Regulation of mouse embryonic stem cell neural differentiation by retinoic acid

Developmental Biology

Volumn 328, Issue 2, 2009, Pages 456-471

  Kim, Mijeong ^a   Habiba, Ayman ^a   Doherty, Jason M ^a   Mills, Jason C ^a   Mercer, Robert W ^a   Huettner, James E ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Serum free; Spinal cord; Telencephalon; Transcriptional profile

Indexed keywords

ION CHANNEL; RETINOIC ACID;

ANIMAL CELL; ARTICLE; CELL AGGREGATION; CELL LINEAGE; CELL MATURATION; CELL POLARITY; CELL PROLIFERATION; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYO; EMBRYONIC STEM CELL; GERM LAYER; IN VITRO STUDY; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; RHOMBENCEPHALON; SPINAL CORD; SYNAPTIC TRANSMISSION; TELENCEPHALON;

EID: 63349094725     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.02.001     Document Type: Article

References (103)

1. Adams L.D., Choi L., Xian H.Q., Yang A., Sauer B., Wei L., and Gottlieb D.I. Double lox targeting for neural cell transgenesis. Mol. Brain Res. 110 (2003) 220-233
2. Akagi H., Hirai K., and Hishinuma F. Cloning of a glycine receptor subtype expressed in rat brain and spinal cord during a specific period of neuronal development. FEBS Lett. 281 (1991) 160-166
3. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., Davis A.P., Dolinski K., Dwight S.S., Eppig J.T., Harris M.A., Hill D.P., Issel-Tarver L., Kasarskis A., Lewis S., Matese J.C., Richardson J.E., Ringwald M., Rubin G.M., and Sherlock G. Gene ontology: tool for the unification of biology. Nat. Genet. 25 (2000) 25-29
4. Aubert J., Dunstan H., Chambers I., and Smith A. Functional gene screening in embryonic stem cells implicates Wnt antagonism in neural differentiation. Nat. Biotechnol. 20 (2002) 1240-1245
5. Bain G., Kitchens D., Yao M., Huettner J.E., and Gottlieb D.I. Embryonic stem cells express neuronal properties in vitro. Dev. Biol. 168 (1995) 342-357
6. Bain G., Ray W.J., Yao M., and Gottlieb D.I. Retinoic acid promotes neural and represses mesodermal gene expression in mouse embryonic stem cells in culture. Biochem. Biophys. Res. Commun. 223 (1996) 691-694
7. 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., and Studer L. Neural subtype specification of fertilization and nuclear transfer embryonic stem cells and application in parkinsonian mice. Nat. Biotechnol. 21 (2003) 1200-1207
8. Bellochio E.E., Reimer R.J., Fremeau R.T., and Edwards R.H. Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289 (2000) 957-960
9. Bibel M., Richter J., Schrenk K., Tucker K.L., Staiger V., Korte M., Goetz M., and Barde Y.A. Differentiation of mouse embryonic stem cells into a defined neuronal lineage. Nat. Neurosci. 7 (2004) 1003-1009
10. Bouhon I.A., Kato H., Chandran S., and Allen N.D. Neural differentiation of mouse embryonic stem cells in chemically defined medium. Brain Res. Bull. 68 (2005) 62-75
11. Bouhon I.A., Joannides A., Kato H., Chandran S., and Allen N.D. Embryonic stem cell-derived neural progenitors display temporal restriction to neural patterning. Stem Cells 24 (2006) 1908-1913
12. Brewer G.J., Torricelli J.R., Everge E.K., and Price P.J. Optimized survival of hippocampal neurons in B27-supplemented neurobasal, a new serum-free medium combination. J. Neurosci. Res. 35 (1993) 567-576
13. Briscoe J., Pierani A., Jessell T.M., and Ericson J. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101 (2000) 435-445
14. Briscoe J., Sussel L., Serup P., Hartigan-O'Connor D., Jessell T.M., Rubenstein J.L.R., and Ericson J. Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling. Nature 398 (1999) 622-627
15. Brüstle O., Jones K.N., Learish R.D., Karram K., Choudhary K., Wiestler O.D., Duncan I.D., and McKay R.D. Embryonic stem cell-derived glial precursors: a source of myelinating transplants. Science 285 (1999) 754-756
16. Burdon T., Smith A., and Savatier P. Signalling, cell cycle and pluripotency in embryonic stem cells. Trends Cell Biol. 12 (2002) 432-438
17. Caccamo D., Katsetos C.D., Herman M.M., Frankfurter A., Collins V.P., and Rubinstein L.J. Immunohistochemistry of a spontaneous murine ovarian teratoma with neuroepithelial differentiation. Neuron-associated beta-tubulin as a marker for primitive neuroepithelium. Lab. Invest. 60 (1989) 390-398
18. Caceres A., Banker G.A., and Binder L. Immunocytochemical localization of tubulin and microtubule-associated protein 2 during the development of hippocampal neurons in culture. J. Neurosci. 6 (1986) 714-722
19. Cahoy J.D., Emery B., Kaushal A., Foo L.C., Zamanian J.L., Christopherson K.S., Xing Y., Lubischer J.L., Krieg P.A., Krupenko S.A., Thompson W.J., and Barres B.A. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 28 (2008) 264-278
20. Cai C., and Grabel L. Directing the differentiation of embryonic stem cells to neural stem cells. Dev. Dyn. 236 (2007) 3255-3266
21. Chang Y.C., and Gottlieb D.I. Characterization of the proteins purified with monoclonal antibodies to glutamic acid decarboxylase. J. Neurosci. 8 (1988) 2123-2130
22. Cheng L., Arata A., Mizuguchi R., Qian Y., Karunaratne A., Gray P.A., Arata S., Shirasawa S., Bouchard M., Luo P., Chen C.L., Busslinger M., Goulding M., Onimaru H., and Ma Q. Tlx3 and Tlx1 are post-mitotic selector genes determining glutamatergic over GABAergic cell fates. Nat. Neurosci. 7 (2004) 510-517
23. Clagett-Dame M., McNeill E.M., and Muley P.D. Role of all-trans retinoic acid in neurite outgrowth and axonal elongation. J. Neurobiol. 66 (2006) 739-756
24. Davis C.A., and Joyner A.L. Expression patterns of the homeo box-containing genes En-1 and En-2 and the proto-oncogene int-1 diverge during mouse development. Genes Dev. 2 (1988) 1736-1744
25. Doetsch F. The glial identity of neural stem cells. Nat. Neurosci. 6 (2003) 1127-1134
26. Doetschman T.C., Eistetter H., Katz M., Schmidt W., and Kemler R. 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 (1985) 27-45
27. Doherty J.M., Carmichael L.K., and Mills J.C. GOurmet: a tool for quantitative comparison and visualization of gene expression profiles based on gene ontology (GO) distributions. BMC Bioinformatics 7 (2006) 151
28. Doherty J.M., Geske M.J., Stappenbeck T.S., and Mills J.C. Diverse adult stem cells share specific higher-order patterns of gene expression. Stem Cells 26 (2008) 2124-2130
29. Dotti C.G., Sullivan C.A., and Banker G.A. The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8 (1988) 1454-1468
30. Englund C., Fink A., Lau C., Pham D., Daza R.A., Bulfone A., Kowalczyk T., and Hevner R.F. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 25 (2005) 247-251
31. Ericson J., Muhr J., Placzek M., Lints T., Jessell T.M., and Edlund T. Sonic hedgehog induces the differentiation of ventral forebrain neurons: a common signal for ventral patterning within the neural tube. Cell 81 (1995) 747-756
32. Ericson J., Rashbass P., Schedl A., Brenner-Morton S., Kawakami A., van Heyningen V., Jessell T.M., and Briscoe J. Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90 (1997) 169-180
33. Finley M.F.A., Kulkarni N., and Huettner J.E. Synapse formation and establishment of neuronal polarity by P19 embryonic carcinoma cells and embryonic stem cells. J. Neurosci. 16 (1996) 1056-1065
34. Finley M.F.A., Devata S., and Huettner J.E. BMP-4 inhibits neural differentiation in murine embryonic stem cells. J. Neurobiol. 40 (1999) 271-287
35. Fortunel N.O., Otu H.H., Ng H.H., Chen J., Mu X., Chevassut T., Li X., Joseph M., Bailey C., Hatzfeld J.A., Hatzfeld A., Usta F., Vega V.B., Long P.M., Libermann T.A., and Lim B. Comment on "'Stemness': transcriptional profiling of embryonic and adult stem cells" and "a stem cell molecular signature". Science. 302 (2003) 393
36. Fotaki V., Yu T., Zaki P.A., Mason J.O., and Price D.J. Abnormal positioning of diencephalic cell types in neocortical tissue in the dorsal telencephalon of mice lacking functional Gli3. J. Neurosci. 26 (2006) 9282-9292
37. Fraichard A., Chassande O., Bilbaut G., Dehay C., Savatier P., and Samarut J. In vitro differentiation of embryonic stem cells into glial cells and functional neurons. J. Cell Sci. 108 (1995) 3181-3188
38. Furushima K., Yamamoto A., Nagano T., Shibata M., Miyachi H., Abe T., Ohshima N., Kiyonari H., and Aizawa S. Mouse homologues of Shisa antagonistic to Wnt and Fgf signalings. Dev. Biol. 306 (2007) 480-492
39. Gaspard N., Bouschet T., Hourez R., Dimidschstein J., Naeije G., van den Ameele J., Espuny-Camacho I., Herpoel A., Passante L., Schiffmann S.N., Gaillard A., and Vanderhaeghen P. An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455 (2008) 351-357
40. Glaser T., and Brüstle O. Retinoic acid induction of ES-cell-derived neurons: the radial glia connection. Trends Neurosci. 28 (2005) 397-400
41. Goetz A.K., Scheffler B., Chen H.X., Wang S., Suslov O., Xiang H., Brüstle O., Roper S.N., and Steindler D.A. Temporally restricted substrate interactions direct fate and specification of neural precursors derived from embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 11063-11068
42. Goldman S. Glia as neural progenitor cells. Trends Neurosci. 26 (2003) 590-596
43. Gould A., Morrison A., Sproat G., White R.A., and Krumlauf R. Positive cross-regulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns. Genes Dev. 11 (1997) 900-913
44. Gotz M., and Barde Y.A. Radial glial cells defined and major intermediates between embryonic stem cells and CNS neurons. Neuron 46 (2005) 369-372
45. Graham A., Papalopulu N., Lorimer J., McVey J.H., Tuddenham E.G., and Krumlauf R. Characterization of a murine homeo box gene, Hox-2.6, related to the Drosophila deformed gene. Genes Dev. 2 (1988) 1424-1438
46. Gratzner H.G. Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218 (1982) 474-475
47. Gross M.K., Dottori M., and Goulding M. Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord. Neuron 34 (2002) 535-549
48. Hadjantonakis A.K., Gertsenstein M., Ikawa M., Okabe M., and Nagy A. Generating green fluorescent mice by germline transmission of green fluorescent ES cells. Mech. Dev. 76 (1998) 79-90
49. Harvey R.J., Schmieden V., Von Holst A., Laube B., Rohrer H., and Betz H. Glycine receptors containing the alpha4 subunit in the embryonic sympathetic nervous system, spinal cord and male genital ridge. Eur. J. Neurosci. 12 (2000) 994-1001
50. Heins N., Malatesta P., Cecconi F., Nakafuku M., Tucker K.L., Hack M.A., Chapouton P., Barde Y.A., and Gotz M. Glial cells generate neurons: the role of the transcription factor Pax6. Nat. Neurosci. 5 (2002) 308-315
51. Helms A.W., and Johnson J.E. Specification of dorsal spinal cord interneurons. Curr. Opin. Neurobiol. 13 (2003) 42-49
52. Hevner R.F., Shi L., Justice N., Hsueh Y., Sheng M., Smiga S., Bulfone A., Goffinet A.M., Campagnoni A.T., and Rubenstein J.L. Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29 (2001) 353-366
53. Hodge R.D., Kowalczyk T.D., Wolf S.A., Encinas J.M., Rippey C., Enikolopov G., Kempermann G., and Hevner R.F. Intermediate progenitors in adult hippocampal neurogenesis: Tbr2 expression and coordinate regulation of neuronal output. J. Neurosci. 28 (2008) 3707-3717
54. Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1 (2000) 20-29
55. Kawasaki H., Mizuseki K., Nishikawa S., Kaneko S., Kuwana Y., Nakanishi S., Nishikawa S.I., and Sasai Y. Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28 (2000) 31-40
56. Kuhse J., Laube B., Magalei D., and Betz H. Assembly of the inhibitory glycine receptor: identification of amino acid sequence motifs governing subunit stoichiometry. Neuron 11 (1993) 1049-1056
57. Lee S.H., Lumelsky N., Studer L., Auerbach J.M., and McKay R.D. Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat. Biotechnol. 18 (2000) 675-679
58. Lendahl U., Zimmerman L.B., and McKay R.D. CNS stem cells express a new class of intermediate filament protein. Cell 60 (1990) 585-595
59. Li C., and Wong W.H. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 31-36
60. Lin T., Chao C., Saito S.I., Mazur S.J., Murphy M.E., Appella E., and Xu Y. p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nat. Cell Biol. 7 (2005) 165-171
61. Liour S.S., and Yu R.K. Differentiation of radial glia-like cells from embryonic stem cells. Glia 42 (2003) 109-117
62. Liour S.S., Kraemer S.A., Dinkins M.B., Su C.Y., Yanagisawa M., and Yu R.K. Further characterization of embryonic stem cell-derived radial glial cells. Glia 53 (2006) 43-56
63. Liu S., Qu Y., Stewart T.J., Howard M.J., Chakrabortty S., Holekamp T.F., and McDonald J.W. Embryonic stem cells differentiate into oligodendrocytes and myelinate in culture and after spinal cord transplantation. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 6126-6131
64. Maden M. Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat. Rev. Neurosci. 8 (2007) 755-765
65. Malatesta P., Hack M.A., Hartfuss E., Kettenmann H., Klinkert W., Kirchhoff F., and Gotz M. Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37 (2003) 751-764
66. Matise M.P., and Joyner A.L. Expression patterns of developmental control genes in normal and Engrailed-1 mutant mouse spinal cord reveal early diversity in developing interneurons. J. Neurosci. 17 (1997) 7805-7816
67. Matsunaga E., Araki I., and Nakamura H. Pax6 defines the di-mesencephalic boundary by repressing En1 and Pax2. Development 127 (2000) 2357-2365
68. Malosio M.L., Marqueze-Pouey B., Kuhse J., and Betz H. Widespread expression of glycine receptor subunit mRNAs in the adult and developing rat brain. EMBO J. 10 (1991) 2401-2409
69. Muller T., Brohmann H., Pierani A., Heppenstall P.A., Lewin G.R., Jessell T.M., and Birchmeier C. The homeodomain factor Lbx1 distinguishes two major programs of neuronal differentiation in the dorsal spinal cord. Neuron 34 (2002) 551-562
70. Murry C.E., and Keller G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 132 (2008) 661-680
71. Muzio L., DiBenedetto B., Stoykova A., Boncinelli E., Gruss P., and Mallamaci A. Conversion of cerebral cortex into basal ganglia in Emx2(-/-) Pax6(Sey/Sey) double-mutant mice. Nat. Neurosci. 5 (2002) 737-745
72. Newcomb R., Sun X., Taylor L., Curthoys N., and Giffard R.G. Increased production of extracellular glutamate by the mitochondrial glutaminase following neuronal death. J. Biol. Chem. 272 (1997) 11276-11282
73. Nieuwkoop P.D. Activation and organization of the central nervous system in amphibians. J. Exp. Zool. 120 (1952) 1-108
74. Nolte C., and Krumlauf R. Expression of Hox genes in the nervous system of vertebrates. In: Papageorgiou S. (Ed). Hox Gene Expression (2007), Springer, New York 14-41
75. Niwa H., Miyazaki J., and Smith A.G. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 24 (2000) 372-376
76. Nordstrom U., Maier E., Jessell T.M., and Edlund T. An early role for WNT signaling in specifying neural patterns of Cdx and Hox gene expression and motor neuron subtype identity. PLoS Biol. 4 (2006) e252
77. Okabe S., Forsberg-Nilsson K., Spiro A.C., Segal M., and McKay R.D. Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech. Dev. 59 (1996) 89-102
78. Ohnuma S., and Harris W.A. Neurogenesis and the cell cycle. Neuron 40 (2003) 199-208
79. Park I.H., Zhao R., West J.A., Yabuuchi A., Huo H., Ince T.A., Lerou P.H., Lensch M.W., and Daley G.Q. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451 (2008) 135-136
80. Pfaff S.L., Mendelsohn M., Stewart C.L., Edlund T., and Jessell T.M. Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84 (1996) 309-320
81. Piechotta K., Weth F., Harvey R.J., and Friauf E. Localization of rat glycine receptor alpha1 and alpha2 subunit transcripts in the developing auditory brainstem. J. Comp. Neurol. 438 (2001) 336-352
82. Pierani A., Brenner-Morton S., Chiang C., and Jessell T.M. A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell 97 (1999) 903-915
83. Ramalho-Santos M., Yoon S., Matsuzaki Y., Mulligan R.C., and Melton D.A. "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 298 (2002) 597-600
84. Remedios R., Huilgol D., Saha B., Hari P., Bhatnagar L., Kowalczyk T., Hevner R.F., Suda Y., Aizawa S., Ohshima T., Stoykova A., and Tole S. A stream of cells migrating from the caudal telencephalon reveals a link between the amygdala and neocortex. Nat. Neurosci. 10 (2007) 1141-1150
85. Rohwedel J., Guan K., and Wobus A.M. Induction of cellular differentiation by retinoic acid in vitro. Cells Tiss. Org. 165 (1999) 190-202
86. Salero E., and Hatten M.E. Differentiation of ES cells into cerebellar neurons. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 2997-3002
87. Savatier P., Lapillonne H., van Grunsven L.A., Rudkin B.B., and Samarut J. Withdrawal of differentiation inhibitory activity/leukemia inhibitory factor up-regulates D-type cyclins and cyclin-dependent kinase inhibitors in mouse embryonic stem cells. Oncogene 12 (1996) 309-322
88. Simon H., Guthrie S., and Lumsden A. Regulation of SC1/DM-GRASP during the migration of motor neurons in the chick embryo brain stem. J. Neurobiol. 25 (1994) 1129-1143
89. Smith C.M., Finger J.H., Hayamizu T.F., McCright I.J., Eppig J.T., Kadin J.A., Richardson J.E., and Ringwald M. The mouse gene expression database (GXD): 2007 update. Nucleic Acids Res. 35 (2007) D618-D623
90. Smukler S.R., Runciman S.B., Xu S., and van der Kooy D. Embryonic stem cells assume a primitive neural stem cell fate in the absence of extrinsic influences. J. Cell Biol. 172 (2006) 79-90
91. Stead E., White J., Faast R., Conn S., Goldstone S., Rathjen J., Dhingra U., Rathjen P., Walker D., and Dalton S. Pluripotent cell division cycles are driven by ectopic Cdk2, cyclin A/E and E2F activities. Oncogene 21 (2002) 8320-8333
92. Strübing C., Ahnert-Hilger G., Shan J., Wiedenmann B., Hescheler J., and Wobus A.M. Differentiation of pluripotent embryonic stem cells into the neuronal lineage in vitro gives rise to mature inhibitory and excitatory neurons. Mech. Dev. 53 (1995) 275-287
93. Suda Y., Suzuki M., Ikawa Y., and Aizawa S. Mouse embryonic stem cells exhibit indefinite proliferative potential. J. Cell. Physiol. 133 (1987) 197-201
94. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., and Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131 (2007) 861-872
95. Takamori S., Rhee J.S., Rosenmund C., and Jahn R. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407 (2000) 189-194
96. Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., Waknitz M.A., Swiergiel J.J., Marshall V.S., and Jones J.M. Embryonic stem cell lines derived from human blastocysts. Science 282 (1998) 1145-1147
97. Tropepe V., Hitoshi S., Sirard C., Mak T.W., Rossant J., and van der Kooy D. Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 30 (2001) 65-78
98. Verani R., Cappuccio I., Spinsanti P., Gradini R., Caruso A., Magnotti M.C., Motolese M., Nicoletti F., and Melchiorri D. Expression of the Wnt inhibitor Dickkopf-1 is required for the induction of neural markers in mouse embryonic stem cells differentiating in response to retinoic acid. J. Neurochem. 100 (2007) 242-250
99. Watanabe K., Kamiya D., Nishiyama A., Katayama T., Nozaki S., Kawasaki H., Watanabe Y., Mizuseki K., and Sasai Y. Directed differentiation of telencephalic precursors from embryonic stem cells. Nat. Neurosci. 8 (2005) 288-296
100. Wichterle H., Lieberam I., Porter J.A., and Jessell T.M. Directed differentiation of embryonic stem cells into motor neurons. Cell 110 (2002) 385-397
101. Wiles M.V., and Johansson B.M. Embryonic stem cell development in a chemically defined medium. Exp. Cell Res. 247 (1999) 241-248
102. Ying Q.L., Stavridis M., Griffiths D., Li M., and Smith A. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 21 (2003) 183-186
103. Yun K., Potter S., and Rubenstein J.L. Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 128 (2001) 193-205