. Lepski, J. Maciaczyk, C. E. Jannes, D. Maciaczyk, J. Bischofberger, and G. Nikkhah, “Delayed functional maturation of human neuronal progenitor cells in vitro,” Molecular and Cellular Neuroscience, vol. 47, no. 1, pp. 36–44, 2011. View at Publisher · View at Google Scholar
  39. C. Lange, E. Mix, J. Frahm et al., “Small molecule GSK-3 inhibitors increase neurogenesis of human neural progenitor cells,” Neuroscience Letters, vol. 488, no. 1, pp. 36–40, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. L. Facci, D. A. Stevens, and S. D. Skaper, “Glycogen synthase kinase-3 inhibitors protect central neurons against excitotoxicity,” NeuroReport, vol. 14, no. 11, pp. 1467–1470, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. D. F. Chen, L. J. Meng, S. H. Du et al., “(+)-Cholesten-3-one induces differentiation of neural stem cells into dopaminergic neurons through BMP signaling,” Neuroscience Research, vol. 68, no. 3, pp. 176–184, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. I. Charalampopoulos, E. Remboutsika, A. N. Margioris, and A. Gravanis, “Neurosteroids as modulators of neurogenesis and neuronal survival,” Trends in Endocrinology and Metabolism, vol. 19, no. 8, pp. 300–307, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. N. F. Díaz, N. E. Díaz-Martínez, I. Velasco, and I. Camacho-Arroyo, “Progesterone increases dopamine neurone number in differentiating mouse embryonic stem cells,” Journal of Neuroendocrinology, vol. 21, no. 8, pp. 730–736, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. N. F. Díaz, N. E. Díaz-Martínez, I. Camacho-Arroyo, and I. Velasco, “Estradiol promotes proliferation of dopaminergic precursors resulting in a higher proportion of dopamine neurons derived from mouse embryonic stem cells,” International Journal of Developmental Neuroscience, vol. 27, no. 5, pp. 493–500, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. N. Sakayori, M. Maekawa, K. Numayama-Tsuruta, T. Katura, T. Moriya, and N. Osumi, “Distinctive effects of arachidonic acid and docosahexaenoic acid on neural stem/progenitor cells,” Genes to Cells, vol. 16, no. 7, pp. 778–790, 2011. View at Publisher · View at Google Scholar
  46. Y. L. Chang et al., “Docosahexaenoic acid promotes dopaminergic differentiation in induced pluripotent stem cells and inhibits teratoma formation in rats with Parkinson-like Pathology,” Cell Transplantation, vol. 21, no. 1, pp. 313–32, 2012. View at Google Scholar
  47. E. Lonardo, C. L. Parish, S. Ponticelli et al., “A small synthetic cripto blocking peptide improves neural induction, dopaminergic differentiation, and functional integration of mouse embryonic stem cells in a rat model of Parkinson's disease,” Stem Cells, vol. 28, no. 8, pp. 1326–1337, 2010. View at Publisher · View at Google Scholar · View at Scopus