Development of human nervous tissue upon differentiation of embryonic stem cells in three-dimensional culture

Stem Cells

Volumn 27, Issue 3, 2009, Pages 509-520

  Preynat Seauve, Olivier ^a,b,f   Suter, David M ^a,b   Tirefort, Diderik ^a,b   Turchi, Laurent ^c   Virolle, Thierry ^c   Chneiweiss, Herve ^c   Foti, Michelangelo ^a   Lobrinus, Johannes Alexander ^b,d   Stoppini, Luc ^e   Feki, Anis ^b   Dubois Dauphin, Michel ^a,b   Krause, Karl Heinz ^a,b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b Geneva Hospital   (Switzerland)

^c INSERM   (France)

^d Geneva Institute of Technology   (Switzerland)

^e University of Applied Sciences   (Switzerland)

^f University of Applied Sciences ^*  (Switzerland)

Author keywords

Developmental biology; Embryonic stem cell; Nervous system; Neural differentiation

Indexed keywords

ARTICLE; ASTROCYTE; CELL CULTURE; CELL DIFFERENTIATION; CELL STRUCTURE; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; EMBRYONIC STEM CELL; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; NERVE CELL; NERVOUS TISSUE; OLIGODENDROGLIA; THREE DIMENSIONAL IMAGING;

CELL DIFFERENTIATION; CELL LINE; ELECTROPHYSIOLOGY; EMBRYONIC STEM CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, ELECTRON, TRANSMISSION; NERVOUS SYSTEM; NEURONS; POLYMERASE CHAIN REACTION; TISSUE CULTURE TECHNIQUES;

EID: 65249134409     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2008-0600     Document Type: Article

References (41)

1. Merkle FT, Alvarez-Buylla A. Neural stem cells in mammalian development. Curr Opin Cell Biol 2006;18:704-709.
2. Stern CD. Neural induction: Old problem, new findings, yet more questions. Development 2005;132:2007-2021.
3. Wilson SI, Edlund T. Neural induction: Toward a unifying mechanism. Nat Neurosci 2001;4(suppl):1161-1168.
4. Gould E. How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 2007;8:481-488.
5. Haubensak W, Attardo A, Denk W et al. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: A major site of neurogenesis. Proc Natl Acad Sci U S A 2004;101:3196-3201.
6. 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.
7. Gotz M, Hartfuss E, Malatesta P. Radial glial cells as neuronal precursors: A new perspective on the correlation of morphology and lineage restriction in the developing cerebral cortex of mice. Brain Res Bull 2002;57:777-788.
8. Malatesta P, Hack MA, Hartfuss E et al. Neuronal or glial progeny: Regional differences in radial glia fate. Neuron 2003;37:751-764.
9. Cho MS, Lee YE, Kim JY et al. Highly efficient and large-scale generation of functional dopamine neurons from human embryonic stem cells. Proc Natl Acad Sci U S A 2008;105:3392-3397.
10. Elkabetz Y, Panagiotakos G, Al Shamy G et al. Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev 2008;22:152-165.
11. Joannides AJ, Webber DJ, Raineteau O et al. Environmental signals regulate lineage choice and temporal maturation of neural stem cells from human embryonic stem cells. Brain 2007;130:1263-1275.
12. Joannides AJ, Fiore-Heriche C, Battersby AA et al. A scaleable and defined system for generating neural stem cells from human embryonic stem cells. Stem Cells 2007;25:731-737.
13. Nat R, Nilbratt M, Narkilahti S et al. 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.
14. Perrier AL, Tabar V, Barberi T et al. Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc Natl Acad Sci USA2004;101:12543- 12548.
15. Schulz TC, Noggle SA, Palmarini GM et al. Differentiation of human embryonic stem cells to dopaminergic neurons in serum-free suspension culture. Stem Cells 2004;22:1218-1238.
16. Yan Y, Yang D, Zarnowska ED et al. Directed differentiation of dopaminergic neuronal subtypes from human embryonic stem cells. Stem Cells 2005;23:781-790.
17. Itoh K, Tezuka H, Sakoda H et al. Reproducible establishment of hemopoietic supportive stromal cell lines from murine bone marrow. Exp Hematol 1989;17:145-153.
18. Thiebaud P, de Rooij NF, Koudelka-Hep M et al. Microelectrode arrays for electrophysiological monitoring of hippocampal organotypic slice cultures. IEEE Trans Biomed Eng 1997;44:1159-1163.
19. van Vliet E, Stoppini L, Balestrino M et al. Electrophysiological recording of re-aggregating brain cell cultures on multi-electrode arrays to detect acute neurotoxic effects. Neurotoxicology 2007;28: 1136-1146.
20. Foti M, Mangasarian A, Piguet V et al. Nef-mediated clathrin-coated pit formation. J Cell Biol 1997;139:37-47.
21. Stoppini L, Buchs PA, Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 1991;37:173-182.
22. Bayatti N, Moss JA, Sun L et al. A molecular neuroanatomical study of the developing human neocortex from 8 to 17 postconceptional weeks revealing the early differentiation of the subplate and subventricular zone. Cereb Cortex 2008;18:1536-1548.
23. Mo Z, Zecevic N. Is Pax6 Critical for Neurogenesis in the Human Fetal Brain? Cereb Cortex 2008;18:1455-1465.
24. Feng L, Hatten ME, Heintz N. Brain lipid-binding protein (BLBP): A novel signaling system in the developing mammalian CNS. Neuron 1994;12:895-908.
25. Quinones-Hinojosa A, Sanai N, Soriano-Navarro M et al. Cellular composition and cytoarchitecture of the adult human subventricular zone: A niche of neural stem cells. J Comp Neurol 2006;494: 415-434.
26. Garcia AD, Doan NB, Imura T et al. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 2004;7:1233-1241.
27. Doetsch F, Caille I, Lim DA et al. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999;97: 703-716.
28. Lee G, Kim H, Elkabetz Y et al. Isolation and directed differentiation of neural crest stem cells derived from human embryonic stem cells. Nat Biotechnol 2007;25:1468-1475.
29. Lee H, Shamy GA, Elkabetz Y et al. Directed differentiation and transplantation of human embryonic stem cell-derived motoneurons. Stem Cells 2007;25:1931-1939.
30. Sonntag KC, Pruszak J, Yoshizaki T et al. Enhanced yield of neuroe- pithelial precursors and midbrain-like dopaminergic neurons from human embryonic stem cells using the bone morphogenic protein antagonist noggin. Stem Cells 2007;25:411-418.
31. Vazin T, Chen J, Lee CT et al. Assessment of stromal-derived inducing activity in the generation of dopaminergic neurons from human embryonic stem cells. Stem Cells 2008;26:1517-1525.
32. Yang D, Zhang ZJ, Oldenburg M et al. Human embryonic stem cell- derived dopaminergic neurons reverse functional deficit in parkinsonian rats. Stem Cells 2008;26:55-63.
33. Gustafsson MV, Zheng X, Pereira T et al. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 2005;9: 617-628.
34. Osafune K, Caron L, Borowiak M et al. Marked differences in differentiation propensity among human embryonic stem cell lines. Nat Biotechnol 2008;26:313-315.
35. Wu H, Xu J, Pang ZP et al. Integrative genomic and functional analyses reveal neuronal subtype differentiation bias in human embryonic stem cell lines. Proc Natl Acad Sci U S A 2007;104:13821-13826.
36. Storch A, Paul G, Csete M et al. Long-term proliferation and dopaminergic differentiation of human mesencephalic neural precursor cells. Exp Neurol 2001;170:317-325.
37. Studer L, Csete M, Lee SH et al. Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. J Neurosci 2000;20:7377-7383.
38. Rezaie P, Male D. Colonisation of the developing human brain and spinal cord by microglia: A review. Microsc Res Tech 1999;45: 359-382.
39. Mallat M, Marin-Teva JL, Cheret C. Phagocytosis in the developing CNS: More than clearing the corpses. Curr Opin Neurobiol 2005;15: 101-107.
40. Roussa E, Krieglstein K. Induction and specification of midbrain dopaminergic cells: Focus on SHH, FGF8, and TGF-beta. Cell Tissue Res 2004;318:23-33.
41. Allegrucci C, Young LE. Differences between human embryonic stem cell lines. Hum Reprod Update 2007;13:103-120.