Neural progenitors adopt specific identities by directly repressing all alternative progenitor transcriptional programs
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In the vertebrate neural tube, a morphogen-induced transcriptional network produces multiple molecularly distinct progenitor domains, each generating different neuronal subtypes. Using an in vitro differentiation system, we defined gene expression signatures of distinct progenitor populations and identified direct gene-regulatory inputs corresponding to locations of specific transcription factor binding. Combined with targeted perturbations of the network, this revealed a mechanism in which a progenitor identity is installed by active repression of the entire transcriptional programs of other neural progenitor fates. In the ventral neural tube, sonic hedgehog (Shh) signaling, together with broadly expressed transcriptional activators, concurrently activates the gene expression programs of several domains. The specific outcome is selected by repressive input provided by Shh-induced transcription factors that act as the key nodes in the network, enabling progenitors to adopt a single definitive identity from several initially permitted options. Together, the data suggest design principles relevant to many developing tissues.
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These TFs form a gene regulatory network that establishes progenitor identities by repressing not only adjacent progenitor identities but also a wide range of alternative fates.
“These TFs form a gene regulatory network that establishes progenitor identities by repressing not only adjacent progenitor identities but also a wide range of alternative fates (Kutejova et al., 2016; Nishi et al., 2015).”
From Single cell transcriptomics reveals spatial and temporal dynamics of gene expression in the developing mouse spinal cord (2019) · cites this paper as Kutejova et al., 2016
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Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849 · see citing works
HTSeq—a Python framework to work with high-throughput sequencing data
Anders, S., Pyl, P. T., & Huber, W. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btu638 · Cited by 21,464 · see citing works
Model-based Analysis of ChIP-Seq (MACS)
Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., Nusbaum, C., Myers, R. M., Brown, M., Li, W., et al. (2008) · Genome Biology · doi:10.1186/gb-2008-9-9-r137 · Cited by 18,386 · 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
Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y. C., Laslo, P., Cheng, J. X., Murre, C., Singh, H., & Glass, C. K. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.05.004 · Cited by 13,382 · see citing works
TopHat: discovering splice junctions with RNA-Seq
Trapnell, C., Pachter, L. S., & Salzberg, S. L. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp120 · Cited by 11,477 · see citing works
Neuronal specification in the spinal cord: inductive signals and transcriptional codes
Jessell, T. M. (2000) · Nature Reviews Genetics · doi:10.1038/35049541 · Cited by 2,089 · see citing works
Quantifying similarity between motifs
Gupta, S., Stamatoyannopoulos, J. A., Bailey, T. L., & Noble, W. S. (2007) · Genome Biology · doi:10.1186/gb-2007-8-2-r24 · Cited by 2,058 · see citing works
Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture
Ying, Q.-L., Stavridis, M., Griffiths, D., Li, M., & Smith, A. (2003) · Nature Biotechnology · doi:10.1038/nbt780 · Cited by 1,504 · see citing works
The long-range interaction landscape of gene promoters
Sanyal, A., Lajoie, B. R., Jain, G., & Dekker, J. (2012) · Nature · doi:10.1038/nature11279 · Cited by 1,489 · see citing works
Cis-regulatory elements: Molecular mechanisms and evolutionary processes underlying divergence
Wittkopp, P. J., & Kalay, G. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3095 · Cited by 1,231 · see citing works
Briscoe, J., Pierani, A., Jessell, T. M., & Ericson, J. (2000) · Cell · doi:10.1016/s0092-8674(00)80853-3 · Cited by 1,111 · see citing works
Self-citationThe bHLH Transcription Factors OLIG2 and OLIG1 Couple Neuronal and Glial Subtype Specification
Zhou, Q., & Anderson, D. J. (2002) · Cell · doi:10.1016/s0092-8674(02)00677-3 · Cited by 1,059 · cited 1× · see citing works
“2 (Table S4), Irx3 expression expands ventrally in theOlig1/Olig2mutant but does not cross the dorsal boundary of the p3 domain (Zhou and Anderson, 2002).”
BackgroundPax6 Controls Progenitor Cell Identity and Neuronal Fate in Response to Graded Shh Signaling
Ericson, J., Rashbass, P., Schedl, A., Brenner‐Morton, S., Kawakami, A., van Heyningen, V., Jessell, T. M., & Briscoe, J. (1997) · Cell · doi:10.1016/s0092-8674(00)80323-2 · Cited by 1,044 · see citing works
Self-citationDensely Interconnected Transcriptional Circuits Control Cell States in Human Hematopoiesis
Novershtern, N., Subramanian, A., Lawton, L. N., Mak, R. H., Haining, W. N., McConkey, M. E., Habib, N., Yosef, N., Chang, C. Y., Shay, T., et al. (2011) · Cell · doi:10.1016/j.cell.2011.01.004 · Cited by 942 · see citing works
Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling
Briscoe, J., Sussel, L., Serup, P., Hartigan-O'Connor, D., Jessell, T., Rubenstein, J., & Ericson, J. (1999) · Nature · doi:10.1038/19315 · Cited by 807 · see citing works
Self-citationDessaud, É., McMahon, A. P., & Briscoe, J. (2008) · Development · doi:10.1242/dev.009324 · Cited by 735 · see citing works
Self-citationAn integrated software system for analyzing ChIP-chip and ChIP-seq data
Ji, H., Jiang, H., Ma, W., Johnson, D. S., Myers, R., & Wong, W. H. (2008) · Nature Biotechnology · doi:10.1038/nbt.1505 · Cited by 716 · see citing works
Zhou, Q., Choi, G. B., & Anderson, D. J. (2001) · Neuron · doi:10.1016/s0896-6273(01)00414-7 · Cited by 625 · see citing works
Novitch, B. G., Chen, A. I., & Jessell, T. M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00407-x · Cited by 615 · see citing works
Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism
Dessaud, É., Yang, L. L., Hill, K., Cox, B., Ulloa, F., Ribeiro, A., Mynett, A., Novitch, B. G., & Briscoe, J. (2007) · Nature · doi:10.1038/nature06347 · Cited by 613 · see citing works
Self-citationIdentification of intrinsic determinants of midbrain dopamine neurons
Andersson, E., Tryggvason, U., Deng, Q., Friling, S., Alekseenko, Z., Robert, B., Perlmann, T., & Ericson, J. (2006) · Cell · doi:10.1016/j.cell.2005.10.037 · Cited by 587 · see citing works
Emerging properties of animal gene regulatory networks
Davidson, E. H. (2010) · Nature · doi:10.1038/nature09645 · Cited by 579 · see citing works
Master Transcription Factors Determine Cell-Type-Specific Responses to TGF-β Signaling
Mullen, A. C., Orlando, D. A., Newman, J. J., Lovén, J., Kumar, R., Bilodeau, S., Reddy, J., Guenther, M. G., DeKoter, R. P., & Young, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.08.050 · Cited by 563 · see citing works
Enhancer loops appear stable during development and are associated with paused polymerase
Ghavi-Helm, Y., Klein, F. A., Pakozdi, T., Ciglar, L., Noordermeer, D., Huber, W., & Furlong, E. E. M. (2014) · Nature · doi:10.1038/nature13417 · Cited by 536 · see citing works
Oscillatory Control of Factors Determining Multipotency and Fate in Mouse Neural Progenitors
Imayoshi, I., Isomura, A., Harima, Y., Kawaguchi, K., Kori, H., Miyachi, H., Fujiwara, T., Ishidate, F., & Kageyama, R. (2013) · Science · doi:10.1126/science.1242366 · Cited by 509 · see citing works
Shadow enhancers as a source of evolutionary novelty
Hong, J.-W., Hendrix, D. A., & Levine, M. S. (2008) · Science · doi:10.1126/science.1160631 · Cited by 474 · see citing works
Mizuguchi, R., Sugimori, M., Takebayashi, H., Kosako, H., Nagao, M., Yoshida, S., Nabeshima, Y., Shimamura, K., & Nakafuku, M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00413-5 · Cited by 471 · see citing works
Chromatin connectivity maps reveal dynamic promoter–enhancer long-range associations
Zhang, Y., Wong, C., Birnbaum, R. Y., Li, G., Favaro, R., Ngan, C. Y., Lim, J., Tai, E., Poh, H. M., Wong, E., et al. (2013) · Nature · doi:10.1038/nature12716 · Cited by 470 · see citing works
Balaskas, N., Ribeiro, A., Panovska, J., Dessaud, E., Sasai, N., Page, K., Briscoe, J., & Ribes, V. (2012) · Cell · doi:10.1016/j.cell.2011.10.047 · Cited by 468 · see citing works
Self-citationTranscriptional Enhancers in Animal Development and Evolution
Levine, M. (2010) · Current Biology · doi:10.1016/j.cub.2010.06.070 · Cited by 449 · see citing works
Muhr, J., Andersson, E., Persson, M., Jessell, T., & Ericson, J. (2001) · Cell · doi:10.1016/s0092-8674(01)00283-5 · Cited by 412 · see citing works
Litingtung, Y., & Chiang, C. C. (2000) · Nature Neuroscience · doi:10.1038/79916 · Cited by 392 · see citing works
Briscoe, J., Chen, Y., Jessell, T. M., & Struhl, G. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00271-4 · Cited by 364 · see citing works
Self-citationNovitch, B. G., Wichterle, H., Jessell, T. M., & Sockanathan, S. (2003) · Neuron · doi:10.1016/j.neuron.2003.08.006 · Cited by 350 · see citing works
SnapShot: spinal cord development
Alaynick, W. A., Jessell, T. M., & Pfaff, S. L. (2011) · Cell · doi:10.1016/j.cell.2011.06.038 · Cited by 338 · see citing works
Dorsal-ventral patterning of the spinal cord requires Gli3 transcriptional repressor activityPreprint
Persson, M., Stamataki, D., Welscher, P. T., Andersson, E., Böse, J., Rüther, U., Ericson, J., & Briscoe, J. (2002) · Genes & Development · doi:10.1101/gad.243402 · Cited by 306 · see citing works
Self-citationSequentially acting Sox transcription factors in neural lineage developmentPreprint
Bergsland, M., Ramsköld, D., Zaouter, C., Klum, S., Sandberg, R., & Muhr, J. (2011) · Genes & Development · doi:10.1101/gad.176008.111 · Cited by 305 · see citing works
Trompouki, E., Bowman, T. V., Lawton, L. N., Fan, Z. P., Wu, D.-C., DiBiase, A., Martin, C., Cech, J. N., Sessa, A. K., LeBlanc, J., et al. (2011) · Cell · doi:10.1016/j.cell.2011.09.044 · Cited by 303 · see citing works
Transcriptional networks regulating neuronal identity in the developing spinal cord
Lee, S., & Pfaff, S. L. (2001) · Nature Neuroscience · doi:10.1038/nn750 · Cited by 290 · see citing works
Vallstedt, A., Muhr, J., Pattyn, A., Pierani, A., Mendelsohn, M., Sander, M., Jessell, T., & Ericson, J. (2001) · Neuron · doi:10.1016/s0896-6273(01)00412-3 · Cited by 288 · see citing works
Canalization of Gene Expression in the Drosophila Blastoderm by Gap Gene Cross Regulation
Manu, Surkova, S. Y., Spirov, A. V., Gursky, V. V., Janssens, H., Kim, A.-R., Radulescu, O., Vanario‐Alonso, C. E., Sharp, D. H., Samsonova, M. G., et al. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000049 · Cited by 280 · see citing works
Sander, M., Paydar, S., Ericson, J., Briscoe, J., Berber, E., German, M., Jessell, T. M., & Rubenstein, J. L. R. (2000) · Genes & Development · doi:10.1101/gad.820400 · Cited by 270 · see citing works
Self-citationGenomic characterization of Gli-activator targets in sonic hedgehog-mediated neural patterning
Vokes, S. A., Ji, H., McCuine, S., Tenzen, T., Giles, S., Zhong, S., Longabaugh, W. J. R., Davidson, E. H., Wong, W. H., & McMahon, A. P. (2007) · Development · doi:10.1242/dev.001966 · Cited by 270 · see citing works
Wijgerde, M., McMahon, J. A., Rule, M. C., & McMahon, A. P. (2002) · Genes & Development · doi:10.1101/gad.1025702 · Cited by 258 · see citing works
Shadow Enhancers Are Pervasive Features of Developmental Regulatory Networks
Cannavò, E., Khoueiry, P., Garfield, D. A., Geeleher, P., Zichner, T., Gustafson, E. H., Ciglar, L., Korbel, J. O., & Furlong, E. E. M. (2016) · Current Biology · doi:10.1016/j.cub.2015.11.034 · Cited by 235 · see citing works
Jeong, J., & McMahon, A. P. (2004) · Development · doi:10.1242/dev.01566 · Cited by 223 · see citing works
Characterization of the Drosophila segment determination morphome
Surkova, S. Y., Kosman, D., Kozlov, K. N., Manu, Myasnikova, E. M., Samsonova, A. A., Spirov, A. V., Vanario‐Alonso, C. E., Samsonova, M. G., & Reinitz, J. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.10.037 · Cited by 197 · see citing works
Ribes, V., Balaskas, N., Sasai, N., Cruz, C., Dessaud, É., Cayuso, J., Tozer, S., Yang, L., Novitch, B. G., Martı́, E., et al. (2010) · Genes & Development · doi:10.1101/gad.559910 · Cited by 193 · see citing works
Self-citationCoordination of progenitor specification and growth in mouse and chick spinal cord
Kicheva, A., Bollenbach, T., Ribeiro, A., Valle, H. P., Lovell-Badge, R., Episkopou, V., & Briscoe, J. (2014) · Science · doi:10.1126/science.1254927 · Cited by 180 · see citing works
Self-citationPeterson, K. A., Nishi, Y., Ma, W., Vedenko, A., Shokri, L., Zhang, X., McFarlane, M., Baizabal, J., Junker, J. P., van Oudenaarden, A., et al. (2012) · Genes & Development · doi:10.1101/gad.207142.112 · Cited by 166 · see citing works
Lee, S.-K., Jurata, L., Funahashi, J., Ruiz, E. C., & Pfaff, S. (2004) · Development · doi:10.1242/dev.01179 · Cited by 142 · see citing works
Barolo, S. (2012) · BioEssays · doi:10.1002/bies.201100121 · Cited by 136 · see citing works
Oosterveen, T., Kurdija, S., Alekseenko, Z., Uhde, C. W., Bergsland, M., Sandberg, M., Andersson, E., Dias, J. M. M., Muhr, J., & Ericson, J. (2012) · Developmental Cell · doi:10.1016/j.devcel.2012.09.015 · Cited by 132 · see citing works
A System of Repressor Gradients Spatially Organizes the Boundaries of Bicoid-Dependent Target Genes
Chen, H., Xu, Z., Mei, C., Yu, D., & Small, S. (2012) · Cell · doi:10.1016/j.cell.2012.03.018 · Cited by 132 · see citing works
Reeves, G. T., Trisnadi, N., Truong, T. V., Nahmad, M., Katz, S. S., & Stathopoulos, A. (2012) · Developmental Cell · doi:10.1016/j.devcel.2011.12.007 · Cited by 112 · see citing works
Selfridge, J., Pow, A. M., McWhir, J., Magin, T. M., & Melton, D. W. (1992) · Somatic Cell and Molecular Genetics · doi:10.1007/bf01235756 · Cited by 110 · see citing works
Xu, Z., Chen, H., Jia, L., Yu, D., Struffi, P., & Small, S. (2014) · Genes & Development · doi:10.1101/gad.234534.113 · Cited by 94 · see citing works
Lek, M., Dias, J. M., Marklund, U., Uhde, C. W., Kurdija, S., Lei, Q., Sussel, L., Rubenstein, J., Matise, M., Arnold, H., et al. (2010) · Development · doi:10.1242/dev.054288 · Cited by 90 · see citing works
A theoretical framework for the regulation of Shh morphogen-controlled gene expression
Cohen, M., Page, K. M., Perez‐Carrasco, R., Barnes, C. P., & Briscoe, J. (2014) · Development · doi:10.1242/dev.112573 · Cited by 79 · see citing works
Self-citationSasai, N., Kutejova, E., & Briscoe, J. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1001907 · Cited by 76 · see citing works
Self-citationSoxB1-driven transcriptional network underlies neural-specific interpretation of morphogen signals
Oosterveen, T., Kurdija, S., Ensterö, M., Uhde, C. W., Bergsland, M., Sandberg, M., Sandberg, R., Muhr, J., & Ericson, J. (2013) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1220010110 · Cited by 61 · see citing works
STAT Is an Essential Activator of the Zygotic Genome in the Early Drosophila Embryo
Tsurumi, A., Fan, X., Li, J., Larson, K., LaFrance, R. M., & Li, W. X. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002086 · Cited by 55 · see citing works
A direct fate exclusion mechanism by Sonic hedgehog-regulated transcriptional repressors
Nishi, Y., Zhang, X., Jeong, J., Peterson, K. A., Vedenko, A., Bulyk, M. L., Hide, W. A., & McMahon, A. P. (2015) · Development · doi:10.1242/dev.124636 · Cited by 53 · see citing works
Six2 functions redundantly immediately downstream of Hoxa2
Kutejova, E., Engist, B., Self, M., Oliver, G. C., Kirilenko, P., & Bobola, N. (2008) · Development · doi:10.1242/dev.017624 · Cited by 49 · see citing works
Self-citationA global genomic transcriptional code associated with CNS-expressed genes
Bailey, P. J., Klos, J. M., Andersson, E., Karlén, M., Källström, M., Ponjavic, J., Muhr, J., Lenhard, B., Sandelin, A., & Ericson, J. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.06.017 · Cited by 46 · see citing works
Rushlow, C. A., & Shvartsman, S. Y. (2012) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2012.08.005 · Cited by 45 · see citing works
Gouti, M., & Gavalas, A. (2008) · Stem Cells · doi:10.1634/stemcells.2008-0182 · Cited by 42 · see citing works
Self-citationÖzdemir, A., Ma, L., White, K. P., & Stathopoulos, A. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.08.005 · Cited by 35 · see citing works
Lovrics, A., Gao, Y., Juhász, B., Bock, I., Byrne, H., Dinnyés, A., & Kovács, K. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0111430 · Cited by 29 · see citing works
Liang, H.-L., Xu, M., Chuang, Y.-C., & Rushlow, C. A. (2012) · Development · doi:10.1242/dev.079772 · Cited by 18 · see citing works
Mansour, A. A., Zisman, S., Netser, Y., Klar, A., & Ben‐Arie, N. (2014) · Development · doi:10.1242/dev.104372 · Cited by 14 · see citing works
Flagged first, then by citations
1 of the 73 references couldn’t be matched to a known paper.
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Transition states and cell fate decisions in epigenetic landscapes
Moris, N., Pina, C., & Arias, A. M. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.98 · Cited by 438 · see citing works
Delile, J., Rayon, T., Melchionda, M., Edwards, A., Briscoe, J., & Sagner, A. (2019) · Development · doi:10.1242/dev.173807 · Cited by 356 · see citing works
Self-citationEstablishing neuronal diversity in the spinal cord: a time and a place
Sagner, A., & Briscoe, J. (2019) · Development · doi:10.1242/dev.182154 · Cited by 282 · see citing works
Self-citationCholesterol activates the G-protein coupled receptor Smoothened to promote Hedgehog signaling
Luchetti, G., Sircar, R., Kong, J. H., Nachtergaele, S., Sagner, A., Byrne, E. F. X., Covey, D. F., Siebold, C., & Rohatgi, R. (2016) · eLife · doi:10.7554/elife.20304 · Cited by 256 · see citing works
Making sense out of spinal cord somatosensory development
Lai, H. C., Seal, R. P., & Johnson, J. E. (2016) · Development · doi:10.1242/dev.139592 · Cited by 188 · see citing works
Morphogen interpretation: concentration, time, competence, and signaling dynamics
Sagner, A., & Briscoe, J. (2017) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.271 · Cited by 164 · see citing works
Self-citationNervous System Regionalization Entails Axial Allocation before Neural Differentiation
Metzis, V., Steinhauser, S., Pakanavicius, E., Gouti, M., Stamataki, D., Ivanovitch, K., Watson, T., Rayón, T., Mousavy-Gharavy, S. N., Lovell-Badge, R. H., et al. (2018) · Cell · doi:10.1016/j.cell.2018.09.040 · Cited by 153 · see citing works
Self-citationHedgehog Signal and Genetic Disorders
Sasai, N., Toriyama, M., & Kondo, T. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.01103 · Cited by 141 · see citing works
Self-citationSagner, A., Gaber, Z. B., Delile, J., Kong, J. H., Rousso, D. L., Pearson, C. A., Weicksel, S. E., Melchionda, M., Mousavy Gharavy, S. N., Briscoe, J., et al. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2003127 · Cited by 96 · see citing works
Self-citationSpatiotemporal, optogenetic control of gene expression in organoids
Legnini, I., Emmenegger, L., Zappulo, A., Rybak‐Wolf, A., Wurmus, R., Oliveras, A., Cerda, C., Boltengagen, A., Hessler, T., Mastrobuoni, G., et al. (2023) · Nature Methods · doi:10.1038/s41592-023-01986-w · Cited by 99 · see citing works
Pervasive translational regulation of the cell signalling circuitry underlies mammalian development
Fujii, K., Shi, Z., Zhulyn, O., Denans, N., & Barna, M. (2017) · Nature Communications · doi:10.1038/ncomms14443 · Cited by 76 · see citing works
The Multiple Roles of FGF Signaling in the Developing Spinal Cord
del Corral, R. D., & Morales, A. V. (2017) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2017.00058 · Cited by 69 · see citing works
Precision of tissue patterning is controlled by dynamical properties of gene regulatory networks
Exelby, K., Herrera-Delgado, E., Garcia-Perez, L., Perez‐Carrasco, R., Sagner, A., Metzis, V., Peter Sollich, A., & Briscoe, J. (2021) · Development · doi:10.1242/dev.197566 · Cited by 67 · see citing works
Self-citationThe multiple facets of Cajal-Retzius neurons
Causeret, F., Moreau, M. X., Pierani, A., & Blanquie, O. (2021) · Development · doi:10.1242/dev.199409 · Cited by 66 · see citing works
Hall, E. T., Dillard, M. E., Stewart, D. P., Zhang, Y., Wagner, B., Levine, R. M., Pruett‐Miller, S. M., Sykes, A. D., Temirov, J. P., Cheney, R. E., et al. (2021) · eLife · doi:10.7554/elife.61432 · Cited by 66 · see citing works
Okamoto, T., Imaizumi, K., & Kaneko, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21113921 · Cited by 60 · see citing works
Meganathan, K., Lewis, E. M. A., Gontarz, P. M., Liu, S., Stanley, E. G., Elefanty, A. G., Huettner, J. E., Zhang, B., & Kroll, K. L. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1712365115 · Cited by 58 · see citing works
TWIST1 and chromatin regulatory proteins interact to guide neural crest cell differentiation
Fan, X., Masamsetti, V. P., Sun, J. Q. J., Engholm‐Keller, K., Osteil, P., Studdert, J. B., Graham, M. E., Fossat, N., & Tam, P. (2021) · eLife · doi:10.7554/elife.62873 · Cited by 51 · see citing works
New perspectives on the mechanisms establishing the dorsal-ventral axis of the spinal cord
Andrews, M. G., Kong, J. H., Novitch, B. G., & Butler, S. J. (2018) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2018.12.010 · Cited by 50 · see citing works
Delás, M., Kalaitzis, C. M., Fawzi, T., Demuth, M., Zhang, I., Stuart, H., Costantini, E., Ivanovitch, K., Tanaka, E. M., & Briscoe, J. (2022) · Developmental Cell · doi:10.1016/j.devcel.2022.11.016 · Cited by 31 · see citing works
Self-citationDesign principles of tissue organisation: How single cells coordinate across scales
Zinner, M., Lukonin, I., & Liberali, P. (2020) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2020.07.004 · Cited by 49 · see citing works
Repression by PRDM13 is critical for generating precision in neuronal identity
Mona, B., Urueña, A., Kollipara, R., Ma, Z., Borromeo, M. D., Chang, J. C., & Johnson, J. E. (2017) · eLife · doi:10.7554/elife.25787 · Cited by 44 · see citing works
Chen, T., & Chen, J. (2019) · eLife · doi:10.7554/elife.50848 · Cited by 41 · see citing works
Belmonte‐Mateos, C., & Pujades, C. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.781160 · Cited by 39 · see citing works
Memory functions reveal structural properties of gene regulatory networks
Herrera-Delgado, E., Pérez-Carrasco, R., Briscoe, J., & Sollich, P. (2017) · PLoS Comput. Biol. · doi:10.1371/journal.pcbi.1006003 · Cited by 31 · see citing works
Self-citationEvolution of vertebrate spinal cord patterning
Leung, B., & Shimeld, S. M. (2019) · Developmental Dynamics · doi:10.1002/dvdy.77 · Cited by 33 · see citing works
From signalling to form: the coordination of neural tube patterning
Frith, T. J. R., Briscoe, J., & Boezio, G. L. M. (2023) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2023.11.004 · Cited by 31 · see citing works
Self-citationSternfeld, M. J., Hinckley, C. A., Moore, N. J., Pankratz, M. T., Hilde, K. L., Driscoll, S. P., Hayashi, M., Amin, N. D., Bonanomi, D., Gifford, W. D., et al. (2017) · eLife · doi:10.7554/elife.21540 · Cited by 31 · see citing works
Rowton, M., Perez-Cervantes, C., Hur, S. S. J., Jacobs-Li, J., Lu, E., Deng, N., Guzzetta, A., Hoffmann, A. D., Stocker, M., Steimle, J. D., et al. (2022) · Developmental Cell · doi:10.1016/j.devcel.2022.08.009 · Cited by 33 · see citing works
Applying gene regulatory network logic to the evolution of social behavior
Baran, N. M., McGrath, P. T., & Streelman, J. T. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1610621114 · Cited by 30 · see citing works
Understanding Pattern Formation in Embryos: Experiment, Theory, and Simulation
Briscoe, J. (2019) · Journal of Computational Biology · doi:10.1089/cmb.2019.0090 · Cited by 30 · see citing works
Self-citationGenerating neural diversity through spatial and temporal patterning
Sen, S. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.06.002 · Cited by 28 · see citing works
Domsch, K., Carnesecchi, J., Disela, V., Friedrich, J., Trost, N., Ermakova, O. V., Polychronidou, M., & Lohmann, I. (2019) · eLife · doi:10.7554/elife.42675 · Cited by 26 · see citing works
Repressive interactions in gene regulatory networks: When you have no other choice.
Delás, M., & Briscoe, J. (2020) · Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2020.03.003 · Cited by 24 · see citing works
Self-citationProgress in the generation of spinal cord organoids over the past decade and future perspectives
Zhou, G., Pang, S., Li, Y.-N., & Gao, J. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.385280 · Cited by 23 · see citing works
Neural induction: Historical views and application to pluripotent stem cells
Sasai, N., Kadoya, M., & Ong, A. L. C. (2020) · Development Growth & Differentiation · doi:10.1111/dgd.12703 · Cited by 22 · see citing works
Self-citationGard, C., Curto, G. G., Frarma, Y. E.-M., Chollet, E., Duval, N., Auzié, V., Aurade, F., Vigier, L., Relaix, F., Pierani, A., et al. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.06.014 · Cited by 22 · see citing works
Azambujá, A. P., & Simões-Costa, M. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009296 · Cited by 19 · see citing works
Yatsuzuka, A., Hori, A., Kadoya, M., Matsuo‐Takasaki, M., Kondo, T., & Sasai, N. (2019) · Development · doi:10.1242/dev.176784 · Cited by 18 · see citing works
Self-citationThe cis-regulatory logic integrating spatial and temporal patterning in the vertebrate neural tube
Zhang, I., Boezio, G. L. M., Cornwall-Scoones, J., Frith, T. J. R., Finnie, E., Luo, J., Jiang, M., Howell, M. T., Lovell-Badge, R. H., Sagner, A., et al. (2025) · Developmental Cell · doi:10.1016/j.devcel.2025.06.029 · Cited by 17 · see citing works
Self-citationTMED2 binding restricts SMO to the ER and Golgi compartments
Minin, G. D., Holzner, M., Grison, A., Dumeau, C.-É., Chan, W., Monfort, A., Jerome‐Majewska, L. A., Roelink, H., & Wutz, A. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001596 · Cited by 16 · see citing works
In vitro models of spinal motor circuit’s development in mammals: achievements and challenges
Nedelec, S., & Martínez-Arias, A. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.12.002 · Cited by 14 · see citing works
Negative Regulation of mTOR Signaling Restricts Cell Proliferation in the Floor Plate
Kadoya, M., & Sasai, N. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01022 · Cited by 15 · see citing works
Self-citationCooperation between HDAC3 and DAX1 mediates lineage restriction of embryonic stem cells
Olivieri, D., Castelli, E., Kawamura, Y., Papasaikas, P., Lukonin, I., Rittirsch, M., Heß, D., Smallwood, S. A., Stadler, M. B., Peters, A. H. F. M., et al. (2021) · The EMBO Journal · doi:10.15252/embj.2020106818 · Cited by 13 · see citing works
Dynamic switching of lateral inhibition spatial patterns
Hawley, J., Manning, C. S., Biga, V., Glendinning, P., & Papalopulu, N. (2022) · Journal of The Royal Society Interface · doi:10.1098/rsif.2022.0339 · Cited by 12 · see citing works
Zebrafish spinal cord oligodendrocyte formation requires boc function
Kearns, C. A., Walker, M. B., Ravanelli, A. M., Scott, K., Arzbecker, M. R., & Appel, B. (2021) · Genetics · doi:10.1093/genetics/iyab082 · Cited by 12 · see citing works
Early enforcement of cell identity by a functional component of the terminally differentiated state
Bahrami-Nejad, Z., Chen, T., Tholen, S., Zhang, Z., Rabiee, A., Zhao, M. L., Kraemer, F. B., & Teruel, M. N. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001900 · Cited by 11 · see citing works
Spatio-temporal, optogenetic control of gene expression in organoidsPreprint
Legnini, I., Emmenegger, L., Zappulo, A., Wurmus, R., Oliveras, A., Cerda, C., Boltengagen, A., Hessler, T., Mastrobuoni, G., Rybak‐Wolf, A., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.09.26.461850 · Cited by 10 · see citing works
Gupta, S. K., & Butler, S. J. (2021) · WIREs Mechanisms of Disease · doi:10.1002/wsbm.1520 · Cited by 8 · see citing works
Origin and circuitry of spinal locomotor interneurons generating different speeds
Boije, H., & Kullander, K. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.04.024 · Cited by 9 · see citing works
Dynamics of morphogen source formation in a growing tissue
Ho, R. D. J. G., Kishi, K., Majka, M., Kicheva, A., & Zagórski, M. (2024) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1012508 · Cited by 8 · see citing works
Vermeiren, S., Cabochette, P., Dannawi, M., Desiderio, S., José, A. S. S., Achouri, Y., Kricha, S., Sitte, M., Salinas, G., Vanhollebeke, B., et al. (2023) · iScience · doi:10.1016/j.isci.2023.108364 · Cited by 7 · see citing works
scMultiome analysis identifies embryonic hindbrain progenitors with mixed rhombomere identities
Kim, Y.-I., O’Rourke, R., & Sagerström, C. G. (2023) · eLife · doi:10.7554/elife.87772 · Cited by 6 · see citing works
Regulating the dorsal neural tube expression of Ptf1a through a distal 3′ enhancer
Mona, B., Avila, J., Meredith, D., Kollipara, R., & Johnson, J. E. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.06.033 · Cited by 7 · see citing works
Sox14 is essential for initiation of neuronal differentiation in the chick spinal cord
Katsuyama, T., Kadoya, M., Shirai, M., & Sasai, N. (2021) · Developmental Dynamics · doi:10.1002/dvdy.392 · Cited by 7 · see citing works
Self-citationZheng, Y., Li, X., Nie, H., Zhang, F., Xun, J., Xu, S., & Wu, L. (2024) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2024.174772 · Cited by 6 · see citing works
Mukaigasa, K., Sakuma, C., & Yaginuma, H. (2021) · Development Growth & Differentiation · doi:10.1111/dgd.12750 · Cited by 5 · see citing works
Kodama, H., Miyata, Y., Kuwajima, M., Izuchi, R., Kobayashi, A., Gyoja, F., Onuma, T. A., Kumano, G., & Nishida, H. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.05.033 · Cited by 6 · see citing works
prdm1a drives a fate switch between hair cells of different mechanosensory organs
Sandler, J. E., Tsai, Y.-Y., Chen, S., Sabin, L., Lush, M. E., Sur, A., Ellis, E., Tran, N. T. T., Cook, M. E., Scott, A. R., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-62942-0 · Cited by 5 · see citing works
Rowton, M., Perez-Cervantes, C., Rydeen, A. B., Hur, S. S. J., Jacobs-Li, J., Deng, N., Lu, E., Guzzetta, A., Steimle, J. D., Hoffmann, A. D., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/270751 · Cited by 5 · see citing works
Rondon, R., Hezez, T., Albert, J. R., Hayashi, S., Drayton‐Libotte, B., Curto, G. G., Aurade, F., Balloul, É., Dugast‐Darzacq, C., Relaix, F., et al. (2025) · PLoS Biology · doi:10.1371/journal.pbio.3003448 · Cited by 3 · see citing works
Applying Spinal Cord Organoids as a quantitative approach to study the mammalian Hedgehog pathway
Holzner, M., Wutz, A., & Minin, G. D. (2024) · PLoS ONE · doi:10.1371/journal.pone.0301670 · Cited by 3 · see citing works
Yamamoto, M., Ong, A. L. C., Shinozuka, T., Shirai, M., & Sasai, N. (2023) · Stem Cells · doi:10.1093/stmcls/sxad018 · Cited by 3 · see citing works
Self-citationTwo ways to skin a new cell fate
Zaret, K. S. (2023) · Developmental Cell · doi:10.1016/j.devcel.2022.12.002 · Cited by 2 · see citing works
Hamann, C. A., Kjar, A., Kim, H., Simmons, A. J., Brien, H. J., Quartey, C. I., Walton, B. L., Lau, K. S., Lippmann, E. S., & Brunger, J. M. (2025) · ACS Synthetic Biology · doi:10.1021/acssynbio.4c00742 · Cited by 2 · see citing works
Tmed2 regulates Smoothened trafficking and Hedgehog signallingPreprint
Minin, G. D., Dumeau, C.-É., Grison, A., Chan, W., Monfort, A., Jerome‐Majewska, L. A., & Wutz, A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.04.20.049957 · Cited by 2 · see citing works
Myosin 10 and a Cytoneme-Localized Ligand Complex Promote Morphogen TransportPreprint
Hall, E. T., Stewart, D. P., Dillard, M. E., Wagner, B., Sykes, A. D., Temirov, J. P., Cheney, R. E., Mori, M., Robinson, C. G., & Ogden, S. K. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.06.080820 · Cited by 2 · see citing works
Chen, X., Sakumura, Y., Kokaji, T., Kunida, K., & Sasai, N. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.08.25.609396 · Cited by 2 · see citing works
Self-citationCell type-specific functions of the PBAF chromatin-remodeling complex in neuronal diversification
Osuma, A., Destain, H., Mann, J., Li, Y., Taylor, S. R., Prahlad, M., Weigle, I. Q., Marques, F., Schulz, N. G., Mathies, L. D., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-67434-9 · Cited by 1 · see citing works
Retinoic acid in health and disease
Angelis, M. T. D., Dattilo, V., Vono, N., Lise, V., Reda, M., Marco, C. D., Rizzuto, A., Trapasso, F., Viglietto, G., & Santamaria, G. (2026) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-026-03055-y · Cited by 1 · see citing works
Homeodomain Transcription Factors Nkx2.2 and Pax6 as Novel Biomarkers for Meningioma Tumor Treatment
Farheen, S., M., M. M. P., Rehman, S., Hoda, M. F., Gupta, Y., Ali, A., Chosdol, K., & Shahi, M. H. (2022) · Indian Journal of Clinical Biochemistry · doi:10.1007/s12291-022-01085-1 · Cited by 1 · see citing works
Sasai, N., Tada, S., Ohshiro, J., Kogiso, C., & Shinozuka, T. (2023) · Development Growth & Differentiation · doi:10.1111/dgd.12905 · Cited by 1 · see citing works
Self-citationMatise, M. P., & Rallo, M. S. (2022) · Springer eBooks · doi:10.1007/978-3-030-88832-9_187 · Cited by 1 · see citing works
Yatsuzuka, A., Hori, A., Kadoya, M., Matsuo‐Takasaki, M., Kondo, T., & Sasai, N. (2018) · bioRxiv · doi:10.1101/424598 · Cited by 2 · see citing works
Self-citationSox14 is essential for initiation of interneuron differentiation in the chick spinal cordPreprint
Katsuyama, T., Kadoya, M., Shirai, M., & Sasai, N. (2021) · Research Square · doi:10.21203/rs.3.rs-243180/v1 · Cited by 1 · see citing works
Self-citationSpatial ciliary signaling regulates the dorsal/ventral regionalization of human brain organoidsPreprint
Shimada, I. S., Goto, A., Hashimoto, Y., Takase, H., Itoh, M., & Kato, Y. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.07.18.604098 · Cited by 1 · see citing works
Rondon, R., Hezez, T., Albert, J. R., Drayton‐Libotte, B., Curto, G. G., Relaix, F., Dugast‐Darzacq, C., Gilardi‐Hebenstreit, P., & Ribes, V. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.11.642668 · Cited by 1 · see citing works
Kalcheim, C. (2021) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.739535968.793585052
Matise, M. P., & Rallo, M. S. (2022) · Springer eBooks · doi:10.1007/978-1-4614-6434-1_187-1
Yamamoto, M., Ong, A. L. C., Shinozuka, T., Shirai, M., & Sasai, N. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.08.23.505035
Self-citationSpinal interneurons and cellular engineering
White, N., & Sakiyama‐Elbert, S. E. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-819260-3.00004-4
Biga, V., Miller, A., Kamath, A., Mak, Y. Q. P., Adamson, A. D., Marinopoulou, E., François, P., Papalopulu, N., & Manning, C. S. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.22.655498
Tesson, B., & Vincent, S. (2025) · Science Advances · doi:10.1126/sciadv.adv0311
Stem cell-based approach to identify regulatory TFs during mammalian cell differentiation
Pei, Y., Li, S., Garipler, G., Kamimoto, K., & Mazzoni, E. O. (2025) · Stem Cell Reports · doi:10.1016/j.stemcr.2025.102716
Pax6-dependent patterning in an annelid informs the evolution of bilaterian nerve cordsPreprint
Doderovic, J., Kolek, M., Zitova, A., Kozmiková, I., & Kozmík, Z. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.27.734823
- Authors
- Kutejova, E., Sasai, N., Shah, A., Gouti, M., & Briscoe, J.
- Affiliations
- National Institute for Medical Research (GB)
- Corresponding author
- Briscoe, James
- Venue
- Developmental Cell
- Publisher
- Elsevier BV
- Published
- 2016-03
- Volume
- 36
- Issue
- 6
- Pages
- 639-653
- ISSN
- 1534-5807 (ISSN-L)
- PMC
- PMC4819439
- OpenAlex
- W2296594992
- Cited by
- 87
- References
- 73
- Citations by year
- 2026: 2 · 2025: 9 · 2024: 5 · 2023: 8 · 2022: 13 · 2021: 15 · 2020: 6 · 2019: 9 · 2018: 7 · 2017: 8 · 2016: 5
- FWCI
- 5.03
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Developmental Cell (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (acceptedVersion)
- Figshare (submittedVersion, cc-by)
- Institutional Repositories DataBase (IRDB) (submittedVersion)
- NAIST Digital Library (Nara Institute of Science and Technology) (submittedVersion, cc-by-nc-nd)
- Funders
- MRC (U117560541)
- Wellcome Trust (WT098326MA)
- EMBO
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Hedgehog Signaling Pathway Studies
- Keywords
- transcriptional repression, neural tube, Sonic hedgehog signaling, transcription factor binding, neuronal subtype specification, progenitor cell differentiation, gene regulatory networks, transcriptional activator, ventral neural tube
- MeSH terms
- Oligodendrocyte Transcription Factor 2, Homeobox Protein Nkx-2.2, Animals, Cell Differentiation, Cell Line, Chick Embryo, Nerve Tissue Proteins, Transcription Factors, Transcription, Genetic, Signal Transduction, Homeodomain Proteins, Gene Expression Regulation, Developmental, Cell Lineage, Body Patterning, Zebrafish Proteins, Mice, Basic Helix-Loop-Helix Transcription Factors, Basic Helix-Loop-Helix Proteins, Neural Stem Cells
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