Directed Differentiation and Functional Maturation of Cortical Interneurons from Human Embryonic Stem Cells
Open accessAbstract
Human pluripotent stem cells are a powerful tool for modeling brain development and disease. The human cortex is composed of two major neuronal populations: projection neurons and local interneurons. Cortical interneurons comprise a diverse class of cell types expressing the neurotransmitter GABA. Dysfunction of cortical interneurons has been implicated in neuropsychiatric diseases, including schizophrenia, autism, and epilepsy. Here, we demonstrate the highly efficient derivation of human cortical interneurons in an NKX2.1::GFP human embryonic stem cell reporter line. Manipulating the timing of SHH activation yields three distinct GFP+ populations with specific transcriptional profiles, neurotransmitter phenotypes, and migratory behaviors. Further differentiation in a murine cortical environment yields parvalbumin- and somatostatin-expressing neurons that exhibit synaptic inputs and electrophysiological properties of cortical interneurons. Our study defines the signals sufficient for modeling human ventral forebrain development in vitro and lays the foundation for studying cortical interneuron involvement in human disease pathology.
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Human PSC-derived pyramidal cortical neurons and interneurons transplanted in the mouse brain develop morphologically and synaptically within their host.
“Human PSC-derived pyramidal cortical neurons and interneurons transplanted in the mouse brain develop morphologically and synaptically within their host”
From Xenotransplanted human cortical neurons reveal species-specific development and functional integration into mouse visual circuits (2019) · cites this paper as Maroof et al., 2013
The Results section on neuronal differentiation and migration reports that transplanted human interneuron precursors migrated within the mouse cortex, but most retained immature morphologies at 1–2 months and had not become mature interneurons. The Discussion reports limited integration at three months; synaptic activity was demonstrated in vitro, not in the transplanted cells. The paper does not report transplanting human PSC-derived pyramidal neurons. (LLM, conf=0.88)
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Experimental — accuracy not yet measuredXenotransplantation of human neurons into the mouse brain can provide a means to study human neuronal maturation under more physiologically realistic conditions.
“xenotransplantation of human neurons into the mouse brain, which can provide a means to study human neuronal maturation under more physiologically realistic conditions”
From Xenotransplanted human cortical neurons reveal species-specific development and functional integration into mouse visual circuits (2019) · cites this paper as Maroof et al., 2013
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Alzheimer's Disease and Senile Dementia: Loss of Neurons in the Basal Forebrain
Whitehouse, P., Price, D., Struble, R., Clark, A., Coyle, J., & DeLong, M. R. (1982) · Science · doi:10.1126/science.7058341 · Cited by 3,627 · see citing works
Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling
Chambers, S. M., Fasano, C. A., Papapetrou, E. P., Tomishima, M., Sadelain, M., & Studer, L. (2009) · Nature Biotechnology · doi:10.1038/nbt.1529 · Cited by 3,620 · see citing works
Self-citationCortical inhibitory neurons and schizophrenia
Lewis, D. A., Hashimoto, T., & Volk, D. W. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1648 · Cited by 2,297 · see citing works
Eiraku, M., Watanabe, K., Matsuo-Takasaki, M., Kawada, M., Yonemura, S., Matsumura, M., Wataya, T., Nishiyama, A., Muguruma, K., & Sasai, Y. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2008.09.002 · Cited by 1,522 · see citing works
Sussel, L., Marin, O., Kimura, S., & Rubenstein, J. L. R. (1999) · Development · doi:10.1242/dev.126.15.3359 · Cited by 873 · see citing works
Origins of Cortical Interneuron Subtypes
Xu, Q., Cobos, I., De La Cruz, E., Rubenstein, J. L., & Anderson, S. A. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5667-03.2004 · Cited by 639 · see citing works
Self-citationFlames, N., Pla, R., Gelman, D. M., Rubenstein, J. L. R., Puelles, L., & Marín, O. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2750-07.2007 · Cited by 560 · see citing works
Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling
Fazzari, P., Paternain, A. V., Valiente, M., Pla, R., Luján, R., Lloyd, K., Lerma, J., Marín, O., & Rico, B. (2010) · Nature · doi:10.1038/nature08928 · Cited by 501 · see citing works
Johnson, M. A., Weick, J. P., Pearce, R. A., & Zhang, S.-C. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4562-06.2007 · Cited by 318 · see citing works
Papapetrou, E. P., Tomishima, M. J., Chambers, S. M., Mica, Y., Reed, E., Menon, J., Tabar, V., Mo, Q., Studer, L., & Sadelain, M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904825106 · Cited by 286 · see citing works
Self-citationCortical Plasticity Induced by Inhibitory Neuron Transplantation
Southwell, D. G., Froemke, R. C., Alvarez-Buylla, A., Stryker, M. P., & Gandhi, S. P. (2010) · Science · doi:10.1126/science.1183962 · Cited by 271 · see citing works
Xu, Q., Guo, L., Moore, H., Waclaw, R. R., Campbell, K., & Anderson, S. A. (2010) · Neuron · doi:10.1016/j.neuron.2010.01.004 · Cited by 218 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 42
- Anderson SA Classey JD Conde F Lund JS Lewis DA 1995 Synchronous development of pyramidal neuron dendritic spines and parvalbumin-immunoreactive chandelier neuron axon terminals in layer III of monkey prefrontal cortex Neuroscience 67 7 22 7477911
- Anderson SA Eisenstat DD Shi L Rubenstein JL 1997 Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes Science 278 474 476 9334308
- Anderson SA Marin O Horn C Jennings K Rubenstein JL 2001 Distinct cortical migrations from the medial and lateral ganglionic eminences Development 128 353 363 11152634
- Baraban SC Southwell DG Estrada RC Jones DL Sebe JY Alfaro-Cervello C Garcia-Verdugo JM Rubenstein JL Alvarez-Buylla A 2009 Reduction of seizures by transplantation of cortical GABAergic interneuron precursors into Kv1.1 mutant mice Proceedings of the National Academy of Sciences of the United States of America 106 15472 15477 19706400 PMC2741275
- Batista-Brito R Fishell G 2009 The developmental integration of cortical interneurons into a functional network Curr Top Dev Biol 87 81 118 19427517 PMC4465088
- Brennand KJ Simone A Jou J Gelboin-Burkhart C Tran N Sangar S Li Y Mu Y Chen G Yu D 2011 Modelling schizophrenia using human induced pluripotent stem cells Nature 473 221 225 21490598 PMC3392969
- Dimos JT Rodolfa KT Niakan KK Weisenthal LM Mitsumoto H Chung W Croft GF Saphier G Leibel R Goland R 2008 Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons Science 321 1218 1221 18669821
- Ebert AD Yu J Rose FF Jr Mattis VB Lorson CL Thomson JA Svendsen CN 2009 Induced pluripotent stem cells from a spinal muscular atrophy patient Nature 457 277 280 19098894 PMC2659408
- Espuny-Camacho I Michelsen Kimmo A Gall D Linaro D Hasche A Bonnefont J Bali C Orduz D Bilheu A Herpoel A 2013 Pyramidal Neurons Derived from Human Pluripotent Stem Cells Integrate Efficiently into Mouse Brain Circuits In Vivo Neuron 77 440 456 23395372
- Fasano CA Chambers SM Lee G Tomishima MJ Studer L 2010 Efficient Derivation of Functional Floor Plate Tissue from Human Embryonic Stem Cells Cell Stem Cell 6 336 347 20362538 PMC4336800
- Fertuzinhos S Krsnik Z Kawasawa YI Rasin MR Kwan KY Chen JG Judas M Hayashi M Sestan N 2009 Selective Depletion of Molecularly Defined Cortical Interneurons in Human Holoprosencephaly with Severe Striatal Hypoplasia Cereb Cortex PMC2722430 19234067
- Fogarty M Grist M Gelman D Marin O Pachnis V Kessaris N 2007 Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex Journal of Neuroscience 27 10935 10946 17928435 PMC6672847
- Gaspard N Bouschet T Hourez R Dimidschstein J Naeije G van den Ameele J Espuny-Camacho I Herpoel A Passante L Schiffmann SN 2008 An intrinsic mechanism of corticogenesis from embryonic stem cells Nature 455 351 357 18716623
- Goulburn AL Alden D Davis RP Micallef SJ Ng ES Yu QC Lim SM Soh CL Elliott DA Hatzistavrou T 2011 A targeted NKX2.1 human embryonic stem cell reporter line enables identification of human basal forebrain derivatives Stem Cells 29 462 473 21425409
- Huang SM Mishina YM Liu S Cheung A Stegmeier F Michaud GA Charlat O Wiellette E Zhang Y Wiessner S 2009 Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling Nature 461 614 620 19759537
- Insel TR 2010 Rethinking schizophrenia Nature 468 187 193 21068826
- Kelly S Bliss TM Shah AK Sun GH Ma M Foo WC Masel J Yenari MA Weissman IL Uchida N 2004 Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex Proc Natl Acad Sci U S A 101 11839 11844 15280535 PMC511061
- Kerwin J Yang Y Merchan P Sarma S Thompson J Wang X Sandoval J Puelles L Baldock R Lindsay S 2010 The HUDSEN Atlas: a three-dimensional (3D) spatial framework for studying gene expression in the developing human brain J Anat 217 289 299 20979583 PMC2967454
- Kim H Lee G Ganat Y Papapetrou EP Lipchina I Socci ND Sadelain M Studer L 2011 miR-371-3 Expression Predicts Neural Differentiation Propensity in Human Pluripotent Stem Cells Cell Stem Cell 8 695 706 21624813
- Kriks S Shim JW Piao J Ganat YM Wakeman DR Xie Z Carrillo-Reid L Auyeung G Antonacci C Buch A 2011 Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson’s disease Nature 480 547 551 22056989 PMC3245796
- Lamba DA Karl MO Ware CB Reh TA 2006 Efficient generation of retinal progenitor cells from human embryonic stem cells Proc Natl Acad Sci U S A 103 12769 12774 16908856 PMC1568922
- Letinic K Zoncu R Rakic P 2002 Origin of GABAergic neurons in the human neocortex Nature 417 645 649 12050665
- Ma L Hu B Liu Y Vermilyea SC Liu H Gao L Sun Y Zhang X Zhang SC 2012 Human Embryonic Stem Cell-Derived GABA Neurons Correct Locomotion Deficits in Quinolinic Acid-Lesioned Mice Cell Stem Cell 10 455 464 22424902 PMC3322292
- Marchetto MC Carromeu C Acab A Yu D Yeo GW Mu Y Chen G Gage FH Muotri AR 2010 A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells Cell 143 527 539 21074045 PMC3003590
- Marin O Anderson SA Rubenstein JL 2000 Origin and molecular specification of striatal interneurons The Journal of neuroscience: the official journal of the Society for Neuroscience 20 6063 6076 10934256 PMC6772576
- Maroof AM Brown K Shi SH Studer L Anderson SA 2010 Prospective Isolation of Cortical Interneuron Precursors from Mouse Embryonic Stem Cells Journal of Neuroscience 30 4667 4675 20357117 PMC2868507
- Martinez-Cerdeno V Noctor SC Espinosa A Ariza J Parker P Orasji S Daadi MM Bankiewicz K Alvarez-Buylla A Kriegstein AR 2010 Embryonic MGE precursor cells grafted into adult rat striatum integrate and ameliorate motor symptoms in 6-OHDA-lesioned rats Cell Stem Cell 6 238 250 20207227 PMC4075336
- Pasca SP Portmann T Voineagu I Yazawa M Shcheglovitov A Pasca AM Cord B Palmer TD Chikahisa S Nishino S 2011 Using iPSC-derived neurons to uncover cellular phenotypes associated with Timothy syndrome Nat Med 17 1657 1662 22120178 PMC3517299
- Penagarikano O Abrahams BS Herman EI Winden KD Gdalyahu A Dong H Sonnenblick LI Gruver R Almajano J Bragin A 2011 Absence of CNTNAP2 leads to epilepsy, neuronal migration abnormalities, and core autism-related deficits Cell 147 235 246 21962519 PMC3390029
- Placzek M Briscoe J 2005 The floor plate: multiple cells, multiple signals Nat Rev Neurosci 6 230 240 15738958
- Rakic S Zecevic N 2003 Emerging complexity of layer I in human cerebral cortex Cereb Cortex 13 1072 1083 12967924
- Shi Y Kirwan P Smith J Robinson HP Livesey FJ 2012 Human cerebral cortex development from pluripotent stem cells to functional excitatory synapses Nat Neurosci 15 477 486 S471 22306606 PMC3882590
- Tekki-Kessaris N Woodruff R Hall AC Gaffield W Kimura S Stiles CD Rowitch DH Richardson WD 2001 Hedgehog-dependent oligodendrocyte lineage specification in the telencephalon Development 128 2545 2554 11493571
- Watanabe K Kamiya D Nishiyama A Katayama T Nozaki S Kawasaki H Watanabe Y Mizuseki K Sasai Y 2005 Directed differentiation of telencephalic precursors from embryonic stem cells Nat Neurosci 8 288 296 15696161
- Wichterle H Garcia-Verdugo JM Herrera DG Alvarez-Buylla A 1999 Young neurons from medial ganglionic eminence disperse in adult and embryonic brain Nat Neurosci 2 461 466 10321251
- Wonders CP Taylor L Welagen J Mbata IC Xiang JZ Anderson SA 2008 A spatial bias for the origins of interneuron subgroups within the medial ganglionic eminence Dev Biol 314 127 136 18155689 PMC2727678
- Wu H Xu J Pang ZP Ge W Kim KJ Blanchi B Chen C Sudhof TC Sun YE 2007 Integrative genomic and functional analyses reveal neuronal subtype differentiation bias in human embryonic stem cell lines Proc Natl Acad Sci U S A 104 13821 13826 17693548 PMC1959466
- Yee CL Wang Y Anderson S Ekker M Rubenstein JL 2009 Arcuate nucleus expression of NKX2.1 and DLX and lineages expressing these transcription factors in neuropeptide Y(+), proopiomelanocortin(+), and tyrosine hydroxylase(+) neurons in neonatal and adult mice J Comp Neurol 517 37 50 19711380 PMC3021751
- Ying SW Jia F Abbas SY Hofmann F Ludwig A Goldstein PA 2007 Dendritic HCN2 channels constrain glutamate-driven excitability in reticular thalamic neurons Journal of Neuroscience 27 8719 8732 17687049 PMC6672930
- Yu X Zecevic N 2011 Dorsal radial glial cells have the potential to generate cortical interneurons in human but not in mouse brain Journal of Neuroscience 31 2413 2420 21325508 PMC3079257
- Yuan SH Martin J Elia J Flippin J Paramban RI Hefferan MP Vidal JG Mu Y Killian RL Israel MA 2011 Cell-surface marker signatures for the isolation of neural stem cells, glia and neurons derived from human pluripotent stem cells PLoS One 6 e17540 21407814 PMC3047583
- Zecevic N Hu F Jakovcevski I 2011 Interneurons in the developing human neocortex Dev Neurobiol 71 18 33 21154907 PMC3117059
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Rapid single-step induction of functional neurons from human pluripotent stem cells
Zhang, Y., Pak, C., Han, Y., Ahlenius, H., Zhang, Z., Chanda, S., Marro, S., Patzke, C., Acuna, C., Covy, J., et al. (2013) · Neuron · doi:10.1016/j.neuron.2013.05.029 · Cited by 1,644 · see citing works
Assembly of functionally integrated human forebrain spheroids
Birey, F., Andersen, J., Makinson, C. D., Islam, S., Wei, W., Huber, N., Fan, H. C., Metzler, K. R. C., Panagiotakos, G., Thom, N., et al. (2017) · Nature · doi:10.1038/nature22330 · Cited by 1,365 · see citing works
Hippocampal GABAergic Inhibitory Interneurons
Pelkey, K. A., Chittajallu, R., Craig, M. T., Tricoire, L., Wester, J. C., & McBain, C. J. (2017) · Physiological Reviews · doi:10.1152/physrev.00007.2017 · Cited by 889 · see citing works
Fused cerebral organoids model interactions between brain regions
Bagley, J. A., Reumann, D., Bian, S., Lévi-Strauss, J., & Knoblich, J. A. (2017) · Nature Methods · doi:10.1038/nmeth.4304 · Cited by 790 · see citing works
A viral strategy for targeting and manipulating interneurons across vertebrate species
Dimidschstein, J., Chen, Q., Tremblay, R., Rogers, S. L., Saldi, G.-A., Guo, L., Xu, Q., Liu, R., Lu, C., Chu, J., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4430 · Cited by 541 · see citing works
Self-citationModeling Alzheimer’s disease with iPSC-derived brain cells
Penney, J., Ralvenius, W. T., & Tsai, L.-H. (2020) · Molecular Psychiatry · doi:10.1038/s41380-019-0468-3 · Cited by 471 · see citing works
Generation of pure GABAergic neurons by transcription factor programming
Yang, N., Chanda, S., Marro, S., Ng, Y.-H., Janas, J. A., Haag, D., Ang, C. E., Tang, Y., Flores, Q., Mall, M., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4291 · Cited by 341 · see citing works
Building Models of Brain Disorders with Three-Dimensional Organoids
Amin, N. D., & Paşca, S. P. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.007 · Cited by 312 · see citing works
Neural Subtype Specification from Human Pluripotent Stem Cells
Tao, Y., & Zhang, S.-C. (2016) · Cell Stem Cell · doi:10.1016/j.stem.2016.10.015 · Cited by 287 · see citing works
Early emergence of cortical interneuron diversity in the mouse embryo
Mi, D., Li, Z., Lim, L., Li, M., Moissidis, M., Yang, Y., Gao, T., Hu, T. X., Pratt, T., Price, D. J., et al. (2018) · Science · doi:10.1126/science.aar6821 · Cited by 259 · see citing works
Qi, Y., Zhang, X.-J., Renier, N., Wu, Z., Atkin, T., Sun, Z., Ozair, M. Z., Tchieu, J., Zimmer, B., Fattahi, F., et al. (2017) · Nature Biotechnology · doi:10.1038/nbt.3777 · Cited by 248 · see citing works
Self-citationAn epigenetic barrier sets the timing of human neuronal maturation
Ciceri, G., Baggiolini, A., Cho, H. S., Kshirsagar, M., Benito-Kwiecinski, S., Walsh, R. M., Aromolaran, K. A., Gonzalez-Hernandez, A. J., Munguba, H., Koo, S. Y., et al. (2024) · Nature · doi:10.1038/s41586-023-06984-8 · Cited by 240 · see citing works
Self-citationTchieu, J., Calder, E. L., Guttikonda, S. R., Gutzwiller, E. M., Aromolaran, K. A., Steinbeck, J. A., Goldstein, P. A., & Studer, L. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0035-0 · Cited by 231 · see citing works
Self-citationCunningham, M., Cho, J.-H., Leung, A., Savvidis, G., Ahn, S., Moon, M., Lee, P. K. J., Han, J. J., Azimi, N., Kim, K.-S., et al. (2014) · Cell Stem Cell · doi:10.1016/j.stem.2014.10.006 · Cited by 218 · see citing works
Linaro, D., Vermaercke, B., Iwata, R., Ramaswamy, A., Davis, B. A., Boubakar, L., Libé-Philippot, B., Bilheu, A., Bruyne, L. D., Gall, D., et al. (2019) · doi:10.1101/626218 · Cited by 210 · see citing works
“We and others previously reported a prolonged timeline of morphological development for transplanted human cortical neurons that was proposed to be in line with human cortical neoteny (Anderson and Vanderhaeghen, 2014; Espuny-Camacho et al., 2013; Maroof et al., 2013; Nicholas et al., 2013).”
BackgroundIntegration of GABAergic interneurons into cortical cell assemblies: lessons from embryos and adults
Bartolini, G., Ciceri, G., & Marín, O. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.014 · Cited by 185 · see citing works
Loss of SATB1 Induces p21-Dependent Cellular Senescence in Post-mitotic Dopaminergic Neurons
Riessland, M., Kolisnyk, B., Kim, T. W., Cheng, J., Ni, J., Pearson, J. A., Park, E. J., Dam, K., Acehan, D., Ramos-Espiritu, L. S., et al. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.08.013 · Cited by 180 · see citing works
Self-citationSHANK2 mutations associated with autism spectrum disorder cause hyperconnectivity of human neurons
Zaslavsky, K., Zhang, W.-B., McCready, F. P., Rodrigues, D. C., Deneault, E., Loo, C., Zhao, M., Ross, P. J., El Hajjar, J., Romm, A., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0365-8 · Cited by 174 · see citing works
Developmental mechanisms underlying the evolution of human cortical circuits
Vanderhaeghen, P., & Polleux, F. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00675-z · Cited by 173 · see citing works
Primary Cilia Signaling Shapes the Development of Interneuronal Connectivity
Guo, J., Otis, J. M., Higginbotham, H., Monckton, C., Cheng, J., Asokan, A., Mykytyn, K., Caspary, T., Stuber, G. D., & Anton, E. S. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.07.010 · Cited by 136 · see citing works
Sun, Y., Paşca, S. P., Portmann, T., Goold, C., Worringer, K. A., Guan, W., Chan, K. C., Gai, H., Vogt, D., Chen, Y.-J. J., et al. (2016) · eLife · doi:10.7554/elife.13073 · Cited by 141 · see citing works
Lhx6 directly regulates Arx and CXCR7 to determine cortical interneuron fate and laminar position
Vogt, D., Hunt, R. F., Mandal, S., Sandberg, M., Silberberg, S. N., Nagasawa, T., Yang, Z., Baraban, S. C., & Rubenstein, J. L. R. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.030 · Cited by 129 · see citing works
Stem cell models of Alzheimer’s disease: progress and challenges
Arber, C., Lovejoy, C., & Wray, S. (2017) · Alzheimer's Research & Therapy · doi:10.1186/s13195-017-0268-4 · Cited by 143 · see citing works
Jung, K. B., Lee, H., Son, Y. S., Lee, M.-O., Kim, Y.-D., Oh, S. J., Kwon, O., Cho, S., Cho, H.-S., Kim, D.-S., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05450-8 · Cited by 125 · see citing works
Is this a brain which I see before me? Modeling human neural development with pluripotent stem cells
Suzuki, I. K., & Vanderhaeghen, P. (2015) · Development · doi:10.1242/dev.120568 · Cited by 110 · see citing works
Thinking out of the dish: what to learn about cortical development using pluripotent stem cells
van den Ameele, J., Tiberi, L., Vanderhaeghen, P., & Espuny-Camacho, I. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.03.005 · Cited by 110 · see citing works
Lee, D. S., Chen, J.-H., Lundy, D. J., Liu, C.-H., Hwang, S.-M., Pabon, L., Shieh, R.-C., Chen, C.-C., Wu, S.-N., Yan, Y.-T., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.08.042 · Cited by 91 · see citing works
Espuny-Camacho, I., Michelsen, K. A., Linaro, D., Bilheu, A., Acosta-Verdugo, S., Herpoel, A., Giugliano, M., Gaillard, A., & Vanderhaeghen, P. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.04.094 · Cited by 88 · see citing works
Rosebrock, D., Arora, S., Mutukula, N., Volkman, R., Gralinska, E., Balaskas, A., Aragonés Hernández, A., Buschow, R., Brändl, B., Müller, F.-J., et al. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-00929-5 · Cited by 89 · see citing works
Loss of MECP2 Leads to Activation of P53 and Neuronal Senescence
Ohashi, M., Korsakova, E., Allen, D., Lee, P., Fu, K., Vargas, B. S., Cinkornpumin, J., Salas, C., Park, J. C., Germanguz, I., et al. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.04.001 · Cited by 80 · see citing works
Modeling psychiatric disorders with patient-derived iPSCs
Wen, Z., Christian, K. M., Song, H., & Ming, G.-L. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.11.003 · Cited by 84 · see citing works
Human neuronal maturation comes of age: cellular mechanisms and species differences
Wallace, J. L., & Pollen, A. A. (2024) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00760-3 · Cited by 82 · see citing works
Cellular and Molecular Mechanisms Linking Human Cortical Development and Evolution
Libé-Philippot, B., & Vanderhaeghen, P. (2021) · Annual Review of Genetics · doi:10.1146/annurev-genet-071719-020705 · Cited by 78 · see citing works
Rubin, A. N., & Kessaris, N. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077339 · Cited by 69 · see citing works
Optimizing neuronal differentiation from induced pluripotent stem cells to model ASD
Kim, D.-S., Ross, P. J., Zaslavsky, K., & Ellis, J. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00109 · Cited by 70 · see citing works
Genome Editing in iPSC-Based Neural Systems: From Disease Models to Future Therapeutic Strategies
McTague, A., Rossignoli, G., Ferrini, A., Barral, S., & Kurian, M. A. (2021) · Frontiers in Genome Editing · doi:10.3389/fgeed.2021.630600 · Cited by 67 · see citing works
A Guide to Generating and Using hiPSC Derived NPCs for the Study of Neurological Diseases
Topol, A., Tran, N. N., & Brennand, K. J. (2015) · Journal of Visualized Experiments · doi:10.3791/52495 · Cited by 58 · see citing works
Cortical neurogenesis from pluripotent stem cells: complexity emerging from simplicity
Anderson, S., & Vanderhaeghen, P. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.03.012 · Cited by 40 · see citing works
Self-citationEvolving toward a human-cell based and multiscale approach to drug discovery for CNS disorders
Schadt, E. E., Buchanan, S., Brennand, K. J., & Merchant, K. M. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00252 · Cited by 39 · see citing works
Altered patterning of trisomy 21 interneuron progenitors
Giffin-Rao, Y., Sheng, J., Strand, B., Xu, K., Huang, L., Medo, M., Risgaard, K. A., Dantinne, S., Mohan, S., Keshan, A., et al. (2022) · Stem Cell Reports · doi:10.1016/j.stemcr.2022.05.001 · Cited by 38 · see citing works
Duong, T. T., Lim, J., Vasireddy, V., Papp, T., Nguyen, H., Leo, L., Pan, J., Zhou, S., Chen, H. I., Bennett, J., et al. (2019) · Stem Cells International · doi:10.1155/2019/7281912 · Cited by 33 · see citing works
Micali, N., Kim, S.-K., Diaz-Bustamante, M., Stein-O’Brien, G., Seo, S., Shin, J.-H., Rash, B. G., Ma, S., Wang, Y., Olivares, N. A., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107599 · Cited by 31 · see citing works
From Human Pluripotent Stem Cells to Cortical Circuits
Astick, M., & Vanderhaeghen, P. (2018) · Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2018.02.011 · Cited by 34 · see citing works
Flaherty, E. K., & Brennand, K. J. (2017) · Brain Research · doi:10.1016/j.brainres.2015.11.009 · Cited by 19 · see citing works
- Authors
- Maroof, A. M., Keros, S., Tyson, J. A., Ying, S.-W., Ganat, Y. M., Merkle, F. T., Liu, B., Goulburn, A., Stanley, E. G., Elefanty, A. G., Widmer, H. R., Eggan, K., Goldstein, P. A., Anderson, S. A., & Studer, L.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- Weill Cornell Medicine (US)
- Harvard University (US)
- Royal Children's Hospital (AU)
- Children's Hospital of Philadelphia (US)
- Corresponding author
- Anderson, Stewart A.
- Studer, Lorenz
- ORCID
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2013-05
- Volume
- 12
- Issue
- 5
- Pages
- 559-572
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- PMC
- PMC3681523
- OpenAlex
- W2003835684
- Cited by
- 596
- References
- 12
- Citations by year
- 2026: 26 · 2025: 28 · 2024: 49 · 2023: 27 · 2022: 27 · 2021: 52 · 2020: 51 · 2019: 54 · 2018: 40 · 2017: 61 · 2016: 55 · 2015: 57 · 2014: 47 · 2013: 22
- FWCI
- 27.04
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell stem cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- BORIS (University Library Bern) (submittedVersion)
- Apollo (University of Cambridge) (submittedVersion)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (135565)
- National Institutes of Health (5k12ns066274-10)
- National Institute of Mental Health (R01MH066912, RC1MH089690)
- National Cancer Institute (P30CA008748)
- National Institute of Neurological Disorders and Stroke (R01NS066390, K12-NS066274)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD060600)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- cortical interneurons, human embryonic stem cells, directed differentiation, Sonic hedgehog signaling, GABAergic neurons, parvalbumin, somatostatin, neuronal migration, schizophrenia, autism spectrum disorder, epilepsy
- MeSH terms
- Thyroid Nuclear Factor 1, Animals, Cell Cycle, Cell Differentiation, Cell Movement, Cerebral Cortex, Humans, Interneurons, Nuclear Proteins, Phenotype, Synapses, Time Factors, Transcription Factors, Signal Transduction, Cell Lineage, Excitatory Postsynaptic Potentials, Green Fluorescent Proteins, Wnt Proteins, Mice, Inhibitory Postsynaptic Potentials, Embryonic Stem Cells, Hedgehog Proteins, Neural Stem Cells, GABAergic Neurons, Feeder Cells
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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