Generation of a defined and uniform population of CNS progenitors and neurons from mouse embryonic stem cells
Abstract
A detailed protocol is described allowing the generation of essentially pure populations of glutamatergic neurons from mouse embryonic stem (ES) cells. It is based on the culture of ES cells that are kept undifferentiated by repeated splitting and subsequently amplified as non-adherent cell aggregates. Treatment with retinoic acid causes these ES cells to essentially become neural progenitors with the characteristics of Pax6-positive radial glial cells. As they do in vivo, these progenitors differentiate in glutamatergic pyramidal neurons that form functional synaptic contacts and can be kept in culture for long periods of time. This protocol does not require the use of ES lines expressing resistance or fluorescent markers and can thus be applied in principle to any wild-type or mutant ES line of interest. At least 2 weeks are required from starting ES cell culture until plating progenitors and differentiating neurons establish synaptic transmission within about 10 days.
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ES cells are pluripotent cells that self-renew indefinitely and can differentiate in vitro into a larger variety of cell types, such as neuronal cells, in response to RA.
“Concerning ES cells, they are pluripotent cells that self-renew indefi nitely and can differentiate in vitro into a larger variety of cell types ( 137 ), such as neuronal cells, in response to RA ( 138 ).”
From Vitamin A and retinoid signaling: genomic and nongenomic effects (2013) · cites this paper as [138]
Cites
A new mathematical model for relative quantification in real-time RT-PCR
Pfaffl, M. W. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.9.e45 · Cited by 34,610 · see citing works
Greene, L., & Tischler, A. S. (1976) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.73.7.2424 · Cited by 5,594 · see citing works
Directed differentiation of embryonic stem cells into motor neurons.
Wichterle, H., Lieberam, I., Porter, J. A., & Jessell, T. (2002) · Cell · doi:10.1016/s0092-8674(02)00835-8 · Cited by 1,792 · see citing works
Embryo-Derived Stem Cells: Of Mice and Men
Smith, A. G. (2001) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.17.1.435 · Cited by 1,263 · see citing works
Embryonic Stem Cells Express Neuronal Properties in Vitro
Bain, G., Kitchens, D. L., Yao, M., Huettner, J. E., & Gottlieb, D. I. (1995) · Developmental Biology · doi:10.1006/dbio.1995.1085 · Cited by 1,168 · see citing works
Embryonic stem cell differentiation: emergence of a new era in biology and medicinePreprint
Keller, G. M. (2005) · Genes & Development · doi:10.1101/gad.1303605 · Cited by 1,144 · see citing works
Niche-Independent Symmetrical Self-Renewal of a Mammalian Tissue Stem Cell
Conti, L., Pollard, S. M., Gorba, T., Reitano, E., Toselli, M., Biella, G. R., Sun, Y., Sanzone, S., Ying, Q., Cattaneo, E. F., et al. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030283 · Cited by 857 · see citing works
Embryonic Stem Cells: Prospects for Developmental Biology and Cell Therapy
Wobus, A. M., & Boheler, K. R. (2005) · Physiological Reviews · doi:10.1152/physrev.00054.2003 · Cited by 777 · see citing works
Okabe, S., Forsberg‐Nilsson, K., Spiro, A. C., Segal, M., & McKay, R. D. G. (1996) · Mechanisms of Development · doi:10.1016/0925-4773(96)00572-2 · Cited by 770 · see citing works
Malatesta, P., Hack, M. A., Hartfuss, E., Kettenmann, H., Klinkert, W. E. F., Kirchhoff, F., & Götz, M. (2003) · Neuron · doi:10.1016/s0896-6273(03)00116-8 · Cited by 747 · see citing works
Neurotrophins are required for nerve growth during development
Tucker, K. L., Meyer, M., & Barde, Y. (2001) · Nature Neuroscience · doi:10.1038/82868 · Cited by 526 · see citing works
Self-citationGeneration of purified neural precursors from embryonic stem cells by lineage selection
Li, M., Pevny, L., Lovell-Badge, R. H., & Smith, A. G. (1998) · Current Biology · doi:10.1016/s0960-9822(98)70399-9 · Cited by 461 · see citing works
Differentiation of mouse embryonic stem cells into a defined neuronal lineage
Bibel, M., Richter, J., Schrenk, K., Tucker, K. L., Staiger, V., Korte, M., Goetz, M., & Barde, Y.-A. (2004) · Nature Neuroscience · doi:10.1038/nn1301 · Cited by 450 · see citing works
Self-citationHuman embryonic stem cells: prospects for development
Pera, M. F., & Trounson, A. O. (2004) · Development · doi:10.1242/dev.01451 · Cited by 239 · see citing works
Dopaminergic neuronal differentiation from rat embryonic neural precursors by Nurr1 overexpression
Kim, J., Koh, H. C., Lee, J., Chang, M., Kim, Y. C., Chung, H. Y., Son, H., Lee, Y., Studer, L., McKay, R. D. G., et al. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01780.x · Cited by 146 · see citing works
Mouse ES cells: experimental exploitation of pluripotent differentiation potential
Rathjen, J., & Rathjen, P. D. (2001) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00237-9 · Cited by 96 · see citing works
Developmental potential of defined neural progenitors derived from mouse embryonic stem cells
Plachta, N., Bibel, M., Tucker, K. L., & Barde, Y. (2004) · Development · doi:10.1242/dev.01420 · Cited by 75 · see citing works
Self-citationKayser, K., Szymaś, J., & Weinstein, R. S. (1999) · Springer eBooks · doi:10.1007/978-3-642-60055-5_10 · Cited by 5 · see citing works
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DNA-binding factors shape the mouse methylome at distal regulatory regions
Stadler, M. B., Murr, R., Burger, L., Ivanek, R., Lienert, F., Schöler, A., Nimwegen, E. V., Wirbelauer, C., Oakeley, E. J., Gaidatzis, D., et al. (2011) · Nature · doi:10.1038/nature10716 · Cited by 1,383 · see citing works
Visualizing structure and transitions in high-dimensional biological data
Moon, K. R., van Dijk, D., Wang, Z., Gigante, S., Burkhardt, D. B., Chen, W. S., Yim, K., Elzen, A. V. D., Hirn, M. J., Coifman, R. R., et al. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0336-3 · Cited by 1,065 · see citing works
Mohn, F., Weber, M., Rebhan, M., Roloff, T. C., Richter, J., Stadler, M. B., Bibel, M., & Schübeler, D. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.05.007 · Cited by 912 · see citing works
Self-citationChromatin Fibers Are Formed by Heterogeneous Groups of Nucleosomes In Vivo
Ricci, M. A., Manzo, C., García-Parajo, M. F., Lakadamyali, M., & Cosma, M. P. (2015) · Cell · doi:10.1016/j.cell.2015.01.054 · Cited by 736 · see citing works
Retinoic acid in development: Towards an integrated view
Niederreither, K., & Dollé, P. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2340 · Cited by 726 · see citing works
Genomic profiling of DNA methyltransferases reveals a role for DNMT3B in genic methylation
Baubec, T., Colombo, D. F., Wirbelauer, C., Schmidt, J., Burger, L., Krebs, A. R., Akalin, A., & Schübeler, D. (2015) · Nature · doi:10.1038/nature14176 · Cited by 705 · see citing works
Single Cell RNA-Sequencing of Pluripotent States Unlocks Modular Transcriptional Variation
Kolodziejczyk, A. A., Kim, J. K., Tsang, J. C. H., Ilicic, T., Henriksson, J., Natarajan, K. N., Tuck, A. C., Gao, X., Bühler, M., Liu, P., et al. (2015) · Cell Stem Cell · doi:10.1016/j.stem.2015.09.011 · Cited by 570 · see citing works
Mass-spectrometric identification and relative quantification of N-linked cell surface glycoproteins
Wollscheid, B., Bausch-Fluck, D., Henderson, C., O'Brien, R., Bibel, M., Schiess, R., Aebersold, R., & Watts, J. D. (2009) · Nature Biotechnology · doi:10.1038/nbt.1532 · Cited by 547 · see citing works
Self-citationCompetition between DNA methylation and transcription factors determines binding of NRF1
Domcke, S., Bardet, A. F., Adrian Ginno, P., Hartl, D., Burger, L., & Schübeler, D. (2015) · Nature · doi:10.1038/nature16462 · Cited by 508 · see citing works
Wang, J., Gallagher, D., DeVito, L. M., Cancino, G. I., Tsui, D., He, L., Keller, G. M., Frankland, P. W., Kaplan, D. R., & Miller, F. D. (2012) · Cell Stem Cell · doi:10.1016/j.stem.2012.03.016 · Cited by 474 · see citing works
Krol, J., Busskamp, V., Markiewicz, I., Stadler, M. B., Ribi, S., Richter, J., Duebel, J., Bicker, S., Fehling, H. J., Schübeler, D., et al. (2010) · Cell · doi:10.1016/j.cell.2010.03.039 · Cited by 470 · see citing works
Self-citationVitamin A and retinoid signaling: genomic and nongenomic effects
Al Tanoury, Z., Piskunov, A., & Rochette-Egly, C. (2013) · Journal of Lipid Research · doi:10.1194/jlr.r030833 · Cited by 408 · see citing works
Embryonic lethal phenotype reveals a function of TDG in maintaining epigenetic stability
Cortázar, D., Kunz, C., Selfridge, J., Lettieri, T., Saito, Y., MacDougall, E., Wirz, A., Schuermann, D., Jacobs, A. L., Siegrist, F., et al. (2011) · Nature · doi:10.1038/nature09672 · Cited by 389 · see citing works
Identification of genetic elements that autonomously determine DNA methylation states
Lienert, F., Wirbelauer, C., Som, I., Dean, A., Mohn, F., & Schübeler, D. (2011) · Nature Genetics · doi:10.1038/ng.946 · Cited by 385 · see citing works
Fbxl10/Kdm2b Recruits Polycomb Repressive Complex 1 to CpG Islands and Regulates H2A Ubiquitylation
Wu, X., Johansen, J. V., & Helin, K. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.01.016 · Cited by 375 · see citing works
Bulut-Karslioglu, A., De La Rosa-Velázquez, I. A., Ramirez, F., Barenboim, M., Onishi-Seebacher, M., Arand, J., Galán, C., Winter, G. E., Engist, B., Gerle, B., et al. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.05.029 · Cited by 368 · see citing works
Lyssiotis, C. A., Foreman, R. K., Staerk, J., Garcia, M. E., Mathur, D., Markoulaki, S., Hanna, J. H., Lairson, L. L., Charette, B. D., Bouchez, L. C., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903860106 · Cited by 367 · see citing works
Methylation-Dependent and -Independent Genomic Targeting Principles of the MBD Protein Family
Baubec, T., Ivánek, R., Lienert, F., & Schübeler, D. (2013) · Cell · doi:10.1016/j.cell.2013.03.011 · Cited by 365 · see citing works
Hon, G. C., Song, C., Du, T., Jin, F., Selvaraj, S., Lee, A. Y., Yen, C., Ye, Z., Mao, S.-Q., Wang, B.-A., et al. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.08.026 · Cited by 332 · see citing works
Neural stem cell systems: physiological players or in vitro entities?
Conti, L., & Cattaneo, E. F. (2010) · Nature reviews. Neuroscience · doi:10.1038/nrn2761 · Cited by 319 · see citing works
Polycomb complexes in stem cells and embryonic development
Aloia, L., Stefano, B. D., & Croce, L. D. (2013) · Development · doi:10.1242/dev.091553 · Cited by 314 · see citing works
Radial glial cell heterogeneity—The source of diverse progeny in the CNS
Pinto, L., & GOTZ, M. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.02.010 · Cited by 259 · see citing works
Activity-dependent neuroprotective protein recruits HP1 and CHD4 to control lineage-specifying genes
Ostapcuk, V., Mohn, F., Carl, S. H., Basters, A., Heß, D., Iešmantavičius, V., Lampersberger, L., Flemr, M., Pandey, A., Thomä, N. H., et al. (2018) · Nature · doi:10.1038/s41586-018-0153-8 · Cited by 221 · see citing works
Transcription Factor Occupancy Can Mediate Active Turnover of DNA Methylation at Regulatory Regions
Feldmann, A., Ivánek, R., Murr, R., Gaidatzis, D., Burger, L., & Schübeler, D. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003994 · Cited by 215 · see citing works
Neurotrophin receptors TrkA and TrkC cause neuronal death whereas TrkB does not
Nikoletopoulou, V., Lickert, H., Frade, J. M., Rencurel, C., Giallonardo, P., Zhang, L., Bibel, M., & Barde, Y. (2010) · Nature · doi:10.1038/nature09336 · Cited by 217 · see citing works
Self-citationPrimary support cultures of hippocampal and substantia nigra neurons
Fath, T., Ke, Y. D., Gunning, P. W., Götz, J., & Ittner, L. M. (2008) · Nature Protocols · doi:10.1038/nprot.2008.199 · Cited by 210 · see citing works
Jarid1b targets genes regulating development and is involved in neural differentiation
Schmitz, S. U., Albert, M., Malatesta, M., Morey, L., Johansen, J. V., Bak, M., Tommerup, N., Abarrategui, I., & Helin, K. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.383 · Cited by 196 · see citing works
Ginno, P. A., Gaidatzis, D., Feldmann, A., Hoerner, L., Imanci, D., Burger, L., Zilbermann, F., Peters, A. H. F. M., Edenhofer, F., Smallwood, S. A., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-16354-x · Cited by 171 · see citing works
Small heat-shock proteins protect from heat-stroke-associated neurodegeneration
Kourtis, N., Nikoletopoulou, V., & Tavernarakis, N. (2012) · Nature · doi:10.1038/nature11417 · Cited by 169 · see citing works
A small molecule primes embryonic stem cells for differentiation.
Zhu, S.-T., Wurdak, H., Wang, J., Lyssiotis, C., Peters, E., Cho, C., Wu, X., & Schultz, P. (2009) · Cell Stem Cell · doi:10.1016/j.stem.2009.04.001 · Cited by 174 · see citing works
Tiwari, V. K., Burger, L., Nikoletopoulou, V., Deogracias, R., Thakurela, S., Wirbelauer, C., Kaut, J., Terranova, R., Hoerner, L., Mielke, C., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1119798109 · Cited by 161 · see citing works
Self-citationAcetylation of histone H3 at lysine 64 regulates nucleosome dynamics and facilitates transcription
Cerbo, V. D., Mohn, F., Ryan, D., Montellier, E., Kacem, S., Tropberger, P., Kallis, E., Holzner, M., Hoerner, L., Feldmann, A., et al. (2014) · eLife · doi:10.7554/elife.01632 · Cited by 157 · see citing works
Generation of subtype-specific neurons from postnatal astroglia of the mouse cerebral cortex
Heinrich, C., Gascón, S., Masserdotti, G., Lepier, A., Sánchez, R., Simon‐Ebert, T., Schroeder, T., Götz, M., & Berninger, B. (2011) · Nature Protocols · doi:10.1038/nprot.2010.188 · Cited by 144 · see citing works
The rRNA m 6 A methyltransferase METTL5 is involved in pluripotency and developmental programsPreprint
Ignatova, V. V., Stolz, P., Kaiser, S., Gustafsson, H. T., Lastres, P. R., Sanz‐Moreno, A., Cho, Y.-L., Amarie, O. V., Aguilar‐Pimentel, J. A., Klein‐Rodewald, T., et al. (2020) · Genes & Development · doi:10.1101/gad.333369.119 · Cited by 149 · see citing works
ChromID identifies the protein interactome at chromatin marks
Villaseñor, R., Pfaendler, R., Ambrosi, C. M., Butz, S., Giuliani, S., Bryan, E., Sheahan, T. W., Gable, A. L., Schmolka, N., Manzo, M., et al. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0434-2 · Cited by 148 · see citing works
Generation of cortical neurons from mouse embryonic stem cells
Gaspard, N., Bouschet, T., Herpoel, A., Naeije, G., van den Ameele, J., & Vanderhaeghen, P. (2009) · Nature Protocols · doi:10.1038/nprot.2009.157 · Cited by 142 · see citing works
Lienert, F., Mohn, F., Tiwari, V. K., Baubec, T., Roloff, T. C., Gaidatzis, D., Stadler, M. B., & Schübeler, D. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002090 · Cited by 142 · see citing works
Chemical Control of Stem Cell Fate and Developmental Potential
Lyssiotis, C. A., Lairson, L. L., Boitano, A. E., Wurdak, H., Zhu, S., & Schultz, P. G. (2010) · Angewandte Chemie International Edition · doi:10.1002/anie.201004284 · Cited by 141 · see citing works
Mapping gene regulatory circuitry of Pax6 during neurogenesis
Thakurela, S., Tiwari, N., Schick, S., Garding, A., Ivánek, R., Berninger, B., & Tiwari, V. K. (2016) · Cell Discovery · doi:10.1038/celldisc.2015.45 · Cited by 131 · see citing works
Zhou, H.-L., Hinman, M. N., Barron, V. A., Geng, C., Zhou, G., Luo, G., Siegel, R. E., & Lou, H. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1103344108 · Cited by 136 · see citing works
Jermann, P. M., Hoerner, L., Burger, L., & Schübeler, D. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400672111 · Cited by 136 · see citing works
A chromatin-modifying function of JNK during stem cell differentiation
Tiwari, V. K., Stadler, M. B., Wirbelauer, C., Paro, R., Schübeler, D., & Beisel, C. (2011) · Nature Genetics · doi:10.1038/ng.1036 · Cited by 133 · see citing works
Development of Patient-Specific Neurons in Schizophrenia Using Induced Pluripotent Stem Cells
Pedrosa, E., Sandler, V., Shah, A., Carroll, R., Chang, C.-J., Rockowitz, S., Guo, X.-Y., Zheng, D.-Y., & Lachman, H. (2011) · Journal of neurogenetics · doi:10.3109/01677063.2011.597908 · Cited by 123 · see citing works
Weiss, A., Abramowski, D., Bibel, M., Bodner, R. A., Chopra, V., DiFiglia, M., Fox, J. H., Kegel, K. B., Klein, C., Grueninger, S., et al. (2009) · Analytical Biochemistry · doi:10.1016/j.ab.2009.08.001 · Cited by 126 · see citing works
Self-citationIsoform‐specific localization of DNMT3A regulates DNA methylation fidelity at bivalent CpG islands
Manzo, M., Wirz, J., Ambrosi, C. M., Villaseñor, R., Roschitzki, B., & Baubec, T. (2017) · The EMBO Journal · doi:10.15252/embj.201797038 · Cited by 120 · see citing works
Egan, C. M., Nyman, U., Skotte, J., Streubel, G., Turner, S. A., O’Connell, D. J., Rraklli, V., Dolan, M.-J., Chadderton, N., Hansen, K. H., et al. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.07.008 · Cited by 121 · see citing works
Farra, N., Zhang, W.-B., Pasceri, P., Eubanks, J. H., Salter, M. W., & Ellis, J. (2012) · Molecular Psychiatry · doi:10.1038/mp.2011.180 · Cited by 116 · see citing works
Staahl, B. T., Tang, J., Wu, W., Sun, A. X., Gitler, A. D., Yoo, A. S. J., & Crabtree, G. R. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1258-13.2013 · Cited by 115 · see citing works
Modeling of epigenome dynamics identifies transcription factors that mediate Polycomb targetingPreprint
Arnold, P., Schöler, A., Pachkov, M. V., Balwierz, P. J., Jørgensen, H. F., Stadler, M. B., van Nimwegen, E., & Schübeler, D. (2012) · Genome Research · doi:10.1101/gr.142661.112 · Cited by 113 · see citing works
Culturing primary neurons from rat hippocampus and cortex
Sahu, M. P., Nikkilä, O., Lågas, S., Kolehmainen, S., & Ċastrén, E. (2019) · Neuronal Signaling · doi:10.1042/ns20180207 · Cited by 110 · see citing works
Regulation of TET Protein Stability by Calpains
Wang, Y., & Zhang, Y. (2014) · Cell Reports · doi:10.1016/j.celrep.2013.12.031 · Cited by 108 · see citing works
Zhu, Y., Carido, M., Meinhardt, A., Kurth, T., Karl, M., Ader, M., & Tanaka, E. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054552 · Cited by 106 · see citing works
Single-molecule footprinting identifies context-dependent regulation of enhancers by DNA methylation
Kreibich, E., Kleinendorst, R., Barzaghi, G., Kaspar, S., & Krebs, A. R. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.01.017 · Cited by 97 · see citing works
Yin, N., Liang, S., Liang, S., Yang, R., Hu, B., Qin, Z., Liu, A., & Faiola, F. (2018) · Environmental Science & Technology · doi:10.1021/acs.est.8b00414 · Cited by 104 · see citing works
Burgold, T., Voituron, N., Cagánová, M., Tripathi, P. P., Menuet, C., Tusi, B. K., Spreafico, F., Bévengut, M., Gestreau, C., Buontempo, S., et al. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.09.013 · Cited by 100 · see citing works
Chu, J.-F., Majumder, P., Chatterjee, B., Huang, S., & Shen, C.-K. J. (2018) · Cell Reports · doi:10.1016/j.celrep.2019.10.061 · Cited by 97 · see citing works
Peng, C., Li, N., Ng, Y.-K., Zhang, J., Meier, F., Theis, F. J., Merkenschlager, M., Chen, W., Wurst, W., & Prakash, N. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2124-12.2012 · Cited by 99 · see citing works
Rochette‐Egly, C. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2014.04.003 · Cited by 97 · see citing works
Yu, S. P., Tung, J. K., Wei, Z. Z., Chen, D., Berglund, K., Zhong, W., Zhang, J. Y., Gu, X., Song, M., Gross, R. E., et al. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2010-18.2019 · Cited by 94 · see citing works
Baldo, B., Weiss, A., Parker, C. N., Bibel, M., Paganetti, P., & Kaupmann, K. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.294801 · Cited by 89 · see citing works
Self-citationGene regulation and priming by topoisomerase IIα in embryonic stem cells
Thakurela, S., Garding, A., Jung, J., Schübeler, D., Burger, L., & Tiwari, V. K. (2013) · Nature Communications · doi:10.1038/ncomms3478 · Cited by 88 · see citing works
Noh, K., Wang, H., Kim, H. R., Wenderski, W., Fang, F., Li, C. H., Dewell, S. B., Hughes, S., Melnick, A., Patel, D., et al. (2015) · Molecules and Cells · doi:10.1016/j.molcel.2015.05.017 · Cited by 88 · see citing works
Targeted p16Ink4a epimutation causes tumorigenesis and reduces survival in mice
Yu, D.-H., Waterland, R. A., Zhang, P., Schady, D. A., Chen, M.-H., Guan, Y., Gadkari, M., & Shen, L. (2014) · Journal of Clinical Investigation · doi:10.1172/jci76507 · Cited by 88 · see citing works
Atlasi, Y., Noori, R., Gaspar, C., Franken, P., Sacchetti, A., Rafati, H., Mahmoudi, T., Decraene, C., Calin, G. A., Merrill, B. J., et al. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003424 · Cited by 84 · see citing works
Yazdani, M., Deogracias, R., Guy, J., Poot, R. A., Bird, A. P., & Barde, Y. (2012) · Stem Cells · doi:10.1002/stem.1180 · Cited by 82 · see citing works
Self-citationCritical Role of Tet3 in Neural Progenitor Cell Maintenance and Terminal Differentiation
Li, T., Yang, D., Li, J. X., Tang, Y., Yang, J., & Le, W. (2014) · Molecular Neurobiology · doi:10.1007/s12035-014-8734-5 · Cited by 81 · see citing works
Xie, G., Lee, J., Senft, A. D., Park, Y.-K., Jang, Y., Chakraborty, S., Thompson, J. J., McKernan, K. E., Liu, C., Macfarlan, T. S., et al. (2023) · Nature Genetics · doi:10.1038/s41588-023-01356-4 · Cited by 73 · see citing works
MMSET Is Highly Expressed and Associated with Aggressiveness in Neuroblastoma
Hudlebusch, H. R., Skotte, J., Santoni‐Rugiu, E., Zimling, Z. G., Lees, M. J., Simon, R., Sauter, G., Rota, R., Ioris, M. A. D., Quarto, M., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-3810 · Cited by 71 · see citing works
Hubbard, K., Gut, I. M., Lyman, M. E., & McNutt, P. M. (2013) · F1000Research · doi:10.12688/f1000research.2-35.v1 · Cited by 69 · see citing works
Creppe, C., Palau, A., Malinverni, R., Valero, V., & Buschbeck, M. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004851 · Cited by 68 · see citing works
circZNF827 nucleates a transcription inhibitory complex to balance neuronal differentiation
Hollensen, A. K., Thomsen, H. S., Lloret-Llinares, M., Kamstrup, A. B., Jensen, J. M., Luckmann, M., Birkmose, N., Palmfeldt, J., Jensen, T. H., Hansen, T. B., et al. (2020) · eLife · doi:10.7554/elife.58478 · Cited by 68 · see citing works
Patterning of retinoic acid signaling and cell proliferation in the hippocampus
Goodman, T. H., Crandall, J. E., Nanescu, S. E., Quadro, L., Shearer, K., Ross, A., & McCaffery, P. J. A. (2012) · Hippocampus · doi:10.1002/hipo.22037 · Cited by 67 · see citing works
Dependence of hippocampal function on ERRγ-regulated mitochondrial metabolism
Pei, L., Mu, Y., Leblanc, M., Alaynick, W., Barish, G. D., Pankratz, M., Tseng, T. W., Kaufman, S., Liddle, C., Yu, R. T., et al. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.03.004 · Cited by 65 · see citing works
Bexarotene-Activated Retinoid X Receptors Regulate Neuronal Differentiation and Dendritic Complexity
Mounier, A., Georgiev, D., Nam, K. N., Fitz, N. F., Castranio, E. L., Wolfe, C. M., Cronican, A. A., Schug, J., Lefterov, I., & Koldamova, R. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1001-15.2015 · Cited by 64 · see citing works
Li, S., Sheng, J., Hu, J. K., Yu, W., Kishikawa, H., Hu, M. G., Shima, K., Wu, D., Xu, Z., Xin, W. W., et al. (2012) · Angiogenesis · doi:10.1007/s10456-012-9322-9 · Cited by 64 · see citing works
Neural stem cell transplantation in the enteric nervous system: roadmaps and roadblocks
Schäfer, K. ‐., Micci, M., & Pasricha, P. J. (2009) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2008.01257.x · Cited by 64 · see citing works
Biagioli, M., Ferrari, F., Mendenhall, E. M., Zhang, Y., Erdin, S., Vijayvargia, R., Vallabh, S. M., Solomos, N., Manavalan, P., Ragavendran, A., et al. (2015) · Human Molecular Genetics · doi:10.1093/hmg/ddv006 · Cited by 60 · see citing works
Theodorou, E., Dalembert, G., Heffelfinger, C., White, E., Weissman, S. M., Corcoran, L. M., & Snyder, M. P. (2009) · Genes & Development · doi:10.1101/gad.1772509 · Cited by 60 · see citing works
Ravens, S., Fournier, M. L., Ye, T., Stierlé, M., Dembélé, D., Chavant, V., & Tora, L. (2014) · eLife · doi:10.7554/elife.02104 · Cited by 59 · see citing works
Simándi, Z., Czipa, E., Horváth, A., Kőszeghy, Á., Bordás, C., Póliska, S., Juhász, I., Imre, L., Szabó, G., Dezsö, B., et al. (2014) · Stem Cells · doi:10.1002/stem.1894 · Cited by 57 · see citing works
Lin, Y., Persaud, S. D., Nhieu, J., & Wei, L. (2017) · Endocrinology · doi:10.1210/en.2017-00353 · Cited by 57 · see citing works
Bazou, D., Kearney, R., Mansergh, F. C., Bourdon, C., Farrar, J., & Wride, M. A. (2011) · Ultrasound in Medicine & Biology · doi:10.1016/j.ultrasmedbio.2010.10.019 · Cited by 56 · see citing works
Nikoletopoulou, V., Plachta, N., Allen, N. D., Pinto, L., Götz, M., & Barde, Y. (2007) · Cell stem cell · doi:10.1016/j.stem.2007.08.011 · Cited by 54 · see citing works
Self-citationVanzan, L., Soldati, H., Ythier, V., Anand, S. K., Braun, S. M. G., Francis, N. J., & Murr, R. (2021) · Nature Communications · doi:10.1038/s41467-021-23630-x · Cited by 52 · see citing works
Gehre, M., Bunina, D., Sidoli, S., Lübke, M. J., Diaz, N. S., Trovato, M., Garcia, B. A., Zaugg, J. B., & Noh, K. (2020) · Nature Genetics · doi:10.1038/s41588-020-0586-5 · Cited by 50 · see citing works
Kim, J., Jakobsen, S. T., Natarajan, K. N., & Won, K. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa1014 · Cited by 53 · see citing works
Chromatin measurements reveal contributions of synthesis and decay to steady‐state mRNA levels
Tippmann, S. C., Ivánek, R., Gaidatzis, D., Schöler, A., Hoerner, L., van Nimwegen, E., Stadler, P. F., Stadler, M. B., & Schübeler, D. (2012) · Molecular Systems Biology · doi:10.1038/msb.2012.23 · Cited by 50 · see citing works
Anamika, K., Krebs, A. R., Thompson, J., Poch, O., Devys, D., & Tora, L. (2010) · Epigenetics & Chromatin · doi:10.1186/1756-8935-3-18 · Cited by 51 · see citing works
Ortega, F., Costa, M. R., Simon‐Ebert, T., Schroeder, T., Götz, M., & Berninger, B. (2011) · Nature Protocols · doi:10.1038/nprot.2011.404 · Cited by 48 · see citing works
Schrenk-Siemens, K., Pérez‐Alcalá, S., Richter, J., Lacroix, E., Rahuel, J., Körte, M., Müller, U., Barde, Y., & Bibel, M. (2008) · Stem Cells · doi:10.1634/stemcells.2008-0010 · Cited by 48 · see citing works
Self-citationMcNutt, P. M., Celver, J. P., Hamilton, T. A., & Mesngon, M. T. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.12.132 · Cited by 46 · see citing works
Early Actions of Neurotransmitters During Cortex Development and Maturation of Reprogrammed Neurons
Ojeda, J., & Ávila, A. (2019) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2019.00033 · Cited by 46 · see citing works
Marques, S. A., de Almeida, F. M., Fernandes, A. M., Souza, C. D. S., Cadilhe, D. V., Rehen, S. K., & Martinez, A. M. B. (2010) · Brain Research · doi:10.1016/j.brainres.2010.06.028 · Cited by 46 · see citing works
Visualizing Structure and Transitions for Biological Data ExplorationPreprint
Moon, K. R., van Dijk, D., Wang, Z., Gigante, S., Burkhardt, D. B., Chen, W. S., Yim, K., van den Elzen, A. M. G., Hirn, M. J., Coifman, R. R., et al. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/120378 · Cited by 48 · see citing works
Defined extracellular matrix components are necessary for definitive endoderm induction
Taylor‐Weiner, H., Schwarzbauer, J. E., & Engler, A. J. (2013) · Stem Cells · doi:10.1002/stem.1453 · Cited by 45 · see citing works
DNMT1 mutations found in HSANIE patients affect interaction with UHRF1 and neuronal differentiation
Smets, M., Link, S., Wolf, P., Schneider, K., Solis, V., Ryan, J., Meilinger, D., Qin, W., & Leonhardt, H. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx057 · Cited by 45 · see citing works
Tet3 regulates cellular identity and DNA methylation in neural progenitor cells
Santiago, M., Antunes, C., Guedes, M., Iacovino, M., Kyba, M., Reik, W., Sousa, N., Pinto, L., Branco, M. R., & Marques, C. J. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03335-7 · Cited by 44 · see citing works
The RNA hairpin binder TRIM71 modulates alternative splicing by repressing MBNL1Preprint
Welte, T., Tuck, A., Papasaikas, P., Carl, S. H., Flemr, M., Knuckles, P., Rankova, A., Bühler, M., & Großhans, H. (2019) · Genes & Development · doi:10.1101/gad.328492.119 · Cited by 45 · see citing works
In vitro neurogenesis: development and functional implications of iPSC technology
Compagnucci, C., Nizzardo, M., Corti, S. P., Zanni, G., & Bertini, E. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1511-1 · Cited by 43 · see citing works
Yin, N., Liang, S., Liang, S., Hu, B., Yang, R., Zhou, Q., Jiang, G., & Faiola, F. (2018) · Environmental Pollution · doi:10.1016/j.envpol.2018.01.035 · Cited by 44 · see citing works
- Authors
- Bibel, M., Richter, J., Lacroix, E., & Barde, Y.-A.
- Affiliations
- Novartis (Switzerland) (CH)
- University of Basel (CH)
- Corresponding author
- Bibel, Miriam
- ORCID
- Barde, Yves-Alain
- Venue
- Nature Protocols
- Published
- 2007-04-26
- Volume
- 2
- Issue
- 5
- Pages
- 1034-1043
- ISSN
- 1750-2799 (ISSN-L)
- 1754-2189
- OpenAlex
- W2080777953
- Cited by
- 283
- References
- 18
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 11 · 2023: 13 · 2022: 11 · 2021: 12 · 2020: 19 · 2019: 17 · 2018: 16 · 2017: 12 · 2016: 4 · 2015: 20 · 2014: 27 · 2013: 20 · 2012: 27
- FWCI
- 4.34
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Protocols (publishedVersion)
- PubMed (publishedVersion)
- ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
- 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
- mouse embryonic stem cells, neural progenitor cells, glutamatergic neurons, radial glia, Pax6, retinoic acid, neuronal differentiation, synaptic transmission, central nervous system development
- MeSH terms
- Animals, Cell Differentiation, Central Nervous System, Neurons, Tretinoin, Cell Culture Techniques, Mice, Embryonic Stem Cells
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