Embryonic stem cells in non-human primates: An overview of neural differentiation potential

Differentiation - Tập 81 - Trang 142-152 - 2011
Florence Wianny1,2, Pierre-Yves Bourillot1,2, Colette Dehay1,2
1Inserm, U846, Stem Cell and Brain Research Institute, 18 Avenue Doyen Lépine, 69500 Bron, France
2Université de Lyon, Lyon 1, UMR-S 846, 69003 Lyon, France

Tài liệu tham khảo

Amit, 2000, Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture, Dev. Biol., 227, 271, 10.1006/dbio.2000.9912 Androutsellis-Theotokis, 2006, Notch signalling regulates stem cell numbers in vitro and in vivo, Nature, 442, 823, 10.1038/nature04940 Asano, 2002, Highly efficient gene transfer into primate embryonic stem cells with a simian lentivirus vector, Mol. Ther., 6, 162, 10.1006/mthe.2002.0655 Assou, 2007, A meta-analysis of human embryonic stem cells transcriptome integrated into a web-based expression atlas, Stem Cells, 25, 961, 10.1634/stemcells.2006-0352 Banin, 2006, Retinal incorporation and differentiation of neural precursors derived from human embryonic stem cells, Stem Cells, 24, 246, 10.1634/stemcells.2005-0009 Becker, 2006, Self-renewal of human embryonic stem cells is supported by a shortened G1 cell cycle phase, J. Cell Physiol., 209, 883, 10.1002/jcp.20776 Becker, 2010, Human embryonic stem cells are pre-mitotically committed to self-renewal and acquire a lengthened G1 phase upon lineage programming, J. Cell Physiol., 222, 103, 10.1002/jcp.21925 Ben-Hur, 2004, Transplantation of human embryonic stem cell-derived neural progenitors improves behavioral deficit in Parkinsonian rats, Stem Cells, 22, 1246, 10.1634/stemcells.2004-0094 Bjugstad, 2008, Human neural stem cells migrate along the nigrostriatal pathway in a primate model of Parkinson's disease, Exp. Neurol., 211, 362, 10.1016/j.expneurol.2008.01.025 Boeuf, 1997, Leukemia inhibitory factor-dependent transcriptional activation in embryonic stem cells, J. Cell Biol., 138, 1207, 10.1083/jcb.138.6.1207 Borghese, 2010, Inhibition of notch signaling in human embryonic stem cell-derived neural stem cells delays G1/S phase transition and accelerates neuronal differentiation in vitro and in vivo, Stem Cells, 28, 955, 10.1002/stem.408 Brederlau, 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, 10.1634/stemcells.2005-0393 Burdon, 2002, Signalling, cell cycle and pluripotency in embryonic stem cells, Trends Cell Biol., 12, 432, 10.1016/S0962-8924(02)02352-8 Byrne, 2006, Transcriptional profiling of rhesus monkey embryonic stem cells, Biol. Reprod., 75, 908, 10.1095/biolreprod.106.053868 Calhoun, 2003, Differentiation of rhesus embryonic stem cells to neural progenitors and neurons, Biochem. Biophys. Res. Commun., 306, 191, 10.1016/S0006-291X(03)00937-9 Cao, 2010, Conditional deletion of Stat3 promotes neurogenesis and inhibits astrogliogenesis in neural stem cells, Biochem. Biophys. Res. Commun., 394, 843, 10.1016/j.bbrc.2010.03.092 Carpenter, 2001, Enrichment of neurons and neural precursors from human embryonic stem cells, Exp. Neurol., 172, 383, 10.1006/exnr.2001.7832 Chambers, 2009, Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling, Nat. Biotechnol., 27, 275, 10.1038/nbt.1529 Chojnacki, 2003, Glycoprotein 130 signaling regulates Notch1 expression and activation in the self-renewal of mammalian forebrain neural stem cells, J. Neurosci., 23, 1730, 10.1523/JNEUROSCI.23-05-01730.2003 Cibelli, 2002, Parthenogenetic stem cells in nonhuman primates, Science, 295, 819, 10.1126/science.1065637 Conti, 2005, Niche-independent symmetrical self-renewal of a mammalian tissue stem cell, PLoS Biol., 3, e283, 10.1371/journal.pbio.0030283 Correia, 2005, Stem cell-based therapy for Parkinson's disease, Ann. Med., 37, 487, 10.1080/07853890500327967 Daadi, 2008, Adherent self-renewable human embryonic stem cell-derived neural stem cell line: functional engraftment in experimental stroke model, PLoS One, 3, e1644, 10.1371/journal.pone.0001644 Daheron, 2004, LIF/STAT3 signaling fails to maintain self-renewal of human embryonic stem cells, Stem Cells, 22, 770, 10.1634/stemcells.22-5-770 Dehay, 2007, Cell-cycle control and cortical development, Nat. Rev. Neurosci., 8, 438, 10.1038/nrn2097 Dehay, 2009, Transcriptional regulation and alternative splicing make for better brains, Neuron, 62, 455, 10.1016/j.neuron.2009.05.006 Draper, 2004, Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells, Nat. Biotechnol., 22, 53, 10.1038/nbt922 Dvorak, 2005, Expression and potential role of fibroblast growth factor 2 and its receptors in human embryonic stem cells, Stem Cells, 23, 1200, 10.1634/stemcells.2004-0303 Eiraku, 2008, Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals, Cell Stem Cell, 3, 519, 10.1016/j.stem.2008.09.002 Elkabetz, 2008, Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage, Genes Dev., 22, 152, 10.1101/gad.1616208 Evans, 1981, Establishment in culture of pluripotential cells from mouse embryos, Nature, 292, 154, 10.1038/292154a0 Favaro, 2009, Hippocampal development and neural stem cell maintenance require Sox2-dependent regulation of Shh, Nat. Neurosci., 12, 1248, 10.1038/nn.2397 Filipczyk, 2007, Differentiation is coupled to changes in the cell cycle regulatory apparatus of human embryonic stem cells, Stem Cell Res., 1, 45, 10.1016/j.scr.2007.09.002 Fluckiger, 2006, Cell cycle features of primate embryonic stem cells, Stem Cells, 24, 547, 10.1634/stemcells.2005-0194 Gaspard, 2008, An intrinsic mechanism of corticogenesis from embryonic stem cells, Nature, 455, 351, 10.1038/nature07287 Gerrard, 2005, Differentiation of human embryonic stem cells to neural lineages in adherent culture by blocking bone morphogenetic protein signaling, Stem Cells, 23, 1234, 10.1634/stemcells.2005-0110 Glaser, 2007, Tripotential differentiation of adherently expandable neural stem (NS) cells, PLoS One, 2, e298, 10.1371/journal.pone.0000298 Greber, 2007, Fibroblast growth factor 2 modulates transforming growth factor beta signaling in mouse embryonic fibroblasts and human ESCs (hESCs) to support hESC self-renewal, Stem Cells, 25, 455, 10.1634/stemcells.2006-0476 Hamasaki, 2004, EMX2 regulates sizes and positioning of the primary sensory and motor areas in neocortex by direct specification of cortical progenitors, Neuron, 43, 359, 10.1016/j.neuron.2004.07.016 Hansen, 2010, Neurogenic radial glia in the outer subventricular zone of human neocortex, Nature, 464, 554, 10.1038/nature08845 Hayashi, 2006, Primate embryonic stem cell-derived neuronal progenitors transplanted into ischemic brain, J. Cereb. Blood Flow Metab., 26, 906, 10.1038/sj.jcbfm.9600247 Hentze, 2007, Cell therapy and the safety of embryonic stem cell-derived grafts, Trends Biotechnol., 25, 24, 10.1016/j.tibtech.2006.10.010 Hogan, 1977, In vitro culture and differentiation on normal mouse blastocysts, Nature, 265, 626, 10.1038/265626a0 Honig, 2004, Hematopoietic differentiation of rhesus monkey embryonic stem cells, Blood Cells Mol. Dis., 32, 5, 10.1016/j.bcmd.2003.09.008 Humphrey, 2004, Maintenance of pluripotency in human embryonic stem cells is STAT3 independent, Stem Cells, 22, 522, 10.1634/stemcells.22-4-522 Iacovitti, 2007, A protocol for the differentiation of human embryonic stem cells into dopaminergic neurons using only chemically defined human additives: studies in vitro and in vivo, Brain Res., 1127, 19, 10.1016/j.brainres.2006.10.022 Ikeda, 2005, Transplantation of neural cells derived from retinoic acid-treated cynomolgus monkey embryonic stem cells successfully improved motor function of hemiplegic mice with experimental brain injury, Neurobiol. Dis., 20, 38, 10.1016/j.nbd.2005.01.031 Imreh, 2006, In vitro culture conditions favoring selection of chromosomal abnormalities in human ES cells, J. Cell Biochem., 99, 508, 10.1002/jcb.20897 Joannides, 2007, A scaleable and defined system for generating neural stem cells from human embryonic stem cells, Stem Cells, 25, 731, 10.1634/stemcells.2006-0562 Kawasaki, 2002, Generation of dopaminergic neurons and pigmented epithelia from primate ES cells by stromal cell-derived inducing activity, Proc. Natl. Acad. Sci. USA, 29, 29 Ko, 2007, Human embryonic stem cell-derived neural precursors as a continuous, stable, and on-demand source for human dopamine neurons, J. Neurochem., 103, 1417, 10.1111/j.1471-4159.2007.04898.x Koch, 2009, A rosette-type, self-renewing human ES cell-derived neural stem cell with potential for in vitro instruction and synaptic integration, Proc. Natl. Acad. Sci. USA, 106, 3225, 10.1073/pnas.0808387106 Kuo, 2003, Differentiation of monkey embryonic stem cells into neural lineages, Biol. Reprod., 68, 1727, 10.1095/biolreprod.102.012195 Kurokawa, 1998, The oncoprotein Evi-1 represses TGF-beta signalling by inhibiting Smad3, Nature, 394, 92, 10.1038/27945 Lanner, 2010, The role of FGF/Erk signaling in pluripotent cells, Development, 137, 3351, 10.1242/dev.050146 Lerou, 2005, Therapeutic potential of embryonic stem cells, Blood Rev., 19, 321, 10.1016/j.blre.2005.01.005 Lester, 2004, Directed differentiation of rhesus monkey ES cells into pancreatic cell phenotypes, Reprod. Biol. Endocrinol., 2, 42, 10.1186/1477-7827-2-42 Levenstein, M.E., Ludwig, T.E., Xu, R.H., Llanas, R.A., Vandenheuvel-Kramer, K., Manning, D., and Thomson, J.A. (2005) Basic FGF support of human embryonic stem cell self-renewal. Stem Cells Li, 2008, Critical issues of clinical human embryonic stem cell therapy for brain repair, Trends Neurosci., 31, 146, 10.1016/j.tins.2007.12.001 Li, 2005, Transplantable neural progenitor populations derived from rhesus monkey embryonic stem cells, Stem Cells, 23, 1295, 10.1634/stemcells.2005-0026 Li, 2005, Specification of motoneurons from human embryonic stem cells, Nat. Biotechnol., 23, 215, 10.1038/nbt1063 Lowell, 2006, Notch promotes neural lineage entry by pluripotent embryonic stem cells, PLoS Biol., 4, e121, 10.1371/journal.pbio.0040121 Lukaszewicz, 2006, The concerted modulation of proliferation and migration contributes to the specification of the cytoarchitecture and dimensions of cortical areas, Cereb. Cortex, 16, i26, 10.1093/cercor/bhk011 Lukaszewicz, 2005, G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex, Neuron, 47, 353, 10.1016/j.neuron.2005.06.032 Machold, 2003, Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches, Neuron, 39, 937, 10.1016/S0896-6273(03)00561-0 Maitra, 2005, Genomic alterations in cultured human embryonic stem cells, Nat. Genet., 37, 1099, 10.1038/ng1631 Martin, 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, 10.1073/pnas.78.12.7634 Martin, 1975, Differentiation of clonal lines of teratocarcinoma cells: formation of embryoid bodies in vitro, Proc. Natl. Acad. Sci. USA, 72, 1441, 10.1073/pnas.72.4.1441 Matsuda, 1999, STAT3 activation is sufficient to maintain an undifferentiated state of mouse embryonic stem cells, EMBO J., 18, 4261, 10.1093/emboj/18.15.4261 Michaelidis, 2008, Wnt signaling and neural stem cells: caught in the Wnt web, Cell Tissue Res., 331, 193, 10.1007/s00441-007-0476-5 Mitalipov, 2006, Isolation and characterization of novel rhesus monkey embryonic stem cell lines, Stem Cells, 24, 2177, 10.1634/stemcells.2006-0125 Mitalipov, 2006, Genomic imprinting in primate embryos and embryonic stem cells, Reprod. Fertil. Dev., 18, 817, 10.1071/RD06112 Molofsky, 2003, Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation, Nature, 425, 962, 10.1038/nature02060 Monuki, 2001, Mechanisms of cerebral cortical patterning in mice and humans, Nat. Neurosci., Suppl. 1199–1206, 4 Muller, 2009, A novel embryonic stem cell line derived from the common marmoset monkey (Callithrix jacchus) exhibiting germ cell-like characteristics, Hum. Reprod., 24, 1359, 10.1093/humrep/dep012 Nagao, 2007, Cross talk between notch and growth factor/cytokine signaling pathways in neural stem cells, Mol. Cell Biol., 27, 3982, 10.1128/MCB.00170-07 Navara, 2007, Pedigreed primate embryonic stem cells express homogeneous familial gene profiles, Stem Cells, 25, 2695, 10.1634/stemcells.2007-0286 Nichols, 1984, Heterogeneous differentiation of external cells in individual isolated early mouse inner cell masses in culture, J. Embryol. Exp. Morphol., 80, 225 Niwa, 1998, Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3, Genes Dev., 12, 2048, 10.1101/gad.12.13.2048 Ohmachi, 2000, FGF-20, a novel neurotrophic factor, preferentially expressed in the substantia nigra pars compacta of rat brain, Biochem. Biophys. Res. Commun., 277, 355, 10.1006/bbrc.2000.3675 Osakada, 2008, Toward the generation of rod and cone photoreceptors from mouse, monkey and human embryonic stem cells, Nat. Biotechnol., 26, 215, 10.1038/nbt1384 Pankratz, 2007, Directed neural differentiation of human embryonic stem cells via an obligated primitive anterior stage, Stem Cells, 25, 1511, 10.1634/stemcells.2006-0707 Papaioannou, 1975, Fate of teratocarcinoma cells injected into early mouse embryos, Nature, 258, 70, 10.1038/258070a0 Park, 2005, In vitro and in vivo analyses of human embryonic stem cell-derived dopamine neurons, J. Neurochem., 92, 1265, 10.1111/j.1471-4159.2004.03006.x Pau, 2004, Derivation and characterization of monkey embryonic stem cells, Reprod. Biol. Endocrinol., 2, 41, 10.1186/1477-7827-2-41 Pera, 2004, Regulation of human embryonic stem cell differentiation by BMP-2 and its antagonist noggin, J. Cell Sci., 117, 1269, 10.1242/jcs.00970 Pera, 2004, Human embryonic stem cells: prospects for development, Development, 131, 5515, 10.1242/dev.01451 Perrier, 2004, Derivation of midbrain dopamine neurons from human embryonic stem cells, Proc. Natl. Acad. Sci. USA, 101, 12543, 10.1073/pnas.0404700101 Reubinoff, 2001, Neural progenitors from human embryonic stem cells, Nat. Biotechnol., 19, 1134, 10.1038/nbt1201-1134 Reynolds, 1996, Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell, Dev. Biol., 175, 1, 10.1006/dbio.1996.0090 Rowitch, 1999, Sonic hedgehog regulates proliferation and inhibits differentiation of CNS precursor cells, J. Neurosci., 19, 8954, 10.1523/JNEUROSCI.19-20-08954.1999 Roy, 2006, Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes, Nat. Med., 12, 1259, 10.1038/nm1495 Salli, 2004, Serotonin neurons derived from rhesus monkey embryonic stem cells: similarities to CNS serotonin neurons, Exp. Neurol., 188, 351, 10.1016/j.expneurol.2004.04.015 Sanchez-Pernaute, 2005, Long-term survival of dopamine neurons derived from parthenogenetic primate embryonic stem cells (cyno-1) after transplantation, Stem Cells, 23, 914, 10.1634/stemcells.2004-0172 Sasaki, 2005, Establishment of novel embryonic stem cell lines derived from the common marmoset (Callithrix jacchus), Stem Cells, 23, 1304, 10.1634/stemcells.2004-0366 Savatier, 2002, Analysis of the cell cycle in mouse embryonic stem cells, Methods Mol. Biol., 185, 27 Schwanke, 2006, Generation and characterization of functional cardiomyocytes from rhesus monkey embryonic stem cells, Stem Cells, 24, 1423, 10.1634/stemcells.2005-0380 Scott, C.E., Wynn, S.L., Sesay, A., Cruz, C., Cheung, M., Gomez Gaviro, M.V., Booth, S., Gao, B., Cheah, K.S., Lovell-Badge, R., Briscoe, J., 2010. SOX9 induces and maintains neural stem cells. Nat. Neurosci. 13, 1181–1189. Shin, 2006, Long-term proliferation of human embryonic stem cell-derived neuroepithelial cells using defined adherent culture conditions, Stem Cells, 24, 125, 10.1634/stemcells.2004-0150 Simerly, 2009, Establishment and characterization of baboon embryonic stem cell lines: an Old World Primate model for regeneration and transplantation research, Stem Cell Res, 10.1016/j.scr.2009.02.004 Smith, 2008, Inhibition of Activin/Nodal signaling promotes specification of human embryonic stem cells into neuroectoderm, Dev. Biol., 313, 107, 10.1016/j.ydbio.2007.10.003 Solter, 1970, Extrauterine growth of mouse egg-cylinders results in malignant teratoma, Nature, 227, 503, 10.1038/227503a0 Spiliotopoulos, 2009, An optimized experimental strategy for efficient conversion of embryonic stem (ES)-derived mouse neural stem (NS) cells into a nearly homogeneous mature neuronal population, Neurobiol. Dis., 34, 320, 10.1016/j.nbd.2009.02.007 Stevens, 1970, The development of transplantable teratocarcinomas from intratesticular grafts of pre- and postimplantation mouse embryos, Dev. Biol., 21, 364, 10.1016/0012-1606(70)90130-2 Suemori, 2001, Establishment of embryonic stem cell lines from cynomolgus monkey blastocysts produced by IVF or ICSI, Dev. Dyn., 222, 273, 10.1002/dvdy.1191 Sumi, 2004, STAT3 is dispensable for maintenance of self-renewal in nonhuman primate embryonic stem cells, Stem Cells, 22, 861, 10.1634/stemcells.22-5-861 Svendsen, 1998, A new method for the rapid and long term growth of human neural precursor cells, J. Neurosci. Methods, 85, 141, 10.1016/S0165-0270(98)00126-5 Takada, 2002, Monkey embryonic stem cell lines expressing green fluorescent protein, Cell Transplant, 11, 631, 10.3727/000000002783985350 Takagi, 2005, Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model, J. Clin. Invest., 115, 102, 10.1172/JCI21137 Thomson, 1995, Isolation of a primate embryonic stem cell line, Proc. Natl. Acad. Sci. USA, 92, 7844, 10.1073/pnas.92.17.7844 Thomson, 1996, Pluripotent cell lines derived from common marmoset (Callithrix jacchus) blastocysts, Biol. Reprod., 55, 254, 10.1095/biolreprod55.2.254 Tibbitts, 2006, Uniform adherent neural progenitor populations from rhesus embryonic stem cells, Stem Cells Dev, 15, 200, 10.1089/scd.2006.15.200 Uchida, 2000, Direct isolation of human central nervous system stem cells, Proc. Natl. Acad. Sci. USA, 97, 14720, 10.1073/pnas.97.26.14720 Ueda, 2006, Cynomolgus monkey embryonic stem cell lines express green fluorescent protein, J. Biosci. Bioeng., 102, 14, 10.1263/jbb.102.14 Umeda, 2004, Development of primitive and definitive hematopoiesis from nonhuman primate embryonic stem cells in vitro, Development, 131, 1869, 10.1242/dev.01065 Vallier, 2005, Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells, J. Cell Sci., 118, 4495, 10.1242/jcs.02553 Vallier, 2009, Activin/Nodal signalling maintains pluripotency by controlling Nanog expression, Development, 136, 1339, 10.1242/dev.033951 Vallier, 2004, Nodal inhibits differentiation of human embryonic stem cells along the neuroectodermal default pathway, Dev. Biol., 275, 403, 10.1016/j.ydbio.2004.08.031 Vazin, 2008, Assessment of stromal-derived inducing activity in the generation of dopaminergic neurons from human embryonic stem cells, Stem Cells, 26, 1517, 10.1634/stemcells.2008-0039 Vescovi, 1999, Isolation and intracerebral grafting of nontransformed multipotential embryonic human CNS stem cells, J. Neurotrauma, 16, 689, 10.1089/neu.1999.16.689 Vrana, 2003, Nonhuman primate parthenogenetic stem cells, Proc. Natl. Acad. Sci. USA, 100, 11911, 10.1073/pnas.2034195100 Wang, 2005, Human embryonic stem cells maintained in the absence of mouse embryonic fibroblasts or conditioned media are capable of hematopoietic development, Blood, 105, 4598, 10.1182/blood-2004-10-4065 Watanabe, 2005, Directed differentiation of telencephalic precursors from embryonic stem cells, Nat. Neurosci., 8, 288, 10.1038/nn1402 Werbowetski-Ogilvie, 2009, Characterization of human embryonic stem cells with features of neoplastic progression, Nat. Biotechnol., 27, 91, 10.1038/nbt.1516 Wianny, 2008, Derivation and cloning of a novel rhesus embryonic stem cell line stably expressing tau-green fluorescent protein, Stem Cells, 26, 1444, 10.1634/stemcells.2007-0953 Wilson, 2001, Neural induction: toward a unifying mechanism, Nat. Neurosci., 4, 1161, 10.1038/nn747 Wolf, 2004, Progress with nonhuman primate embryonic stem cells, Biol. Reprod., 71, 1766, 10.1095/biolreprod.104.029413 Wu, 2003, DACH1 inhibits transforming growth factor-beta signaling through binding Smad4, J. Biol. Chem., 278, 51673, 10.1074/jbc.M310021200 Xiao, 2006, Activin A maintains self-renewal and regulates fibroblast growth factor, Wnt, and bone morphogenic protein pathways in human embryonic stem cells, Stem Cells, 24, 1476, 10.1634/stemcells.2005-0299 Xu, 2001, Feeder-free growth of undifferentiated human embryonic stem cells, Nat. Biotechnol., 19, 971, 10.1038/nbt1001-971 Xu, 2005, Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells, Nat. Methods, 2, 185, 10.1038/nmeth744 Xu, 2008, NANOG is a direct target of TGFbeta/activin-mediated SMAD signaling in human ESCs, Cell Stem Cell, 3, 196, 10.1016/j.stem.2008.07.001 Yan, 2005, Directed differentiation of dopaminergic neuronal subtypes from human embryonic stem cells, Stem Cells, 23, 781, 10.1634/stemcells.2004-0365 Yang, 2008, Human embryonic stem cell-derived dopaminergic neurons reverse functional deficit in Parkinsonian rats, Stem Cells, 26, 55, 10.1634/stemcells.2007-0494 Yoshimatsu, 2006, Non-cell-autonomous action of STAT3 in maintenance of neural precursor cells in the mouse neocortex, Development, 133, 2553, 10.1242/dev.02419 Zeng, 2004, Dopaminergic differentiation of human embryonic stem cells, Stem Cells, 22, 925, 10.1634/stemcells.22-6-925 Zhang, 2006, Neural subtype specification from embryonic stem cells, Brain Pathol., 16, 132, 10.1111/j.1750-3639.2006.00008.x Zhang, 2001, In vitro differentiation of transplantable neural precursors from human embryonic stem cells, Nat. Biotechnol., 19, 1129, 10.1038/nbt1201-1129 Zhang, 2010, Pax6 is a human neuroectoderm cell fate determinant, Cell Stem Cell, 7, 90, 10.1016/j.stem.2010.04.017