Neurogenic potential of hESC-derived human radial glia is amplified by human fetal cells

Stem Cell Research

Volumn 11, Issue 1, 2013, Pages 587-600

  Reinchisi, Gisela ^a   Limaye, Pallavi V ^a   Singh, Mandakini B ^a   Antic, Srdjan D ^a   Zecevic, Nada ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR PAX6;

ARTICLE; CELL DIFFERENTIATION; COCULTURE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; FETUS; FETUS CELL; FOREBRAIN; GLIA; HUMAN; HUMAN CELL; MACROGLIA; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIAL GLIAL CELL; TISSUE CULTURE;

CELL DIFFERENTIATION; CELL GROWTH PROCESSES; CELL SURVIVAL; CELLS, CULTURED; COCULTURE TECHNIQUES; EMBRYONIC STEM CELLS; FETUS; HUMANS; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; PROSENCEPHALON;

EID: 84877318875     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2013.03.004     Document Type: Article

References (62)

1. Abramova N., Charniga C., Goderie S.K., Temple S. Stage-specific changes in gene expression in acutely isolated mouse CNS progenitor cells. Dev. Biol. 2005, 283(2):269-281.
2. Anlar B., Atilla P., Cakar A.N., Kose M.F., Beksaç M.S., Dagdeviren A., Akçören Z. Expression of adhesion and extracellular matrix molecules in the developing human brain. J. Child Neurol. 2002, 17(9):707-713.
3. Belinsky G.S., Moore A.R., Short S.M., Rich M.T., Antic S.D. Physiological properties of neurons derived from human embryonic stem cells using a dibutyryl cyclic AMP-based protocol. Stem Cells Dev. 2011, 20(10):1733-1746.
4. Bentivoglio M., Mazzarello P. The history of radial glia. Brain Res. Bull. 1999, 49(5):305-315.
5. Bibel M., Richter J., Schrenk K., Tucker K.L., Staiger V., Korte M., Goetz M., Barde Y.A. Differentiation of mouse embryonic stem cells into a defined neuronal lineage. Nat. Neurosci. 2004, 7(9):1003-1009.
6. Borghese L., Dolezalova D., Opitz T., Haupt S., Leinhaas A., Steinfarz B., Koch P., Edenhofer F., Hampl A., Brüstle O. 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 2010, 28(5):955-964.
7. Brustle O., Jones K.N., Learish R.D., Karram K., Choudhary K., Wiestler O.D., Duncan I.D., McKay R.D. Embryonic stem cell-derived glial precursors: a source of myelinating transplants. Science 1999, 285(5428):754-756.
8. Campbell K., Gotz M. Radial glia: multi-purpose cells for vertebrate brain development. Trends Neurosci. 2002, 25(5):235-238.
9. Capela A., Temple S. LeX is expressed by principle progenitor cells in the embryonic nervous system, is secreted into their environment and binds Wnt-1. Dev. Biol. 2006, 291(2):300-313.
10. Chang M.Y., Son H., Lee Y.S., Lee S.H. Neurons and astrocytes secret factors that cause stem cells to differentiate into neurons and astrocytes respectively. Mol. Cell. Neurosci. 2003, 23(3):414-426.
11. Connors B.W., Gutnick M.J. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci. 1990, 13(3):99-104.
12. Conti L., Pollard S.M., Gorba T., Reitano E., Toselli M., Biella G., Sun Y., Sanzone S., Ying Q.L., Cattaneo E., Smith A. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol. 2005, 3:e283.
13. Flanagan L.A., Rebaza L.M., Derzic S., Schwartz P.H., Monuki E.S. Regulation of human neural precursor cells by laminin and integrins. J. Neurosci. Res. 2006, 83(5):845-856.
14. Glaser T., Brustle O. Retinoic acid induction of ES-cell-derived neurons: the radial glia connection. Trends Neurosci. 2005, 28(8):397-400.
15. Götz M., Huttner W.B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 2005, 6(10):777-788.
16. Götz M., Stoykova A., Gruss P. Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 1998, 21(5):1031-1044.
17. Gregg C., Weiss S. Generation of functional radial glial cells by embryonic and adult forebrain neural stem cells. J. Neurosci. 2003, 23(37):11587-11601.
18. Gupta A., Wang Y., Markram H. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 2000, 287(5451):273-278.
19. 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(7288):554-561.
20. Hartfuss E., Galli R., Heins N., Götz M. Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 2001, 229(1):15-30.
21. Hebsgaard J.B., Nelander J., Sabelström H., Jönsson M.E., Stott S., Parmar M. Dopamine neuron precursors within the developing human mesencephalon show radial glial characteristics. Glia 2009, 57(15):1648-1658.
22. Heins N., Malatesta P., Cecconi F., Nakafuku M., Tucker K.L., Hack M.A., Chapouton P., Barde Y.A., Götz M. Glial cells generate neurons: the role of the transcription factor Pax6. Nat. Neurosci. 2002, 5(4):308-315.
23. Hockfield S., McKay R.D. Identification of major cell classes in the developing mammalian nervous system. J. Neurosci. 1985, 5(12):3310-3328.
24. Howard B., Chen Y., Zecevic N. Cortical progenitor cells in the developing human telencephalon. Glia 2006, 53(1):57-66.
25. Jakovcevski I., Zecevic N. Olig transcription factors are expressed in oligodendrocyte and neuronal cells in human fetal CNS. J. Neurosci. 2005, 25(44):10064-10073.
26. Kelly S., Bliss T.M., Shah A.K., Sun G.H., Ma M., Foo W.C., Masel J., Yenari M.A., Weissman I.L., Uchida N., Palmer T., Steinberg G.K. Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc. Natl. Acad. Sci. 2004, 101(32):11839-11844.
27. Kim M., Morshead C.M. Distinct populations of forebrain neural stem and progenitor cells can be isolated using side-population analysis. J. Neurosci. 2003, 23(33):10703-10709.
28. Li W., Cogswell C.A., LoTurco J.J. Neuronal differentiation of precursors in the neocortical ventricular zone is triggered by BMP. J. Neurosci. 1998, 18(21):8853-8862.
29. Li X.J., Du Z.W., Zarnowska E.D., Pankratz M., Hansen L.O., Pearce R.A., Zhang S.C. Specification of motoneurons from human embryonic stem cells. Nat. Biotechnol. 2005, 23(2):215-221.
30. Li X.J., Zhang X., Johnson M.A., Wang Z.B., Lavaute T., Zhang S.C. Coordination of sonic hedgehog and Wnt signaling determines ventral and dorsal telencephalic neuron types from human embryonic stem cells. Development 2009, 136(23):4055-4063.
31. Lindvall O., Kokaia Z. Stem cell for treatment of neurological disorders. Nature 2006, 441(7097):1094-1096.
32. Liour S.S., Yu R.K. Differentiation of radial glia-like cells from embryonic stem cells. Glia 2003, 42(2):109-117.
33. 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(1):43-56.
34. Ma W., Tavakoli T., Derby E., Serebryakova Y., Rao M.S., Mattson M.P. Cell-extracellular matrix interactions regulate neural differentiation of human embryonic stem cells. BMC Dev. Biol. 2008, 8:90.
35. Malatesta P., Hartfuss E., Götz M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 2000, 127(24):5253-5263.
36. Malatesta P., Hack M.A., Hartfuss E., Kettenmann H., Klinkert W., Kirchhoff F., Götz M. Neuronal or glial progeny: regional differences in radial glia fate. Neuron 2003, 37(5):751-764.
37. Miyata T., Kawaguchi A., Okano H., Ogawa M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 2001, 31(5):727-774.
38. Mizuseki K., Sakamoto T., Watanabe K., Muguruma K., Ikeya M., Nishiyama A., Arakawa A., Suemori H., Nakatsuji N., Kawasaki H., Murakami F., Sasai Y. Generation of neural crest-derived peripheral neurons and floor plate cells from mouse and primate embryonic stem cells. Proc. Natl. Acad. Sci. 2003, 100(10):5828-5833.
39. Mo Z., Zecevic N. Is Pax6 critical for neurogenesis in the human fetal brain?. Cereb. Cortex 2008, 18(6):1455-1465.
40. Mo Z., Zecevic N. Human fetal radial glia cells generate oligodendrocytes in vitro. Glia 2009, 57(5):490-498.
41. Mo Z., Moore A.R., Filipovic R., Ogawa Y., Kazuhiro I., Antic S.D., Zecevic N. Human cortical neurons originate from radial glia and neuron-restricted progenitors. J. Neurosci. 2007, 27(15):4132-4145.
42. Moore A.R., Filipovic R., Mo Z., Rasband M.N., Zecevic N., Antic S.D. Electrical excitability of early neurons in the human cerebral cortex during the second trimester of gestation. Cereb. Cortex 2009, 19(8):1795-1805.
43. Muroyama Y., Kondoh H., Takada S. Wnt proteins promote neuronal differentiation in neural stem cell culture. Biochem. Biophys. Res. Commun. 2004, 313(4):915-921.
44. Nakayama T., Momoki-Soga T., Inoue N. Astrocyte-derived factors instruct differentiation of embryonic stem cells into neurons. Neurosci. Res. 2003, 46(2):241-249.
45. 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(4):385-399.
46. Noctor S.C., Flint A.C., Weissman T.A., Dammmerman R.S., Kriegstein A.R. Neurons derived from radial glia cells establish radial units in neocortex. Nature 2001, 409(6821):714-720.
47. Politis M., Lindvall O. Clinical application of stem cell therapy in Parkinson's disease. BMC Med. 2012, 10:1.
48. Pollard S.M., Conti L. Investigating radial glia in vitro. Prog. Neurobiol. 2007, 83(1):53-67.
49. Pollard S.M., Conti L., Sun Y., Goffredo D., Smith A. Adherent neural stem (NS) cells from fetal and adult forebrain. Cereb. Cortex 2006, 16(Suppl. 1):i112-i120.
50. Rakic P. Developmental and evolutionary adaptations of cortical radial glia. Cereb. Cortex 2003, 13(6):541-549.
51. Roy N.S., Cleren C., Singh S.K., Yang L., Beal M.F., Goldman S.A. Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes. Nat. Med. 2006, 12(11):1259-1268.
52. Song H., Stevens C.F., Gage F.H. Astroglia induce neurogenesis from adult neural stem cells. Nature 2002, 417(6884):39-44.
53. Suh H., Consiglio A., Ray J., Sawai T., D'Amour K.A., Gage F.H. In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell 2007, 1(5):515-528.
54. Tao W., Lai E. Telencephalon-restricted expression of BF-1, a new member of the HNF-3/fork head gene family, in the developing rat brain. Neuron 1992, 8(5):957-966.
55. Tate M.C., García A.J., Keselowsky B.G., Schumm M.A., Archer D.R., LaPlaca M.C. Specific beta1 integrins mediate adhesion, migration, and differentiation of neural progenitors derived from embryonic striatum. Mol. Cell. Neurosci. 2004, 27(1):22-31.
56. Yan Y., Yang D., Zarnowska E.D., Du Z., Werbel B., Valliere C., Pearce R.A., Thomson J.A., Zhang S.C. Directed differentiation of dopaminergic neuronal subtypes from human embryonic stem cells. Stem Cells 2005, 23(6):781-790.
57. Yang D., Zhang Z.J., Oldenburg M., Ayala M., Zhang S.C. Human embryonic stem cell-derived dopaminergic neurons reverse functional deficit in parkinsonian rats. Stem Cells 2008, 26(1):55-63.
58. Zecevic N. Specific characteristic of radial glia in the human fetal telencephalon. Glia 2004, 48(1):27-35.
59. Zecevic N., Chen Y., Filipovic R. Contributions of cortical subventricular zone to the development of the human cerebral cortex. J. Comp. Neurol. 2005, 491(1):109-122.
60. Zhang S.C., Wernig M., Duncan I.D., Brustle O., Thompson J.A. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol. 2001, 19(12):1129-1133.
61. Zhang X., Huang C.T., Chen J., Pankratz M.T., Xi J., Li J., Yang Y., Lavaute T.M., Li X.J., Ayala M., Bondarenko G.I., Du Z.W., Jin Y., Golos T.G., Zhang S.C. Pax6 is a human neuroectoderm cell fate determinant. Cell Stem Cell 2010, 7(1):90-100.
62. Zhu G., Mehler M.F., Zhao J., Yu Yung S., Kessler J.A. Sonic hedgehog and BMP2 exert opposing actions on proliferation and differentiation of embryonic neural progenitor cells. Dev. Biol. 1999, 215(1):118-129.