The DOI matches its Crossref record; 50 of the 51 references it cites were found in a registry or an index.
Vertebrate neurogenesis is counteracted by Sox1–3 activity
Abstract
The generation of neurons from stem cells involves the activity of proneural basic helix-loop-helix (bHLH) proteins, but the mechanism by which these proteins irreversibly commit stem cells to neuronal differentiation is not known. Here we report that expression of the transcription factors Sox1, Sox2 and Sox3 (Sox1-3) is a critical determinant of neurogenesis. Using chick in ovo electroporation, we found that Sox1-3 transcription factors keep neural cells undifferentiated by counteracting the activity of proneural proteins. Conversely, the capacity of proneural bHLH proteins to direct neuronal differentiation critically depends on their ability to suppress Sox1-3 expression in CNS progenitors. These data suggest that the generation of neurons from stem cells depends on the inhibition of Sox1-3 expression by proneural proteins.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Members of SoxB1 and SoxB2 subgroups are especially important during neurogenesis [68,69].”
From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [68]
Citations
Cites
Multipotent cell lineages in early mouse development depend on SOX2 functionPreprint
Avilion, A. A., Nicolis, S. K., Pevny, L., Pérez, L., Vivian, N., & Lovell-Badge, R. H. (2003) · Genes & Development · doi:10.1101/gad.224503 · Cited by 2,372
NeuN, a neuronal specific nuclear protein in vertebratesxs
Mullen, R. J., Buck, C. R., & Smith, A. M. (1992) · Development · doi:10.1242/dev.116.1.201 · Cited by 2,351
Proneural genes and the specification of neural cell types
Bertrand, N., Castro, D. S., & Guillemot, F. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn874 · Cited by 1,572
Briscoe, J., Pierani, A., Jessell, T. M., & Ericson, J. (2000) · Cell · doi:10.1016/s0092-8674(00)80853-3 · Cited by 1,111
Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes
Tsuchida, T., Ensini, M., Brenner‐Morton, S., Baldassare, M., Edlund, H., Jessell, T. M., & Pfaff, S. L. (1994) · Cell · doi:10.1016/0092-8674(94)90027-2 · Cited by 997
PCNA: structure, functions and interactions
Kelman, Z. (1997) · Oncogene · doi:10.1038/sj.onc.1200886 · Cited by 929
From head to toes: the multiple facets of Sox proteins
Wegner, M. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.6.1409 · Cited by 890
Identification of neurogenin, a vertebrate neuronal determination gene.
Ma, Q.-F., Kintner, C., & Anderson, D. J. (1996) · Cell · doi:10.1016/s0092-8674(00)81321-5 · Cited by 874
Yuan, H., Corbi, N., Basilico, C., & Dailey, L. (1995) · Genes & Development · doi:10.1101/gad.9.21.2635 · Cited by 811
Pairing SOX off: with partners in the regulation of embryonic development
Kamachi, Y., Uchikawa, M., & Kondoh, H. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(99)01955-1 · Cited by 641
Novitch, B. G., Chen, A. I., & Jessell, T. M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00407-x · Cited by 615
Self-citationSOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells.
Kim, J., Lo, L., Dormand, E., & Anderson, D. J. (2003) · Neuron · doi:10.1016/s0896-6273(03)00163-6 · Cited by 584
Specification of neuronal fates in the ventral neural tube
Briscoe, J., & Ericson, J. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00172-0 · Cited by 548
A comparison of the properties of Sox-3 with Sry and two related genes, Sox-1 and Sox-2
Collignon, J., Sockanathan, S., Hacker, A., Cohen‐Tannoudji, M., Norris, D. P., Rastan, S., Stevanović, M. J., Goodfellow, P. N., & Lovell-Badge, R. H. (1996) · Development · doi:10.1242/dev.122.2.509 · Cited by 496
A role for SOX1 in neural determination
Pevny, L., Sockanathan, S., Placzek, M., & Lovell-Badge, R. H. (1998) · Development · doi:10.1242/dev.125.10.1967 · Cited by 475
Generation of neurons by transient expression of neural bHLH proteins in mammalian cells
Farah, M. H., Olson, J. M., Sucic, H. B., Hume, R. I., Tapscott, S. J., & Turner, D. L. (2000) · Development · doi:10.1242/dev.127.4.693 · Cited by 472
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
Schuurmans, C. J., Gradwohl, G., Morin, X., Dierich, A., LeMeur, M., Goridis, C., & Guillemot, F. (1998) · Neuron · doi:10.1016/s0896-6273(00)80989-7 · Cited by 444
Muhr, J., Andersson, E., Persson, M., Jessell, T., & Ericson, J. (2001) · Cell · doi:10.1016/s0092-8674(01)00283-5 · Cited by 412
Self-citationDavis, R. L., & Turner, D. L. (2001) · Oncogene · doi:10.1038/sj.onc.1205094 · Cited by 392
Uwanogho, D., Rex, M., Cartwright, E. J., Pearl, G., Healy, C., Scotting, P. J., & Sharpe, P. T. (1995) · Mechanisms of Development · doi:10.1016/0925-4773(94)00299-3 · Cited by 391
Nishimoto, M., Fukushima, A., Okuda, A., & Muramatsu, M. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.8.5453 · Cited by 376
Ambrosetti, D. C., Basilico, C., & Dailey, L. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.11.6321 · Cited by 370
NeuroD regulates multiple functions in the developing neural retina in rodent
Morrow, E. M., Furukawa, T., Lee, J. E., & Cepko, C. L. (1999) · Development · doi:10.1242/dev.126.1.23 · Cited by 360
Helix-loop-helix factors in growth and differentiation of the vertebrate nervous system
Kageyama, R., & Nakanishi, S. (1997) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(97)80014-7 · Cited by 357
Zappone, M., Galli, R., Catena, R., Meani, N., Biasi, S. D., Mattei, E., Tiveron, C., Vescovi, A. L., Lovell-Badge, R. H., Ottolenghi, S., et al. (2000) · Development · doi:10.1242/dev.127.11.2367 · Cited by 349
Chapter 10 Manipulating Gene Expression with Replication--Competent Retroviruses
Morgan, B. A., & Fekete, D. M. (1996) · Methods in cell biology · doi:10.1016/s0091-679x(08)60629-9 · Cited by 343
Involvement of Sox1, 2 and 3 in the early and subsequent molecular events of lens induction
Kamachi, Y., Uchikawa, M., Collignon, J., Lovell-Badge, R. H., & Kondoh, H. (1998) · Development · doi:10.1242/dev.125.13.2521 · Cited by 334
Jouve, C., Palmeirim, I., Henrique, D., Beckers, J., Gossler, A., Ish‐Horowicz, D., & Pourquié, O. (2000) · Development · doi:10.1242/dev.127.7.1421 · Cited by 332
An early requirement for FGF signalling in the acquisition of neural cell fate in the chick embryo
Wilson, S. I., Graziano, E., Harland, R. M., Jessell, T. M., & Edlund, H. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00431-0 · Cited by 325
Botquin, V., Hess, H., Fuhrmann, G., Anastassiadis, K., Gross, M. K., Vriend, G., & Schöler, H. R. (1998) · Genes & Development · doi:10.1101/gad.12.13.2073 · Cited by 315
Sox1 directly regulates the gamma -crystallin genes and is essential for lens development in micePreprint
Nishiguchi, S., Wood, H. B., Kondoh, H., Lovell-Badge, R. H., & Episkopou, V. (1998) · Genes & Development · doi:10.1101/gad.12.6.776 · Cited by 290
Smith, S. T., & Jaynes, J. B. (1996) · Development · doi:10.1242/dev.122.10.3141 · Cited by 284
Gradwohl, G., Fode, C., & Guillemot, F. (1996) · Developmental Biology · doi:10.1006/dbio.1996.0297 · Cited by 264
SOX3 is an X-linked gene related to SRY
Stevanović, M. J., Lovell-Badge, R. H., Collignon, J., & Goodfellow, P. N. (1993) · Human Molecular Genetics · doi:10.1093/hmg/2.12.2013 · Cited by 259
WESTENDORF, J. M., Rao, P. N., & Gerace, L. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.2.714 · Cited by 255
Crossregulation between Neurogenin2 and pathways specifying neuronal identity in the spinal cord.
Scardigli, R., Schuurmans, C., Gradwohl, G., & Guillemot, F. (2001) · Neuron · doi:10.1016/s0896-6273(01)00358-0 · Cited by 253
Perez, S. E., Rebelo, S., & Anderson, D. J. (1999) · Development · doi:10.1242/dev.126.8.1715 · Cited by 237
Yokota, Y. (2001) · Oncogene · doi:10.1038/sj.onc.1205090 · Cited by 222
Lo, L., Dormand, E., Greenwood, A. L., & Anderson, D. J. (2002) · Development · doi:10.1242/dev.129.7.1553 · Cited by 158
Roztocil, T., Matter-Sadzinski, L., Alliod, C., Ballivet, M., & Matter, J. (1997) · Development · doi:10.1242/dev.124.17.3263 · Cited by 154
Hes6 acts in a positive feedback loop with the neurogenins to promote neuronal differentiation
Koyano‐Nakagawa, N., Kim, J., Anderson, D. J., & Kintner, C. R. (2000) · Development · doi:10.1242/dev.127.19.4203 · Cited by 149
Takebayashi, K., Takahashi, S., Yokota, C., Tsuda, H., Nakanishi, S., Asashima, M., & Kageyama, R. (1997) · The EMBO Journal · doi:10.1093/emboj/16.2.384 · Cited by 148
Vertebrate bHLH Genes and the Determination of Neuronal Fates
Guillemot, F. (1999) · Experimental Cell Research · doi:10.1006/excr.1999.4717 · Cited by 141
Neurogenesis in Embryos and in Adult Neural Stem Cells
Kintner, C. R. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-03-00639.2002 · Cited by 138
Buescher, M., Hing, F. S., & Chia, W. (2002) · Development · doi:10.1242/dev.129.18.4193 · Cited by 133
Overton, P. M., Meadows, L. A., Urban, J., & Russell, S. R. H. (2002) · Development · doi:10.1242/dev.129.18.4219 · Cited by 131
Jasoni, C. L., Walker, M. B., Morris, M. D., & Reh, T. A. (1994) · Development · doi:10.1242/dev.120.4.769 · Cited by 131
Caccamo, D. V., Katsetos, C. D., Herman, M. M., Frankfurter, A. J., Collins, V. P., & Rubinstein, L. J. (1989) · PubMed · Cited by 97
Mechanisms of Viral ActivatorsPreprint
Berk, A. J., Boyer, T., Kapanidis, A. N., Ebright, R. H., KOBAYASHI, N. N., Horn, P. J., SULLIVAN, S. M., Koop, R., Surby, M. A., & Triezenberg, S. J. (1998) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1998.63.243 · Cited by 25
Cited by
Sorted by citations
The Sox Family of Transcription Factors: Versatile Regulators of Stem and Progenitor Cell Fate
Sarkar, A., & Hochedlinger, K. (2013) · Cell stem cell · doi:10.1016/j.stem.2012.12.007 · Cited by 915
Suh, H., Consiglio, A., Ray, J., Sawai, T., D’Amour, K. A., & Gage, F. H. (2007) · Cell stem cell · doi:10.1016/j.stem.2007.09.002 · Cited by 851
Sox2+ Adult Stem and Progenitor Cells Are Important for Tissue Regeneration and Survival of Mice
Arnold, K., Sarkar, A., Yram, M. A., Polo, J. M., Bronson, R. T., Sengupta, S., Seandel, M., Geijsen, N., & Hochedlinger, K. (2011) · Cell stem cell · doi:10.1016/j.stem.2011.09.001 · Cited by 770
Developmental genetics of vertebrate glial–cell specification
Rowitch, D. H., & Kriegstein, A. R. (2010) · Nature · doi:10.1038/nature09611 · Cited by 774
Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain
Ferri, L., Cavallaro, M., Braida, D., Cristofano, A. D., Canta, A., Vezzani, A., Ottolenghi, S., Pandolfi, P. P., Sala, M., Debiasi, S., et al. (2004) · Development · doi:10.1242/dev.01204 · Cited by 688
Metadata
- Authors
- Bylund, M., Andersson, E., Novitch, B. G., & Muhr, J.
- Affiliations
- Karolinska Institutet (SE)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Muhr, Jonas
- Venue
- Nature Neuroscience
- Published
- 2003-09-28
- Volume
- 6
- Issue
- 11
- Pages
- 1162-1168
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2031683488
- Cited by
- 825
- References
- 51
- Citations by year
- 2026: 15 · 2025: 12 · 2024: 27 · 2023: 28 · 2022: 27 · 2021: 23 · 2020: 35 · 2019: 27 · 2018: 39 · 2017: 23 · 2016: 32 · 2015: 51 · 2014: 45 · 2013: 55 · 2012: 54
- FWCI
- 7.72
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- neurogenesis, SOX1, SOX2, SOX3, neuronal differentiation, neural stem cells, transcriptional repression, chick embryo, in ovo electroporation
- MeSH terms
- Animals, Bromodeoxyuridine, Cell Differentiation, Chick Embryo, DNA-Binding Proteins, Drosophila, Embryonic Induction, Eye Proteins, High Mobility Group Proteins, Membrane Glycoproteins, Nerve Tissue Proteins, Neurons, Neuropeptides, Nuclear Proteins, Phosphopyruvate Hydratase, Spinal Cord, Stem Cells, Time Factors, Transcription Factors, Tubulin, Vertebrates, Proto-Oncogene Proteins c-myc, Neurofilament Proteins, Helix-Loop-Helix Motifs, Electroporation, Homeodomain Proteins, Gene Expression Regulation, Developmental, HMGB Proteins, Drosophila Proteins, Avian Proteins, Mice, PAX7 Transcription Factor, Basic Helix-Loop-Helix Proteins, SOXB1 Transcription Factors, LIM-Homeodomain Proteins
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 ›
Are you an author, or do you see a problem with this page? Request a review