Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro

Mechanisms of Development

Volumn 59, Issue 1, 1996, Pages 89-102

  Okabe, Shigeo ^a   Forsberg Nilsson, Karin ^a   Spiro, A Cyril ^a   Segal, Menahem ^b   McKay, Ronald D G ^a,c  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Central nervous system; Embryonic stem cell; In vitro culture; Neuronal precursor cell; Synapse

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; GLIA; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; STEM CELL; SYNAPSE;

ANIMALIA;

EID: 0030248408     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/0925-4773(96)00572-2     Document Type: Article

References (44)

1. Bading, H., Ginty, D.D. and Greenberg, M.E. (1993) Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 260, 181-186.
2. Bain, G., Kitchens, D., Yao, M., Huettner, J.E. and Gottlieb, D.I. (1995) Embryonic stem cells express neuronal properties in vitro. Dev. Biol. 168, 342-357.
3. Barres, B.A., Lazar, M.A. and Raff, M.C. (1994) A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development 120, 1097-1108.
4. Caceres, A., Banker, G., Steward, O., Binder, L. and Payne, M. (1984) MAP2 is localized to the dendrites of hippocampal neurons which develop in culture. Dev. Brain Res. 13, 314-318.
5. Cattaneo, E. and McKay, R.G. (1990) Proliferation and differentiation of neuronal stem cells regulated by nerve growth factor. Nature 347, 762-765.
6. Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
7. Collazo, D., Takahashi, H. and McKay, R.D.G. (1992) Cellular targets and trophic functions of neurotrophin-3 in the developing rat hippocampus. Neuron 9, 643-656.
8. DeCamilli, P., Miller, P.E., Navone, F., Theurkauf, W.E. and Vallee, R.B. (1984) Distribution of microtubule-associated protein 2 in the nervous system of the rat studied by immunofluorescence. Neuroscience 11, 817-846.
9. Deng, C.-X., Wynshaw-Boris, A., Shen, M.M., Daugherty, C., Ornitz, D.M. and Leder, P. (1994) Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev. 8, 3045-3057.
10. Doetschman, T.C., Eistetter, H., Katz, M., Schmidt, W. and Kemler, R. (1985) The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J. Embryol. Exp. Morphol. 87, 27-45.
11. Doniach, T. (1995) Basic FGF as an inducer of anteroposterior neural pattern. Cell 83, 1067-1070.
12. Finley, M.F.A., Kulkarni, N. and Huettner, J.E. (1996) Synapse formation and establishment of neuronal polarity by P19 embryonic carcinoma cells and embryonic stem cells. J. Neurosci. 16, 1056-1065.
13. Fletcher, T.L., Cameron, P., DeCamilli, P. and Banker, G. (1991) The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture. J. Neurosci. 11, 1617-1626.
14. 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 Science 108, 3181-3188.
15. Frederiksen, K. and McKay, R.D.G. (1988) Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J. Neurosci. 8, 1144-1151.
16. Gensburger, C., Labourdette, G. and Sensenbrenner, M. (1987) Brain basic fibroblast growth factor stimulates the proliferation of rat neuronal precursor cells in vitro. FEBS Lett. 217, 1-5.
17. Ghosh, A. and Greenberg, M.E. (1995) Distinct roles for bFGF and NT-3 in the regulation of cortical neurogenesis. Neuron 15, 89-103.
18. Ginty, D.D., Kornhauser, J.M., Thompson, M.A., Bading, H., Mayo, K.E., Takahashi, J.S. and Greenberg, M.E. (1993) Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science 260, 238-241.
19. Joyner, A.L. and Martin, G.R. (1987) En-1 and En-2, two mouse genes with sequence homology to the Drosophila engrailed gene: expression during embryogenesis. Genes Dev. 1, 29-38.
20. Kemler, R., Brulet, P., Schnebelen, M.-T., Gaillard, J. and Jacob, F. (1981) Reactivity of monoclonal antibodies against intermediate filament proteins during embryonic development. J. Embryol. Exp. Morphol. 64, 45-60.
21. Kilpatrick, T.J. and Bartlet, P.F. (1993) Cloning and growth of multipotential neuronal precursors: requirements for proliferation and differentiation. Neuron 10, 255-265.
22. Kimelberg, H.K., Narumi, S. and Bourke, R.S. (1978) Enzymatic and morphologic properties of primary rat brain astrocyte cultures and enzymatic development in vivo. Brain Res. 153, 55-77.
23. Kimelman, D. and Kirschner, M. (1987) Synergistic induction of mesoderm by FGF and TGF-beta and the identification of an mRNA coding for FGF in the early Xenopus embryo. Cell 51, 869-877.
24. Kurtz, A., Zimmer, A., Schnutgen, F., Bruhing, G., Spener, F. and Müller, T. (1994) The expression pattern of a novel gene encoding brain-fatty acid binding protein correlates with neuronal and glial cell development. Development 120, 2637-2649.
25. Lee, K.-F., Li, E., Huber, J., Landis, S., Sharpe, A.H., Chao, M.V. and Jaenisch, R. (1992) Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69, 737-749.
26. Lendahl, U., Zimmerman, L.B. and McKay, R.D.G. (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60, 585-595.
27. Mahon, K.A., Westphal, H. and Gruss, P. (1988) Expression of homeobox gene Hox 1.1 during mouse embryogenesis. Development 104 (Suppl.), 187-195.
28. Martin, G.R. (1981) Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. USA 78, 7634-7638.
29. Mortensen, R.M., Conner, D.A., Chao, S., Geisterfer-Lowrance, A.A.T. and Seidman, J.G. (1992) Production of homozygous mutant ES cells with a single targeting construct. Mol. Cell Biol 12, 2391-2395.
30. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W. and Roder, J.C. (1993) Derivation of completely cell-culture-derived mice from early -passage embryonic stem cells. Proc. Natl. Acad. Sci. USA 90, 8424-8428.
31. Ray, J., Peterson, D.A., Schinstine, M. and Gage, F.H. (1993) Proliferation, differentiation and long-term culture of primary hippocampal neurons. Proc. Natl. Acad. Sci. USA 90, 3602-3606.
32. Rizzino, A. and Growley, C. (1980) Growth and differentiation of embryonal cartinoma cell line F9 in defined media. Proc. Natl. Acad. Sci. USA 77, 457-461.
33. Robertson, E.J. (1987) Embryo-derived stem cell lines. In Robertson, E.J. (ed.), Teratocarcinoma and Embryonic Stem Cells: a Practical Approach, IRL Press, Washington, D.C., pp. 71-112.
34. Segal, M. (1983) Rat hippocampal neurons in culture: responses to electrical and chemical stimuli. J Neurophysiol 50, 1249-64.
35. Segal, M. and Barker, J.L. (1984) Rat hippocampal neurons in culture: potassium conductances. J Neurophysiol 51, 1409-33.
36. Shaw, G., Banker, G.A. and Weber, K. (1985) An immunofluorescence study of neurofilament protein expression by developing hippocampal neurons in tissue culture. Eur. J. Cell Biol. 39, 205-216.
37. Simeone, A., Acampora, D., Arcioni, L., Andrews, P.W., Boncinelli, E. and Mavilio, F. (1990) Sequential activation of HOX2 homeobox genes by retinoic acid in human embryonal carcinoma cells. Nature 346, 763-766.
38. Simeone, A., Acampora, D., Gulisano, M., Stornaiuolo, A. and Boncinelli, E. (1992) Nested expression domains of four homeobox genes in developing rostral brain. Nature 358, 687-690.
39. Sommer, I. and Schachner, M. (1981) Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev. Biol. 83, 311-27.
40. Stemple, D.L. and Anderson, D.J. (1992) Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71, 973-985.
41. Swiatek, P.J. and Gridley, T. (1993) Perinatal lethality and defects in hindbrain development in mice homozygous for a targeted mutation of the zinc finger gene Krox20. Genes Dev. 7, 2071-2084.
42. Vicario-Abejon, C., Johe, K.K., Hazel, T.G., Collazo, D. and McKay, R.D.G. (1995) Functions of basic-fibroblast growth factor and neurotrophins in the differentiation of hippocampal neurons. Neuron 15, 105-114.
43. Yamaguchi, T., Harpal, K., Henkemeyer, M. and Rossant, J. (1994) fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev. 8, 3032-3044.
44. Zackenfels, K., Oppenheim, R.W. and Rohrer, H. (1995) Evidence for an important role of IGF-I and IGF-II for the early development of chick sympathetic neurons. Neuron 14, 731-41.