Assembly of functionally integrated human forebrain spheroids
Open accessAbstract
The development of the nervous system involves a coordinated succession of events including the migration of GABAergic (γ-aminobutyric-acid-releasing) neurons from ventral to dorsal forebrain and their integration into cortical circuits. However, these interregional interactions have not yet been modelled with human cells. Here we generate three-dimensional spheroids from human pluripotent stem cells that resemble either the dorsal or ventral forebrain and contain cortical glutamatergic or GABAergic neurons. These subdomain-specific forebrain spheroids can be assembled in vitro to recapitulate the saltatory migration of interneurons observed in the fetal forebrain. Using this system, we find that in Timothy syndrome-a neurodevelopmental disorder that is caused by mutations in the Ca V 1.2 calcium channel-interneurons display abnormal migratory saltations. We also show that after migration, interneurons functionally integrate with glutamatergic neurons to form a microphysiological system. We anticipate that this approach will be useful for studying neural development and disease, and for deriving spheroids that resemble other brain regions to assemble circuits in vitro.
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Human brain organoids can replicate the complex brain microenvironment better than 2D in vitro models.
“With their 3D structures and cell components resembling the human brain, these organoids can replicate the complex brain microenvironment better than 2D in vitro models (15–17, 19)”
From Understanding monocyte-driven neuroinflammation in Alzheimer’s disease using human cortical organoid microphysiological systems (2025) · cites this paper as [19]
The Discussion (page unavailable) says the assembled 3D forebrain spheroids have advantages over adherent methods and capture developmental processes, including interneuron migration. The Assembly of Forebrain Spheroids section (page unavailable) reports that migration was inefficient or absent when spheroids were plated on a coverslip. These findings support an advantage for this specific 3D model, but not the broader claim that human brain organoids generally replicate the complex brain microenvironment better than 2D models. (LLM, conf=0.83)
Experimental — accuracy not yet measuredThe extrinsic organoid model shows promise for better reproducibility.
“The ‘extrinsic’ organoid model whereby patterning is influenced by externally added molecules rather than relying on intrinsic self-organization shows promise with regard to better reproducibility5,6,25.”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [6]
Both studies demonstrated disruption of interneuron migration by antagonism of CXCR4.
“These findings were further supported by another report documenting interneuron migration following fusion of dorsal and ventral brain organoids26, and both studies demonstrated disruption of migration by antagonism of C-X-C chemokine receptor type 4 (CXCR4), which has an important role in interneuron migration6,26.”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [6]
In the dorsal-ventral fused model, cells that migrated from the subpallial spheroid to the cortical spheroid expressed cortical interneuron markers, and whole-cell voltage-clamp recordings showed that these interneuron-like cells can receive excitatory inputs from dorsal cortical organoid cells and that dorsal cortical cells can receive inputs from inhibitory interneurons.
“In the dorsal-ventral fused model mentioned earlier6, cells that migrated from the subpallial spheroid to the cortical spheroid expressed cortical interneuron markers, and whole-cell voltage-clamp recordings demonstrated that these interneuron-like cells can receive excitatory inputs from cells in the dorsal cortical organoids; conversely, the cells in the dorsal cortical organoids can receive”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [6]
Organoid-derived interneurons migrated in a manner similar to that of their in vivo counterparts.
“The organoid-derived interneurons migrated in a manner similar to that of their in vivo counterparts.”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [6]
Migrated cells fired action potentials at twice the rate of cells in unfused subpallial spheres or non-migrated cells in the fused organoid, suggesting maturation of membrane properties.
“The cells that had migrated into the cortical spheroids also fired action potentials at twice the rate of cells in unfused subpallial spheres or non-migrated cells in the fused organoid, suggesting maturation of membrane properties.”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [6]
Fusion of human cortical spheroids and human subpallial spheroids was used to model migration of interneurons from the subpallium to the cortex.
“For example, the fusion of human cortical spheroids and human subpallial spheroids was used to model the migration of interneurons from the subpallium to the cortex6.”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [6]
Fused dorsal and ventral forebrain organoids from three patients with Timothy syndrome revealed a cell-autonomous migration defect in Timothy syndrome-derived interneurons.
“This revealed a cell-autonomous migration defect in Timothy syndrome-derived interneurons.”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [6]
Brain organoid models have recapitulated cell proliferation effects in microcephaly and have been used to study neural migration defects in Timothy syndrome.
“Brain organoid models have been shown to recapitulate cell proliferation effects in microcephaly (Thomas et al., 2017) and have been used to study neural migration defects in Timothy syndrome, a rare ASD form caused by mutations in the Cav1.2 calcium channel gene (Birey et al., 2017).”
From Getting to the cores of autism (2019) · cites this paper as Birey et al., 2017
Region-specific spheroids or organoids can be fused in vitro to generate 3D assembloids that model complex cellular interactions during human brain development.
“We have previously developed an approach to model complex cellular interactions during human brain development by specifying region-specific spheroids or organoids and then fusing them in vitro to generate three-dimensional (3D) assembloids”
From Generation of Functional Human 3D Cortico-Motor Assembloids (2020) · cites this paper as Birey et al., 2017
hCS contain deep and superficial glutamatergic neurons.
“We previously described the generation of 3D spheroids resembling the cerebral cortex (human cortical spheroids [hCS]) (Birey et al., 2017; Paşca et al., 2015; Sloan et al., 2017, 2018), which contain deep and superficial glutamatergic neurons.”
From Generation of Functional Human 3D Cortico-Motor Assembloids (2020) · cites this paper as Birey et al., 2017
hCS express cortico-spinal-associated markers FEZF2, BCL11B, and SOX5 in a glutamatergic neuron population but not in a subpallial-derived GABAergic cluster.
“We verified expression of cortico-spinal-associated markers in hCS, including FEZF2, BCL11B (CTIP2), and SOX5, using single-cell profiling of hCS (Birey et al., 2017) and found a population of cells co-expressing these genes in the glutamatergic neuron cluster but not in a subpallial-derived GABAergic cluster”
From Generation of Functional Human 3D Cortico-Motor Assembloids (2020) · cites this paper as Birey et al., 2017
The authors had earlier reported that spheroids patterned to specific brain regions offer a modular way to examine human interneuron movement and uncover disease-related phenotypes.
“We previously showed the potential of using region-specific spheroids as a modular approach to study human interneuron migration and identify disease phenotypes (Birey et al., 2017).”
From Generation of Functional Human 3D Cortico-Motor Assembloids (2020) · cites this paper as Birey et al., 2017
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Cites
(2008) · Journal of Machine Learning Research · Cited by 33,051 · see citing works
Differential expression analysis for sequence count data
Anders, S., & Huber, W. (2010) · Genome Biology · doi:10.1186/gb-2010-11-10-r106 · Cited by 15,581 · see citing works
Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,949 · see citing works
Biological insights from 108 schizophrenia-associated genetic loci
Schizophrenia Working Group of the Psychiatric Genomics Consortium (2014) · Nature · doi:10.1038/nature13595 · Cited by 7,577 · see citing works
Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets.
Macosko, E. Z., Basu, A., Satija, R., Nemesh, J., Shekhar, K., Goldman, M., Tirosh, I., Bialas, A. R., Kamitaki, N., Martersteck, E. M., et al. (2015) · Cell · doi:10.1016/j.cell.2015.05.002 · Cited by 7,110 · see citing works
Spatial reconstruction of single-cell gene expression data
Satija, R., Farrell, J. A., Gennert, D., Schier, A. F., & Regev, A. (2015) · Nature Biotechnology · doi:10.1038/nbt.3192 · Cited by 7,055 · see citing works
Cerebral organoids model human brain development and microcephaly
Lancaster, M. A., Renner, M., Martin, C.-A., Wenzel, D., Bicknell, L. S., Hurles, M. E., Homfray, T., Penninger, J. M., Jackson, A. P., & Knoblich, J. A. (2013) · Nature · doi:10.1038/nature12517 · Cited by 5,372 · see citing works
Meijer, L., Nelson, D. J., Riazanski, V., Gabdoulkhakova, A. G., Héry-Arnaud, G., Berre, R. L., Loaëc, N., Oumata, N., Galons, H., Nowak, E., et al. (2016) · Journal of Innate Immunity · doi:10.1159/000444256 · Cited by 4,992 · see citing works
(2013) · The Lancet · doi:10.1016/s0140-6736(12)62129-1 · Cited by 3,010 · see citing works
Model of autism: increased ratio of excitation/inhibition in key neural systems
Rubenstein, J. L. R., & Merzenich, M. M. (2003) · Genes, Brain and Behavior · doi:10.1034/j.1601-183x.2003.00037.x · Cited by 2,768 · see citing works
Smart-seq2 for sensitive full-length transcriptome profiling in single cells
Picelli, S., Björklund, Å. K., Faridani, O. R., Sagasser, S., Winberg, G., & Sandberg, R. (2013) · Nature Methods · doi:10.1038/nmeth.2639 · Cited by 2,358 · see citing works
Zhang, Y., Sloan, S. A., Clarke, L. E., Caneda, C., Plaza, C. A., Blumenthal, P. D., Vogel, H., Steinberg, G. K., Edwards, M. S. B., Li, G., et al. (2016) · Neuron · doi:10.1016/j.neuron.2015.11.013 · Cited by 2,295 · see citing works
Brain-Region-Specific Organoids Using Mini-bioreactors for Modeling ZIKV Exposure
Qian, X., Nguyen, H. N., Song, M. M., Hadiono, C., Ogden, S. C., Hammack, C., Yao, B., Hamersky, G. R., Jacob, F., Zhong, C., et al. (2016) · Cell · doi:10.1016/j.cell.2016.04.032 · Cited by 2,127 · see citing works
iDISCO: A Simple, Rapid Method to Immunolabel Large Tissue Samples for Volume Imaging
Renier, N., Wu, Z., Simon, D. J., Yang, J. H., Ariel, P., & Tessier‐Lavigne, M. (2014) · Cell · doi:10.1016/j.cell.2014.10.010 · Cited by 1,838 · see citing works
Functional cortical neurons and astrocytes from human pluripotent stem cells in 3D culture
Paşca, A. M., Sloan, S. A., Clarke, L. E., Tian, Y., Makinson, C. D., Huber, N., Kim, C. H., Park, J.-Y., O'Rourke, N. A., Nguyen, K. D., et al. (2015) · Nature Methods · doi:10.1038/nmeth.3415 · Cited by 1,609 · see citing works
Self-citationCaV1.2 Calcium Channel Dysfunction Causes a Multisystem Disorder Including Arrhythmia and Autism
Splawski, I., Timothy, K. W., Sharpe, L. M., Decher, N., Kumar, P., Bloise, R., Napolitano, C., Schwartz, P. J., Joseph, R. M., Condouris, K., et al. (2004) · Cell · doi:10.1016/j.cell.2004.09.011 · Cited by 1,586 · see citing works
Interneuron dysfunction in psychiatric disorders
Marín, O. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3155 · Cited by 1,190 · see citing works
Interneuron cell types are fit to function
Kepecs, A., & Fishell, G. (2014) · Nature · doi:10.1038/nature12983 · Cited by 1,110 · see citing works
Cre-dependent selection yields AAV variants for widespread gene transfer to the adult brain
Deverman, B. E., Pravdo, P. L., Simpson, B. P., Kumar, S. R., Chan, K. Y., Banerjee, A., Wu, W.-L., Yang, B., Huber, N., Pasca, S. P., et al. (2016) · Nature Biotechnology · doi:10.1038/nbt.3440 · Cited by 1,061 · see citing works
Self-citationElectroporation and RNA interference in the rodent retina in vivo and in vitro
Matsuda, T., & Cepko, C. L. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2235688100 · Cited by 1,032 · see citing works
Kadoshima, T., Sakaguchi, H., Nakano, T., Soen, M., Ando, S., Eiraku, M., & Sasai, Y. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1315710110 · Cited by 999 · see citing works
The origin and specification of cortical interneurons
Wonders, C. P., & Anderson, S. A. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1954 · Cited by 980 · see citing works
Accounting for technical noise in single-cell RNA-seq experiments
Brennecke, P., Anders, S., Kim, J. K., Kołodziejczyk, A. A., Zhang, X., Proserpio, V., Baying, B., Benes, V., Teichmann, S. A., Marioni, J. C., et al. (2013) · Nature Methods · doi:10.1038/nmeth.2645 · Cited by 979 · see citing works
The Cellular and Molecular Landscapes of the Developing Human Central Nervous System
Silbereis, J. C., Pochareddy, S., Zhu, Y., Li, M., & Sestan, N. (2016) · Neuron · doi:10.1016/j.neuron.2015.12.008 · Cited by 818 · see citing works
Using induced pluripotent stem cells to investigate cardiac phenotypes in Timothy syndrome
Yazawa, M., Hsueh, B., Jia, X., Pasca, A. M., Bernstein, J. A., Hallmayer, J., & Dolmetsch, R. E. (2011) · Nature · doi:10.1038/nature09855 · Cited by 677 · see citing works
Self-citationDistinct cortical migrations from the medial and lateral ganglionic eminences
Anderson, S. A., Marín, Ó., Horn, C., Jennings, K., & Rubenstein, J. L. R. (2001) · Development · doi:10.1242/dev.128.3.353 · Cited by 651 · see citing works
Severe arrhythmia disorder caused by cardiac L-type calcium channel mutations
Splawski, I., Timothy, K. W., Decher, N., Kumar, P., Sachse, F. B., Beggs, A. H., Sanguinetti, M. C., & Keating, M. T. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502506102 · Cited by 624 · see citing works
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., et al. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2013.04.008 · Cited by 596 · see citing works
Using iPSC-derived neurons to uncover cellular phenotypes associated with Timothy syndrome
Paşca, S. P., Portmann, T., Voineagu, I., Yazawa, M., Shcheglovitov, A., Paşca, A. M., Cord, B., Palmer, T. D., Chikahisa, S., Nishino, S., et al. (2011) · Nature Medicine · doi:10.1038/nm.2576 · Cited by 585 · see citing works
Self-citationModeling human cortical development in vitro using induced pluripotent stem cells
Mariani, J., Simonini, M. V., Palejev, D., Tomasini, L., Coppola, G., Szekely, A. M., Horvath, T. L., & Vaccarino, F. M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1202944109 · Cited by 526 · see citing works
Nicholas, C. R., Chen, J., Tang, Y., Southwell, D. G., Chalmers, N., Vogt, D. L., Arnold, C. M., Chen, Y.-J. J., Stanley, E. G., Elefanty, A. G., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.04.005 · Cited by 513 · see citing works
Combinatorial labeling of single cells for gene expression cytometry
Fan, H. C., Fu, G. K., & Fodor, S. P. A. (2015) · Science · doi:10.1126/science.1258367 · Cited by 455 · see citing works
Self-citationCXCR4 Regulates Interneuron Migration in the Developing Neocortex
Stumm, R. K., Zhou, C., Ara, T., Lazarini, F., Dubois-Dalcq, M. E., Nagasawa, T., Höllt, V., & Schulz, S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-12-05123.2003 · Cited by 450 · see citing works
Pluripotent stem cells in regenerative medicine: challenges and recent progress
Tabar, V., & Studer, L. (2014) · Nature reviews genetics · doi:10.1038/nrg3563 · Cited by 434 · see citing works
Bortone, D., & Polleux, F. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.034 · Cited by 387 · see citing works
Bellion, A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1030-05.2005 · Cited by 354 · see citing works
Single-Synapse Analysis of a Diverse Synapse Population: Proteomic Imaging Methods and Markers
Micheva, K. D., Busse, B. L., Weiler, N. C., O’Rourke, N. A., & Smith, S. J. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.024 · Cited by 336 · see citing works
Self-citationKrey, J. F., Pașca, S. P., Shcheglovitov, A., Yazawa, M., Schwemberger, R., Rasmusson, R. L., & Dolmetsch, R. E. (2013) · Nature Neuroscience · doi:10.1038/nn.3307 · Cited by 252 · see citing works
Self-citationVentricle-directed migration in the developing cerebral cortex
Nadarajah, B., Alifragis, P., Wong, R., & Parnavelas, J. G. (2002) · Nature Neuroscience · doi:10.1038/nn813 · Cited by 219 · see citing works
Romero, I. G., Pavlovic, B. J., Hernando-Herraez, I., Zhou, X., Ward, M. C., Banovich, N. E., Kagan, C. L., Burnett, J. E., Huang, C. H., Mitrano, A., et al. (2015) · eLife · doi:10.7554/elife.07103 · Cited by 194 · see citing works
Integration 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
Sensory experience regulates cortical inhibition by inducing IGF1 in VIP neurons
Mardinly, A. R., Spiegel, I., Patrizi, A., Centofante, E., Bazinet, J. E., Tzeng, C. P., Mandel-Brehm, C., Harmin, D. A., Adesnik, H., Fagiolini, M., et al. (2016) · Nature · doi:10.1038/nature17187 · Cited by 176 · see citing works
Radial glia require PDGFD-PDGFRβ signalling in human but not mouse neocortex
Lui, J. H., Nowakowski, T. J., Pollen, A. A., Javaherian, A., Kriegstein, A. R., & Oldham, M. C. (2014) · Nature · doi:10.1038/nature13973 · Cited by 166 · 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
Self-citationGene Expression in Cortical Interneuron Precursors is Prescient of their Mature Function
Batista‐Brito, R., Machold, R. P., Klein, C., & Fishell, G. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm258 · Cited by 130 · see citing works
Potter, G. B., Petryniak, M. A., Shevchenko, E., McKinsey, G. L., Ekker, M., & Rubenstein, J. L. R. (2008) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2008.10.003 · Cited by 122 · see citing works
GRIP1 and 2 regulate activity-dependent AMPA receptor recycling via exocyst complex interactions
Mao, L., Takamiya, K., Thomas, G., Lin, D.-T., & Huganir, R. L. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1013494107 · Cited by 94 · see citing works
Tian, Y., Voineagu, I., Paşca, S. P., Won, H., Chandran, V., Horvath, S., Dolmetsch, R. E., & Geschwind, D. H. (2014) · Genome Medicine · doi:10.1186/s13073-014-0075-5 · Cited by 93 · see citing works
Self-citationTCF4, Schizophrenia, and Pitt-Hopkins Syndrome
Blake, D. J., Forrest, M. P., Chapman, R. M., Tinsley, C. L., O’Donovan, M. C., & Owen, M. J. (2010) · Schizophrenia Bulletin · doi:10.1093/schbul/sbq035 · Cited by 76 · see citing works
Generating Human Neurons In Vitro and Using Them to Understand Neuropsychiatric Disease
Pașca, S. P., Panagiotakos, G., & Dolmetsch, R. E. (2014) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062012-170328 · Cited by 64 · see citing works
Self-citationYarotskyy, V, & Elmslie, K. S. (2007) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0707414 · Cited by 49 · see citing works
Yarotskyy, V., Gao, G., Du, L., Ganapathi, S. B., Peterson, B. Z., & Elmslie, K. S. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.076448 · Cited by 36 · see citing works
Zechel, S., Zając, P., Lönnerberg, P., Ibáñez, C. F., & Linnarsson, S. (2014) · Genome biology · doi:10.1186/s13059-014-0486-z · Cited by 34 · see citing works
Lacaria, M., Gu, W., & Lupski, J. R. (2013) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.35941 · Cited by 28 · see citing works
Uylings, H. B. M., Delalle, I., Petanjek, Z., & Koenderink, M. J. T. (2002) · Neuroembryology and Aging · doi:10.1159/000066268 · Cited by 17 · see citing works
The Development of Phasic and Tonic Inhibition in the Rat Visual Cortex
Jang, H., Cho, K., Park, S., Kim, M.-J., Yoon, S. H., & Rhie, D. (2010) · Korean Journal of Physiology and Pharmacology · doi:10.4196/kjpp.2010.14.6.399 · Cited by 12 · see citing works
Ex Utero Electroporation and Organotypic Slice Culture of Mouse Hippocampal Tissue
Venkataramanappa, S., Simon, R., & Britsch, S. (2015) · Journal of Visualized Experiments · doi:10.3791/52550 · Cited by 4 · see citing works
Generation and Assembly of Forebrain Spheroids
Birey, F., Andersen, J., & Pașca, S. P. (2017) · Protocol Exchange · doi:10.1038/protex.2017.044 · Cited by 1 · see citing works
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Human organoids: model systems for human biology and medicine
Kim, J., Koo, B.-K., & Knoblich, J. A. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0259-3 · Cited by 2,187 · see citing works
Single-Cell Multi-omic Integration Compares and Contrasts Features of Brain Cell Identity
Welch, J. D., Kozareva, V., Ferreira, A., Vanderburg, C., Martin, C., & Macosko, E. Z. (2019) · Cell · doi:10.1016/j.cell.2019.05.006 · Cited by 1,193 · see citing works
Hofer, M., & Lutolf, M. P. (2021) · Nature Reviews Materials · doi:10.1038/s41578-021-00279-y · Cited by 1,184 · see citing works
Individual brain organoids reproducibly form cell diversity of the human cerebral cortex
Velasco, S., Kedaigle, A. J., Simmons, S. K., Nash, A., Rocha, M., Quadrato, G., Paulsen, B., Nguyen, L., Adiconis, X., Regev, A., et al. (2019) · Nature · doi:10.1038/s41586-019-1289-x · Cited by 1,094 · see citing works
Trujillo, C. A., Gao, R., Negraes, P. D., Gu, J., Buchanan, J., Preissl, S., Wang, A., Wu, W., Haddad, G. G., Chaim, I. A., et al. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.08.002 · Cited by 974 · see citing works
Organoid single-cell genomic atlas uncovers human-specific features of brain development
Kanton, S., Boyle, M. J., He, Z., Santel, M., Weigert, A., Sanchís-Calleja, F., Guijarro, P., Sidow, L., Fleck, J. S., Han, D., et al. (2019) · Nature · doi:10.1038/s41586-019-1654-9 · Cited by 761 · 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
The use of brain organoids to investigate neural development and disease
Di Lullo, E., & Kriegstein, A. R. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.107 · Cited by 788 · see citing works
Brain organoids: advances, applications and challenges
Qian, X., Song, H., & Ming, G.-L. (2019) · Development · doi:10.1242/dev.166074 · Cited by 724 · see citing works
Xiang, Y., Tanaka, Y., Patterson, B., Kang, Y., Govindaiah, G., Roselaar, N., Çakır, B., Kim, K.-Y., Lombroso, A., Hwang, S., et al. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.07.007 · Cited by 696 · see citing works
Cerebral organoids at the air-liquid interface generate diverse nerve tracts with functional output
Giandomenico, S. L., Mierau, S. B., Gibbons, G. M., Wenger, L. M. D., Masullo, L., Sit, T., Sutcliffe, M., Boulanger, J., Tripodi, M., Derivery, E., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0350-2 · Cited by 651 · see citing works
Tissue clearing and its applications in neuroscience
Ueda, H. R., Ertürk, A., Chung, K., Gradinaru, V., Chédotal, A., Tomančák, P., & Keller, P. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0250-1 · Cited by 619 · see citing works
Generation of Functional Human 3D Cortico-Motor Assembloids
Andersen, J., Revah, O., Miura, Y., Thom, N., Amin, N. D., Kelley, K. W., Singh, M., Chen, X., Thete, M. V., Walczak, E. M., et al. (2020) · Cell · doi:10.1016/j.cell.2020.11.017 · Cited by 593 · see citing works
Self-citationSloan, S. A., Darmanis, S., Huber, N., Khan, T. A., Birey, F., Caneda, C., Reimer, R., Quake, S. R., Barres, B. A., & Paşca, S. P. (2017) · Neuron · doi:10.1016/j.neuron.2017.07.035 · Cited by 593 · see citing works
Self-citationGeneration of human brain region–specific organoids using a miniaturized spinning bioreactor
Qian, X.-Y., Jacob, F., Song, M., Nguyen, H. N., Song, H.-J., & Ming, G. (2018) · Nature Protocols · doi:10.1038/nprot.2017.152 · Cited by 474 · see citing works
SARS‐CoV‐2 targets neurons of 3D human brain organoids
Ramani, A., Müller, L., Ostermann, P. N., Gabriel, E., Abida‐Islam, P., Müller‐Schiffmann, A., Mariappan, A., Goureau, O., Gruell, H., Walker, A., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2020106230 · Cited by 518 · see citing works
Reliability of human cortical organoid generation
Yoon, S.-J., Elahi, L. S., Pașca, A. M., Marton, R. M., Gordon, A., Revah, O., Miura, Y., Walczak, E. M., Holdgate, G. M., Fan, H. C., et al. (2019) · Nature Methods · doi:10.1038/s41592-018-0255-0 · Cited by 507 · see citing works
Self-citationMaturation and circuit integration of transplanted human cortical organoids
Revah, O., Gore, F., Kelley, K. W., Andersen, J., Sakai, N., Chen, X., Li, M.-Y., Birey, F., Yang, X., Saw, N. L., et al. (2022) · Nature · doi:10.1038/s41586-022-05277-w · Cited by 504 · see citing works
Self-citationThe rise of three-dimensional human brain cultures
Pașca, S. P. (2018) · Nature · doi:10.1038/nature25032 · Cited by 509 · see citing works
Self-citationHuman organoids in basic research and clinical applications
Tang, X., Wu, S., Wang, D., Chu, C., Hong, Y., Tao, M., Hu, H., Xu, M., Guo, X., & Liu, Y. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01024-9 · Cited by 424 · see citing works
Generation and assembly of human brain region-specific three-dimensional cultures
Sloan, S. A., Andersen, J., Pașca, A. M., Birey, F., & Pașca, S. P. (2018) · Nature Protocols · doi:10.1038/s41596-018-0032-7 · Cited by 490 · see citing works
Self-citationhESC-Derived Thalamic Organoids Form Reciprocal Projections When Fused with Cortical Organoids
Xiang, Y., Tanaka, Y., Cakir, B., Patterson, B., Kim, K.-Y., Sun, P., Kang, Y.-J., Zhong, M., Liu, X., Patra, P., et al. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2018.12.015 · Cited by 485 · see citing works
Modeling 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
Daly, A. C., Davidson, M. D., & Burdick, J. A. (2021) · Nature Communications · doi:10.1038/s41467-021-21029-2 · Cited by 470 · see citing works
Miura, Y., Li, M.-Y., Birey, F., Ikeda, K., Revah, O., Thete, M. V., Park, J.-Y., Puno, A., Lee, S. H., Porteus, M. H., et al. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-00763-w · Cited by 418 · see citing works
Self-citationEngineered materials for organoid systems
Kratochvil, M. J., Seymour, A. J., Li, T. L., Pașca, S. P., Kuo, C. J., & Heilshorn, S. C. (2019) · Nature Reviews Materials · doi:10.1038/s41578-019-0129-9 · Cited by 413 · see citing works
Self-citationCho, A.-N., Jin, Y., An, Y., Kim, J., Choi, Y. S., Lee, J. S., Kim, J., Choi, W.-Y., Koo, D.-J., Yu, W., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24775-5 · Cited by 397 · see citing works
Disease modelling in human organoids
Lancaster, M. A., & Huch, M. (2019) · Disease Models & Mechanisms · doi:10.1242/dmm.039347 · Cited by 379 · see citing works
Engineering Stem Cell Self-organization to Build Better Organoids
Brassard, J. A., & Lütolf, M. P. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.05.005 · Cited by 379 · see citing works
Long-term maturation of human cortical organoids matches key early postnatal transitions
Gordon, A., Yoon, S., Tran, S. S., Makinson, C. D., Park, J. Y., Andersen, J., Valencia, A. M., Horvath, S., Xiao, X. G., Huguenard, J. R., et al. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00802-y · Cited by 352 · see citing works
Self-citationDifferentiation and maturation of oligodendrocytes in human three-dimensional neural cultures
Marton, R. M., Miura, Y., Sloan, S. A., Li, Q., Revah, O., Levy, R. J., Huguenard, J. R., & Pașca, S. P. (2019) · Nature Neuroscience · doi:10.1038/s41593-018-0316-9 · Cited by 362 · see citing works
Self-citationLiver organoids: from basic research to therapeutic applications
Prior, N., Inacio, P., & Huch, M. (2019) · Gut · doi:10.1136/gutjnl-2019-319256 · Cited by 356 · see citing works
Induction of myelinating oligodendrocytes in human cortical spheroids
Madhavan, M., Nevin, Z. S., Shick, H. E., Garrison, E., Clarkson-Paredes, C., Karl, M., Clayton, B. L. L., Factor, D. C., Allan, K. C., Barbar, L., et al. (2018) · Nature Methods · doi:10.1038/s41592-018-0081-4 · Cited by 353 · see citing works
Brain organoids for the study of human neurobiology at the interface of in vitro and in vivo
Chiaradia, I., & Lancaster, M. A. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-00730-3 · Cited by 343 · see citing works
Self-Organizing 3D Human Trunk Neuromuscular Organoids
Martins, J.-M. F., Fischer, C., Urzi, A., Vidal, R. O., Kunz, S., Ruffault, P.-L., Kabuss, L., Hube, I., Gazzerro, E., Birchmeier, C., et al. (2020) · Cell stem cell · doi:10.1016/j.stem.2019.12.007 · Cited by 339 · see citing works
Progress in Understanding and Treating SCN2A-Mediated Disorders
Sanders, S. J., Campbell, A. J., Cottrell, J. R., Moller, R. S., Wagner, F. F., Auldridge, A. L., Bernier, R. A., Catterall, W. A., Chung, W. K., Empfield, J. R., et al. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.03.011 · Cited by 338 · see citing works
“Patientderived induced pluripotent stem cell-based approaches including neuronal cultures [64,65] and organoids [66,67] hold great promise in this regard, as they would allow researchers to probe for the functional effects of SCN2A genetic variants on many levels including neuronal excitability, developmental progress…”
BackgroundDaly, A. C., Prendergast, M. E., Hughes, A. J., & Burdick, J. A. (2021) · Cell · doi:10.1016/j.cell.2020.12.002 · Cited by 345 · see citing works
Specification of positional identity in forebrain organoids
Cederquist, G., Asciolla, J. J., Tchieu, J. H., Walsh, R. M., Cornacchia, D., Resh, M. D., & Studer, L. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0085-3 · Cited by 327 · see citing works
Rethinking organoid technology through bioengineering
Garreta, E., Kamm, R. D., Lopes, S. M. C. D. S., Lancaster, M. A., Weiss, R., Trepat, X., Hyun, I., & Montserrat, N. (2020) · Nature Materials · doi:10.1038/s41563-020-00804-4 · Cited by 326 · 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
Self-citationHuman cerebral organoids — a new tool for clinical neurology research
Eichmüller, O. L., & Knoblich, J. A. (2022) · Nature Reviews Neurology · doi:10.1038/s41582-022-00723-9 · Cited by 260 · see citing works
Multi-lineage human iPSC-derived platforms for disease modeling and drug discovery
Sharma, A., Sances, S., Workman, M. J., & Svendsen, C. N. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.02.011 · Cited by 296 · see citing works
Identification of neural oscillations and epileptiform changes in human brain organoids
Samarasinghe, R. A., Miranda, O. A., Buth, J. E., Mitchell, S. A., Ferando, I., Watanabe, M., Allison, T. F., Kurdian, A., Fotion, N. N., Gandal, M. J., et al. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00906-5 · Cited by 278 · see citing works
Stalled developmental programs at the root of pediatric brain tumors
Jessa, S., Blanchet-Cohen, A., Krug, B., Vladoiu, M. C., Coutelier, M., Faury, D., Poreau, B., Jay, N. D., Hébert, S., Monlong, J., et al. (2019) · Nature Genetics · doi:10.1038/s41588-019-0531-7 · Cited by 282 · see citing works
Park, Y., Franz, C. K., Ryu, H., Luan, H., Cotton, K. Y., Kim, J. U., Chung, T. S., Zhao, S., Vázquez‐Guardado, A., Yang, D. S., et al. (2021) · Science Advances · doi:10.1126/sciadv.abf9153 · Cited by 287 · see citing works
Centeno, E. G. Z., Cimarosti, H., & Bithell, A. (2018) · Molecular Neurodegeneration · doi:10.1186/s13024-018-0258-4 · Cited by 268 · see citing works
Ecker, J. R., Geschwind, D. H., Kriegstein, A. R., Ngai, J., Osten, P., Polioudakis, D., Regev, A., Šestan, N., Wickersham, I. R., & Zeng, H. (2017) · Neuron · doi:10.1016/j.neuron.2017.10.007 · Cited by 254 · see citing works
Signalling pathways in autism spectrum disorder: mechanisms and therapeutic implications
Jiang, C.-C., Lin, L., Long, S., Ke, X., Fukunaga, K., Lu, Y., & Han, F. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01081-0 · Cited by 272 · see citing works
Getting to the cores of autism
Iakoucheva, L. M., Muotri, A. R., & Sebat, J. (2019) · Cell · doi:10.1016/j.cell.2019.07.037 · Cited by 260 · see citing works
Cheroni, C., Caporale, N., & Testa, G. (2020) · Molecular Autism · doi:10.1186/s13229-020-00370-1 · Cited by 268 · see citing works
Marton, R. M., & Pașca, S. (2019) · Trends in Cell Biology · doi:10.1016/j.tcb.2019.11.004 · Cited by 202 · see citing works
Self-citationChallenges of Organoid Research
Andrews, M., & Kriegstein, A. (2022) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-111020-090812 · Cited by 216 · see citing works
Chromatin accessibility dynamics in a model of human forebrain development
Trevino, A. E., Sinnott-Armstrong, N., Andersen, J., Yoon, S.-J., Huber, N., Pritchard, J. K., Chang, H. Y., Greenleaf, W. J., & Pașca, S. P. (2020) · Science · doi:10.1126/science.aay1645 · Cited by 251 · see citing works
Self-citationSynthetic Analyses of Single-Cell Transcriptomes from Multiple Brain Organoids and Fetal Brain
Tanaka, Y., Çakır, B., Xiang, Y., Sullivan, G. J., & Park, I. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.01.038 · Cited by 238 · see citing works
A connectomic study of a petascale fragment of human cerebral cortex
Shapson-Coe, A., Januszewski, M., Berger, D. R., Pope, A., Wu, Y., Blakely, T., Schalek, R. L., Li, P. H., Wang, S., Maitin-Shepard, J., et al. (2021) · doi:10.1101/2021.05.29.446289 · Cited by 243 · see citing works
A comprehensive library of human transcription factors for cell fate engineering
Ng, A. H. M., Khoshakhlagh, P., Arias, J. E. R., Pasquini, G., Wang, K., Swiersy, A., Shipman, S. L., Appleton, E., Kiaee, K., Kohman, R. E., et al. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0742-6 · Cited by 235 · see citing works
Human brain organogenesis: Toward a cellular understanding of development and disease
Kelley, K. W., & Pașca, S. P. (2021) · Cell · doi:10.1016/j.cell.2021.10.003 · Cited by 233 · see citing works
Self-citationSynergistic effects of common schizophrenia risk variants
Schrode, N., Ho, S., Yamamuro, K., Dobbyn, A. L., Huckins, L. M., Matos, M. R., Cheng, E., Deans, P. J. M., Flaherty, E. K., Barretto, N., et al. (2019) · Nature Genetics · doi:10.1038/s41588-019-0497-5 · Cited by 223 · see citing works
Organ‐on‐chip models: Implications in drug discovery and clinical applications
Mittal, R., Woo, F. W., Castro, C. S., Cohen, M. A., Karanxha, J., Mittal, J., Chhibber, T., & Jhaveri, V. M. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27729 · Cited by 235 · see citing works
Three-Dimensional Cell Cultures: The Bridge between In Vitro and In Vivo Models
Urzì, O., Gasparro, R., Costanzo, E., Luca, A. D., Giavaresi, G., Fontana, S., & Alessandro, R. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241512046 · Cited by 247 · see citing works
Genomics, convergent neuroscience and progress in understanding autism spectrum disorder
Willsey, H. R., Willsey, A. J., Wang, B., & State, M. W. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00576-7 · Cited by 229 · see citing works
The Emerging Neurobiology of Bipolar Disorder
Harrison, P. J., Geddes, J. R., & Tunbridge, E. M. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2017.10.006 · Cited by 235 · see citing works
Functional neuronal circuitry and oscillatory dynamics in human brain organoids
Sharf, T., van der Molen, T., Glasauer, S. M. K., Guzman, E., Buccino, A., Luna, G., Cheng, Z., Audouard, M., Ranasinghe, K., Kudo, K., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-32115-4 · Cited by 218 · see citing works
Rifes, P., Isaksson, M., Rathore, G. S., Aldrin-Kirk, P., Møller, O. K., Barzaghi, G., Lee, J., Egerod, K. L., Rausch, D. M., Parmar, M., et al. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0525-0 · Cited by 217 · see citing works
Cerebral organoids: ethical issues and consciousness assessment
Lavazza, A., & Massimini, M. (2018) · Journal of Medical Ethics · doi:10.1136/medethics-2017-104555 · Cited by 217 · see citing works
Lineage recording in human cerebral organoids
He, Z., Maynard, A., Jain, A., Gerber, T., Petri, R., Lin, H., Santel, M., Ly, K. C. H., Dupré, J.-S., Sidow, L., et al. (2021) · Nature Methods · doi:10.1038/s41592-021-01344-8 · Cited by 204 · see citing works
The ethics of experimenting with human brain tissue
Farahany, N. A., Greely, H. T., Hyman, S. E., Christof Koch, A., Grady, C., Pașca, S. P., Šestan, N., Arlotta, P., Bernat, J. L., Ting, J. T., et al. (2018) · Nature · doi:10.1038/d41586-018-04813-x · Cited by 212 · see citing works
Self-citationTaoufik, E., Kouroupi, G., Zygogianni, O., & Matsas, R. (2018) · Open Biology · doi:10.1098/rsob.180138 · Cited by 206 · see citing works
Assembling human brain organoids
Paşca, S. P. (2019) · Science · doi:10.1126/science.aau5729 · Cited by 208 · see citing works
Self-citationThe diversity of GABAergic neurons and neural communication elements
Huang, Z. J., & Paul, A. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0195-4 · Cited by 201 · see citing works
Interneuron Types as Attractors and Controllers
Fishell, G., & Kepecs, Á. (2019) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070918-050421 · Cited by 197 · see citing works
Integrating organoids and organ-on-a-chip devices
Zhao, Y., Landau, S., Okhovatian, S., Liu, C., Lu, R. X. Z., Lai, B. F. L., Wu, Q., Kieda, J., Cheung, K., Rajasekar, S., et al. (2024) · Nature Reviews Bioengineering · doi:10.1038/s44222-024-00207-z · Cited by 206 · see citing works
Human Models Are Needed for Studying Human Neurodevelopmental Disorders
Zhao, X., & Bhattacharyya, A. (2018) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2018.10.009 · Cited by 192 · see citing works
Functionalization of Brain Region-specific Spheroids with Isogenic Microglia-like Cells
Song, L., Yuan, X., Jones, Z., Vied, C., Yu, M., Marzano, M., Hua, T., Sang, Q. A., Guan, J., Ma, T., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-47444-6 · Cited by 186 · see citing works
Engineering brain assembloids to interrogate human neural circuits
Miura, Y., Li, M.-Y., Revah, O., Yoon, S., Narazaki, G., & Pașca, S. P. (2022) · Nature Protocols · doi:10.1038/s41596-021-00632-z · Cited by 182 · see citing works
Self-citationNeuronal defects in a human cellular model of 22q11.2 deletion syndrome
Khan, T. A., Revah, O., Gordon, A., Yoon, S.-J., Krawisz, A. K., Goold, C., Sun, Y., Kim, C. H., Tian, Y., Li, M.-Y., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-1043-9 · Cited by 186 · see citing works
Self-citationSabaté‐Soler, S., Nickels, S., Saraiva, C., Berger, E., Dubonyte, U., Barmpa, K., Lan, Y. J., Kouno, T., Jarazo, J., Robertson, G., et al. (2022) · Glia · doi:10.1002/glia.24167 · Cited by 191 · see citing works
Human brain organoids assemble functionally integrated bilateral optic vesicles
Gabriel, E., Albanna, W., Pasquini, G., Ramani, A., Josipović, N., Mariappan, A., Schinzel, F., Karch, C. M. M., Bao, G., Gottardo, M., et al. (2021) · Cell stem cell · doi:10.1016/j.stem.2021.07.010 · Cited by 180 · see citing works
An atlas of nano-enabled neural interfaces
Ledesma, H. A., Li, X., Carvalho-de-Souza, J. L., Wei, W., Bezanilla, F., & Tian, B. (2019) · Nature Nanotechnology · doi:10.1038/s41565-019-0487-x · Cited by 181 · see citing works
Self-citationFair, S. R., Julian, D. L., Hartlaub, A. M., Pusuluri, S. T., Malik, G., Summerfied, T. L., Zhao, G., Hester, A. B., Ackerman, W. E., Hollingsworth, E. W., et al. (2020) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.08.017 · Cited by 176 · see citing works
Human 3D cellular model of hypoxic brain injury of prematurity
Pașca, A. M., Park, J.-Y., Shin, H.-W., Qi, Q., Revah, O., Krasnoff, R., O’Hara, R., Willsey, A. J., Palmer, T. D., & Pașca, S. P. (2019) · Nature Medicine · doi:10.1038/s41591-019-0436-0 · Cited by 174 · see citing works
Self-citationModeling Neurological Diseases With Human Brain Organoids
Wang, H. (2018) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2018.00015 · Cited by 172 · 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
Human iPSC-Derived Endothelial Cells and Microengineered Organ-Chip Enhance Neuronal Development
Sances, S., Ho, R., Vatine, G. D., West, D., Laperle, A., Meyer, A. S., Godoy, M. I., Kay, P., Mandefro, B., Hatata, S., et al. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.02.012 · Cited by 169 · see citing works
Human organoids: New strategies and methods for analyzing human development and disease
Corsini, N. S., & Knoblich, J. A. (2022) · Cell · doi:10.1016/j.cell.2022.06.051 · Cited by 171 · see citing works
Brain organoids: an ensemble of bioassays to investigate human neurodevelopment and disease
Sidhaye, J., & Knoblich, J. A. (2020) · Cell Death and Differentiation · doi:10.1038/s41418-020-0566-4 · Cited by 167 · see citing works
Yu, X., Liu, Z., & Sun, X. (2022) · Plant Communications · doi:10.1016/j.xplc.2022.100508 · Cited by 173 · see citing works
Genetics of human brain development
Zhou, Y. F., Song, H., & Ming, G. (2023) · Nature Reviews Genetics · doi:10.1038/s41576-023-00626-5 · Cited by 173 · see citing works
Viral Strategies for Targeting the Central and Peripheral Nervous Systems
Bedbrook, C. N., Deverman, B. E., & Gradinaru, V. (2018) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-080317-062048 · Cited by 168 · see citing works
Song, L., Yuan, X., Jones, Z., Griffin, K., Zhou, Y., Ma, T., & Li, Y. (2019) · Scientific Reports · doi:10.1038/s41598-019-42439-9 · Cited by 169 · see citing works
Kang, Y., Zhou, Y., Li, Y., Han, Y., Xu, J., Niu, W., Li, Z., Liu, S., Feng, H., Huang, W., et al. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00913-6 · Cited by 166 · see citing works
Skylar-Scott, M. A., Huang, J. Y., Lu, A., Ng, A. H. M., Duenki, T., Liu, S., Nam, L. L., Damaraju, S., Church, G. M., & Lewis, J. A. (2022) · Nature Biomedical Engineering · doi:10.1038/s41551-022-00856-8 · Cited by 160 · see citing works
Vascularization of Human Brain Organoids
Matsui, T. K., Tsuru, Y., Hasegawa, K., & Kuwako, K.-I. (2021) · Stem Cells · doi:10.1002/stem.3368 · Cited by 160 · see citing works
Mitochondrial STAT3 exacerbates LPS-induced sepsis by driving CPT1a-mediated fatty acid oxidation
Li, R., Li, X., Zhao, J., Meng, F., Yao, C., Bao, E.-S., Sun, N., Chen, X., Cheng, W., Hua, H. M., et al. (2021) · Theranostics · doi:10.7150/thno.63751 · Cited by 158 · see citing works
Birey, F., Li, M.-Y., Gordon, A., Thete, M. V., Valencia, A. M., Revah, O., Pașca, A. M., Geschwind, D. H., & Pașca, S. P. (2022) · Cell stem cell · doi:10.1016/j.stem.2021.11.011 · Cited by 155 · see citing works
Self-citationAn integrated transcriptomic cell atlas of human neural organoids
He, Z., Dony, L., Fleck, J. S., Szałata, A., Li, K. X., Slišković, I., Lin, H., Santel, M., Atamian, A., Quadrato, G., et al. (2024) · Nature · doi:10.1038/s41586-024-08172-8 · Cited by 169 · see citing works
Self-citationOne-Stop Microfluidic Assembly of Human Brain Organoids To Model Prenatal Cannabis Exposure
Ao, Z., Cai, H., Havert, D., Wu, Z., Gong, Z., Beggs, J. M., Mackie, K., & Guo, F. (2020) · Analytical Chemistry · doi:10.1021/acs.analchem.0c00205 · Cited by 158 · see citing works
Fiorenzano, A., Sozzi, E., Birtele, M., Kajtez, J., Giacomoni, J., Nilsson, F., Bruzelius, A., Sharma, Y., Zhang, Y., Mattsson, B., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-27464-5 · Cited by 156 · see citing works
Yang, X., Forró, C., Li, T. L., Miura, Y., Zaluska, T. J., Tsai, C., Kanton, S., McQueen, J. P., Chen, X., Mollo, V., et al. (2024) · Nature Biotechnology · doi:10.1038/s41587-023-02081-3 · Cited by 164 · see citing works
Self-citationAssembloid CRISPR screens reveal impact of disease genes in human neurodevelopment
Meng, X., Yao, D., Imaizumi, K., Chen, X., Kelley, K. W., Reis, N., Thete, M. V., McKinney, A. A., Kulkarni, S., Panagiotakos, G., et al. (2023) · Nature · doi:10.1038/s41586-023-06564-w · Cited by 145 · see citing works
Self-citation
- Authors
- Birey, F., Andersen, J., Makinson, C. D., Islam, S., Wei, W., Huber, N., Fan, H. C., Metzler, K. R. C., Panagiotakos, G., Thom, N., O’Rourke, N. A., Steinmetz, L. M., Bernstein, J. A., Hallmayer, J., Huguenard, J. R., & Paşca, S. P.
- Affiliations
- Stanford Medicine (US)
- University of California, San Francisco (US)
- ORCID
- Venue
- Nature
- Published
- 2017-04-26
- Volume
- 545
- Issue
- 7652
- Pages
- 54-59
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC5805137
- OpenAlex
- W2609473806
- Cited by
- 1,365
- References
- 58
- Citations by year
- 2026: 148 · 2025: 169 · 2024: 164 · 2023: 135 · 2022: 161 · 2021: 165 · 2020: 168 · 2019: 135 · 2018: 84 · 2017: 34
- FWCI
- 48.69
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R33MH100717, R01MH107800, R01MH100900)
- National Human Genome Research Institute (P01HG000205)
- National Institute of Neurological Disorders and Stroke (R01NS090911, R01NS034774)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- human pluripotent stem cells, GABAergic interneurons, interneuron migration, Timothy syndrome, Cav1.2 calcium channel, glutamatergic neurons, brain organoids, neural development
- MeSH terms
- Autistic Disorder, Cell Line, Cell Movement, Cells, Cultured, Female, Humans, Interneurons, Long QT Syndrome, Male, Models, Biological, Neurons, Synapses, Syndactyly, Prosencephalon, Glutamic Acid, Spheroids, Cellular, Pluripotent Stem Cells, Neurogenesis, GABAergic Neurons
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.
What counts as a claim ›How we measure confidence ›How we check this ›
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