Neurons derived in vitro from ES cells express homeoproteins characteristic of motoneurons and interneurons

Mechanisms of Development

Volumn 79, Issue 1-2, 1998, Pages 185-197

  Renoncourt, Yannick ^a   Carroll, Patrick ^a   Filippi, Pierre ^a   Arce, Vilma ^a   Alonso, Serge ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Homeobox; Motoneuron; Mouse embryonic stem cells; Neuronal differentiation; Retinoic acid

Indexed keywords

HOMEODOMAIN PROTEIN;

ARTICLE; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; INTERNEURON; MOTONEURON; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TISSUE DISTRIBUTION;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CHOLINE O-ACETYLTRANSFERASE; DNA-BINDING PROTEINS; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUTAMATE DECARBOXYLASE; HOMEODOMAIN PROTEINS; INTERMEDIATE FILAMENT PROTEINS; INTERNEURONS; MEMBRANE GLYCOPROTEINS; MICE; MOTOR NEURONS; MUSCLE PROTEINS; NERVE TISSUE PROTEINS; PAIRED BOX TRANSCRIPTION FACTORS; PAX7 TRANSCRIPTION FACTOR; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEM CELLS; TRANSCRIPTION FACTORS; TRETINOIN; TYROSINE 3-MONOOXYGENASE;

EID: 0032444244     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0925-4773(98)00189-0     Document Type: Article

References (51)

1. Arvidsson, U., Riedl, M., Elde, R., Meister, B., 1997. Vesicular acetylcholine transporter (VAChT) protein: a novel and unique marker for cholinergic neurons in the central and peripheral nervous systems. J. Comp. Neurol. 378, 454-467.
2. Bain, G., Kitchens, D., Yao, M., Huettner, J.E., Gottlieb, D.I., 1995. Embryonic stem cells express neuronal properties in vitro. Dev. Biol. 168, 342-357.
3. Bain, G., Kitchens, D., Yao, M., Huettner, J.E., Gottlieb, D.I., 1995. Embryonic stem cells express neuronal properties in vitro. Dev. Biol. 168, 342-357.
4. Bain, G., Ray, W.J., Yao, M., Gottlieb, D.I., 1994. From embryonal carcinoma cells to neurons: the P19 pathway. Bioessays 16, 343-348.
5. Bain, G., Ray, W.J., Yao, M., Gottlieb, D.I., 1996. Retinoic acid promotes neural and represses mesodermal gene expression in mouse embryonic stem cells in culture. Biochem. Biophys. Res. Commun. 223, 691-694.
6. Baker, R.K., Hacndel, M.A., Swanson, B.J., Shambaugh, J.C., Micales, B.K., Lyons, G.E., 1997. In vitro preselection of gene-trapped embryonic stem cell clones for characterizing novel developmentally regulated genes in the mouse. Dev. Biol. 185, 201-214.
7. Barbacid, M., 1994. The Trk family of neurotrophin receptors. J. Neurobiol. 25, 1386-1403.
8. Blumberg, B., Bolado, J. Jr., Moreno, T.A., Kintner, C., Evans, R.M., Papalopulu, N., 1997. An essential role for retinoid signaling in anteroposterior neural patterning. Development 124, 373-379.
9. Brüstle, O., McKay, R.D., 1996. Neuronal progenitors as tools for cell replacement in the nervous system. Curr. Opin. Neurobiol. 6, 688-695.
10. Chang, B.E., Blader, P., Fischer, N., Ingham, P.W., Strahle, U., 1997. Axial (HNF3beta) and retinoic acid receptors are regulators of the zebrafish sonic hedgehog promoter. Embo J. 16, 3955-3964.
11. Chomczynski, P., Sacchi, N., 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
12. Djabali, K., Portier, M.M., Gros, F., Blobel, G., Georgatos, S.D., 1991. Network antibodies identify nuclear lamin B as a physiological attachment site for peripherin intermediate filaments. Cell 64, 109-121.
13. Doetschman, T.C., Eistetter, H., Katz, M., Schmidt, W., 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.
14. Ericson, J., Morton, S., Kawakami, A., Roelink, H., Jessell, T.M., 1996. Two critical periods of Sonic Hedgehog signaling required for the specification of motor neuron identity. Cell 87, 661-673.
15. Ericson, J., Rashbass, P., Schedl, A., Brenner-Morton, S., Kawakami, A., van Heyningen, V., Jessell, T.M., Briscoe, J., 1997. Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90, 169-180.
16. Escurat, M., Djabali, K., Gumpel, M., Gros, F., Portier, M.M., 1990. Differential expression of two neuronal intermediate-filament proteins, peripherin and the low-molecular-mass neurofilament protein (NF-L), during the development of the rat. J. Neurosci. 10, 764-784.
17. Evans, M.J., Kaufman, M.H., 1981. Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154-156.
18. Fraichard, A., Chassande, O., Bilbaut, G., Dehay, C., Savatier, P., Samarut, J., 1995. In vitro differentiation of embryonic stem cells into glial cells and functional neurons. J. Cell. Sci. 108, 3181-3188.
19. Gajovic, S., St. Onge, L., Yokota, Y., Gruss, P., 1997. Retinoic acid mediates Pax6 expression during in vitro differentiation of embryonic stem cells. Differentiation 62, 187-192.
20. Harrison, K.A., Druey, K.M., Deguchi, Y., Tuscano, J.M., Kehrl, J.H., 1994. A novel human homeobox gene distantly related to proboscipedia is expressed in lymphoid and pancreatic tissues. J. Biol. Chem. 269, 19968-19975.
21. Jones-Villeneuve, E.M., McBurney, M.W., Rogers, K.A., Kalnins, V.I., 1982. Retinoic acid induces embryonal carcinoma cells to differentiate into neurons and glial cells. J. Cell. Biol. 94, 253-262.
22. Keller, G., Kennedy, M., Papayannopoulou, T., Wiles, M.V., 1993. Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol. Cell. Biol. 13, 473-486.
23. Keller, G.M., 1995. In vitro differentiation of embryonic stem cells. Curr. Opin. Cell. Biol. 7, 862-869.
24. Lendahl, U., Zimmerman, L.B., McKay, R.D., 1990. CNS stem cells express a new class of intermediate filament protein. Cell 60, 585-595.
25. Liem, K.F. Jr., Tremml, G., Jessell, T.M., 1997. A role for the roof plate and its resident TGFbeta-related proteins in neuronal patterning in the dorsal spinal cord. Cell 91, 127-138.
26. Lumsden, A., Krumlauf, R., 1996. Patterning the vertebrate neuraxis. Science 274, 1109-1115.
27. Maden, M., Gale, E., Kostetskii, I., Zile, M., 1996. Vitamin A-deficient quail embryos have half a hindbrain and other neural defects. Curr. Biol. 6, 417-426.
28. Maden, M., Holder, N., 1992. Retinoic acid and development of the central nervous system. Bioessays 14, 431-438.
29. -/- mutant mice. Development 122, 831-838.
30. 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.
31. Meyer, D., Birchmeier, C., 1995. Multiple essential functions of neuregulin in development. Nature 378, 386-390.
32. Meyer, D., Yamaai, T., Garratt, A., Riethmacher-Sonnenberg, E., Kane, D., Theill, L.E., Birchmeier, C., 1997. Isoform-specific expression and function of neuregulin. Development 124, 3575-3586.
33. Okabe, S., Forsberg-Nilsson, K., Spiro, A.C., Segal, M., McKay, R.D., 1996. Development: of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech. Dev. 59, 89-102.
34. Pattyn, A., Morin, X., Cremer, H., Goridis, C., Brunet, J.F., 1997. Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 124, 4065-4075.
35. Pfaff, S.L., Mendelsohn, M., Stewart, C.L., Edlund, T., Jessell, T.M., 1996. Requirement for LIM homeobox gene Isll in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84, 309-320.
36. Robertson, E., Bradley, A., Kuehn, M., Evans, M., 1986. Germ-line transmission of genes introduced into cultured pluripotential cells by retroviral vector. Nature 323, 445-448.
37. Rohwedel, J., Maltsev, V., Bober, E., Arnold, H.H., Hescheler, J., Wobus, A.M., 1994. Muscle cell differentiation of embryonic stem cells reflects myogenesis in vivo: developmentally regulated expression of myogenic determination genes and functional expression of ionic currents. Dev. Biol. 164, 87-101.
38. Salvatore, A.M., Cozzolino, M., Gargano, N., Galanti, S., Levi, A., Alema, S., 1995. Neuronal differentiation of P19 embryonal cells exhibits cell-specific regulation of neurotrophin receptors. NeuroReport 6, 873-877.
39. Schaeren-Wiemers, N., Gerfin-Moser, A., 1993. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100, 431-440.
40. Sejersen, T., Lendahl, U., 1993. Transient expression of the intermediate filament nestin during skeletal muscle development. J. Cell. Sci. 106, 1291-1300.
41. Sharpe, C.R., Goldstone, K., 1997. Retinoid receptors promote primary neurogenesis in Xenopus. Development 124, 515-523.
42. Sockanathan, S., Jessell, T.M., 1998. Motor neuron-derived retinoid signaling specifies the subtype identity of spinal motor neurons. Cell 94, 503-514.
43. Strübing, C., Ahnert-Hilger, G., Shan, J., Wiedenmann, B., Hescheler, J., 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.
44. Tanabe, Y., Jessell, T.M., 1996. Diversity and pattern in the developing spinal cord. Science 274, 1115-1123.
45. Thor, S., Ericson, J., Brannstrom, T., Edlund, T., 1991. The homeodomain LIM protein Isl-1 is expressed in subsets of neurons and endocrine cells in the adult rat. Neuron 7, 881-889.
46. Tosney, K.W., Hotary, K.B., Lance-Jones, C., 1995. Specifying the target identity of motoneurons. Bioessays 17, 379-382.
47. Tsuchida, T., Ensini, M., Morton, S.B., Baldassare, M., Edlund, T., Jessell, T.M., Pfaff, S.L., 1994. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox. Cell 79, 957-970.
48. Varela-Echavarria, A., Pfaff, S.L., Guthrie, S., 1996. Differential expression of LIM homeobox genes among motor neuron subpopulations in the developing chick brain stem. Mol. Cell. Neurosci. 8, 242-257.
49. Walther, C., Gruss, P., 1991. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113, 1435-1449.
50. Williams, R.L., Hilton, D.J., Pease, S., Willson, T.A., Stewart, C.L., Gearing, D.P., Wagner, E.F., Metcalf, D., Nicola, N.A., Gough, N.M., 1988. Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature 336, 684-687.
51. Wobus, A.M., Grosse, R., Schoneich, J., 1988. Specific effects of nerve growth factor on the differentiation pattern of mouse embryonic stem cells in vitro. Biomed. Biochim. Acta 47, 965-973.