Abstract
There are three controversial and undetermined models of neurogenesis and gliogenesis from neuroepithelial cells in the early neural tube; the first in which neurons and glia were proposed to originate from a single homogenous population, the second from two separate pools of committed glial and neuronal progenitors, or, lastly, from transit radial glial (RG). Issues concerning embryonic neural lineage development in primates are not well understood due to restrictions imposed by ethics and material sources. In this study, early neural lineage development was investigated in vitro with rhesus monkey embryonic stem cells (rESC) by means of immunofluorescence with lineage specific markers. It was revealed that neural differentiation likely progresses in a sequential lineage restriction pathway from neuroepithelial stem/progenitor cells to neurons and glia via RG and intermediate precursors: neuronal precursors and glial progenitors. In conclusion, our results suggest that the early neural lineage development of rESC in vitro supported the model in which neuroepithelial cells develop into RG capable of generating both neurons and glia. This work should facilitate understanding of the mechanism of development of the nervous system in primates.
[1] Copp A.J., Greene N.D., Murdoch J.N., The genetic basis of mammalian neurulation, Nat. Rev. Genet., 2003, 4, 784–793 http://dx.doi.org/10.1038/nrg118110.1038/nrg1181Search in Google Scholar
[2] Sauvageot C.M., Stiles C.D., Molecular mechanisms controlling cortical gliogenesis, Curr. Opin. Neurobiol., 2002, 12, 244–249 http://dx.doi.org/10.1016/S0959-4388(02)00322-710.1016/S0959-4388(02)00322-7Search in Google Scholar
[3] His W., Die Neuroblasten und deren Entstehung im embryonal Mark, Leipzig, DE: S. Hirzel, 1889 Search in Google Scholar
[4] Delaunay D., Heydon K., Cumano A., Schwab M.H., Thomas J.L., Suter U., et al., Early neuronal and glial fate restriction of embryonic neural stem cells, J. Neurosci., 2008, 28, 2551–2562 http://dx.doi.org/10.1523/JNEUROSCI.5497-07.200810.1523/JNEUROSCI.5497-07.2008Search in Google Scholar
[5] Schaper A., The earliest differentiation in the central nervous system of vertebrates, Science, 1897, 430–431 Search in Google Scholar
[6] Sauer F.C., Mitosis in the neural tube, J. Comp. Neurol. 1935, 377–405 10.1002/cne.900620207Search in Google Scholar
[7] Fujita H., Fujita S., [Electron microscopic studies on the histogenesis of nerve cells and neuroglia in domestic flow. II. On neurogia], Kaibogaku Zasshi, 1963, 38, 95–108 (in Japanese) Search in Google Scholar
[8] Williams B.P., Read J., Price J., The generation of neurons and oligodendrocytes from a common precursor cell, Neuron, 1991, 7, 685–693 http://dx.doi.org/10.1016/0896-6273(91)90381-910.1016/0896-6273(91)90381-9Search in Google Scholar
[9] Udolph G., Prokop A., Bossing T., Technau G.M., A common precursor for glia and neurons in the embryonic CNS of Drosophila gives rise to segment-specific lineage variants, Development, 1993, 118, 765–775 10.1242/dev.118.3.765Search in Google Scholar
[10] Doe C.Q., Fuerstenberg S., Peng C.Y., Neural stem cells: from fly to vertebrates, J. Neurobiol., 1998, 36, 111–127 http://dx.doi.org/10.1002/(SICI)1097-4695(199808)36:2<111::AID-NEU2>3.0.CO;2-410.1002/(SICI)1097-4695(199808)36:2<111::AID-NEU2>3.0.CO;2-4Search in Google Scholar
[11] Bertrand N., Castro D.S., Guillemot F., Proneural genes and the specification of neural cell types, Nat. Rev. Neurosci., 2002, 3, 517–530 http://dx.doi.org/10.1038/nrn87410.1038/nrn874Search in Google Scholar
[12] Fan G., Martinowich K., Chin M.H., He F., Fouse S.D., Hutnick L., et al., DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling, Development, 2005, 132, 3345–3356 http://dx.doi.org/10.1242/dev.0191210.1242/dev.01912Search in Google Scholar
[13] Malatesta P., Hartfuss E., Gotz M., Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage, Development, 2000, 127, 5253–5263 10.1242/dev.127.24.5253Search in Google Scholar
[14] Alvarez-Buylla A., Garcia-Verdugo J.M., Tramontin A.D., A unified hypothesis on the lineage of neural stem cells, Nat. Rev. Neurosci., 2001, 2, 287–293 http://dx.doi.org/10.1038/3506758210.1038/35067582Search in Google Scholar PubMed
[15] Noctor S.C., Flint A.C., Weissman T.A., Dammerman R.S., Kriegstein A.R., Neurons derived from radial glial cells establish radial units in neocortex, Nature, 2001, 409, 714–720 http://dx.doi.org/10.1038/3505555310.1038/35055553Search in Google Scholar PubMed
[16] Rakic P., Developmental and evolutionary adaptations of cortical radial glia, Cereb. Cortex. 2003, 13, 541–549 http://dx.doi.org/10.1093/cercor/13.6.54110.1093/cercor/13.6.541Search in Google Scholar PubMed
[17] Evans M.J., Kaufman M.H., Establishment in culture of pluripotential cells from mouse embryos, Nature, 1981, 292, 154–156 http://dx.doi.org/10.1038/292154a010.1038/292154a0Search in Google Scholar PubMed
[18] Thomson J.A., Kalishman J., Golos T.G., Durning M., Harris C.P., Becker R.A., et al., Isolation of a primate embryonic stem cell line, Proc. Natl. Acad. Sci. USA, 1995, 92, 7844–7848 http://dx.doi.org/10.1073/pnas.92.17.784410.1073/pnas.92.17.7844Search in Google Scholar PubMed PubMed Central
[19] Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., Waknitz M.A., Swiergiel J.J., Marshall V.S., et al., Embryonic stem cell lines derived from human blastocysts, Science, 1998, 282, 1145–1147 http://dx.doi.org/10.1126/science.282.5391.114510.1126/science.282.5391.1145Search in Google Scholar PubMed
[20] Reubinoff B.E., Itsykson P., Turetsky T., Pera M.F., Reinhartz E., Itzik A., et al., Neural progenitors from human embryonic stem cells, Nat. Biotechnol., 2001, 19, 1134–1140 http://dx.doi.org/10.1038/nbt1201-113410.1038/nbt1201-1134Search in Google Scholar PubMed
[21] Liour S.S., Yu R.K., Differentiation of radial glia-like cells from embryonic stem cells, Glia, 2003, 42, 109–117 http://dx.doi.org/10.1002/glia.1020210.1002/glia.10202Search in Google Scholar PubMed
[22] Liour S.S., Kraemer S.A., Dinkins M.B., Su C.Y., Yanagisawa M., Yu R.K., Further characterization of embryonic stem cell-derived radial glial cells, Glia, 2006, 53, 43–56 http://dx.doi.org/10.1002/glia.2025710.1002/glia.20257Search in Google Scholar PubMed
[23] Gotz M., Barde Y.A., Radial glial cells defined and major intermediates between embryonic stem cells and CNS neurons, Neuron, 2005, 46, 369–372 http://dx.doi.org/10.1016/j.neuron.2005.04.01210.1016/j.neuron.2005.04.012Search in Google Scholar PubMed
[24] Bonfanti L., Peretto P., Radial glial origin of the adult neural stem cells in the subventricular zone, Prog. Neurobiol., 2007, 83, 24–36 http://dx.doi.org/10.1016/j.pneurobio.2006.11.00210.1016/j.pneurobio.2006.11.002Search in Google Scholar PubMed
[25] Mujtaba T., Piper D.R., Kalyani A., Groves A.K., Lucero M.T., Rao M.S., Lineage-restricted neural precursors can be isolated from both the mouse neural tube and cultured ES cells, Dev. Biol., 1999, 214, 113–127 http://dx.doi.org/10.1006/dbio.1999.941810.1006/dbio.1999.9418Search in Google Scholar PubMed
[26] Nistor G.I., Totoiu M.O., Haque N., Carpenter M.K., Keirstead H.S., Human embryonic stem cells differentiate into oligodendrocytes in high purity and myelinate after spinal cord transplantation, Glia, 2005, 49, 385–396 http://dx.doi.org/10.1002/glia.2012710.1002/glia.20127Search in Google Scholar PubMed
[27] Shin S., Dalton S., Stice S.L., Human motor neuron differentiation from human embryonic stem cells, Stem Cells Dev., 2005, 14, 266–269 http://dx.doi.org/10.1089/scd.2005.14.26610.1089/scd.2005.14.266Search in Google Scholar PubMed
[28] Takagi Y., Takahashi J., Saiki H., Morizane A., Hayashi T., Kishi Y., Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model, J. Clin. Invest., 2005, 102–109 10.1172/JCI21137Search in Google Scholar PubMed PubMed Central
[29] Yue F., Cui L., Johkura K., Ogiwara N., Sasaki K., Induction of midbrain dopaminergic neurons from primate embryonic stem cells by coculture with sertoli cells, Stem Cells, 2006, 24, 1695–1706 http://dx.doi.org/10.1634/stemcells.2005-040910.1634/stemcells.2005-0409Search in Google Scholar PubMed
[30] Mizuseki K., Sakamoto T., Watanabe K., Muguruma K., Ikeya M., Nishiyama A., Generation of neural crest-derived peripheral neurons and floor plate cells from mouse and primate embryonic stem cells, Proc. Natl. Acad. Sci. USA, 2003, 100, 5828–5833 http://dx.doi.org/10.1073/pnas.103728210010.1073/pnas.1037282100Search in Google Scholar PubMed PubMed Central
[31] Watanabe K., Kamiya D., Nishiyama A., Katayama T., Nozaki S., Kawasaki H., et al., Directed differentiation of telencephalic precursors from embryonic stem cells, Nat. Neurosci., 2005, 8, 288–296 http://dx.doi.org/10.1038/nn140210.1038/nn1402Search in Google Scholar PubMed
[32] Lazzari G., Colleoni S., Giannelli S.G., Brunetti D., Colombo E., Lagutina I., et al, Direct derivation of neural rosettes from cloned bovine blastocysts: a model of early neurulation events and neural crest specification in vitro, Stem Cells, 2006, 24, 2514–2521 http://dx.doi.org/10.1634/stemcells.2006-014910.1634/stemcells.2006-0149Search in Google Scholar PubMed
[33] Cazillis M., Rasika S., Mani S., Gressens P., Lelievre V., In vitro induction of neural differentiation of embryonic stem (ES) cells closely mimics molecular mechanisms of embryonic brain development, Pediatr. Res., 2006, 59, 48R–53R http://dx.doi.org/10.1203/01.pdr.0000203566.01600.8c10.1203/01.pdr.0000203566.01600.8cSearch in Google Scholar PubMed
[34] Wolf D.P., Kuo H.C., Pau K.Y., Lester L., Progress with nonhuman primate embryonic stem cells, Biol. Reprod., 2004, 71, 1766–1771 http://dx.doi.org/10.1095/biolreprod.104.02941310.1095/biolreprod.104.029413Search in Google Scholar
[35] Kuo H.C., Pau K.Y., Yeoman R.R., Mitalipov S.M., Okano H., Wolf D.P., Differentiation of monkey embryonic stem cells into neural lineages, Biol. Reprod., 2003, 68, 1727–1735 http://dx.doi.org/10.1095/biolreprod.102.01219510.1095/biolreprod.102.012195Search in Google Scholar
[36] Levitt P., Cooper M.L., Rakic P., Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: an ultrastructural immunoperoxidase analysis, J. Neurosci., 1981, 1, 27–39 10.1523/JNEUROSCI.01-01-00027.1981Search in Google Scholar
[37] Levitt P., Cooper M.L., Rakic P., Early divergence and changing proportions of neuronal and glial precursor cells in the primate cerebral ventricular zone, Dev. Biol., 1983, 96, 472–484 http://dx.doi.org/10.1016/0012-1606(83)90184-710.1016/0012-1606(83)90184-7Search in Google Scholar
[38] Mayer-Proschel M., Kalyani A.J., Mujtaba T., Rao M.S., Isolation of lineage-restricted neuronal precursors from multipotent neuroepithelial stem cells, Neuron, 1997, 19, 773–785 http://dx.doi.org/10.1016/S0896-6273(00)80960-510.1016/S0896-6273(00)80960-5Search in Google Scholar
[39] Nat R., Nilbratt M., Narkilahti S., Winblad B., Hovatta O., Nordberg A., Neurogenic neuroepithelial and radial glial cells generated from six human embryonic stem cell lines in serum-free suspension and adherent cultures, Glia, 2007, 55, 385–399 http://dx.doi.org/10.1002/glia.2046310.1002/glia.20463Search in Google Scholar
[40] Bystron I., Rakic P., Molnar Z., Blakemore C., The first neurons of the human cerebral cortex, Nat. Neurosci., 2006, 9, 880–886 http://dx.doi.org/10.1038/nn172610.1038/nn1726Search in Google Scholar
[41] Anthony T.E., Klein C., Fishell G., Heintz N., Radial glia serve as neuronal progenitors in all regions of the central nervous system, Neuron, 2004, 41, 881–890 http://dx.doi.org/10.1016/S0896-6273(04)00140-010.1016/S0896-6273(04)00140-0Search in Google Scholar
[42] Mo Z., Moore A.R., Filipovic R., Ogawa Y., Kazuhiro I., Antic S.D., et al., Human cortical neurons originate from radial glia and neuronrestricted progenitors, J. Neurosci., 2007, 27, 4132–4145 http://dx.doi.org/10.1523/JNEUROSCI.0111-07.200710.1523/JNEUROSCI.0111-07.2007Search in Google Scholar PubMed PubMed Central
[43] Hansen D.V., Lui J.H., Parker P.R., Kriegstein A.R., Neurogenic radial glia in the outer subventricular zone of human neocortex, Nature, 2010, 464, 554–561 http://dx.doi.org/10.1038/nature0884510.1038/nature08845Search in Google Scholar PubMed
[44] Reinchisi G., Limaye P.V., Singh M.B., Antic S.D., Zecevic N., Neurogenic potential of hESC-derived human radial glia is amplified by human fetal cells, Stem Cell Res., 2013, 11, 587–600 http://dx.doi.org/10.1016/j.scr.2013.03.00410.1016/j.scr.2013.03.004Search in Google Scholar PubMed PubMed Central
[45] Pinto L., Gotz M., Radial glial cell heterogeneity—the source of diverse progeny in the CNS, Prog. Neurobiol., 2007, 83, 2–23 http://dx.doi.org/10.1016/j.pneurobio.2007.02.01010.1016/j.pneurobio.2007.02.010Search in Google Scholar PubMed
[46] Li H., Babiarz J., Woodbury J., Kane-Goldsmith N., Grumet M., Spatiotemporal heterogeneity of CNS radial glial cells and their transition to restricted precursors, Dev. Biol., 2004, 271, 225–238 http://dx.doi.org/10.1016/j.ydbio.2004.02.02810.1016/j.ydbio.2004.02.028Search in Google Scholar PubMed
[47] Howard B.M., Mo Z., Filipovic R., Moore A.R., Antic S.D., Zecevic N., Radial glia cells in the developing human brain, Neuroscientist, 2008, 14, 459–473 http://dx.doi.org/10.1177/107385840731351210.1177/1073858407313512Search in Google Scholar PubMed PubMed Central
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