Persistent Wnt/β-catenin signaling determines dorsalization of the postnatal subventricular zone and neural stem cell specification into oligodendrocytes and glutamatergic neurons
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In the postnatal and adult central nervous system (CNS), the subventricular zone (SVZ) of the forebrain is the main source of neural stem cells (NSCs) that generate olfactory neurons and oligodendrocytes (OLs), the myelinating cells of the CNS. Here, we provide evidence of a primary role for canonical Wnt/β-catenin signaling in regulating NSC fate along neuronal and oligodendroglial lineages in the postnatal SVZ. Our findings demonstrate that glutamatergic neuronal precursors (NPs) and oligodendrocyte precursors (OPs) are derived strictly from the dorsal SVZ (dSVZ) microdomain under the control of Wnt/β-catenin, whereas GABAergic NPs are derived mainly from the lateral SVZ (lSVZ) microdomain independent of Wnt/β-catenin. Transcript analysis of microdissected SVZ microdomains revealed that canonical Wnt/β-catenin signaling was more pronounced in the dSVZ microdomain. This was confirmed using the β-catenin-activated Wnt-reporter mouse and by pharmacological stimulation of Wnt/β-catenin by infusion of the specific glycogen synthase kinase 3β inhibitor, AR-A014418, which profoundly increased the generation of cycling cells. In vivo genetic/pharmacological stimulation or inhibition of Wnt/β-catenin, respectively, increased and decreased the differentiation of dSVZ-NSCs into glutamatergic NPs, and had a converse effect on GABAergic NPs. Activation of Wnt/β-catenin dramatically stimulated the generation of OPs, but its inhibition had no effect, indicating other factors act in concert with Wnt/β-catenin to fine tune oligodendrogliogenesis in the postnatal dSVZ. These results demonstrate a role for Wnt/β-catenin signaling within the dorsal microdomain of the postnatal SVZ, in regulating the genesis of glutamatergic neurons and OLs.
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Wnt and Smoothened signaling, as well as primary cilium pathways, were up-regulated in male lateral and female septal samples.
“Wnt and Smoothened signaling, as well as primary cilium pathways (Ahn and Joyner, 2005; Azim et al., 2014; Ihrie et al., 2011), were up-regulated in male lateral and female septal samples.”
From Single-Cell Analysis of Regional Differences in Adult V-SVZ Neural Stem Cell Lineages (2019) · cites this paper as Azim et al., 2014
Cites
Subventricular zone astrocytes are neural stem cells in the adult mammalian brain
Doetsch, F., Caillé, I., Lim, D. A., García-Verdugo, J. M., & Alvarez-Buylla, A. (1999) · Cell · doi:10.1016/s0092-8674(00)80783-7 · Cited by 3,898 · see citing works
Long-Distance Neuronal Migration in the Adult Mammalian Brain
Lois, C., & Álvarez-Buylla, A. (1994) · Science · doi:10.1126/science.8178174 · Cited by 2,331 · see citing works
Doetsch, F. K., García‐Verdugo, J. M., & Álvarez-Buylla, A. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-13-05046.1997 · Cited by 1,909 · see citing works
Intestinal polyposis in mice with a dominant stable mutation of the β‐catenin gene
Harada, N., Tamai, Y., Ishikawa, T., Sauer, B., Takaku, K., Oshima, M., & Taketo, M. M. (1999) · The EMBO Journal · doi:10.1093/emboj/18.21.5931 · Cited by 1,198 · see citing works
Kessaris, N., Fogarty, M., Iannarelli, P., Grist, M., Wegner, M., & Richardson, W. D. (2006) · Nature Neuroscience · doi:10.1038/nn1620 · Cited by 1,195 · see citing works
Brault, V., Moore, R., Kutsch, S., Ishibashi, M., Rowitch, D. H., McMahon, A. P., Sommer, L., Boussadia, O., & Kemler, R. (2001) · Development · doi:10.1242/dev.128.8.1253 · Cited by 1,089 · see citing works
Self-citationOrigin of oligodendrocytes in the subventricular zone of the adult brain
Menn, B., Garcia-Verdugo, J. M., Yaschine, C., Gonzalez-Perez, O., Rowitch, D., & Alvarez-Buylla, A. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1299-06.2006 · Cited by 972 · see citing works
Mosaic Organization of Neural Stem Cells in the Adult Brain
Merkle, F. T., Mirzadeh, Z., & Álvarez-Buylla, A. (2007) · Science · doi:10.1126/science.1144914 · Cited by 821 · see citing works
Mapping Wnt/β-catenin signaling during mouse development and in colorectal tumors
Maretto, S., Cordenonsi, M., Dupont, S., Braghetta, P., Broccoli, V., Hassan, A. B., Volpin, D., Bressan, G. M., & Piccolo, S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0434590100 · Cited by 759 · see citing works
Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNSPreprint
Fancy, S. P. J., Baranzini, S. E., Zhao, C., Yuk, D., Irvine, K., Kaing, S., Sanai, N., Franklin, R. J. M., & Rowitch, D. H. (2009) · Genes & Development · doi:10.1101/gad.1806309 · Cited by 639 · see citing works
Sonic hedgehog controls stem cell behavior in the postnatal and adult brain
Palma, V., Lim, D. A., Dahmane, N., Sánchez‐Gómez, P., Brionne, T. C., Herzberg, C. D., Gitton, Y., Carleton, A., Álvarez-Buylla, A., & Altaba, A. R. I. (2004) · Development · doi:10.1242/dev.01567 · Cited by 610 · see citing works
Origin and function of olfactory bulb interneuron diversity
Lledo, P., Merkle, F. T., & Álvarez-Buylla, A. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.05.006 · Cited by 422 · see citing works
GSK-3 is a master regulator of neural progenitor homeostasis
Kim, W.-Y., Wang, X., Wu, Y., Doble, B. W., Patel, S., Woodgett, J. R., & Snider, W. D. (2009) · Nature Neuroscience · doi:10.1038/nn.2408 · Cited by 399 · see citing works
Adult generation of glutamatergic olfactory bulb interneurons
Brill, M. S., Ninkovic, J., Winpenny, E. M., Hodge, R. D., Ozen, I., Yang, R., Lepier, A., Gascón, S., Erdélyi, F., Szabó, G., et al. (2009) · Nature Neuroscience · doi:10.1038/nn.2416 · Cited by 364 · see citing works
Self-citationYoung, K. M., Fogarty, M., Kessaris, N., & Richardson, W. D. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0476-07.2007 · Cited by 343 · see citing works
Beckervordersandforth, R., Tripathi, P., Ninkovic, J., Bayam, E., Lepier, A., Stempfhuber, B., Kirchhoff, F., Hirrlinger, J., Haslinger, A., Lie, D. C., et al. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.11.017 · Cited by 335 · see citing works
Kohwi, M., Petryniak, M. A., Long, J. E., Ekker, M., Obata, K., Yanagawa, Y., Rubenstein, J. L. R., & Álvarez-Buylla, A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0254-07.2007 · Cited by 270 · see citing works
Genomic 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
Persistent Sonic Hedgehog Signaling in Adult Brain Determines Neural Stem Cell Positional Identity
Ihrie, R. A., Shah, J. K., Harwell, C. C., Levine, J. H., Guinto, C. D., Lezameta, M., Kriegstein, A. R., & Alvarez-Buylla, A. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.018 · Cited by 255 · see citing works
Ortega, F., Gascón, S., Masserdotti, G., Deshpande, A., Simon, C., Fischer, J., Dimou, L., Chichung Lie, D., Schroeder, T., & Berninger, B. (2013) · Nature Cell Biology · doi:10.1038/ncb2736 · Cited by 247 · see citing works
Effects of canonical Wnt signaling on dorso-ventral specification of the mouse telencephalon.
Backman, M., Machoň, O., Mygland, L., van den Bout, C. J., Zhong, W., Taketo, M., & Krauss, S. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2004.12.010 · Cited by 243 · see citing works
Adachi, K., Mirzadeh, Z., Sakaguchi, M., Yamashita, T., Nikolcheva, T., Gotoh, Y., Peltz, G., Gong, L., Kawase, T., Álvarez-Buylla, A., et al. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0177 · Cited by 243 · see citing works
GSK3β negatively regulates oligodendrocyte differentiation and myelination in vivo
Azim, K., & Butt, A. M. (2011) · Glia · doi:10.1002/glia.21122 · Cited by 188 · see citing works
Self-citationNeuroD1 induces terminal neuronal differentiation in olfactory neurogenesis
Boutin, C., Hardt, O., de Chevigny, A., Coré, N., Goebbels, S., Seidenfaden, R., Bosio, A., & Cremer, H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909015107 · Cited by 169 · see citing works
The transcription factor Otx2 regulates choroid plexus development and function
Johansson, P. A., Irmler, M., Acampora, D., Beckers, J., Simeone, A., & Götz, M. (2013) · Development · doi:10.1242/dev.090860 · Cited by 130 · see citing works
Probing transcription-specific outputs of β-catenin in vivoPreprint
Valenta, T., Gay, M. H., Steiner, S. N., Draganova, K., Zemke, M., Hoffmans, R., Cinelli, P., Aguet, M., Sommer, L., & Basler, K. (2011) · Genes & Development · doi:10.1101/gad.181289.111 · Cited by 116 · see citing works
Self-citationKelsch, W., Mosley, C., Lin, C.-W., & Lois, C. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050300 · Cited by 100 · see citing works
Transcriptome signature of the adult mouse choroid plexus
Marques, F., Sousa, J. C., Coppola, G., Gao, F., Puga, R., Brentani, H., Geschwind, D. H., Sousa, N., Correia‐Neves, M., & Palha, J. A. (2011) · Fluids and Barriers of the CNS · doi:10.1186/2045-8118-8-10 · Cited by 95 · see citing works
Sequential generation of olfactory bulb glutamatergic neurons by Neurog2-expressing precursor cells
Winpenny, E. M., Lebel, M., Fernandez, M. E., Brill, M. S., Götz, M., Guillemot, F., & Raineteau, O. (2011) · Neural Development · doi:10.1186/1749-8104-6-12 · Cited by 78 · see citing works
Self-citationAzim, K., Raineteau, O., & Butt, A. M. (2012) · Glia · doi:10.1002/glia.22413 · Cited by 71 · see citing works
Self-citationFernández, M. E., Croce, S., Boutin, C., Cremer, H., & Raineteau, O. (2011) · Neural Development · doi:10.1186/1749-8104-6-13 · Cited by 58 · see citing works
Self-citationWnt Signaling Has Opposing Roles in the Developing and the Adult Brain That Are Modulated by Hipk1
Marinaro, C., Pannese, M., Weinandy, F., Sessa, A., Bergamaschi, A., Taketo, M. M., Broccoli, V., Comı, G., Götz, M., Martino, G., et al. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr320 · Cited by 39 · see citing works
Azim, K., Fiorelli, R., Zweifel, S., Hurtado‐Chong, A., Yoshikawa, K., Slomianka, L., & Raineteau, O. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049087 · Cited by 34 · see citing works
Self-citationBowyer, J. F., Thomas, M., Patterson, T. A., George, N. I., Runnells, J. A., & Levi, M. S. (2012) · Journal of Visualized Experiments · doi:10.3791/4285 · Cited by 32 · see citing works
Bowyer, J. F., Thomas, M., Patterson, T. A., George, N. I., Runnells, J. A., & Levi, M. S. (2012) · Journal of Visualized Experiments · doi:10.3791/4285-v · Cited by 11 · see citing works
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Basak, O., Krieger, T. G., Muraro, M. J., Wiebrands, K., Stange, D. E., Frias-Aldeguer, J., Rivron, N. C., van de Wetering, M., van Es, J. H., van Oudenaarden, A., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1715911114 · Cited by 186 · see citing works
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Bengoa‐Vergniory, N., & Kypta, R. M. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-2028-6 · Cited by 161 · see citing works
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Fiorelli, R., Azim, K., Fischer, B., & Raineteau, O. (2015) · Development · doi:10.1242/dev.119966 · Cited by 116 · see citing works
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Gruchot, J., Weyers, V., Göttle, P., Förster, M., Hartung, H., Küry, P., & Kremer, D. (2019) · Cells · doi:10.3390/cells8080825 · Cited by 109 · see citing works
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Guo, F., Lang, J., Sohn, J., Hammond, E., Chang, M., & Pleasure, D. (2015) · Glia · doi:10.1002/glia.22813 · Cited by 107 · see citing works
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Butt, A. M., Rocha, I. C. D. L., & Rivera, A. D. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-981-13-9913-8_12 · Cited by 95 · see citing works
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Soares, L. C., Al‐Dalahmah, O., Hillis, J. M., Young, C. C., Asbed, I., Sakaguchi, M., O’Neill, E. E., & Szele, F. G. (2021) · Cells · doi:10.3390/cells10113047 · Cited by 94 · see citing works
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Chang, E. H., Adorján, I., Mundim, M. V., Sun, B., Dizon, M. L. V., & Szele, F. G. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00332 · Cited by 92 · see citing works
Chavali, M., Klingener, M., Kokkosis, A. G., Garkun, Y., Felong, S., Maffei, A., & Aguirre, A. A. (2017) · Nature Communications · doi:10.1038/s41467-017-02440-0 · Cited by 85 · see citing works
Gengatharan, A., Bammann, R. R., & Saghatelyan, A. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00149 · Cited by 81 · see citing works
Meffre, D., Massaad, C., & Grenier, J. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.10.064 · Cited by 76 · see citing works
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Hu, X.-L., Chen, G., Zhang, S., Zheng, J., Wu, J., Bai, Q., Wang, Y., Li, J., Wang, H., Han, F., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.047 · Cited by 66 · see citing works
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Mizrak, D., Bayin, N. S., Yuan, J., Liu, Z., Suciu, R. M., Niphakis, M. J., Ngo, N., Lum, K. M., Cravatt, B. F., Joyner, A. L., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107805 · Cited by 59 · see citing works
Rivera, A. D., Pieropan, F., Chacon‐De‐La‐Rocha, I., Lecca, D., Abbracchio, M. P., Azim, K., & Butt, A. M. (2021) · Aging Cell · doi:10.1111/acel.13335 · Cited by 61 · see citing works
Self-citationAzim, K., Angonin, D., Marcy, G., Pieropan, F., Rivera, A. D., Donega, V., Cantù, C., Williams, G. H., Berninger, B., Butt, A. M., et al. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2000698 · Cited by 55 · see citing works
Self-citationThyroid hormone regulation of neural stem cell fate: From development to ageing
Gothié, J. M., Vancamp, P., DEMENEIX, B. A., & Remaud, S. (2019) · Acta Physiologica · doi:10.1111/apha.13316 · Cited by 51 · see citing works
Azim, K., Rivera, A. D., Raineteau, O., & Butt, A. M. (2014) · Glia · doi:10.1002/glia.22641 · Cited by 51 · see citing works
Self-citationYuan, Y., Tang, X., Bai, Y., Wang, S., An, J., Wu, Y., Xu, Q., Zhang, Y. A., & Chen, Z. (2018) · Theranostics · doi:10.7150/thno.26643 · Cited by 45 · see citing works
Transcriptional Hallmarks of Heterogeneous Neural Stem Cell Niches of the Subventricular Zone
Azim, K., Hurtado‐Chong, A., Fischer, B., Kumar, N., Zweifel, S., Taylor, V., & Raineteau, O. (2015) · Stem Cells · doi:10.1002/stem.2017 · Cited by 42 · see citing works
Self-citationVancamp, P., Gothié, J. M., Luongo, C., Sébillot, A., Blay, K. L., Butruille, L., Pagnin, M., Richardson, S. J., DEMENEIX, B. A., & Remaud, S. (2019) · Scientific Reports · doi:10.1038/s41598-019-56156-w · Cited by 45 · see citing works
Fischer, B., Azim, K., Hurtado‐Chong, A., Ramelli, S., Fernández, M., & Raineteau, O. (2014) · Neural Development · doi:10.1186/1749-8104-9-23 · Cited by 44 · see citing works
Self-citationAdult NSC diversity and plasticity: the role of the niche
Llorens-Bobadilla, E., & Martín-Villalba, A. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.11.008 · Cited by 43 · see citing works
HOPX Defines Heterogeneity of Postnatal Subventricular Zone Neural Stem Cells
Zweifel, S., Marcy, G., Giudice, Q. L., Li, D., Heinrich, C., Azim, K., & Raineteau, O. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.08.006 · Cited by 43 · see citing works
Self-citationPlatel, J., & Bordey, A. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.10.053 · Cited by 38 · see citing works
Pediatric brain repair from endogenous neural stem cells of the subventricular zone
Niimi, Y., & Levison, S. W. (2017) · Pediatric Research · doi:10.1038/pr.2017.261 · Cited by 39 · see citing works
Mosaic Subventricular Origins of Forebrain Oligodendrogenesis
Azim, K., Berninger, B., & Raineteau, O. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00107 · Cited by 33 · see citing works
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Hou, Z., Wu, Q., Sun, X., Chen, H., Li, Y., Zhang, Y., Mori, M., Yang, Y., Jiang, M. Z., & Que, J. (2019) · Development · doi:10.1242/dev.171496 · Cited by 33 · see citing works
Galectin‐3 modulates postnatal subventricular zone gliogenesis
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Mastrodonato, A., Barbati, S. A., Leone, L., Colussi, C., Gironi, K., Rinaudo, M., Piacentini, R., Denny, C. A., & Grassi, C. (2018) · Scientific Reports · doi:10.1038/s41598-017-18676-1 · Cited by 31 · see citing works
Borrett, M. J., Innes, B. T., Tahmasian, N., Bader, G. D., Kaplan, D. R., & Miller, F. D. (2022) · eNeuro · doi:10.1523/eneuro.0271-21.2021 · Cited by 31 · see citing works
Roles of Wnt Signaling in the Neurogenic Niche of the Adult Mouse Ventricular–Subventricular Zone
Hirota, Y., Sawada, M., Huang, S.-H., Ogino, T., Ohata, S., Kubo, A., & Sawamoto, K. (2015) · Neurochemical Research · doi:10.1007/s11064-015-1766-z · Cited by 30 · see citing works
Xu, J., Cheng, S., Jiao, Z., Zhao, Z., Cai, Z., Su, N. Y., Liu, B., Zhou, Z., & Li, Y. (2019) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527318666190204111701 · Cited by 30 · see citing works
Mechanisms of Cortical Differentiation
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Heterogeneous populations of neural stem cells contribute to myelin repair
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Subventricular zone progenitors in time and space: generating neuronal diversity
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Vancamp, P., Blay, K. L., Butruille, L., Sébillot, A., Boelen, A., DEMENEIX, B. A., & Remaud, S. (2022) · Stem Cell Reports · doi:10.1016/j.stemcr.2022.01.002 · Cited by 27 · see citing works
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Self-citationStem Cell Therapy in Children with Traumatic Brain Injury
Lin, W.-Y., Wu, K.-H., Chen, C.-Y., Guo, B., Chang, Y.-J., Lee, T.-A., Lin, M.-J., & Wu, H.-P. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241914706 · Cited by 10 · see citing works
McMurtrey, R. J. (2016) · Journal of Tissue Engineering · doi:10.1177/2041731416671926 · Cited by 13 · see citing works
Postnatal Neural Stem Cells: Probing Their Competence for Cortical Repair
Donega, V., & Raineteau, O. (2017) · The Neuroscientist · doi:10.1177/1073858417697036 · Cited by 11 · see citing works
Self-citationGalectin-3 diminishes Wnt signaling in the postnatal subventricular zone
Al‐Dalahmah, O., Nicholson, J., Draijer, S., Soares, L. C., & Szele, F. G. (2020) · Stem Cells · doi:10.1002/stem.3202 · Cited by 10 · see citing works
Neuronal Subtype Generation During Postnatal Olfactory Bulb Neurogenesis
Angelova, A., Tiveron, M.-C., Cremer, H., & Béclin, C. (2018) · Journal of Experimental Neuroscience · doi:10.1177/1179069518755670 · Cited by 10 · see citing works
Rivera, A. D., Normanton, J. R., Butt, A. M., & Azim, K. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25084452 · Cited by 10 · see citing works
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Chidambaram, S., Velloso, F. J., Rothbard, D. E., Deshpande, K. S., Cajuste, Y., Snyder, K. M., Fajardo, E. J., Fiser, A., Tapinos, N., Levison, S. W., et al. (2022) · Stem Cell Reports · doi:10.1016/j.stemcr.2022.04.007 · Cited by 9 · see citing works
Foucault, L., Capeliez, T., Angonin, D., Lentini, C., Bezin, L., Heinrich, C., Parras, C. M., Donega, V., Marcy, G., & Raineteau, O. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113734 · Cited by 8 · see citing works
Self-citationButt, A. M., Niu, J., Yi, C., & Verkhratsky, A. (2026) · Physiological Reviews · doi:10.1152/physrev.00023.2025 · Cited by 7 · see citing works
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Marymonchyk, A., Malvaut, S., & Saghatelyan, A. (2021) · Development · doi:10.1242/dev.199778 · Cited by 6 · see citing works
The Role of Oligodendrocytes in Alzheimer’s Disease Pathogenesis and Therapy
Guo, S., Yu, X., & Zhang, H. (2025) · Neuroglia · doi:10.3390/neuroglia6040046 · Cited by 5 · see citing works
Oligodendroglial physiology and function
Verkhratsky, A., & Butt, A. M. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-821565-4.00017-1 · Cited by 4 · see citing works
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Sun, S., Guo, W., Zhang, Z., Qiu, M. S., & Dai, Z. (2015) · Neuroscience Bulletin · doi:10.1007/s12264-014-1513-5 · Cited by 4 · see citing works
Could the inhibitor of DNA binding 2 and 4 play a role in white matter injury?
Gou, X., Tang, Y., Qu, Y., Xiao, D.-Q., Ying, J.-J., & Mu, D. (2019) · Reviews in the Neurosciences · doi:10.1515/revneuro-2018-0090 · Cited by 4 · see citing works
Heterogeneity of Neural Stem Cells in the Ventricular–Subventricular Zone
Rushing, G. V., Bollig, M. K., & Ihrie, R. A. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-24108-7_1 · Cited by 3 · see citing works
Marcy, G., Foucault, L., Babina, E., Texeraud, E., Zweifel, S., Heinrich, C., Hernández‐Vargas, H., Parras, C. M., Jabaudon, D., & Raineteau, O. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.05.20.492790 · Cited by 3 · see citing works
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Angonin, D., Marcy, G., & Raineteau, O. (2015) · médecine/sciences · doi:10.1051/medsci/20153111010 · Cited by 2 · see citing works
Self-citationmiRNAs in Mammalian Adult Olfactory Neurogenesis
de Chevigny, A., Cremer, H., & Coré, N. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-804402-5.00008-x · Cited by 2 · see citing works
Chidambaram, S., Rothbard, D. E., Deshpande, K. S., Cajuste, Y., Snyder, K. M., Fajardo, E. J., Fiser, A., Tapinos, N., Levison, S. W., & Wood, T. L. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.03.10.985598 · Cited by 2 · see citing works
Azim, K., Calzolari, F., Cantone, M., Akkermann, R., Vera, J., Hartung, H., Başak, O., Butt, A. M., & Küry, P. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.18.423285 · Cited by 2 · see citing works
Self-citationSchouten, M., Papaloukas, N., Bielefeld, P., Fratantoni, S. A., & Fitzsimons, C. P. (2016) · Springer eBooks · doi:10.1007/978-3-319-27583-3_5 · Cited by 1 · see citing works
Butt, A. M. (2016) · Colloquium Series on Neuroglia in Biology and Medicine From Physiology to Disease · doi:10.4199/c00143ed1v01y201610ngl009 · Cited by 1 · see citing works
Self-citationNeurogenesis in the damaged mammalian brain
Nakafuku, M., & Grande, A. W. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814405-3.00023-0 · Cited by 1 · see citing works
Pieropan, F., Rivera, A., Williams, G. H., Calzolari, F., Butt, A., & Azim, K. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.09.05.284372 · Cited by 1 · see citing works
Self-citationDerkach, D. (2019) · TSpace (University of Toronto)
Neural stem cells-from quiescence to differentiation and potential clinical uses
Dobranici, A., Dinescu, S., & Costache, M. (2021) · Reviews in Biological and Biomedical Sciences · doi:10.31178/rbbs.2021.4.1.2
Zhang, X., Jiang, Y., Wang, H., & Hu, R. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-40423-8.00008-7
Nakane, A., Kitahara, K., Fukushima, R., Nariai, T., Yamazaki, K., & Nagata, H. (2026) · Pharmaceuticals · doi:10.3390/ph19040536
Exploring Transcriptional Heterogeneity in the Postnatal SVZ
Zweifel, S. (2018) · theses.fr (ABES) · doi:10.70675/03ef449dz10baz4170z8ee3z0e9fe3c44a0f
- Authors
- Azim, K., Fischer, B., Hurtado‐Chong, A., Draganova, K., Cantù, C., Zemke, M., Sommer, L., Butt, A., & Raineteau, O.
- Affiliations
- University of Zurich (CH)
- Brain Research Institute, University of Zürich/ETHZZürich Switzerland
- University of Portsmouth (GB)
- Inserm (FR)
- Corresponding author
- Butt, Arthur
- Raineteau, Olivier
- Venue
- Stem Cells
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-04-17
- Volume
- 32
- Issue
- 5
- Pages
- 1301-1312
- ISSN
- 1066-5099 (ISSN-L)
- 1549-4918
- OpenAlex
- W1936856856
- Cited by
- 88
- References
- 35
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 2 · 2023: 3 · 2022: 4 · 2021: 5 · 2020: 6 · 2019: 15 · 2018: 11 · 2017: 10 · 2016: 13 · 2015: 11 · 2014: 4
- FWCI
- 4.40
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- Locations
- Stem Cells (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Agence Nationale de la Recherche (ANR-11-IDEX-0007)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- Wnt/β-catenin signaling, subventricular zone, oligodendrocyte precursor cells, glutamatergic neurons, GABAergic neurons, neuronal lineage specification, glycogen synthase kinase-3β inhibition, AR-A014418
- MeSH terms
- Animals, Mice, Transgenic, Neurons, Oligodendroglia, Thiazoles, Urea, Blotting, Western, Signal Transduction, Microscopy, Confocal, Glutamic Acid, Reverse Transcriptase Polymerase Chain Reaction, Lateral Ventricles, Glycogen Synthase Kinase 3, Cell Proliferation, Green Fluorescent Proteins, beta Catenin, Neural Stem Cells, Wnt3 Protein
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