Functional maturation of hPSC-derived forebrain interneurons requires an extended timeline and mimics human neural development

Cell Stem Cell

Volumn 12, Issue 5, 2013, Pages 573-586

  Nicholas, Cory R ^a   Chen, Jiadong ^a   Tang, Yunshuo ^b   Southwell, Derek G ^b,f   Chalmers, Nadine ^a   Vogt, Daniel ^a   Arnold, Christine M ^b   Chen, Ying Jiun J ^a   Stanley, Edouard G ^d,e   Elefanty, Andrew G ^d,e   Sasai, Yoshiki ^c   Alvarez Buylla, Arturo ^b   Rubenstein, John L R ^a   Kriegstein, Arnold R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c RIKEN Center for Biosystems Dynamics Research   (Japan)

^d ROYAL CHILDREN'S HOSPITAL   (Australia)

^e MONASH UNIVERSITY   (Australia)

^f STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALBINDIN; TRANSCRIPTION FACTOR NKX2.2;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; BRAIN ELECTROPHYSIOLOGY; CELL MATURATION; CONTROLLED STUDY; DEMYELINATING DISEASE; DOWN REGULATION; EMBRYO; FETUS; FETUS DEVELOPMENT; FIBROBLAST; FOREBRAIN; GABAERGIC SYSTEM; GANGLION; GLOBUS PALLIDUS; HUMAN; HUMAN CELL; HYPOTHALAMUS; IN VITRO STUDY; INHIBITION KINETICS; INTERNEURON; MICROARRAY ANALYSIS; MITOSIS; MOUSE; NEOCORTEX; NERVE CELL DIFFERENTIATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; TELENCEPHALON;

ACTION POTENTIALS; ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL DIVISION; GABAERGIC NEURONS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HUMANS; INTERNEURONS; MEDIAN EMINENCE; MICE; NEURAL STEM CELLS; NEUROGENESIS; NEUROGLIA; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROSENCEPHALON; SYNAPSES; TELENCEPHALON; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 84877301288     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2013.04.005     Document Type: Article

References (45)

1. S.A. Anderson, O. Marín, C. Horn, K. Jennings, and J.L. Rubenstein Distinct cortical migrations from the medial and lateral ganglionic eminences Development 128 2001 353 363
2. J.M. Bráz, R. Sharif-Naeini, D. Vogt, A. Kriegstein, A. Alvarez-Buylla, J.L. Rubenstein, and A.I. Basbaum Forebrain GABAergic neuron precursors integrate into adult spinal cord and reduce injury-induced neuropathic pain Neuron 74 2012 663 675
3. S.J. Butt, M. Fuccillo, S. Nery, S. Noctor, A. Kriegstein, J.G. Corbin, and G. Fishell The temporal and spatial origins of cortical interneurons predict their physiological subtype Neuron 48 2005 591 604
4. S.M. Chambers, C.A. Fasano, E.P. Papapetrou, M. Tomishima, M. Sadelain, and L. Studer Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling Nat. Biotechnol. 27 2009 275 280
5. H.T. Chao, H. Chen, R.C. Samaco, M. Xue, M. Chahrour, J. Yoo, J.L. Neul, S. Gong, H.C. Lu, and N. Heintz Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes Nature 468 2010 263 269
6. C.S. Cheah, F.H. Yu, R.E. Westenbroek, F.K. Kalume, J.C. Oakley, G.B. Potter, J.L. Rubenstein, and W.A. Catterall Specific deletion of NaV1.1 sodium channels in inhibitory interneurons causes seizures and premature death in a mouse model of Dravet syndrome Proc. Natl. Acad. Sci. USA 109 2012 14646 14651
7. I. Cobos, M.E. Calcagnotto, A.J. Vilaythong, M.T. Thwin, J.L. Noebels, S.C. Baraban, and J.L. Rubenstein Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy Nat. Neurosci. 8 2005 1059 1068
8. N.C. de Lanerolle, J.H. Kim, A. Williamson, S.S. Spencer, H.P. Zaveri, T. Eid, and D.D. Spencer A retrospective analysis of hippocampal pathology in human temporal lobe epilepsy: evidence for distinctive patient subcategories Epilepsia 44 2003 677 687
9. M. Eiraku, K. Watanabe, M. Matsuo-Takasaki, M. Kawada, S. Yonemura, M. Matsumura, T. Wataya, A. Nishiyama, K. Muguruma, and Y. Sasai Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals Cell Stem Cell 3 2008 519 532
10. Y. Elkabetz, G. Panagiotakos, G. Al Shamy, N.D. Socci, V. Tabar, and L. Studer Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage Genes Dev. 22 2008 152 165
11. I. Espuny-Camacho, K.A. Michelsen, D. Gall, D. Linaro, A. Hasche, J. Bonnefont, C. Bali, D. Orduz, A. Bilheu, and A. Herpoel Pyramidal neurons derived from human pluripotent stem cells integrate efficiently into mouse brain circuits in vivo Neuron 77 2013 440 456
12. P. Fazzari, A.V. Paternain, M. Valiente, R. Pla, R. Luján, K. Lloyd, J. Lerma, O. Marín, and B. Rico Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling Nature 464 2010 1376 1380
13. S. Fertuzinhos, Z. Krsnik, Y.I. Kawasawa, M.R. Rasin, K.Y. Kwan, J.G. Chen, M. Judas, M. Hayashi, and N. Sestan Selective depletion of molecularly defined cortical interneurons in human holoprosencephaly with severe striatal hypoplasia Cereb. Cortex 19 2009 2196 2207
14. S.A. Fietz, I. Kelava, J. Vogt, M. Wilsch-Bräuninger, D. Stenzel, J.L. Fish, D. Corbeil, A. Riehn, W. Distler, R. Nitsch, and W.B. Huttner OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling Nat. Neurosci. 13 2010 690 699
15. E.M. Goldberg, H.Y. Jeong, I. Kruglikov, R. Tremblay, R.M. Lazarenko, and B. Rudy Rapid developmental maturation of neocortical FS cell intrinsic excitability Cereb. Cortex 21 2011 666 682
16. A.L. Goulburn, D. Alden, R.P. Davis, S.J. Micallef, E.S. Ng, Q.C. Yu, S.M. Lim, C.L. Soh, D.A. Elliott, and T. Hatzistavrou A targeted NKX2.1 human embryonic stem cell reporter line enables identification of human basal forebrain derivatives Stem Cells 29 2011 462 473
17. D.V. Hansen, J.H. Lui, P.R. Parker, and A.R. Kriegstein Neurogenic radial glia in the outer subventricular zone of human neocortex Nature 464 2010 554 561
18. M.A. Johnson, J.P. Weick, R.A. Pearce, and S.C. Zhang Functional neural development from human embryonic stem cells: accelerated synaptic activity via astrocyte coculture J. Neurosci. 27 2007 3069 3077
19. J.E. Kim, M.L. O'Sullivan, C.A. Sanchez, M. Hwang, M.A. Israel, K. Brennand, T.J. Deerinck, L.S. Goldstein, F.H. Gage, M.H. Ellisman, and A. Ghosh Investigating synapse formation and function using human pluripotent stem cell-derived neurons Proc. Natl. Acad. Sci. USA 108 2011 3005 3010
20. C. Kim, J. Wong, J. Wen, S. Wang, C. Wang, S. Spiering, N.G. Kan, S. Forcales, P.L. Puri, and T.C. Leone Studying arrhythmogenic right ventricular dysplasia with patient-specific iPSCs Nature 494 2013 105 110
21. A.R. Kriegstein, and M. Götz Radial glia diversity: a matter of cell fate Glia 43 2003 37 43
22. C. Le Magueresse, and H. Monyer GABAergic interneurons shape the functional maturation of the cortex Neuron 77 2013 388 405
23. X.J. Li, X. Zhang, M.A. Johnson, Z.B. Wang, T. Lavaute, and S.C. Zhang Coordination of sonic hedgehog and Wnt signaling determines ventral and dorsal telencephalic neuron types from human embryonic stem cells Development 136 2009 4055 4063
24. J.H. Lui, D.V. Hansen, and A.R. Kriegstein Development and evolution of the human neocortex Cell 146 2011 18 36
25. L. Ma, B. Hu, Y. Liu, S.C. Vermilyea, H. Liu, L. Gao, Y. Sun, X. Zhang, and S.C. Zhang Human embryonic stem cell-derived GABA neurons correct locomotion deficits in quinolinic acid-lesioned mice Cell Stem Cell 10 2012 455 464
26. H. Markram, M. Toledo-Rodriguez, Y. Wang, A. Gupta, G. Silberberg, and C. Wu Interneurons of the neocortical inhibitory system Nat. Rev. Neurosci. 5 2004 793 807
27. A.M. Maroof, K. Brown, S.H. Shi, L. Studer, and S.A. Anderson Prospective isolation of cortical interneuron precursors from mouse embryonic stem cells J. Neurosci. 30 2010 4667 4675
28. V. Martínez-Cerdeño, S.C. Noctor, A. Espinosa, J. Ariza, P. Parker, S. Orasji, M.M. Daadi, K. Bankiewicz, A. Alvarez-Buylla, and A.R. Kriegstein Embryonic MGE precursor cells grafted into adult rat striatum integrate and ameliorate motor symptoms in 6-OHDA-lesioned rats Cell Stem Cell 6 2010 238 250
29. G. Miyoshi, S.J. Butt, H. Takebayashi, and G. Fishell Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-expressing precursors J. Neurosci. 27 2007 7786 7798
30. A.R. Moore, R. Filipovic, Z. Mo, M.N. Rasband, N. Zecevic, and S.D. Antic Electrical excitability of early neurons in the human cerebral cortex during the second trimester of gestation Cereb. Cortex 19 2009 1795 1805
31. S. Nóbrega-Pereira, D. Gelman, G. Bartolini, R. Pla, A. Pierani, and O. Marín Origin and molecular specification of globus pallidus neurons J. Neurosci. 30 2010 2824 2834
32. M. Rallu, J.G. Corbin, and G. Fishell Parsing the prosencephalon Nat. Rev. Neurosci. 3 2002 943 951
33. R.J. Robbins, M.L. Brines, J.H. Kim, T. Adrian, N. de Lanerolle, S. Welsh, and D.D. Spencer A selective loss of somatostatin in the hippocampus of patients with temporal lobe epilepsy Ann. Neurol. 29 1991 325 332
34. T. Schmandt, E. Meents, G. Gossrau, V. Gornik, S. Okabe, and O. Brüstle High-purity lineage selection of embryonic stem cell-derived neurons Stem Cells Dev. 14 2005 55 64
35. Y. Shi, P. Kirwan, J. Smith, H.P. Robinson, and F.J. Livesey Human cerebral cortex development from pluripotent stem cells to functional excitatory synapses Nat. Neurosci. 15 2012 477 486 S1
36. K. Shimamura, and J.L. Rubenstein Inductive interactions direct early regionalization of the mouse forebrain Development 124 1997 2709 2718
37. V.H. Sousa, G. Miyoshi, J. Hjerling-Leffler, T. Karayannis, and G. Fishell Characterization of Nkx6-2-derived neocortical interneuron lineages Cereb. Cortex 19 Suppl 1 2009 i1 i10
38. D.G. Southwell, R.C. Froemke, A. Alvarez-Buylla, M.P. Stryker, and S.P. Gandhi Cortical plasticity induced by inhibitory neuron transplantation Science 327 2010 1145 1148
39. D.G. Southwell, M.F. Paredes, R.P. Galvao, D.L. Jones, R.C. Froemke, J.Y. Sebe, C. Alfaro-Cervello, Y. Tang, J.M. Garcia-Verdugo, and J.L. Rubenstein Intrinsically determined cell death of developing cortical interneurons Nature 491 2012 109 113
40. L. Verret, E.O. Mann, G.B. Hang, A.M. Barth, I. Cobos, K. Ho, N. Devidze, E. Masliah, A.C. Kreitzer, and I. Mody Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model Cell 149 2012 708 721
41. Y. Wang, G. Li, A. Stanco, J.E. Long, D. Crawford, G.B. Potter, S.J. Pleasure, T. Behrens, and J.L. Rubenstein CXCR4 and CXCR7 have distinct functions in regulating interneuron migration Neuron 69 2011 61 76
42. K. Watanabe, M. Ueno, D. Kamiya, A. Nishiyama, M. Matsumura, T. Wataya, J.B. Takahashi, S. Nishikawa, S. Nishikawa, K. Muguruma, and Y. Sasai A ROCK inhibitor permits survival of dissociated human embryonic stem cells Nat. Biotechnol. 25 2007 681 686
43. H. Wichterle, D.H. Turnbull, S. Nery, G. Fishell, and A. Alvarez-Buylla In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain Development 128 2001 3759 3771
44. A.V. Zaitsev, N.V. Povysheva, G. Gonzalez-Burgos, D. Rotaru, K.N. Fish, L.S. Krimer, and D.A. Lewis Interneuron diversity in layers 2-3 of monkey prefrontal cortex Cereb. Cortex 19 2009 1597 1615
45. Y. Zhao, P. Flandin, J.E. Long, M.D. Cuesta, H. Westphal, and J.L. Rubenstein Distinct molecular pathways for development of telencephalic interneuron subtypes revealed through analysis of Lhx6 mutants J. Comp. Neurol. 510 2008 79 99