Human pluripotent stem cell-derived radial glia recapitulate developmental events and provide real-time access to cortical neurons and astrocytes

Stem Cells Translational Medicine

Volumn 4, Issue 5, 2015, Pages 437-447

  Duan, Lishu ^a   Peng, Chian Yu ^a   Pan, Liuliu ^a   Kessler, John A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Astrocytes; Cortical interneuron; Cortical neuron; Human embryonic stem cells; Human iPS cells; Radial glia

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; BONE MORPHOGENETIC PROTEIN 4; BUPRENORPHINE; CALRETININ; EDOXUDINE; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEIN; JAGGED1; LIPID BINDING PROTEIN; NESTIN; PROTEIN S100B; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR FOXC1; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR SOX2; VESICULAR GLUTAMATE TRANSPORTER 1; VIMENTIN;

ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL CYCLE; CELL DIFFERENTIATION ASSAY; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; FEMALE; GLIA CELL; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IN UTERO STEM CELL TRANSPLANTATION; INTERNEURON; MOUSE; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; PROTEIN INTERACTION; RADIAL GLIA; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; GENETICS; GLIA; MACROGLIA; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT;

IPS;

ANIMALS; ASTROCYTES; CELL DIFFERENTIATION; CEREBRAL CORTEX; EPENDYMOGLIAL CELLS; HUMANS; MICE; NEUROGENESIS; NEUROGLIA; NEURONS; PLURIPOTENT STEM CELLS;

EID: 84930459370     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2014-0137     Document Type: Article

References (41)

1. Götz M, Huttner WB. The cell biology of neurogenesis. Nat Rev Mol Cell Biol 2005;6: 777–788.
2. Anthony TE, Klein C, Fishell G et al. Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 2004;41: 881–890.
3. Malatesta P, Appolloni I, Calzolari F. Radial glia and neural stem cells. Cell Tissue Res 2008; 331:165–178.
4. Howard B, Chen Y, Zecevic N. Cortical progenitor cells in the developing human telenceph-alon. Glia 2006;53:57–66.
5. Desai AR, McConnell SK. Progressive restriction in fate potential by neural progenitors during cerebral cortical development. Development 2000;127:2863–2872.
6. Shen Q, Wang Y, Dimos JT et al. The timing of cortical neurogenesis is encoded within line-agesof individual progenitor cells. Nat Neurosci 2006;9:743–751.
7. LaMonica BE, Lui JH, Wang X et al. OSVZ progenitors in the human cortex: An updated perspective on neurodevelopmental disease. Curr Opin Neurobiol 2012;22:747–753.
8. Bonfanti L, Peretto P. Radial glial origin of the adult neural stem cellsin the subventricular zone. Prog Neurobiol 2007;83:24–36.
9. Merkle FT, Tramontin AD, Garc´ıa-Verdugo JMetal. Radial glia give risetoadult neural stem cells in the subventricular zone. Proc Natl Acad Sci USA 2004;101:17528–17532.
10. LaMonica BE, Lui JH, Hansen DVetal. Mi-totic spindle orientation predicts outer radial glial cell generation in human neocortex. Nat Commun 2013;4:1665.
11. Wilson PG, Stice SS. Development and differentiation of neural rosettes derived from human embryonic stem cells. Stem Cell Rev 2006;2:67–77.
12. Nat R, Nilbratt M, Narkilahti S et al. Neu-rogenic 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.
13. Liour SS, Yu RK. Differentiation of radial glia-like cells from embryonic stem cells. Glia 2003;42:109–117.
14. Liour SS, Kraemer SA, Dinkins MB et al. Fur-ther characterization of embryonic stem cell-derived radial glial cells. Glia 2006;53:43–56.
15. Shi Y, Kirwan P, Smith J et al. Human cerebral cortex development from pluripotent stem cells to functional excitatory synapses. Nat Neurosci 2012;15:477–486.
16. Mariani J, Simonini MV, Palejev D et al. Modeling human cortical development in vitro using induced pluripotent stem cells. Proc Natl Acad Sci USA 2012;109:12770–12775.
17. Espuny-Camacho I, Michelsen KA, Gall D et al. Pyramidal neurons derived from human plu-ripotent stem cells integrate efficiently into mouse brain circuits in vivo. Neuron 2013;77:440–456.
18. Duan L, Bhattacharyya BJ, Belmadani A et al.Stemcell derivedbasal forebrain cholinergic neurons from Alzheimer’s disease patients are more susceptible to cell death. Mol Neurode-gener 2014;9:3.
19. Watanabe K, Kamiya D, Nishiyama A et al. Directed differentiation of telencephalic precursors from embryonic stem cells. Nat Neuro-sci 2005;8:288–296.
20. Hevner RF, Neogi T, Englund C et al. Cajal-Retzius cells in the mouse: Transcription factors, neurotransmitters, and birthdays suggest a pallial origin. Brain Res Dev Brain Res 2003;141:39–53.
21. Haubst N, Berger J, Radjendirane V et al. Molecular dissection of Pax6 function: The specific roles of the paired domain and homeodo-main in brain development. Development 2004; 131:6131–6140.
22. Heins N, Malatesta P, Cecconi F et al. Glial cells generate neurons: The role of the transcription factor Pax6. Nat Neurosci 2002;5: 308–315.
23. Ahlgren S, Vogt P, Bronner-Fraser M. Excess FoxG1 causes overgrowth of the neural tube. J Neurobiol 2003;57:337–349.
24. Miyoshi G, Fishell G. Dynamic FoxG1 expression coordinates the integration of multi-polar pyramidal neuron precursors into the cortical plate. Neuron 2012;74:1045–1058.
25. Sessa A, Mao CA, Hadjantonakis AK et al. Tbr2 directs conversion of radial glia into basal precursors and guides neuronal amplification by indirect neurogenesisin the developing neo-cortex. Neuron 2008;60:56–69.
26. Shi Y, Kirwan P, Livesey FJ. Directed differentiation of human pluripotent stem cells to cerebral cortex neurons and neural networks. Nat Protoc 2012;7:1836–1846.
27. Gaiano N, Nye JS, Fishell G. Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 2000;26:395–404.
28. Hatakeyama J, Bessho Y, Katoh K et al. Hes genes regulate size, shape and histogenesis of the nervous system by control of the timing of neural stem cell differentiation. Development 2004;131:5539–5550.
29. Patten BA, Sardi SP, Koirala S et al. Notch1 signaling regulates radial glia differentiation through multiple transcriptional mechanisms. J Neurosci 2006;26:3102–3108.
30. Molofsky AV, Krencik R, Ullian EM et al. Astrocytes and disease: A neurodevelopmental perspective. Genes Dev 2012;26:891–907.
31. Voigt T. Development of glial cells in the cerebral wall of ferrets: Direct tracing of their transformation from radial glia into astrocytes. J Comp Neurol 1989;289:74–88.
32. Cameron RS, Rakic P. Glial cell lineage in the cerebral cortex:Areview and synthesis. Glia 1991;4:124–137.
33. Conti L, Pollard SM, Gorba T et al. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 2005;3: e283.
34. Falk A, Koch P, KesavanJ et al. Capture of neuroepithelial-like stem cells from pluripotent stemcells providesaversatilesystemforinvitro production of human neurons. PLoS One 2012; 7:e29597.
35. Hewett JA. Determinants of regional and local diversity within the astroglial lineage of the normal central nervous system. J Neuro-chem 2009;110:1717–1736.
36. Krencik R, Weick JP, Liu Y et al. Specification of transplantable astroglial subtypes from human pluripotent stem cells. Nat Biotechnol 2011;29:528–534.
37. Xu Q, Cobos I, DeLaCruz E et al. Origins of cortical interneuron subtypes. J Neurosci 2004; 24:2612–2622.
38. Ventura RE, Goldman JE. Dorsal radial glia generate olfactory bulb interneurons in the postnatal murine brain. J Neurosci 2007; 27:4297–4302.
39. Yu X, Zecevic N. Dorsal radial glial cells have the potential to generate cortical inter-neurons in human but not in mouse brain. J Neurosci 2011;31:2413–2420.
40. Wernig M, Tucker KL, Gornik V et al. Tau EGFP embryonic stem cells:An efficient tool for neuronal lineage selection and transplantation. J Neurosci Res 2002;69:918–924.
41. Koch P, Opitz T, Steinbeck JA et al. 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 2009;106: 3225–3230.