Sox21 promotes the progression of vertebrate neurogenesis
Abstract
The generation of neurons constitutes the foundation of nervous system development, yet the mechanisms underlying neurogenesis are not well established. The HMG-box transcription factors Sox1, Sox2 and Sox3 (Sox1-3) have previously been shown to suppress neurogenesis by maintaining neural cells in an undifferentiated state. Here we report that another HMG-box protein, Sox21, has the opposite activity and promotes neuronal differentiation. Using genetic studies in the chick embryo, we found that Sox21 mediates this function by counteracting the activity of Sox1-3. Accordingly, the balance of Sox21 and Sox1-3 activities determines whether neural cells remain as progenitors or commit to differentiation. Proneural basic helix-loop-helix proteins are essential for the establishment of neuronal fates. We now show that proneural proteins promote neurogenesis by upregulating Sox21 expression. These data establish a key role for Sox21 in the progression of neuronal differentiation and indicate that an important role of proneural proteins is their capacity to upregulate the expression of Sox21.
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Members of SoxB1 and SoxB2 subgroups are especially important during neurogenesis.
“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 [69]
Sox21 is known to act in a repressive manner.
“This explanation is unlikely, however, because Sox21 is known to act in a repressive manner (29, 30).”
From Transphyletic conservation of developmental regulatory state in animal evolution (2011) · cites this paper as [30]
Cites
Hannon, G. J. (2002) · Nature · doi:10.1038/418244a · Cited by 3,583 · see citing works
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 · see citing works
Short hairpin RNAs (shRNAs) induce sequence-specific silencing in mammalian cellsPreprint
Paddison, P. J., Caudy, A. A., Bernstein, E., Hannon, G. J., & Conklin, D. S. (2002) · Genes & Development · doi:10.1101/gad.981002 · Cited by 1,554 · see citing works
SOX2 Functions to Maintain Neural Progenitor Identity
Graham, V., Khudyakov, J. I., Ellis, P., & Pevny, L. (2003) · Neuron · doi:10.1016/s0896-6273(03)00497-5 · Cited by 1,344 · see citing works
Schaeren‐Wiemers, N., & Gerfin-Moser, A. (1993) · Histochemistry and Cell Biology · doi:10.1007/bf00267823 · Cited by 1,162 · see citing works
Pax6 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
Conversion of <i>Xenopus</i> Ectoderm into Neurons by NeuroD, a Basic Helix-Loop-Helix Protein
Lee, J. E., Hollenberg, S. M., Snider, L., Turner, D. L., Lipnick, N., & Weintraub, H. (1995) · Science · doi:10.1126/science.7754368 · Cited by 1,023 · see citing works
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 · see citing works
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 · see citing works
Tajbakhsh, S., Rocancourt, D., Cossu, G., & BUCKINGHAM, M. E. (1997) · Cell · doi:10.1016/s0092-8674(00)80189-0 · Cited by 842 · see citing works
Vertebrate neurogenesis is counteracted by Sox1–3 activity
Bylund, M., Andersson, E., Novitch, B. G., & Muhr, J. (2003) · Nature Neuroscience · doi:10.1038/nn1131 · Cited by 825 · see citing works
Self-citationPairing 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 · 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
SOX10 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 · see citing works
Ma, Q., Schuurmans, C. J., Guillemot, F., & Anderson, D. J. (1999) · Genes & Development · doi:10.1101/gad.13.13.1717 · Cited by 509 · see citing works
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 · see citing works
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 · 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
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 · see citing works
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 · see citing works
Davis, R. L., & Turner, D. L. (2001) · Oncogene · doi:10.1038/sj.onc.1205094 · Cited by 387 · see citing works
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 365 · see citing works
Specification of Motor Neuron Identity by the MNR2 Homeodomain Protein
Tanabe, Y., William, C. M., & Jessell, T. M. (1998) · Cell · doi:10.1016/s0092-8674(00)81783-3 · Cited by 341 · see citing works
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 · see citing works
Uchikawa, M., Kamachi, Y., & Kondoh, H. (1999) · Mechanisms of Development · doi:10.1016/s0925-4773(99)00083-0 · Cited by 330 · see citing works
Smith, S. T., & Jaynes, J. B. (1996) · Development · doi:10.1242/dev.122.10.3141 · Cited by 284 · see citing works
The bHLH gene Hes6, an inhibitor of Hes1, promotes neuronal differentiation
Bae, S., Bessho, Y., Hojo, M., & Kageyama, R. (2000) · Development · doi:10.1242/dev.127.13.2933 · Cited by 268 · see citing works
Yokota, Y. (2001) · Oncogene · doi:10.1038/sj.onc.1205090 · Cited by 224 · see citing works
Roztocil, T., Matter-Sadzinski, L., Alliod, C., Ballivet, M., & Matter, J. (1997) · Development · doi:10.1242/dev.124.17.3263 · Cited by 154 · see citing works
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 · see citing works
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 · see citing works
Komatsu, T., Mizusaki, H., Mukai, T., Ogawa, H., Baba, D., Shirakawa, M., Hatakeyama, S., Nakayama, K. I., Yamamoto, H., Kikuchi, A., et al. (2004) · Molecular Endocrinology · doi:10.1210/me.2004-0173 · Cited by 111 · see citing works
The role of Phox2b in synchronizing pan-neuronal and type-specific aspects of neurogenesis
Dubreuil, V., Hirsch, M., Jouve, C., Brunet, J., & Goridis, C. (2002) · Development · doi:10.1242/dev.129.22.5241 · Cited by 70 · see citing works
Muscle Differentiation Is Antagonized by SOX15, a New Member of the SOX Protein Family
Béranger, F., Méjean, C., Moniot, B., Berta, P., & Vandromme, M. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.21.16103 · Cited by 53 · see citing works
Rex, M., Uwanogho, D., Orme, A. T., Scotting, P. J., & Sharpe, P. T. (1997) · Mechanisms of Development · doi:10.1016/s0925-4773(97)00086-5 · Cited by 50 · see citing works
The stage series of the chick embryo
Hamburger, V. (1992) · Developmental Dynamics · doi:10.1002/aja.1001950405 · Cited by 48 · see citing works
Caccamo, D. V., Herman, M. M., Frankfurter, A. J., Katsetos, C. D., Collins, V. P., & Rubinstein, L. J. (1989) · PubMed Central · Cited by 39 · see citing works
Sox21 is a repressor of neuronal differentiation and is antagonized by YB-1
Ohba, H., Chiyoda, T., Endo, E., Yano, M., Hayakawa, Y., Sakaguchi, M., Darnell, R. B., Okano, H. J., & Okano, H. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.01.026 · Cited by 35 · see citing works
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 · see citing works
Flagged first, then by citations
1 of the 40 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Developmental genetics of vertebrate glial–cell specification
Rowitch, D., & Kriegstein, A. (2010) · Nature · doi:10.1038/nature09611 · Cited by 685 · see citing works
Sox proteins: regulators of cell fate specification and differentiation
Kamachi, Y., & Kondoh, H. (2013) · Development · doi:10.1242/dev.091793 · Cited by 568 · see citing works
The role of SOX family members in solid tumours and metastasis
Grimm, D. G., Bauer, J. W., Wise, P. M., Krüger, M., Simonsen, U., Wehland, M., Infanger, M., & Corydon, T. J. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.03.004 · Cited by 487 · see citing works
Lefebvre, V., Dumitriu, B., Penzo‐Méndez, A., Han, Y., & Bhattaram, P. (2007) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2007.05.019 · Cited by 466 · see citing works
From stem cells to neurons and glia: a Soxist's view of neural development
Wegner, M., & Stolt, C. C. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.08.008 · Cited by 426 · see citing works
YAP regulates neural progenitor cell number via the TEA domain transcription factorPreprint
Cao, X., Pfaff, S. L., & Gage, F. H. (2008) · Genes & Development · doi:10.1101/gad.1726608 · Cited by 398 · see citing works
The establishment of neuronal properties is controlled by Sox4 and Sox11Preprint
Bergsland, M., Werme, M., Malewicz, M., Perlmann, T., & Muhr, J. (2006) · Genes & Development · doi:10.1101/gad.403406 · Cited by 341 · see citing works
Self-citationSpatial and temporal specification of neural fates by transcription factor codes
Guillemot, F. (2007) · Development · doi:10.1242/dev.006379 · Cited by 308 · see citing works
Stolt, C. C., Schlierf, A., Lommes, P., Hillgärtner, S., Werner, T., Kosian, T., Sock, E., Kessaris, N., Richardson, W. D., Lefebvre, V., et al. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.08.011 · Cited by 299 · see citing works
Gontan, C., Munck, A. B., Vermeij, M., Grosveld, F. G., Tibboel, D., & Rottier, R. J. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.02.035 · Cited by 294 · see citing works
Dy, P., Penzo‐Méndez, A., Wang, H., Pedraza, C. E., Macklin, W. B., & Lefebvre, V. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn162 · Cited by 245 · see citing works
Cell fate specification in the mammalian telencephalon
Guillemot, F. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.02.009 · Cited by 243 · see citing works
All purpose Sox: The many roles of Sox proteins in gene expression
Wegner, M. (2009) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2009.07.006 · Cited by 231 · see citing works
Kiefer, J. C. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21218 · Cited by 212 · see citing works
Titulaer, M. J., Klooster, R., Potman, M., Sabater, L., Graus, F., Hegeman, I. M., Thijssen, P. E., Wirtz, P. W., Twijnstra, A., Smitt, P. A. E. S., et al. (2009) · Journal of Clinical Oncology · doi:10.1200/jco.2008.20.6169 · Cited by 204 · see citing works
Schlosser, G. (2010) · International review of cytology · doi:10.1016/s1937-6448(10)83004-7 · Cited by 195 · 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
Kondoh, H., & Kamachi, Y. (2009) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2009.09.003 · Cited by 186 · see citing works
SOX family transcription factors involved in diverse cellular events during development
She, Z., & Yang, W. (2015) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2015.08.002 · Cited by 174 · see citing works
Having it both ways: Sox protein function between conservation and innovation
Guth, S. I. E., & Wegner, M. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8138-7 · Cited by 176 · see citing works
Transient inactivation of Notch signaling synchronizes differentiation of neural progenitor cells
Nelson, B. R., Hartman, B. H., Georgi, S. A., Lan, M. S., & Reh, T. A. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.01.001 · Cited by 174 · see citing works
Stevanović, M. J., Drakulić, D., Lazic, A., Ninković, D. S., Schwirtlich, M., & Mojsin, M. M. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.654031 · Cited by 158 · see citing works
Layden, M. J., Rentzsch, F., & Röttinger, É. (2016) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.222 · Cited by 148 · see citing works
Briscoe, J., & Novitch, B. G. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.2012 · Cited by 162 · see citing works
Hoser, M., Potzner, M. R., Koch, J. M. C., Bösl, M. R., Wegner, M., & Sock, E. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.00338-08 · Cited by 136 · see citing works
Richards, G. S., & Rentzsch, F. (2014) · Development · doi:10.1242/dev.112029 · Cited by 110 · see citing works
Identification of Sox17 as a Transcription Factor That Regulates Oligodendrocyte Development
Sohn, J., Natale, J., Chew, L.-J., Belachew, S., Cheng, Y., Aguirre, A., Lytle, J., Nait-Oumesmar, B., Kerninon, C., Kanai-Azuma, M., et al. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1716-06.2006 · Cited by 124 · see citing works
Single-cell transcriptomics identifies conserved regulators of neuroglandular lineages
Steger, J., Cole, A. G., Denner, A., Lebedeva, T. S., Genikhovich, G., Ries, A., Reischl, R., Taudes, E., Lassnig, M., & Technau, U. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111370 · Cited by 120 · see citing works
The SOX family of genes in cancer development: biological relevance and opportunities for therapy
Castillo, S. D., & Sánchez‐Céspedes, M. (2012) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2012.709239 · Cited by 117 · see citing works
Mallanna, S. K., Ormsbee, B. D., Iacovino, M., Gilmore, J. M., Cox, J. L., Kyba, M., Washburn, M. P., & Rizzino, A. (2010) · Stem Cells · doi:10.1002/stem.494 · Cited by 114 · see citing works
Biological determinants of bladder cancer gene expression subtypes
Aine, M., Eriksson, P., Liedberg, F., Sjödahl, G., & Höglund, M. (2015) · Scientific Reports · doi:10.1038/srep10957 · Cited by 113 · see citing works
Transcription factor Sox11 is essential for both embryonic and adult neurogenesis
Wang, Y., Lin, L., Lai, H. C., Parada, L. F., & Lei, L. (2013) · Developmental Dynamics · doi:10.1002/dvdy.23962 · Cited by 108 · see citing works
Nervous system development and regeneration in freshwater planarians
Ross, K. G., Currie, K. W., Pearson, B. J., & Zayas, R. M. (2017) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.266 · Cited by 105 · see citing works
Kumar, P., & Mistri, T. K. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.06.016 · Cited by 103 · see citing works
The Yin and Yang of Sox proteins: Activation and repression in development and disease
Chew, L., & Gallo, V. (2009) · Journal of Neuroscience Research · doi:10.1002/jnr.22128 · Cited by 102 · see citing works
Spatiotemporal transcriptomic maps of whole mouse embryos at the onset of organogenesis
Kumar, A. S., Tian, L., Bolondi, A., Hernández, A. A., Stickels, R. R., Kretzmer, H., Murray, E. M., Wittler, L., Walther, M., Barakat, G., et al. (2023) · Nature Genetics · doi:10.1038/s41588-023-01435-6 · Cited by 105 · see citing works
Wei, L., Yang, C., Tao, W., & Wang, D. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17030270 · Cited by 99 · see citing works
Bernard, P., & Harley, V. R. (2009) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2009.10.017 · Cited by 99 · see citing works
Grimaudo, M. A., Krishnakumar, G. S., Giusto, E., Furlani, F., Bassi, G., Rossi, A., Molinari, F., Lista, F. R., Montesi, M., & Panseri, S. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.11.038 · Cited by 98 · see citing works
The Prosensory Function of Sox2 in the Chicken Inner Ear Relies on the Direct Regulation of Atoh1
Neves, J., Uchikawa, M., Bigas, A., & Giráldez, F. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030871 · Cited by 97 · see citing works
Differentiation of Mesenchymal Stem Cells to Neuroglia: in the Context of Cell Signalling
George, S., Hamblin, M. R., & Abrahamse, H. (2019) · Stem Cell Reviews and Reports · doi:10.1007/s12015-019-09917-z · Cited by 97 · see citing works
Transphyletic conservation of developmental regulatory state in animal evolution
Royo, J. L., Maeso, I., Irimia, M., Gao, F., Peter, I. S., Lopes, C. S., D'Aniello, S., Casares, F., Davidson, E. H., Garcia-Fernández, J., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1109037108 · Cited by 93 · see citing works
A functional genomics screen in planarians reveals regulators of whole-brain regeneration
Roberts-Galbraith, R. H., Brubacher, J. L., & Newmark, P. A. (2016) · eLife · doi:10.7554/elife.17002 · Cited by 89 · see citing works
miR-218 is essential to establish motor neuron fate as a downstream effector of Isl1–Lhx3
Thiebes, K. P., Nam, H., Cambronne, X. A., Shen, R., Glasgow, S. M., Cho, H.-H., Kwon, J.-S., Goodman, R. H., Lee, J. W., Lee, S., et al. (2015) · Nature Communications · doi:10.1038/ncomms8718 · Cited by 78 · see citing works
Regulation of Nematostella neural progenitors by SoxB, Notch and bHLH genes
Richards, G. S., & Rentzsch, F. (2015) · Development · doi:10.1242/dev.123745 · Cited by 80 · see citing works
Zebrafish Pou5f1‐dependent transcriptional networks in temporal control of early development
Onichtchouk, D., Geier, F. M., Polok, B., Messerschmidt, D. M., Mössner, R., Wendik, B., Song, S., Taylor, V., Timmer, J., & Driever, W. (2010) · Molecular Systems Biology · doi:10.1038/msb.2010.9 · Cited by 86 · see citing works
Vertebrate-like regeneration in the invertebrate chordate amphioxus
Somorjai, I., Somorjai, R. L., García‐Fernàndez, J., & Escrivá, H. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100045109 · Cited by 86 · see citing works
Evolution of eumetazoan nervous systems: insights from cnidarians
Kelava, I., Rentzsch, F., & Technau, U. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0065 · Cited by 84 · see citing works
Kofink, D., Boks, M. P. M., Timmers, H. T. M., & Kas, M. J. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.03.020 · Cited by 83 · see citing works
Direct reprogramming with SOX factors: masters of cell fate
Julian, L. M., McDonald, A., & Stanford, W. L. (2017) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2017.06.005 · Cited by 83 · see citing works
SOX after SOX: SOXession regulates neurogenesis: Figure 1.Preprint
Wegner, M. (2011) · Genes & Development · doi:10.1101/gad.181487.111 · Cited by 83 · see citing works
Sequential actions of β-catenin and Bmp pattern the oral nerve net in Nematostella vectensis
Watanabe, H., Kuhn, A., Fushiki, M., Agata, K., Özbek, S., Fujisawa, T., & Holstein, T. W. (2014) · Nature Communications · doi:10.1038/ncomms6536 · Cited by 79 · see citing works
The Amphioxus SoxB Family: Implications for the Evolution of Vertebrate Placodes
Meulemans, D., & Bronner-Fraser, M. E. (2007) · International Journal of Biological Sciences · doi:10.7150/ijbs.3.356 · Cited by 79 · see citing works
From CNS stem cells to neurons and glia: Sox for everyone
Reiprich, S., & Wegner, M. (2014) · Cell and Tissue Research · doi:10.1007/s00441-014-1909-6 · Cited by 83 · see citing works
Human SRY inhibits β-catenin-mediated transcription
Bernard, P., Sim, H., Knower, K. C., Vilain, E. J. N., & Harley, V. R. (2008) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2008.06.006 · Cited by 77 · see citing works
Co-ordination of cell cycle and differentiation in the developing nervous system
Hindley, C., & Philpott, A. (2012) · Biochemical Journal · doi:10.1042/bj20112040 · Cited by 76 · see citing works
Panayi, H., Panayiotou, E., Orford, M., Genethliou, N., Mean, R. J., Lapathitis, G., Li, S., Xiang, M., Kessaris, N., Richardson, W. D., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2402-10.2010 · Cited by 76 · see citing works
Failure of SOX9 Regulation in 46XY Disorders of Sex Development with SRY, SOX9 and SF1 Mutations
Knower, K. C., Kelly, S., Ludbrook, L. M., Bagheri‐Fam, S., Sim, H., Bernard, P., Sekido, R., Lovell-Badge, R. H., & Harley, V. R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017751 · Cited by 74 · see citing works
The disruption of Sox21-mediated hair shaft cuticle differentiation causes cyclic alopecia in mice
Kiso, M., Tanaka, S., Saba, R., Matsuda, S., Shimizu, A., Ohyama, M., Okano, H. J., Shiroishi, T., Okano, H., & Saga, Y. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808324106 · Cited by 74 · see citing works
Holmberg, J., Hansson, E. M., Malewicz, M., Sandberg, M., Perlmann, T., Lendahl, U., & Muhr, J. (2008) · Development · doi:10.1242/dev.020180 · Cited by 73 · see citing works
Self-citationAlginate Hydrogels as Scaffolds and Delivery Systems to Repair the Damaged Spinal Cord
Grijalvo, S., Nieto‐Díaz, M., Maza, R. M., Eritja, R., & Díaz, D. D. (2019) · Biotechnology Journal · doi:10.1002/biot.201900275 · Cited by 74 · see citing works
Martínez‐Morales, P., Quiroga, A. C., Barbas, J. A., & Morales, A. V. (2010) · EMBO Reports · doi:10.1038/embor.2010.61 · Cited by 72 · see citing works
Regeneration of Xenopus laevis spinal cord requires Sox2/3 expressing cells
Muñoz, R., Edwards‐Faret, G., Moreno, M., Zuñiga, N. R., Cline, H. T., & Larraı́n, J. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.03.009 · Cited by 70 · see citing works
Transcription-Factor-Dependent Control of Adult Hippocampal NeurogenesisPreprint
Beckervordersandforth, R., Zhang, C., & Lie, D. C. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018879 · Cited by 70 · see citing works
Elkouris, M., Balaskas, N., Poulou, M., Politis, P. K., Panayiotou, E., Malas, S., Thomaidou, D., & Remboutsika, E. (2010) · Stem Cells · doi:10.1002/stem.554 · Cited by 69 · see citing works
Sox2 acts through Sox21 to regulate transcription in pluripotent and differentiated cells
Kuzmichev, A. N., Kim, S.-K., D’Alessio, A. C., Chenoweth, J. G., Wittko, I. M., Campanati, L., & McKay, R. D. (2012) · Current Biology · doi:10.1016/j.cub.2012.07.013 · Cited by 69 · see citing works
Transcriptional regulation of the peripheral nervous system in Ciona intestinalis
Tang, W. J., Chen, J. S., & Zeller, R. W. (2013) · Developmental Biology · doi:10.1016/j.ydbio.2013.03.016 · Cited by 67 · see citing works
Uchikawa, M., Yoshida, M., Iwafuchi, M., Matsuda, K., Ishida, Y., Takemoto, T., & Kondoh, H. (2011) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2011.01286.x · Cited by 69 · see citing works
Sox21 Promotes Hippocampal Adult Neurogenesis via the Transcriptional Repression of theHes5Gene
Matsuda, S., Kuwako, K.-I., Okano, H. J., Tsutsumi, S., Aburatani, H., Saga, Y., Matsuzaki, Y., Akaike, A., Sugimoto, H., & Okano, H. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5803-11.2012 · Cited by 73 · see citing works
Aldh1L1 is expressed by postnatal neural stem cells in vivo
Foo, L. C., & Dougherty, J. D. (2013) · Glia · doi:10.1002/glia.22539 · Cited by 62 · see citing works
Transcription factors and neural stem cell self-renewal, growth and differentiation
Ahmed, S., Gan, H. T., Lam, C. S., Poonepalli, A., Ramasamy, S., Tay, Y., Tham, M., & Yu, Y. H. (2009) · Cell Adhesion & Migration · doi:10.4161/cam.3.4.8803 · Cited by 64 · see citing works
SoxC transcription factors: multifunctional regulators of neurodevelopment
Kavyanifar, A., Turan, S., & Lie, D. C. (2017) · Cell and Tissue Research · doi:10.1007/s00441-017-2708-7 · Cited by 65 · see citing works
Spiliotopoulos, D., Goffredo, D., Conti, L., Febo, F. D., Biella, G. R., Toselli, M., & Cattaneo, E. F. (2009) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.02.007 · Cited by 64 · see citing works
Evolution of the insect Sox genes
Wilson, M. J., & Dearden, P. K. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-120 · Cited by 59 · see citing works
Regulation of spinal interneuron development by the Olig-related protein Bhlhb5 and Notch signaling
Skaggs, K., Martin, D. M., & Novitch, B. G. (2011) · Development · doi:10.1242/dev.057281 · Cited by 60 · see citing works
Mateo, J. L., van den Berg, D. L. C., Haeussler, M., Drechsel, D., Gaber, Z. B., Castro, D. S., Robson, P., Lu, Q. R., Crawford, G. E., Flicek, P., et al. (2014) · Genome Research · doi:10.1101/gr.173435.114 · Cited by 58 · see citing works
Göke, J., Jung, M., Behrens, S., Chávez, L., O’Keeffe, S., Timmermann, B., Lehrach, H., Adjaye, J., & Vingron, M. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002304 · Cited by 54 · see citing works
Kerner, P., Simionato, E., Gouar, M. L., & Vervoort, M. (2009) · Evolution & Development · doi:10.1111/j.1525-142x.2009.00359.x · Cited by 56 · see citing works
PHF3 regulates neuronal gene expression through the Pol II CTD reader domain SPOC
Appel, L.-M., Franke, V., Bruno, M., Grishkovskaya, I., Kasiliauskaitė, A., Kaufmann, T., Schoeberl, U. E., Puchinger, M. G., Kostrhon, S., Ebenwaldner, C., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-26360-2 · Cited by 53 · see citing works
Forced expression of Sox21 inhibits Sox2 and induces apoptosis in human glioma cells
Ferletta, M., Çağlayan, D., Mokvist, L., Jiang, Y., Kastemar, M., Uhrbom, L., & Westermark, B. (2010) · International Journal of Cancer · doi:10.1002/ijc.25647 · Cited by 52 · see citing works
Transcriptional regulation of neuronal phenotype in mammals
Ma, Q. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.113449 · Cited by 50 · see citing works
Sox21 regulates the progression of neuronal differentiation in a dose-dependent manner
Whittington, N. C., Cunningham, D. D., Le, T.-K., Maria, D. D., & Casey, E. S. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.11.012 · Cited by 50 · see citing works
Westermark, B. (2012) · Upsala Journal of Medical Sciences · doi:10.3109/03009734.2012.676574 · Cited by 48 · see citing works
Bonnert, T. P., Bilsland, J., Guest, P. C., HEAVENS, R. P., McLaren, D., Dale, C., Thakur, M., McAllister, G., & Muñoz-Sanjuán, I. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04912.x · Cited by 46 · see citing works
Combinatorial signalling controls Neurogenin2 expression at the onset of spinal neurogenesis.
Ribes, V., Stutzmann, F., Bianchetti, L., Guillemot, F., Dollé, P., & Roux, I. L. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.06.003 · Cited by 55 · see citing works
A 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
Self-citationSox2 regulation of hair cell development: incoherence makes sense
Neves, J., Vachkov, I. H., & Giráldez, F. (2012) · Hearing Research · doi:10.1016/j.heares.2012.11.003 · Cited by 45 · see citing works
Zaletel, I., Schwirtlich, M., Perović, M., Jovanović, M., Stevanović, M., Kanazir, S., & Puškaš, N. (2018) · Journal of Alzheimer's Disease · doi:10.3233/jad-180277 · Cited by 44 · see citing works
SOX5/6/21 Prevent Oncogene-Driven Transformation of Brain Stem Cells
Kurtsdotter, I., Topcic, D., Karlén, A., Singla, B., Hagey, D. W., Bergsland, M., Siesjö, P., Nistér, M., Carlson, J. W., Lefebvre, V., et al. (2017) · Cancer Research · doi:10.1158/0008-5472.can-17-0704 · Cited by 42 · see citing works
Self-citationChromatin remodeler CHD7 regulates the stem cell identity of human neural progenitorsPreprint
MuhChyi, C., Sanosaka, T., Okuno, H., Zhou, Z., Koya, I., Banno, S., Andoh-Noda, T., Tabata, Y., Shimamura, R., Hayashi, T., et al. (2018) · Genes & Development · doi:10.1101/gad.301887.117 · Cited by 43 · see citing works
Hsieh, T.-H. S., Cattoglio, C., Slobodyanyuk, E., Hansen, A. S., Darzacq, X., & Tjian, R. (2021) · doi:10.1101/2021.07.14.452365 · Cited by 42 · see citing works
Focareta, L., & Cole, A. G. (2016) · PLoS ONE · doi:10.1371/journal.pone.0157821 · Cited by 41 · see citing works
Spatiotemporal regulation of nervous system development in the annelid Capitella teleta
Sur, A., Magie, C. R., Seaver, E. C., & Meyer, N. P. (2017) · EvoDevo · doi:10.1186/s13227-017-0076-8 · Cited by 39 · see citing works
Lin, Y., Chen, D., Fan, Q., & Zhang, H. (2009) · Science in China Series C Life Sciences · doi:10.1007/s11427-009-0111-7 · Cited by 39 · see citing works
Playing with the cell cycle to build the spinal cord
Molina, A., & Pituello, F. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.12.022 · Cited by 37 · see citing works
Clinical Relevance of Autoantibody Detection in Lung Cancer
Solassol, J., Maudelondé, T., Mangé, A., & Pujol, J.-L. (2011) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e318215a0a4 · Cited by 37 · see citing works
Ferrero, E. A., Fischer, B., & Russell, S. R. H. (2014) · Genome biology · doi:10.1186/gb-2014-15-5-r74 · Cited by 36 · see citing works
Vidal, B., Santella, A., Serrano‐Saiz, E., Bao, Z., Chuang, C., & Hobert, O. (2015) · Development · doi:10.1242/dev.125740 · Cited by 36 · see citing works
Flexibility of Neural Stem Cells
Remboutsika, E., Elkouris, M., Iulianella, A., Andoniadou, C. L., Poulou, M., Mitsiadis, T. A., Trainor, P. A., & Lovell-Badge, R. H. (2011) · Frontiers in Physiology · doi:10.3389/fphys.2011.00016 · Cited by 36 · see citing works
Temporal and epigenetic regulation of neurodevelopmental plasticity
Allen, N. D. (2007) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.2010 · Cited by 35 · see citing works
- Authors
- Sandberg, M., Källström, M., & Muhr, J.
- Affiliations
- Karolinska Institutet (SE)
- Corresponding author
- Muhr, Jonas
- Venue
- Nature Neuroscience
- Published
- 2005-07-03
- Volume
- 8
- Issue
- 8
- Pages
- 995-1001
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W1985888836
- Cited by
- 210
- References
- 40
- Citations by year
- 2026: 1 · 2025: 7 · 2024: 2 · 2023: 5 · 2022: 4 · 2021: 12 · 2020: 6 · 2019: 7 · 2018: 6 · 2017: 8 · 2016: 10 · 2015: 13 · 2014: 11 · 2013: 15 · 2012: 17
- FWCI
- 3.17
- 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
- Sox21, neurogenesis, neuronal differentiation, HMG-box transcription factor, neural progenitor cells, chick embryo, brain development, transcriptional regulation
- MeSH terms
- Animals, Central Nervous System, Chick Embryo, DNA-Binding Proteins, High Mobility Group Proteins, Transcription Factors, Up-Regulation, HMGB Proteins, SOXB1 Transcription Factors, SOXB2 Transcription Factors
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