Meningeal cells induce dopaminergic neurons from embryonic stem cells

European Journal of Neuroscience

Volumn 27, Issue 2, 2008, Pages 261-268

  Hayashi, Hideki ^a,b   Morizane, Asuka ^b   Koyanagi, Masaomi ^b   Ono, Yuichi ^c   Sasai, Yoshiki ^d   Hashimoto, Nobuo ^b   Takahashi, Jun ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c KAN Research Institute Inc ^*  (Japan)

^d RIKEN   (Japan)

Author keywords

Differentiation; Stromal cell derived inducing activity; TGF b3; Wnt 5a

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA3; WNT5A PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL TRANSPLANTATION; DEVELOPMENTAL STAGE; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; EMBRYO; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; MENINGEAL CELL; MOUSE; NONHUMAN; POTASSIUM STIMULI; PRIORITY JOURNAL; PROTEIN EXPRESSION; STIMULUS; STROMAL CELL DERIVED INDUCING ACTIVITY;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; DOPAMINE; EMBRYONIC STEM CELLS; HUMANS; MENINGES; MICE; MICE, INBRED C57BL; NEURONS;

EID: 38349164092     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06027.x     Document Type: Article

References (35)

1. Aubert, J., Dunstan, H., Chambers, I. Smith, A. (2002) Functional gene screening in embryonic stem cells implicates Wnt antagonism in neural differentiation. Nat. Biotechnol., 20, 1240 1245.
2. Barberi, T., Klivenyi, P., Calingasan, N.Y., Lee, H., Kawamata, H., Loonam, K., Perrier, A.L., Bruses, J., Rubio, M.E., Topf, N., Tabar, V., Harrison, N.L., Beal, M.F., Moore, M.A. Studer, L. (2003) Neural subtype specification of fertilization and nuclear transfer embryonic stem cells and application in parkinsonian mice. Nat. Biotechnol., 21, 1200 1207.
3. Bergwitz, C., Wendlandt, T., Kispert, A. Brabant, G. (2001) Wnts differentially regulate colony growth and differentiation of chondrogenic rat calvaria cells. Biochim. Biophys. Acta, 1538, 129 140.
4. Brederlau, A., Correia, A.S., Anisimov, S.V., Elmi, M., Paul, G., Roybon, L., Morizane, A., Bergquist, F., Riebe, I., Nannmark, U., Carta, M., Hanse, E., Takahashi, J., Sasai, Y., Funa, K., Brundin, P., Eriksson, P.S. Li, J.Y. (2006) Transplantation of human embryonic stem cell-derived cells to a rat model of Parkinson's disease: effect of in vitro differentiation on graft survival and teratoma formation. Stem Cells, 24, 1433 1440.
5. Castelo-Branco, G., Wagner, J., Rodriguez, F.J., Kele, J., Sousa, K., Rawal, N., Pasolli, H.A., Fuchs, E., Kitajewski, J. Arenas, E. (2003) Differential regulation of midbrain dopaminergic neuron development by Wnt-1, Wnt-3a, and Wnt-5a. Proc. Natl Acad. Sci. USA, 100, 12747 12752.
6. Farkas, L.M., Dunker, N., Roussa, E., Unsicker, K. Krieglstein, K. (2003) Transforming growth factor-beta(s) are essential for development of midbrain dopaminergic neurons and in vivo. J. Neurosci., 23, 5178 5186.
7. Greenwald, J.A., Mehrara, B.J., Spector, J.A., Chin, G.S., Steinbrech, D.S., Saadeh, P.B., Luchs, J.S., Paccione, M.F., Gittes, G.K. Longaker, M.T. (2000) Biomolecular mechanisms of calvarial bone induction: immature versus mature dura mater. Plast. Reconstr. Surg., 105, 1382 1392.
8. Ito, Y., Yeo, J.Y., Chytil, A., Han, J., Bringas, P., Nakajima, A., Shuler, C.F., Moses, H.L. Chai, Y. (2003) Conditional inactivation of Tgfbr2in cranial neural crest causes cleft palate and calvaria defects. Development, 130, 5269 5280.
9. Jiang, X., Iseki, S., Maxson, R.E., Sucov, H.M. Morriss-Kay, G.M. (2002) Tissue origins and interactions in the mammalian skull vault. Dev. Biol., 241, 106 116.
10. Kawasaki, H., Mizuseki, K., Nishikawa, S., Kaneko, S., Kuwana, Y., Nakanishi, S., Nishikawa, S.I. Sasai, Y. (2000) Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron, 28, 31 40.
11. Kodama, H., Hagiwara, H., Sudo, H., Amagai, Y., Yokota, T., Arai, N. Kitamura, Y. (1986) MC3T3-G2/PA6 preadipocytes support in vitro proliferation of hemopoietic stem cells through a mechanism different from that of interleukin 3. J. Cell. Physiol., 129, 20 26.
12. Lee, S.H., Lumelsky, N., Studer, L., Auerbach, J.M. McKay, R.D. (2000) Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat. Biotechnol., 18, 675 679.
13. de Melker, A.A., Desban, N. Duband, J.L. (2004) Cellular localization and signaling activity of b-catenin in migrating neural crest cells. Dev. Dyn., 230, 708 726.
14. Morizane, A., Takahashi, J., Takagi, Y., Sasai, Y. Hashimoto, N. (2002) Optimal conditions for in vivo induction of dopaminergic neurons from embryonic stem cells through stromal cell-derived inducing activity. J. Neurosci. Res., 69, 934 939.
15. Morizane, A., Takahashi, J., Shinoyama, M., Ideguchi, M., Takagi, Y., Fukuda, H., Koyanagi, M., Sasai, Y. Hashimoto, N. (2006) Generation of graftable dopaminergic neuron progenitors from mouse ES cells by a combination of coculture and neurosphere methods. J. Neurosci. Res., 83, 1025 1027.
16. Murdoch, B., Chadwick, K., Martin, M., Shojaei, F., Shah, K.V., Gallacher, L., Moon, R.T. Bhatia, M. (2003) Wnt-5A augments repopulating capacity and primitive hematopoietic development of human blood stem cells in vivo. Proc. Natl Acad. Sci. USA, 100, 3422 3427.
17. Nagano, Y., Yamashita, H., Takahashi, T., Kishida, S., Nakamura, T., Iseki, E., Hattori, N., Mizuno, Y., Kikuchi, A. Matsumoto, M. (2003) Siah-1 facilitates ubiquitination and degradation of synphilin-1. J. Biol. Chem., 278, 51504 51514.
18. Ohe, Y., Ishikawa, K., Itoh, Z. Tatemoto, K. (1996) Cultured leptomeningeal cells secrete CSF proteins. J. Neurochem., 67, 964 971.
19. Ono, Y., Nakatani, T., Sakamoto, Y., Mizuhara, E., Minaki, Y., Kumai, M., Hamaguchi, A., Nishimura, M., Inoue, Y., Hayashi, H., Takahashi, J. Imai, T. (2007) Differences in neurogenic potential in floor plate cells along an anteroposterior location: midbrain dopaminergic neurons originate from mesencephalic floor plate cells. Development, 134, 3213 3225.
20. Opperman, L.A., Nolen, A.A. Ogle, R.C. (1997) TGF-β1, TGF-β2, and TGF-β3 exhibit distinct patterns of expression during cranial suture formation and obliteration in vivo and in vitro. J. Bone Miner. Res., 12, 301 310.
21. Perrier, A.L., Tabar, V., Barberi, T., Rubio, M.E., Bruses, J., Topf, N., Harrison, N.L. Studer, L. (2004) Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc. Natl Acad. Sci. USA, 101, 12543 12548.
22. Sato, N., Meijer, L., Skaltsounis, L., Greengard, P. Brivanlou, A.H. (2004) Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat. Med., 10, 55 63.
23. Schick, B., Wolf, G., Romeike, B.F., Mestres, P., Praetorius, M. Plinkert, P.K. (2003) Dural cell culture. A new approach to study duraplasty. Cells Tiss. Organs, 173, 129 137.
24. Schulte, G., Bryja, V., Rawal, N., Castelo-Branco, G., Sousa, K.M. Arenas, E. (2005) Purified Wnt-5a increases differentiation of midbrain dopaminergic cells and dishevelled phosphorylation. J. Neurochem., 92, 1550 1553.
25. Shearer, M.C. Fawcett, J.W. (2001) The astrocyte/meningeal cell interface - a barrier to successful nerve regeneration? Cell Tiss. Res., 305, 267 273.
26. Struckhoff, G. (1995) Coculture of meningeal and astrocytic cells - a model for the formation of the glial-limiting membrane. Int. J. Dev. Neurosci., 13, 595 606.
27. Takagi, Y., Takahashi, J., Saiki, H., Morizane, A., Hayashi, T., Kishi, Y., Fukuda, H., Okamoto, Y., Koyanagi, M., Ideguchi, M., Hayashi, H., Imazato, T., Kawasaki, H., Suemori, H., Omachi, S., Iida, H., Itoh, N., Nakatsuji, N., Sasai, Y. Hashimoto, N. (2005) Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J. Clin. Invest., 115, 102 109.
28. Tropepe, V., Hitoshi, S., Sirard, C., Mak, T.W., Rossant, J. van der Kooy, D. (2001) Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron, 30, 65 78.
29. Warren, S.M., Greenwald, J.A., Nacamuli, R.P., Fong, K.D., Song, H.J., Fang, T.D., Mathy, J.A. Longaker, M.T. (2003) Regional dura mater differentially regulates osteoblast gene expression. J. Craniofacial Surg., 14, 363 370.
30. Watanabe, K., Kamiya, D., Nishiyama, A., Katayama, T., Nozaki, S., Kawasaki, H., Watanabe, Y., Mizuseki, K. Sasai, Y. (2005) Direct differentiation of telencephalic precursors from embryonic stem cell. Nat. Neurosci., 8, 288 296.
31. Yamazoe, H., Murakami, Y., Mizuseki, K., Sasai, Y. Iwata, H. (2005) Collection of neural inducing factors from PA6 cells using heparin solution and their immobilization on plastic culture dishes for the induction of neurons from embryonic stem cells. Biomaterials, 26, 5746 5754.
32. Ying, Q.L., Stavridis, M., Griffiths, D., Li, M. Smith, A. (2003) Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol., 21, 183 186.
33. Ye, W., Shimamura, K., Rubenstein, J.L.R., Hynes, M.A. Rosenthal, A. (1998) FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell, 93, 755 766.
34. Zeng, X., Cai, J., Chen, J., Luo, Y., You, Z.B., Fotter, E., Wang, Y., Harvey, B., Miura, T., Backman, C., Chen, G.J., Rao, M.S. Freed, W.J. (2004) Dopaminergic differentiation of human embryonic stem cells. Stem Cells, 22, 925 940.
35. Zhu, Y., Yu, T., Zhang, X.C., Nagasawa, T., Wu, J.Y. Rao, Y. (2002) Role of the chemokine SDF-1 as the meningeal attractant for embryonic cerebellar neurons. Nat. Neurosci., 5, 719 720.