Human cerebral cortex development from pluripotent stem cells to functional excitatory synapses

Nature Neuroscience

Volumn 15, Issue 3, 2012, Pages 477-486

  Shi, Yichen ^a,b   Kirwan, Peter ^a,b   Smith, James ^a,b   Robinson, Hugh P C ^b   Livesey, Frederick J ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EOMESODERMIN; RETINOID; TRANSCRIPTION FACTOR PAX6;

ANIMAL CELL; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN ELECTROPHYSIOLOGY; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NERVE CELL NETWORK; NERVE ENDING; NERVOUS SYSTEM DEVELOPMENT; NEUROEPITHELIUM; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; ROSETTE FORMATION; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTOGENESIS;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; CEREBRAL CORTEX; EMBRYONIC STEM CELLS; EXCITATORY AMINO ACID ANTAGONISTS; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUTAMIC ACID; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KI-67 ANTIGEN; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; NEUROGENESIS; PATCH-CLAMP TECHNIQUES; PIPERIDINES; PLURIPOTENT STEM CELLS; POTASSIUM CHANNEL BLOCKERS; RETINOIDS; RNA, MESSENGER; SIGNAL TRANSDUCTION; SODIUM CHANNEL BLOCKERS; SYNAPSES; SYNAPTIC POTENTIALS; TETRODOTOXIN; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 84862778046     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3041     Document Type: Article

References (46)

1. Mountcastle, V. B. The Cerebral Cortex (Harvard University Press, Cambridge, Massachusetts, 1998).
2. Finlay, B. L. & Darlington, R. B. Linked regularities in the development and evolution of mammalian brains. Science 268, 1578-1584 (1995).
3. Rakic, P. Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 10, 724-735 (2009).
4. Hill, R. S. & Walsh, C. A. Molecular insights into human brain evolution. Nature 437, 64-67 (2005).
5. Wonders, C. P. & Anderson, S. A. The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 7, 687-696 (2006).
6. Caviness, V. S. Jr., Takahashi, T. & Nowakowski, R. S. Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model. Trends Neurosci. 18, 379-383 (1995).
7. Douglas, R. J. & Martin, K. A. Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 27, 419-451 (2004).
8. Fame, R. M., MacDonald, J. L. & Macklis, J. D. Development, specification, and diversity of callosal projection neurons. Trends Neurosci. 34, 41-50 (2011).
9. López-Bendito, G. & Molnar, Z. Thalamocortical development: how are we going to get there? Nat. Rev. Neurosci. 4, 276-289 (2003).
10. Bibel, M. et al. Differentiation of mouse embryonic stem cells into a defined neuronal lineage. Nat. Neurosci. 7, 1003-1009 (2004).
11. Gaspard, N. et al. An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455, 351-357 (2008).
12. Eiraku, M. et al. Self-organized formation of polarized cortical tissues from ES cells and its active manipulation by extrinsic signals. Cell Stem Cell 3, 519-532 (2008).
13. Au, E. & Fishell, G. Cortex shatters the glass ceiling. Cell Stem Cell 3, 472-474 (2008).
14. Hansen, D. V., Rubenstein, J. L. & Kriegstein, A. R. Deriving excitatory neurons of the neocortex from pluripotent stem cells. Neuron 70, 645-660 (2011).
15. Hansen, D. V., Lui, J. H., Parker, P. R. & Kriegstein, A. R. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464, 554-561 (2010).
16. Wang, X., Tsai, J. W., Lamonica, B. & Kriegstein, A. R. A new subtype of progenitor cell in the mouse embryonic neocortex. Nat. Neurosci. 14, 555-561 (2011).
17. Fietz, S. A. et al. OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat. Neurosci. 13, 690-699 (2010).
18. Ying, Q. L., Stavridis, M., Griffiths, D., Li, M. & Smith, A. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 21, 183-186 (2003).
19. Chambers, S. M. et al. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol. 27, 275-280 (2009).
20. Hu, B. Y. & Zhang, S. C. Directed differentiation of neural-stem cells and subtypespecific neurons from human ES cells. Methods Mol. Biol. 636, 123-137 (2010).
21. Elkabetz, Y. et al. Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev. 22, 152-165 (2008).
22. Zhang, S. C., Wernig, M., Duncan, I. D., Brustle, O. & Thomson, J. A. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol. 19, 1129-1133 (2001).
23. Götz, M. & Huttner, W. B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6, 777-788 (2005).
24. Fietz, S. A. & Huttner, W. B. Cortical progenitor expansion, self-renewal and neurogenesis: a polarized perspective. Curr. Opin. Neurobiol. 21, 23-35 (2011).
25. Takahashi, T., Nowakowski, R. S. & Caviness, V. S. Jr. The leaving or Q fraction of the murine cerebral proliferative epithelium: a general model of neocortical neuronogenesis. J. Neurosci. 16, 6183-6196 (1996).
26. Cahoy, J. D. et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 28, 264-278 (2008).
27. Polleux, F. & Ghosh, A. The slice overlay assay: a versatile tool to study the influence of extracellular signals on neuronal development. Sci. STKE 136, pl9 (2002).
28. Molyneaux, B. J., Arlotta, P., Menezes, J. R. & Macklis, J. D. Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 8, 427-437 (2007).
29. Bedogni, F. et al. Tbr1 regulates regional and laminar identity of postmitotic neurons in developing neocortex. Proc. Natl. Acad. Sci. USA 107, 13129-13134 (2010).
30. Bulfone, A. et al. T-brain-1: a homolog of Brachyury whose expression defines molecularly distinct domains within the cerebral cortex. Neuron 15, 63-78 (1995).
31. Arlotta, P. et al. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45, 207-221 (2005).
32. Nieto, M. et al. Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex. J. Comp. Neurol. 479, 168-180 (2004).
33. Alcamo, E. A. et al. Satb2 regulates callosal projection neuron identity in the developing cerebral cortex. Neuron 57, 364-377 (2008).
34. Britanova, O. et al. Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron 57, 378-392 (2008).
35. McCormick, D. A. & Prince, D. A. Postnatal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. J. Physiol. (Lond.) 393, 743-762 (1987).
36. Connors, B. W., Gutnick, M. J. & Prince, D. A. Electrophysiological properties of neocortical neurons in vitro. J. Neurophysiol. 48, 1302-1320 (1982).
37. Maden, M., Gale, E., Kostetskii, I. & Zile, M. Vitamin A-deficient quail embryos have half a hindbrain and other neural defects. Curr. Biol. 6, 417-426 (1996).
38. Siegenthaler, J. A. et al. Retinoic acid from the meninges regulates cortical neuron generation. Cell 139, 597-609 (2009).
39. Vallier, L. et al. Early cell fate decisions of human embryonic stem cells and mouse epiblast stem cells are controlled by the same signaling pathways. PLoS ONE 4, e6082 (2009).
40. Livesey, F. J. & Cepko, C. L. Vertebrate neural cell-fate determination: lessons from the retina. Nat. Rev. Neurosci. 2, 109-118 (2001).
41. Shen, Q. et al. The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat. Neurosci. 9, 743-751 (2006).
42. Caviness, V. S. Jr. et al. Cell output, cell cycle duration and neuronal specification: a model of integrated mechanisms of the neocortical proliferative process. Cereb. Cortex 13, 592-598 (2003).
43. Groc, L., Gustafsson, B. & Hanse, E. AMPA signaling in nascent glutamatergic synapses: there and not there! Trends Neurosci. 29, 132-139 (2006).
44. Bystron, I., Blakemore, C. & Rakic, P. Development of the human cerebral cortex: Boulder Committee revisited. Nat. Rev. Neurosci. 9, 110-122 (2008).
45. Rashid, S. T. et al. Modeling inherited metabolic disorders of the liver using human induced pluripotent stem cells. J. Clin. Invest. 120, 3127-3136 (2010).
46. Vallier, L. et al. Signaling pathways controlling pluripotency and early cell fate decisions of human induced pluripotent stem cells. Stem Cells 27, 2655-2666 (2009).