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Neural lineage development in the rhesus monkey with embryonic stem cells

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Translational Neuroscience

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.

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References

  1. Copp A.J., Greene N.D., Murdoch J.N., The genetic basis of mammalian neurulation, Nat. Rev. Genet., 2003, 4, 784–793

    Article  PubMed  Google Scholar 

  2. Sauvageot C.M., Stiles C.D., Molecular mechanisms controlling cortical gliogenesis, Curr. Opin. Neurobiol., 2002, 12, 244–249

    Article  PubMed  CAS  Google Scholar 

  3. His W., Die Neuroblasten und deren Entstehung im embryonal Mark, Leipzig, DE: S. Hirzel, 1889

    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

    Article  PubMed  CAS  Google Scholar 

  5. Schaper A., The earliest differentiation in the central nervous system of vertebrates, Science, 1897, 430–431

    Google Scholar 

  6. Sauer F.C., Mitosis in the neural tube, J. Comp. Neurol. 1935, 377–405

    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)

    PubMed  CAS  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

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  10. Doe C.Q., Fuerstenberg S., Peng C.Y., Neural stem cells: from fly to vertebrates, J. Neurobiol., 1998, 36, 111–127

    Article  PubMed  CAS  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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  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

    PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  16. Rakic P., Developmental and evolutionary adaptations of cortical radial glia, Cereb. Cortex. 2003, 13, 541–549

    Article  PubMed  Google Scholar 

  17. Evans M.J., Kaufman M.H., Establishment in culture of pluripotential cells from mouse embryos, Nature, 1981, 292, 154–156

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  21. Liour S.S., Yu R.K., Differentiation of radial glia-like cells from embryonic stem cells, Glia, 2003, 42, 109–117

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  24. Bonfanti L., Peretto P., Radial glial origin of the adult neural stem cells in the subventricular zone, Prog. Neurobiol., 2007, 83, 24–36

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  27. Shin S., Dalton S., Stice S.L., Human motor neuron differentiation from human embryonic stem cells, Stem Cells Dev., 2005, 14, 266–269

    Article  PubMed  CAS  Google Scholar 

  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

    Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  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

    PubMed  CAS  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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  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

    Article  PubMed  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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  45. Pinto L., Gotz M., Radial glial cell heterogeneity—the source of diverse progeny in the CNS, Prog. Neurobiol., 2007, 83, 2–23

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

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Correspondence to Hongwei Chen.

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Chen, H., Wei, Q., Zhang, J. et al. Neural lineage development in the rhesus monkey with embryonic stem cells. Translat.Neurosci. 4, 378–384 (2013). https://doi.org/10.2478/s13380-013-0135-0

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  • DOI: https://doi.org/10.2478/s13380-013-0135-0

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