Generation of neuronal progenitor cells and neurons from mouse sleeping beauty transposon-generated induced pluripotent stem cells

Cellular Reprogramming

Volumn 14, Issue 5, 2012, Pages 390-397

  Klincumhom, Nuttha ^a,b   Pirity, Melinda K ^b,d   Berzsenyi, Sara ^b   Ujhelly, Olga ^b   Muenthaisong, Suchitra ^b   Rungarunlert, Sasitorn ^a,c   Tharasanit, Theerawat ^a   Techakumphu, Mongkol ^a   Dinnyes, Andras ^b,e,f  

^a CHULALONGKORN UNIVERSITY   (Thailand)

^b BIOTALENTUM LTD   (Hungary)

^c MAHIDOL UNIVERSITY   (Thailand)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^e SZENT ISTVÁN UNIVERSITY   (Hungary)

^f UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TUBULIN; NESTIN; RETINOIC ACID; TRANSCRIPTION FACTOR PAX6;

ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; EMBRYONIC STEM CELL; FLOW CYTOMETRY; IMMUNOCYTOCHEMISTRY; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SINGLE CELL ANALYSIS; STAINING; TRANSGENICS; TRANSPOSON;

ANIMALS; CELL DIFFERENTIATION; DNA TRANSPOSABLE ELEMENTS; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; MICE; NEUROGENESIS; NEURONS; PLURIPOTENT STEM CELLS; STEM CELLS;

IPS; MAMMALIA;

EID: 84867006849     PISSN: 21524971     EISSN: 21524998     Source Type: Journal    
DOI: 10.1089/cell.2012.0010     Document Type: Article

References (60)

1. Aubert, J., Stavridis, M.P., Tweedie, S., O'Reilly, M., Vierlinger, K., Li, M., Ghazal, P., Pratt, T., Mason, J.O., Roy, D., and Smith, A. (2003). Screening for mammalian neural genes via fluorescence-activated cell sorter purification of neural precursors from Sox1-gfp knock-in mice. Proc. Natl. Acad. Sci. USA 100(Suppl 1), 11836-11841.
2. Bain, G., Kitchens, D., Yao, M., Huettner, J.E., and Gottlieb, D.I. (1995). Embryonic stem cell express neuronal properties in vitro. Dev. Biol. 168, 342-357.
3. Bar-Nur, O., Russ, H.A., Efrat, S., and Benvenisty, N. (2011). Epigenetic memory and preferential lineage-specific differentiation in induced pluripotent stem cells derived from human pancreatic islet beta cells. Cell Stem Cell. 9, 17-23.
4. Bibel, M., Richter, J., Schrenk, K., Tucker, K.L., Staiger, V., Korte, M., Goetz, M., and Barde, Y.A. (2004). Differentiation of mouse embryonic stem cells into a defined neuronal lineage. Nat. Neurosci. 7, 1003-1009.
5. Bibel, M., Richter, J., Lacroix, E., and Barde, Y.A. (2007). Generation of a defined and uniform population of CNS progenitors and neurons from mouse embryonic stem cells. Nat. Protoc. 2, 1034-1043.
6. Chamberlain, S.J., Li, X.J., and Lalande, M. (2008). Induced pluripotent stem (iPS) cells as in vitro models of human neurogenetic disorders. Neurogenetics 9, 227-235.
7. Duval, N., Gomès, D., Calaora, V., Calabrese, A., Meda, P., and Bruzzone, R. (2002). Cell coupling and Cx43 expression in embryonic mouse neural progenitor cells. J. Cell Sci. 115(Pt 16), 3241-3251.
8. Ellis, P., Fagan, B.M., Magness, S.T., Hutton, S., Taranova, O., Hayashi, S., McMahon, A., Rao, M. and Pevny, L. (2004). SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev. Neurosci. 26, 148-165.
9. Essner, J.J, McIvor, R.S., and Hackett, P.B. (2005). Awakening gene therapy with Sleeping Beauty transposons. Curr. Opin. Pharmacol. 5, 513-519.
10. Evans, M.J., and Kaufman, M.H. (1981). Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154-156.
11. Fraichard, A., Chassande, O., Bilbaut, G., Dehay, C., Savatier, P., and Samarut, J. (1995). In vitro differentiation of embryonic stem cells into glial cells and functional neurons. J. Cell Sci. 108(Pt 10), 3181-3188.
12. Hockfield, S., and McKay, R.D. (1985). Identification of major cell classes in the developing mammalian nervous system. J. Neurosci. 5, 3310-3328.
13. Hu, B.Y., and Zhang, S.C. (2010). Directed differentiation of neural-stem cells and subtype-specific neurons from hESCs. Methods Mol Biol. 636, 123-137.
14. Hu, B.Y., Weick, J.P., Yu, J., Ma, L.X., Zhang, X.Q., Thomson. J.A. and Zhang, S.C. (2010). Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proc. Natl. Acad. Sci. USA 107, 4335-4340.
15. Ivics, Z., Hackett, P.B., Plasterk, R.H., and Izsvák, Z. (1997). Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 91, 501-510.
16. 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., Fox, I.J., and Kobayashi, N. (2010). Hepatic differentiation of mouse iPS cells in vitro. Cell Transplant. 19, 841-847.
17. Izsvák, Z., Chuah, M.K., Vandendriessche, T., and Ivics, Z. (2009). Efficient stable gene transfer into human cells by the Sleeping Beauty transposon vectors. Methods 49, 287-297.
18. Kaji, K., Norrby, K., Paca, A., Mileikovsky, M., Mohseni, P., and Woltjen, K. (2009). Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature 458, 771-775.
19. Kalyani, A.J., Piper, D., Mujtaba, T., Lucero, M.T., and Rao, M.S. (1998). Spinal cord neuronal precursors generate multiple neuronal phenotypes in culture. J Neurosci. 18, 7856-7868.
20. Kawasaki, H., Mizuseki, K., Nishikawa, S., and Kaneko, S. (2000). Induction of midbrain dopaminergic neurons from ESC by stromal cell-derived inducing activity. Neuron 28, 31-40.
21. Keller, G.M. (1995). In vitro differentiation of embryonic stem cells. Curr. Opin. Cell Biol. 7, 862-869.
22. Langston, J.W. (2005).The promise of stem cells in Parkinson disease. J. Clin. Invest. 115, 23-25.
23. Lee, V.M., and Pixley, S.K. (1994). Age and differentiationrelated differences in neuron-specific tubulin immunostaining of olfactory sensory neurons. Brain Res. Dev. Brain Res. 83, 209-215.
24. Lendahl, U., Zimmerman, L.B., and McKay, R.D. (1990). CNS stem cells express a new class of intermediate filament protein. Cell 60, 585-595.
25. Liao, J.,Wu, Z.,Wang, Y., Cheng, L., Cui, C., Gao, Y., Chen, T., Rao, L., Chen, S., Jia, N., Dai, H., Xin, S., Kang, J., Pei, G., and Xiao, L. (2008). Enhanced efficiency of generating induced pluripotent stem (iPS) cells from human somatic cells by a combination of six transcription factors. Cell Res. 18, 600-603.
26. Lin, R.C., Matesic, D.F., Marvin, M., McKay, R.D., and Brü stle, O. (1995). Re-expression of the intermediate filament nestin in reactive astrocytes. Neurobiol. Dis. 2, 79-85.
27. Lu, J., Tan, L., Li, P., Gao, H., Fang, B., Ye, S., Geng, Z., Zheng, P., and Song, H. (2009). All-trans retinoic acid promotes neural lineage entry by pluripotent embryonic stem cells via multiple pathways. BMC Cell Biol. 10, 57.
28. MacNicol, A.M., Wilczynska, A., and MacNicol, M.C. (2008). Function and regulation of the mammalian Musashi mRNA translational regulator. Biochem. Soc. Trans. 36(Pt 3), 528-530.
29. Maden, M. (2001). Role and distribution of retinoic acid during CNS development. Int. Rev. Cytol. 209, 1-77.
30. Magin, T.M., McWhir, J., and Melton, D.W. (1992). A new mouse embryonic stem cell line with good germ line contribution and gene targeting frequency. Nucleic Acids Res. 20, 3795-3796
31. Maherali, N., Sridharan, R., Xie, W., Utika,l J., Eminli, S., Arnold, K., Stadtfeld, M., Yachechko, R., Tchieu, J., Jaenisch, R., Plath, K., and Hochedlinger, K. (2007). Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell. 1, 55-70.
32. Martinez, Y., Béna, F., Gimelli, S., Tirefort, D., Dubois-Dauphin, M., Krause, K.H., and Preynat-Seauve, O. (2011). Cellular diversity within embryonic stem cells: pluripotent clonal sublines show distinct differentiation potential. J. Cell. Mol. Med. doi: 10.1111/j.1582-4934.2011.01334.x. (Epub ahead of print).
33. Mayer-Proschel, M., Kalyani, A.J., Mujtaba, T., and Rao, M.S. (1997). Isolation of lineage-restricted neuronal precursors from multipotent neuroepithelial stem cells. Neuron 19, 773-785.
34. Muenthaisong, S., Ujhelly, O., Polgar, Z., Varga, E., Ivics, Z., Pirity, M.K., and Dinnyes A. (2012). Generation and Characterization of mouse induced pluripotent stem (iPS) cell lines by Sleeping Beauty transposon. Exp Cell. Res. (accepted).
35. Nagy, K., Sung, H.K., Zhang, P., Laflamme, S., Vincent, P., Agha-Mohammadi, S., Woltjen, K., Monetti, C., Michael, I.P., Smith, L.C., and Nagy, A. (2011). Induced pluripotent stem cell lines derived from equine fibroblasts. Stem Cell Rev. 7, 693-702.
36. Ohi Y., Qin H., Hong C., Blouin L., Polo J.M., Guo T., Qi Z., Downey S.L., Manos P.D., Rossi D.J., Yu J., Hebrok M., Hochedlinger K., Costello J.F., Song J.S., Ramalho-Santos M. (2011). Incomplete DNA methylation underlies a transcriptional memory of somatic cells in human iPS cells. Nat. Cell Biol. 13 541-549.
37. Okabe, S., Forsberg-Nilsson, K., Spiro, A., Segal, M., and McKay, R. (1996). Development of neuronal precursor cells and functional postmitotic neurons form embryonic stem cells in vitro. Mech. Dev. 59, 89-102.
38. Pevny, L., and Rao, M.S. (2003). The stem-cell menagerie. Trends Neurosci. 26, 351-359.
39. Rohwedel, J., Guan, K., and Wobus, A.M. (1999). Induction of cellular differentiation by retinoic acid in vitro. Cells Tissues Organs 165, 190-202.
40. Ross, S.A., McCaffery, P.J., Drager, U.C., and De Luca, L.M. (2000). Retinoids in embryonal development. Physiol Rev. 80, 1021-1054.
41. Rungarunlert, S., Techakumphu, M., Pirity, M.K., and Dinnyes, A. (2009). Embryoid body formation from embryonic and induced pluripotent stem cells: Benefits of bioreactors. World J. Stem Cells. 1, 11-21
42. Rungarunlert, S., Klincumhom, N., Bock, I., Nemes, C., Techakumphu, M., Pirity, M.K., and Dinnyes, A. (2011). Enhanced cardiac differentiation of mouse embryonic stem cells by use of the slow-turning, lateral vessel (STLV) bioreactor. Biotechnol. Lett. 33, 1565-1573.
43. Salewski, R.P., Eftekharpour, E., and Fehlings, M.G. (2010). Are induced pluripotent stem cells the future of cell-based regenerative therapies for spinal cord injury? J. Cell Physiol. 222, 515-521.
44. Sansom, S.N., Griffiths, D.S., Faedo, A., Kleinjan, D.J., Ruan, Y., Smith, J., van Heyningen, V., Rubenstein, J.L., and Livesey, F.J. (2009). The level of the transcription factor Pax6 is essential for controlling the balance between neural stem cell self-renewal and neurogenesis. PLoS Genet. 5, e1000511.
45. Schwarz, S.C., and Schwarz, J. (2010). Translation of stem cell therapy for neurological diseases. Transl. Res. 156, 155-160.
46. Selfridge, J., Pow, A.M., McWhir, J., Magin, T.M., and Melton, D.W. (1992). Gene targeting using a mouse HPRT minigene/HPRT-deficient embryonic stem cell system: Inactivation of the mouse ERCC-1 gene. Somat. Cell Mol. Genet. 18, 325-336.
47. Strü bing, C., Ahnert-Hilger, G., Shan, J., Wiedenmann, B., Hescheler, J., and Wobus, A. M. (1995). Differentiation of pluripotent embryonic stem cells into the neuronal lineage in vitro gives rise to mature inhibitory and excitatory neurons. Mech. Dev. 53, 275-287.
48. Suter, D.M., Tirefort, D., Julien, S., and Krause, K.H. (2009). A Sox1 to Pax6 switch drives neuroectoderm to radial glia progression during differentiation of mouse embryonic stem cells. Stem Cells 27, 49-58.
49. Takahashi, K., and Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676.
50. Takahashi, K., Okita, K., Nakagawa, M., and Yamanaka, S. (2007). Induction of pluripotent stem cells from fibroblast cultures. Nat. Protoc. 2, 3081-3089.
51. Taupin, P. (2006). Neurogenesis in the adult central nervous system. C. R. Biol. 329, 465-475.
52. Tolar, J., Park, I.H., Xia, L., Lees, C.J., Peacock, B., Webber, B., McElmurry, R.T., Eide, C.R., Orchard, P.J., Kyba, M., Osborn, M.J., Lund, T.C., Wagner, J.E., Daley, G.Q., and Blazar, B.R. (2011). Hematopoietic differentiation of induced pluripotent stem cells from patients with mucopolysaccharidosis type I (Hurler syndrome). Blood 117, 839-847.
53. Ulven, S.M., Gundersen, T.E., Weedon, M.S., Landaas, V.O., Sakhi, A.K., Fromm, S.H., Geronimo, B.A., Moskaug, J.O., and Blomhoff, R. (2000). Identification of endogenous retinoids, enzymes, binding proteins, and receptors during early postimplantation development in mouse: important role of retinal dehydrogenase type 2 in synthesis of all-trans-retinoic acid. Dev. Biol. 220, 379-391.
54. VandenDriessche, T., Ivics, Z., Izsvák, Z., and Chuah, M.K. (2009). Emerging potential of transposons for gene therapy and generation of induced pluripotent stem cells. Blood 114, 1461-1468.
55. Warren, L., Manos, P.D., Ahfeldt, T., Loh, Y.H., Li, H., Lau, F., Ebina, W., Mandal, P.K., Smith, Z.D., Meissner, A., Daley, G.Q., Brack, A.S., Collins, J.J, Cowan, C., Schlaeger, T.M., and Rossi, D.J. (2010). Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell. 7, 618-630.
56. Woltjen, K., Michael, I.P., Mohseni, P., Desai, R., Mileikovsky, M., Hämä lä inen, R., Cowling, R., Wang, W., Liu, P., Gertsenstein, M., Kaji, K., Sung, H.K., and Nagy, A. (2009). piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458, 766-770.
57. Yamazoe, H., and Iwata, H. (2006). Efficient generation of dopaminergic neurons from mouse embryonic stem cells enclosed in hollow fibers. Biomaterials 27, 4871-4880.
58. Ying, Q.L., Stavridis, M., Griffiths, D., Li, M., and Smith, A. (2003). Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol 21,183-186.
59. Zhou, H., Wu, S., Joo, J.Y., Zhu, S., Han, D.W., Lin, T., Trauger, S., Bien, G., Yao, S., Zhu, Y., Siuzdak, G., Schö ler, H.R., Duan, L., and Ding, S. (2009). Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell. 4, 381-384.
60. Zwi, L., Caspi, O., Arbel, G., Huber, I., Gepstein, A., Park, I.H., and Gepstein, L. (2009). Cardiomyocyte differentiation of human induced pluripotent stem cells. Circulation. 120, 1513-1523.