The Adult Ventricular–Subventricular Zone (V-SVZ) and Olfactory Bulb (OB) Neurogenesis
Open accessAbstract
A large population of neural stem/precursor cells (NSCs) persists in the ventricular-subventricular zone (V-SVZ) located in the walls of the lateral brain ventricles.V-SVZ NSCs produce large numbers of neuroblasts that migrate a long distance into the olfactory bulb (OB) where they differentiate into local circuit interneurons.Here, we review a broad range of discoveries that have emerged from studies of postnatal V-SVZ neurogenesis: the identification of NSCs as a subpopulation of astroglial cells, the neurogenic lineage, new mechanisms of neuronal migration, and molecular regulators of precursor cell proliferation and migration.It has also become evident that V-SVZ NSCs are regionally heterogeneous, with NSCs located in different regions of the ventricle wall generating distinct OB interneuron subtypes.Insights into the developmental origins and molecular mechanisms that underlie the regional specification of V-SVZ NSCs have also begun to emerge.Other recent studies have revealed new cellintrinsic molecular mechanisms that enable lifelong neurogenesis in the V-SVZ.Finally, we discuss intriguing differences between the rodent V-SVZ and the corresponding human brain region.The rapidly expanding cellular and molecular knowledge of V-SVZ NSC biology provides key insights into postnatal neural development, the origin of brain tumors, and may inform the development regenerative therapies from cultured and endogenous human neural precursors.N ew neurons continue to be added through- out life to the olfactory bulb (OB) in the brain of many mammals.In rodents, the adult germinal region for OB neurogenesis is located along the walls of the brain lateral ventricles.Recent results regarding the spatial arrangement and cellular morphology of the primary neural precursors-or, neural stem cells (NSCs)-indicate that this region has characteristics similar to both the embryonic ventricular zone (VZ) and subventricular zone (SVZ).Given this new understanding, we now refer to this region as the ventricular-subventricular zone (V-SVZ).Neuroblasts born from NSCs in the mouse V-SVZ migrate rostrally into the OB where they then disperse radially and differentiate into functional interneurons (Fig. 1).Several distinct interneuron subtypes are generated by the V-SVZ, and estimates indicate that thousands of new OB neurons are generated every day in the young adult rodent brain.The adult V-SVZ is also the birthplace of oligodendro-
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Neurogenesis continues during adulthood in the dentate gyrus of the hippocampus and the subventricular zone, where new neurons are generated throughout life from stem cells.
“Neurogenesis continues during adulthood in two specific neurogenic niches, the dentate gyrus of the hippocampus and the subventricular zone (SVZ) adjacent to lateral ventricles, where new neurons are generated throughout life from stem cells (Kempermann et al., 2015;Lim and Alvarez-Buylla, 2016).”
From Depression and adult neurogenesis: Positive effects of the antidepressant fluoxetine and of physical exercise (2018) · cites this paper as Lim and Alvarez-Buylla, 2016
The Conclusion (page unavailable) describes the adult ventricular–subventricular zone as a stem-cell niche involved in long-term neurogenesis, and Figure 2 identifies cells there that give rise to new neurons in adult mice. The paper does not establish the same lifelong production in the hippocampal dentate gyrus; that location appears in the retrieved passages only in references to other studies. (LLM, conf=0.86)
Experimental — accuracy not yet measuredAstro-TE clusters 5229 and 5230, located in the lateral ventricle bordering rostral dorsal STR, and clusters belonging to the Astro-OLF subclass (5231-5236) match the path of the RMS; the trajectory of these astrocyte clusters on the UMAP matches well with the corresponding spatial gradients.
“Astro-TE clusters 5229 and 5230, located in the lateral ventricle bordering rostral dorsal STR, and clusters belonging to the Astro-OLF subclass (5231–5236) match the path of the RMS70–72 (Extended Data Fig. 12h); the trajectory of these astrocyte clusters on the UMAP matches well with the corresponding spatial gradients”
From A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain (2023) · cites this paper as [72]
Split into 2 atoms — 0 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 1 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredThe dentate gyrus gives rise to excitatory DG granule cells, whereas the SVZ produces migrating cells that follow the RMS and differentiate into inhibitory OB granule cells in the olfactory bulb.
“The first gives rise to the excitatory DG granule cells, whereas the second produces migrating cells that follow the RMS and in the olfactory bulb differentiate into inhibitory OB granule cells72,84,85.”
From A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain (2023) · cites this paper as [72]
The Figure 1 caption describes V-SVZ neuroblasts migrating through the RMS into the olfactory bulb and differentiating into granule cells. The section on diverse OB interneurons says most OB granule cells are GABAergic, supporting the inhibitory characterization with that qualifier. The cited paper does not establish the sentence’s separate claim that the dentate gyrus produces excitatory granule cells. (LLM, conf=0.88)
Experimental — accuracy not yet measuredAstro-TE clusters 5229 and 5230 and clusters in the Astro-OLF subclass match the path of the rostral migratory stream (RMS).
“Astro-TE clusters 5229 and 5230 and clusters in the Astro-OLF subclass match the path of the rostral migratory stream70–72 (RMS; see below).”
From A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain (2023) · cites this paper as [72]
In mammals there are two canonical neurogenic regions, the subventricular zone (SVZ) and subgranular zone (SGZ) at the dentate gyrus of the hippocampus.
“In mammals there are two canonical regions, the subventricular zone (SVZ) and subgranular zone (SGZ) at the dentate gyrus of the hippocampus [159,161].”
From P2X7 Receptor Signaling in Stress and Depression (2019) · cites this paper as [161]
Neurogenesis in the adult brain takes place at sites in which the pool of NPCs is active, called neurogenic niches.
“Neurogenesis in the adult brain may therefore takes place at the sites in which the pool of NPCs is active, called neurogenic niches.”
From P2X7 Receptor Signaling in Stress and Depression (2019) · cites this paper as [161]
The SEZ generates neuroblasts that migrate to the OB, where they differentiate and integrate.
“The largest NSC niche, the sub-ependymal zone (SEZ), generates neuroblasts that migrate to the distant olfactory bulb (OB), where they differentiate and integrate”
From Defining the Adult Neural Stem Cell Niche Proteome Identifies Key Regulators of Adult Neurogenesis (2020) · cites this paper as Lim and Alvarez-Buylla, 2016
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
Bertani, S., Sauer, S., Bolotin, E., & Sauer, F. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.08.019 · Cited by 220 · see citing works
RetractedChromatin modifications and their function
Kouzarides, T. (2007) · Cell · doi:10.1016/j.cell.2007.02.005 · Cited by 10,883 · see citing works
Jenuwein, T., & Allis, C. D. (2001) · Science · doi:10.1126/science.1063127 · Cited by 9,756 · see citing works
Polazzi, E., Mengoni, I., Caprini, M., Peña‐Altamira, E., Kurtys, E., & Monti, B. (2012) · Neurosignals · doi:10.1159/000337115 · Cited by 9,023 · see citing works
Molecular Mechanisms of Depression: Perspectives on New Treatment Strategies
Lang, U. E., & Borgwardt, S. (2013) · Cellular Physiology and Biochemistry · doi:10.1159/000350094 · Cited by 8,501 · see citing works
Neurogenesis in the adult human hippocampus
Eriksson, P. S., Perfilieva, E., Björk-Eriksson, T., Alborn, A.-M., Nordborg, C., Peterson, D. A., & Gage, F. H. (1998) · Nature Medicine · doi:10.1038/3305 · Cited by 6,369 · see citing works
Chen, X., Xiu, M., Xing, J., Yu, S., Min, D., & Guo, F. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000479439 · Cited by 5,759 · see citing works
Reynolds, B. A., & Weiss, S. (1992) · Science · doi:10.1126/science.1553558 · Cited by 5,387 · see citing works
Genome Regulation by Long Noncoding RNAs
Rinn, J. L., & Chang, H. Y. (2012) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-051410-092902 · Cited by 4,011 · see citing works
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
Establishing, maintaining and modifying DNA methylation patterns in plants and animals
Law, J. A., & Jacobsen, S. E. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2719 · Cited by 3,868 · see citing works
The Canonical Notch Signaling Pathway: Unfolding the Activation Mechanism
Kopan, R., & Ilagan, M. X. G. (2009) · Cell · doi:10.1016/j.cell.2009.03.045 · Cited by 3,631 · see citing works
Cabili, M. N., Trapnell, C., Goff, L. A., Koziol, M. J., Tazón‐Vega, B., Regev, A., & Rinn, J. L. (2011) · Genes & Development · doi:10.1101/gad.17446611 · Cited by 3,473 · see citing works
Khalil, A. M., Guttman, M., Huarte, M., Garber, M., Raj, A., Rivea Morales, D., Thomas, K., Presser, A., Bernstein, B. E., van Oudenaarden, A., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904715106 · Cited by 2,872 · see citing works
The Glial Nature of Embryonic and Adult Neural Stem Cells
Kriegstein, A., & Alvarez-Buylla, A. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135600 · Cited by 2,475 · 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
The relationship between the spleen colony-forming cell and the haemopoietic stem cell.
Schofield, R. (1978) · PubMed · Cited by 2,319 · see citing works
A unique chromatin signature uncovers early developmental enhancers in humans
Rada-Iglesias, A., Bajpai, R., Swigut, T., Brugmann, S. A., Flynn, R. A., & Wysocka, J. (2011) · Nature · doi:10.1038/nature09692 · Cited by 2,233 · see citing works
Ying, Q.-L., Nichols, J., Chambers, I., & Smith, A. G. (2003) · Cell · doi:10.1016/s0092-8674(03)00847-x · Cited by 2,114 · see citing works
Neurons derived from radial glial cells establish radial units in neocortex
Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S., & Kriegstein, A. R. (2001) · Nature · doi:10.1038/35055553 · Cited by 2,016 · see citing works
A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression
Wang, K., Yang, Y. W., Liu, B., Sanyal, A., Corces, M. R., Chen, Y., Lajoie, B. R., Protacio, A., Flynn, R. A., Gupta, R. A., et al. (2011) · Nature · doi:10.1038/nature09819 · Cited by 1,963 · 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
Out of Eden: Stem Cells and Their Niches
Watt, F. M., & Hogan, A. B. L. M. (2000) · Science · doi:10.1126/science.287.5457.1427 · Cited by 1,754 · see citing works
Socializing with the Neighbors
Fuchs, E. V., Tumbar, T., & Guasch, G. (2004) · Cell · doi:10.1016/s0092-8674(04)00255-7 · Cited by 1,711 · see citing works
Endothelial Cells Stimulate Self-Renewal and Expand Neurogenesis of Neural Stem Cells
Shen, Q., Goderie, S. K., Jin, L., Karanth, N., Sun, Y., Abramova, N. E., Vincent, P. A., Pumiglia, K. M., & Temple, S. (2004) · Science · doi:10.1126/science.1095505 · Cited by 1,538 · see citing works
Vascular endothelial growth factor (VEGF) stimulates neurogenesis <i>in vitro</i> and <i>in vivo</i>
Jin, K., Zhu, Y., Sun, Y., Mao, X. O., Xie, L., & Greenberg, D. A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.182296499 · Cited by 1,507 · see citing works
Morshead, C. M., Reynolds, B. A., Craig, C. G., McBurney, M. W., Staines, W. A., Morassutti, D., Weiss, S., & van der Kooy, D. (1994) · Neuron · doi:10.1016/0896-6273(94)90046-9 · Cited by 1,403 · see citing works
Adult neurogenesis and functional plasticity in neuronal circuits
Lledo, P., Alonso, M., & Grubb, M. S. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn1867 · Cited by 1,365 · see citing works
Chain Migration of Neuronal Precursors
Lois, C., García-Verdugo, J.-M., & Alvarez-Buylla, A. (1996) · Science · doi:10.1126/science.271.5251.978 · Cited by 1,331 · see citing works
Self-citationÁlvarez-Buylla, A., & Lim, D. A. (2004) · Neuron · doi:10.1016/s0896-6273(04)00111-4 · Cited by 1,320 · see citing works
Self-citationUnique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration
Sanai, N., Tramontin, A. D., Quiñones‐Hinojosa, A., Barbaro, N. M., Gupta, N. M., Kunwar, S., Lawton, M. T., McDermott, M. W., Parsa, A. T., García‐Verdugo, J. M., et al. (2004) · Nature · doi:10.1038/nature02301 · Cited by 1,315 · see citing works
Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation
Molofsky, A. V., Pardal, R., Iwashita, T., Park, I.-K., Clarke, M. F., & Morrison, S. J. (2003) · Nature · doi:10.1038/nature02060 · Cited by 1,301 · see citing works
Chromatin remodelling during development
Ho, L., & Crabtree, G. R. (2010) · Nature · doi:10.1038/nature08911 · Cited by 1,114 · see citing works
Noggin Antagonizes BMP Signaling to Create a Niche for Adult Neurogenesis
Lim, D. A., Tramontin, A. D., Trevejo, J., Herrera, D. G., García‐Verdugo, J. M., & Álvarez-Buylla, A. (2000) · Neuron · doi:10.1016/s0896-6273(00)00148-3 · Cited by 1,090 · see citing works
Self-citationEGF Converts Transit-Amplifying Neurogenic Precursors in the Adult Brain into Multipotent Stem Cells
Doetsch, F. K., Petreanu, L., Caillé, I., García‐Verdugo, J. M., & Álvarez-Buylla, A. (2002) · Neuron · doi:10.1016/s0896-6273(02)01133-9 · Cited by 1,048 · see citing works
A specialized vascular niche for adult neural stem cells
Tavazoie, M., Van der Veken, L., Silva-Vargas, V., Louissaint, M., Colonna, L., Zaidi, B., Garcia-Verdugo, J. M., & Doetsch, F. (2008) · Cell stem cell · doi:10.1016/j.stem.2008.07.025 · Cited by 1,033 · see citing works
Shen, Q., Wang, Y., Kokovay, E., Lin, G., Chuang, S.-M., Goderie, S. K., Roysam, B., & Temple, S. (2008) · Cell stem cell · doi:10.1016/j.stem.2008.07.026 · Cited by 1,027 · see citing works
Mirzadeh, Z., Merkle, F. T., Soriano-Navarro, M., Garcia-Verdugo, J. M., & Alvarez-Buylla, A. (2008) · Cell stem cell · doi:10.1016/j.stem.2008.07.004 · Cited by 1,015 · see citing works
Cremer, H., Lange, R., Christoph, A., Plomann, M., Vopper, G., Roes, J., Brown, R. W., Baldwin, S. A., Kraemer, P. J., Scheff, S. W., et al. (1994) · Nature · doi:10.1038/367455a0 · Cited by 1,007 · see citing works
Francis, F., Koulakoff, A., Boucher, D., Chafey, P., Schaar, B. T., Vinet, M. C., Friocourt, G., McDonnell, N., Reiner, O., Kahn, A., et al. (1999) · Neuron · doi:10.1016/s0896-6273(00)80777-1 · Cited by 1,000 · see citing works
Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing
Molofsky, A. V., Slutsky, S. G., Joseph, N. M., He, S., Pardal, R., Krishnamurthy, J., Sharpless, N. E., & Morrison, S. J. (2006) · Nature · doi:10.1038/nature05091 · Cited by 972 · see citing works
Origin 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
Self-citationDe Santa, F., Totaro, M. G., Prosperini, E., Notarbartolo, S., Testa, G., & Natoli, G. (2007) · Cell · doi:10.1016/j.cell.2007.08.019 · Cited by 965 · see citing works
Dopamine depletion impairs precursor cell proliferation in Parkinson disease
Höglinger, G. U., Rizk, P., Mp, M., Duyckaerts, C. J., Oertel, W. H., Caillé, I., & Hirsch, É. C. (2004) · Nature Neuroscience · doi:10.1038/nn1265 · Cited by 946 · see citing works
Neurogenesis in the striatum of the adult human brain
Ernst, A., Alkass, K., Bernard, S., Salehpour, M., Perl, S., Tisdale, J., Possnert, G., Druid, H., & Frisén, J. (2014) · Cell · doi:10.1016/j.cell.2014.01.044 · Cited by 937 · see citing works
Pencea, V., Bingaman, K. D., Wiegand, S. J., & Luskin, M. B. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-17-06706.2001 · Cited by 928 · see citing works
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 · see citing works
Ogawa, M., Miyata, T., Nakajimat, K., Yagyu, K., Seike, M., Ikenaka, K., Yamamoto, H., & Mikoshibat, K. (1995) · Neuron · doi:10.1016/0896-6273(95)90329-1 · Cited by 889 · see citing works
miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche
Cheng, L.-C., Pastrana, E., Tavazoie, M., & Doetsch, F. (2009) · Nature Neuroscience · doi:10.1038/nn.2294 · Cited by 865 · see citing works
Corridors of migrating neurons in the human brain and their decline during infancy
Sanai, N., Nguyen, T., Ihrie, R. A., Mirzadeh, Z., Tsai, H.-H., Wong, M., Gupta, N., Berger, M. S., Huang, E., Garcia-Verdugo, J.-M., et al. (2011) · Nature · doi:10.1038/nature10487 · Cited by 849 · see citing works
Self-citationRadial glia give rise to adult neural stem cells in the subventricular zone
Merkle, F. T., Tramontin, A. D., García‐Verdugo, J. M., & Álvarez-Buylla, A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407893101 · Cited by 849 · see citing works
Radial Glia Serve as Neuronal Progenitors in All Regions of the Central Nervous System
Anthony, T. E., Klein, C., Fishell, G., & Heintz, N. (2004) · Neuron · doi:10.1016/s0896-6273(04)00140-0 · Cited by 834 · see citing works
Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms.
Sun, Y., Nadal-Vicens, M., Misono, S., Lin, M. Z., Zubiaga, A., Hua, X., Fan, G., & Greenberg, M. (2001) · Cell · doi:10.1016/s0092-8674(01)00224-0 · Cited by 823 · 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
Becoming a new neuron in the adult olfactory bulb
Carleton, A., Petreanu, L., Lansford, R. D., Álvarez-Buylla, A., & Lledo, P. (2003) · Nature Neuroscience · doi:10.1038/nn1048 · Cited by 808 · see citing works
New Neurons Follow the Flow of Cerebrospinal Fluid in the Adult Brain
Sawamoto, K., Wichterle, H., González-Pérez, Ó., Cholfin, J. A., Yamada, M., Spassky, N., Murcia, N. S., García‐Verdugo, J. M., Marín, Ó., Rubenstein, J. L. R., et al. (2006) · Science · doi:10.1126/science.1119133 · Cited by 803 · see citing works
Silber, J., Lim, D. A., Petritsch, C., Persson, A. I., Maunakea, A. K., Yu, M., Vandenberg, S. R., Ginzinger, D. G., James, C. D., Costello, J. F., et al. (2008) · BMC Medicine · doi:10.1186/1741-7015-6-14 · Cited by 765 · see citing works
Self-citationCoordinated Interaction of Neurogenesis and Angiogenesis in the Adult Songbird Brain
Louissaint, A., Rao, S., Leventhal, C., & Goldman, S. A. (2002) · Neuron · doi:10.1016/s0896-6273(02)00722-5 · Cited by 735 · see citing works
Network of tangential pathways for neuronal migration in adult mammalian brain
Doetsch, F. K., & Álvarez-Buylla, A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.25.14895 · Cited by 735 · see citing works
Hes1 and Hes5 as Notch effectors in mammalian neuronal differentiation
Ohtsuka, T., Ishibashi, M., Gradwohl, G., Nakanishi, S., Guillemot, F., & Kageyama, R. (1999) · The EMBO Journal · doi:10.1093/emboj/18.8.2196 · Cited by 735 · see citing works
Ellis, P., Fagan, B. M., Magness, S. T., Hutton, S. R., Taranova, O., Hayashi, S., McMahon, A. P., Rao, M. S., & Pevny, L. (2004) · Developmental Neuroscience · doi:10.1159/000082134 · Cited by 733 · see citing works
Radial Glial Identity Is Promoted by Notch1 Signaling in the Murine Forebrain
Gaiano, N., Nye, J. S., & Fishell, G. (2000) · Neuron · doi:10.1016/s0896-6273(00)81172-1 · Cited by 727 · see citing works
Imayoshi, I., Sakamoto, M., Yamaguchi, M., Mori, K., & Kageyama, R. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4987-09.2010 · Cited by 716 · see citing works
Sonic Hedgehog Is Required for Progenitor Cell Maintenance in Telencephalic Stem Cell Niches
Machold, R. P., Hayashi, S., Rutlin, M. L., Muzumdar, M. D., Nery, S. V., Corbin, J. G., Gritli-Linde, A., Dellovade, T., Porter, J. A., Rubin, L. L., et al. (2003) · Neuron · doi:10.1016/s0896-6273(03)00561-0 · Cited by 710 · see citing works
In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog
Ahn, S., & Joyner, A. L. (2005) · Nature · doi:10.1038/nature03994 · Cited by 699 · see citing works
Bai, C. B., Auerbach, W., Lee, J. S., Stephen, D., & Joyner, A. L. (2002) · Development · doi:10.1242/dev.129.20.4753 · Cited by 692 · see citing works
Gross, R. E., Mehler, M. F., Mabie, P. C., Zang, Z., Santschi, L. A., & Kessler, J. A. (1996) · Neuron · doi:10.1016/s0896-6273(00)80193-2 · Cited by 690 · see citing works
Maturation and Death of Adult-Born Olfactory Bulb Granule Neurons: Role of Olfaction
Petreanu, L., & Álvarez-Buylla, A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-14-06106.2002 · Cited by 680 · see citing works
LeX/ssea-1 Is Expressed by Adult Mouse CNS Stem Cells, Identifying Them as Nonependymal
Capela, A., & Temple, S. (2002) · Neuron · doi:10.1016/s0896-6273(02)00835-8 · Cited by 671 · see citing works
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 666 · see citing works
Sasai, Y., Kageyama, R., Tagawa, Y., Shigemoto, R., & Nakanishi, S. (1992) · Genes & Development · doi:10.1101/gad.6.12b.2620 · Cited by 665 · see citing works
Regeneration of a germinal layer in the adult mammalian brain
Doetsch, F. K., García‐Verdugo, J. M., & Álvarez-Buylla, A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.20.11619 · Cited by 662 · see citing works
The cerebrospinal fluid provides a proliferative niche for neural progenitor cells
Lehtinen, M. K., Zappaterra, M. W., Chen, X., Yang, Y. J., Hill, A. D., Lun, M., Maynard, T., Gonzalez, D., Kim, S., Ye, P., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.01.023 · Cited by 648 · see citing works
Neuronal fate determinants of adult olfactory bulb neurogenesis
Hack, M., Saghatelyan, A., de Chevigny, A., Pfeifer, A., Ashery-Padan, R., Lledo, P., & Götz, M. (2005) · Nature Neuroscience · doi:10.1038/nn1479 · Cited by 648 · see citing works
Codega, P., Silva-Vargas, V., Paul, A., Maldonado-Soto, A. R., DeLeo, A. M., Pastrana, E., & Doetsch, F. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.039 · Cited by 634 · see citing works
Nishino, J., Kim, I., Chada, K. K., & Morrison, S. J. (2008) · Cell · doi:10.1016/j.cell.2008.09.017 · Cited by 623 · see citing works
Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo
Suhonen, J., Peterson, D. A., Ray, J., & Gage, F. H. (1996) · Nature · doi:10.1038/383624a0 · Cited by 622 · 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
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
Self-citationDnmt3a-Dependent Nonpromoter DNA Methylation Facilitates Transcription of Neurogenic Genes
Wu, H., Coskun, V., Tao, J., Xie, W., Ge, W., Yoshikawa, K., Li, E., Zhang, Y., & Sun, Y. E. (2010) · Science · doi:10.1126/science.1190485 · Cited by 604 · see citing works
The Role of Notch in Promoting Glial and Neural Stem Cell Fates
Gaiano, N., & Fishell, G. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.030702.130823 · Cited by 598 · see citing works
Jackson, E., García-Verdugo, J., Gil-Perotín, S., Roy, M., Quiñones-Hinojosa, A., Vandenberg, S., & Álvarez-Buylla, A. (2006) · Neuron · doi:10.1016/j.neuron.2006.06.012 · Cited by 587 · see citing works
Molofsky, A. V., He, S., Bydon, M., Morrison, S. J., & Pardal, R. (2005) · Genes & Development · doi:10.1101/gad.1299505 · Cited by 586 · see citing works
Hatakeyama, J., Bessho, Y., Katoh, K., Ookawara, S., Fujioka, M., Guillemot, F., & Kageyama, R. (2004) · Development · doi:10.1242/dev.01436 · Cited by 575 · see citing works
Nait‐Oumesmar, B., Decker, L., Lachapelle, F., Avellana‐Adalid, V., Bachelin, C., & Van Evercooren, A. B. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00873.x · Cited by 560 · see citing works
Quiñones‐Hinojosa, A., Sanai, N., Soriano‐Navarro, M., González-Pérez, Ó., Mirzadeh, Z., Gil‐Perotín, S., Romero-Rodriguez, R., Berger, M. S., García‐Verdugo, J. M., & Álvarez-Buylla, A. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20798 · Cited by 555 · see citing works
Brezun, J. M., & Daszuta, A. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00693-9 · Cited by 549 · see citing works
Banasr, M., Héry, M., Printemps, R., & Daszuta, A. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300320 · Cited by 539 · see citing works
MicroRNA-mediated switching of chromatin-remodelling complexes in neural development
Yoo, A. S., Staahl, B. T., Chen, L., & Crabtree, G. R. (2009) · Nature · doi:10.1038/nature08139 · Cited by 537 · see citing works
From angiogenesis to neuropathology
Greenberg, D. A., & Jin, K. (2005) · Nature · doi:10.1038/nature04481 · Cited by 532 · see citing works
van der Vlag, J., & Otte, A. P. (1999) · Nature Genetics · doi:10.1038/70602 · Cited by 527 · see citing works
Directional guidance of neuronal migration in the olfactory system by the protein Slit
Wu, W., Wong, K., Chen, J., Jiang, Z., Dupuis, S., Wu, J. Y., & Rao, Y. (1999) · Nature · doi:10.1038/22477 · Cited by 525 · see citing works
Zigova, T., Pencea, V., Wiegand, S. J., & Luskin, M. B. (1998) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.1998.0684 · Cited by 525 · see citing works
Zhao, C., Sun, G., Li, S., & Shi, Y. (2009) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1576 · Cited by 521 · see citing works
Cross talk between microRNA and epigenetic regulation in adult neurogenesis
Szulwach, K. E., Li, X., Smrt, R. D., Li, Y., Luo, Y., Lin, L., Santistevan, N. J., Li, W., Zhao, X., & Jin, P. (2010) · Journal of Cell Biology · doi:10.1083/jcb.200908151 · Cited by 493 · see citing works
Embryonic origin of postnatal neural stem cells
Fuentealba, L. C., Rompani, S. B., Parraguez, J. I., Obernier, K., Romero, R., Cepko, C. L., & Alvarez-Buylla, A. (2015) · Cell · doi:10.1016/j.cell.2015.05.041 · Cited by 488 · cited 2× · see citing works
“Curiously, this regional specification is already established in the embryo at very early stages of development (Fuentealba et al. 2015).”
BackgroundConover, J. C., Doetsch, F. K., García‐Verdugo, J. M., Gale, N. W., Yancopoulos, G. D., & Álvarez-Buylla, A. (2000) · Nature Neuroscience · doi:10.1038/80606 · Cited by 482 · see citing works
Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal
Aguirre, A. A., Rubio, M. E., & Gallo, V. (2010) · Nature · doi:10.1038/nature09347 · Cited by 482 · see citing works
Roles of bHLH genes in neural stem cell differentiation
Kageyama, R., Ohtsuka, T., Hatakeyama, J., & Ohsawa, R. (2005) · Experimental Cell Research · doi:10.1016/j.yexcr.2005.03.015 · Cited by 482 · see citing works
Tomasiewicz, H. G., Ono, K., Yee, D., Thompson, C., Goridis, C., Rutishauser, U. S., & Magnuson, T. (1993) · Neuron · doi:10.1016/0896-6273(93)90228-j · Cited by 475 · see citing works
Neurod1 is essential for the survival and maturation of adult-born neurons
Gao, Z., Ure, K., Ables, J. L., Lagace, D. C., Nave, K.-A., Goebbels, S., Eisch, A. J., & Hsieh, J. (2009) · Nature Neuroscience · doi:10.1038/nn.2385 · Cited by 473 · 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
Picard-Riéra, N., Decker, L., Delarasse, C., Goude, K., Nait‐Oumesmar, B., Liblau, R., Pham-Dinh, D., & Evercooren, A. B. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.192314199 · Cited by 469 · see citing works
Not(ch) just development: Notch signalling in the adult brain
Ables, J. L., Breunig, J. J., Eisch, A. J., & RAKIC, P. T. (2011) · Nature reviews. Neuroscience · doi:10.1038/nrn3024 · Cited by 460 · see citing works
Li, H.-S., Chen, J., Wu, W., Fagaly, T., Zhou, L., Yuan, W., Dupuis, S., Jiang, Z., Nash, W. E., Gick, C., et al. (1999) · Cell · doi:10.1016/s0092-8674(00)80591-7 · Cited by 460 · see citing works
Pigment epithelium–derived factor is a niche signal for neural stem cell renewal
Ramírez‐Castillejo, C., Sánchez‐Sánchez, F., Andreu-Agulló, C., Ferrón, S. R., Aroca‐Aguilar, J., Sánchez‐Gómez, P., Mira, H., Escribano, J., & Fariñas, I. (2006) · Nature Neuroscience · doi:10.1038/nn1657 · Cited by 446 · see citing works
Liu, X., Wang, Q., Haydar, T. F., & Bordey, A. (2005) · Nature Neuroscience · doi:10.1038/nn1522 · Cited by 446 · see citing works
Tropepe, V., Craig, C. G., Morshead, C. M., & van der Kooy, D. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-20-07850.1997 · Cited by 442 · see citing works
Expression and function of orphan nuclear receptor TLX in adult neural stem cells
Shi, Y., Lie, D. C., Taupin, P., Nakashima, K., Ray, J., Yu, R. T., Gage, F. H., & Evans, R. M. (2003) · Nature · doi:10.1038/nature02211 · Cited by 417 · see citing works
Direct Evidence for Homotypic, Glia-Independent Neuronal Migration
Wichterle, H., García‐Verdugo, J. M., & Álvarez-Buylla, A. (1997) · Neuron · doi:10.1016/s0896-6273(00)80317-7 · Cited by 416 · see citing works
Ono, K., Tomasiewicz, H. G., Magnuson, T., & Rutishauser, U. S. (1994) · Neuron · doi:10.1016/0896-6273(94)90028-0 · Cited by 414 · see citing works
Mash1 specifies neurons and oligodendrocytes in the postnatal brain
Parras, C., Galli, R., Britz, O., Soares, S., Galichet, C., Battiste, J., Johnson, J. E., Nakafuku, M., Vescovi, A., & Guillemot, F. (2004) · EMBO Journal · doi:10.1038/sj.emboj.7600447 · Cited by 404 · see citing works
Ohtsuka, T., Sakamoto, M., Guillemot, F., & Kageyama, R. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m102420200 · Cited by 402 · see citing works
Chromatin remodelling factor Mll1 is essential for neurogenesis from postnatal neural stem cells
Lim, D., Huang, Y.-C., Swigut, T., Mirick, A. L., García-Verdugo, J., Wysocka, J., Ernst, P., & Álvarez-Buylla, A. (2009) · Nature · doi:10.1038/nature07726 · Cited by 400 · see citing works
Self-citationMicroglia instruct subventricular zone neurogenesis
Walton, N. M., Sutter, B. M., Laywell, E. D., Levkoff, L. H., Kearns, S. M., Marshall, G. P., Scheffler, B., & Steindler, D. A. (2006) · Glia · doi:10.1002/glia.20419 · Cited by 400 · see citing works
Bond, A. M., VanGompel, M. J. W., Sametsky, E. A., Clark, M. F., Savage, J. C., Disterhoft, J. F., & Kohtz, J. D. (2009) · Nature Neuroscience · doi:10.1038/nn.2371 · Cited by 399 · see citing works
Radial glia: multi-purpose cells for vertebrate brain development
Campbell, K., & Götz, M. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02156-2 · Cited by 389 · see citing works
Leventhal, C., Rafii, S., Rafii, D., Shahar, A., & Goldman, S. A. (1999) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.1999.0762 · Cited by 389 · see citing works
Ishibashi, M., Moriyoshi, K., Sasai, Y., Shiota, K., Nakanishi, S., & Kageyama, R. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06448.x · Cited by 388 · see citing works
Zhao, C., Sun, G., Li, S., Lang, M., Su, Y., Li, W., & Shi, Y. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908750107 · Cited by 388 · see citing works
Huntingtin aggregates may not predict neuronal death in Huntington's disease
Kuemmerle, S., Gutekunst, C., Klein, A., Li, X., Li, S.-H., Beal, M. F., Hersch, S. M., & Ferrante, R. J. (1999) · Annals of Neurology · doi:10.1002/1531-8249(199912)46:6 · Cited by 387 · see citing works
Anatomy of the brain neurogenic zones revisited: Fractones and the fibroblast/macrophage network
Mercier, F., Kitasako, J. T., & Hatton, G. I. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10342 · Cited by 384 · see citing works
Pastrana, É., Cheng, L.-C., & Doetsch, F. K. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810407106 · Cited by 381 · see citing works
Adult Neural Stem Cells Bridge Their Niche
Fuentealba, L. C., Obernier, K., & Álvarez-Buylla, A. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.05.012 · Cited by 367 · 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
Cytoskeletal coordination during neuronal migration
Schaar, B. T., & McConnell, S. K. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506008102 · Cited by 364 · see citing works
Hu, H., Tomasiewicz, H. G., Magnuson, T., & Rutishauser, U. S. (1996) · Neuron · doi:10.1016/s0896-6273(00)80094-x · Cited by 361 · see citing works
Ramos, A. D., Andersen, R. E., Liu, S. J., Nowakowski, T. J., Hong, S. J., Gertz, C. C., Salinas, R. D., Zarabi, H., Kriegstein, A. R., & Lim, D. A. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.02.007 · Cited by 359 · see citing works
Kokovay, E., Goderie, S. K., Wang, Y., Lotz, S., Lin, G., Sun, Y., Roysam, B., Shen, Q., & Temple, S. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.05.019 · Cited by 358 · see citing works
Lake-Front Property: A Unique Germinal Niche by the Lateral Ventricles of the Adult Brain
Ihrie, R. A., & Álvarez-Buylla, A. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.004 · Cited by 346 · see citing works
Quantitative analysis of neuronal diversity in the mouse olfactory bulb
Parrish-Aungst, S., Shipley, M. T., Erdélyi, F., Szabó, G., & Puché, A. C. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21205 · 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
Dependence of Olfactory Bulb Neurogenesis on Prokineticin 2 Signaling
Ng, K., Li, J., Cheng, M., Leslie, F. M., Lee, A. G., & Zhou, Q. (2005) · Science · doi:10.1126/science.1112103 · Cited by 332 · see citing works
CD133 + neural stem cells in the ependyma of mammalian postnatal forebrain
Coskun, V., Wu, H., Blanchi, B., Tsao, S. W., Kim, K., Zhao, J., Biancotti, J. C., Hutnick, L. K., Krueger, R. C., Fan, G., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710000105 · Cited by 331 · see citing works
Slowly dividing neural progenitors are an embryonic origin of adult neural stem cells
Furutachi, S., Miya, H., Watanabe, T., Kawai, H., Yamasaki, N., Harada, Y., Imayoshi, I., Nelson, M., Nakayama, K. I., Hirabayashi, Y., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.3989 · Cited by 329 · see citing works
Kohwi, M., Osumi, N., Rubenstein, J. L. R., & Álvarez-Buylla, A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1435-05.2005 · Cited by 329 · see citing works
H3K27 Demethylases, at Long Last
Swigut, T., & Wysocka, J. (2007) · Cell · doi:10.1016/j.cell.2007.09.026 · Cited by 327 · see citing works
Sequential actions of BMP receptors control neural precursor cell production and fatePreprint
Panchision, D. M., Pickel, J. M., Studer, L., Lee, S., Turner, P. A., Hazel, T. G., & McKay, R. D. G. (2001) · Genes & Development · doi:10.1101/gad.894701 · Cited by 327 · see citing works
Bulfone, A., Wang, F., Hevner, R. F., Anderson, S. A., Cutforth, T., Chen, S., Meneses, J. J., Pedersen, R. A., Axel, R., & Rubenstein, J. L. R. (1998) · Neuron · doi:10.1016/s0896-6273(00)80647-9 · Cited by 325 · see citing works
GABA Release and Uptake Regulate Neuronal Precursor Migration in the Postnatal Subventricular Zone
Bolteus, A. J., & Bordey, A. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1999-04.2004 · Cited by 319 · see citing works
Stem cells and pattern formation in the nervous system: the possible versus the actual.
Anderson, D. J. (2001) · Neuron · doi:10.1016/s0896-6273(01)00260-4 · Cited by 318 · see citing works
Rašin, M.-R., Gazula, V., Breunig, J. J., Kwan, K. Y., Johnson, M. B., Liu‐Chen, S., Li, H.-S., Jan, L. Y., Jan, Y. N., RAKIC, P. T., et al. (2007) · Nature Neuroscience · doi:10.1038/nn1924 · Cited by 316 · see citing works
Nitric oxide negatively regulates mammalian adult neurogenesis
Packer, M. A., Stasiv, Y., Benraiss, A., Chmielnicki, E., Grinberg, A., Westphal, H., Goldman, S. A., & Enikolopov, G. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1633579100 · Cited by 314 · see citing works
Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis
Hack, I., Bancila, M., Loulier, K., Carroll, P., & Cremer, H. (2002) · Nature Neuroscience · doi:10.1038/nn923 · Cited by 313 · see citing works
Chen, H., Thiagalingam, A., Chopra, H., Borges, M., Feder, J. N., Nelkin, B., Baylin, S., & Ball, D. W. (1997) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.94.10.5355 · Cited by 310 · see citing works
Electrophysiological Differentiation of New Neurons in the Olfactory Bulb
Belluzzi, O., Benedusi, M., Ackman, J. B., & LoTurco, J. J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-32-10411.2003 · Cited by 309 · see citing works
Montgomery, R. L., Hsieh, J., Barbosa, A. C. C., Richardson, J. A., & Olson, E. N. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902750106 · Cited by 307 · see citing works
Chazal, G., Durbec, P. L., Jankovski, A., Rougon, G. N., & Cremer, H. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-04-01446.2000 · Cited by 304 · see citing works
Adult Stem Cell Plasticity: Fact or Artifact?
RAFF, M. C. (2003) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.19.111301.143037 · Cited by 296 · see citing works
The Distinct Temporal Origins of Olfactory Bulb Interneuron Subtypes
Batista‐Brito, R., Close, J., Machold, R. P., & Fishell, G. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5625-07.2008 · Cited by 285 · see citing works
Protective astrogenesis from the SVZ niche after injury is controlled by Notch modulator Thbs4
Benner, E. J., Luciano, D., Jo, R., Abdi, K., Paez-Gonzalez, P., Sheng, H., Warner, D. S., Liu, C., Eroglu, C., & Kuo, C. T. (2013) · Nature · doi:10.1038/nature12069 · Cited by 282 · see citing works
Slit2-Mediated Chemorepulsion and Collapse of Developing Forebrain Axons
Nguyen-Ba-Charvet, K. T., Brose, K., Marillat, V., Kidd, T., Goodman, C. S., Tessier‐Lavigne, M., Sotelo, C., & Chédotal, A. (1999) · Neuron · doi:10.1016/s0896-6273(00)80702-3 · Cited by 282 · see citing works
Mabie, P. C., Mehler, M. F., & Kessler, J. A. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-16-07077.1999 · Cited by 281 · see citing works
Direct cell–cell contact with the vascular niche maintains quiescent neural stem cells
Ottone, C., Krusche, B., Whitby, A., Clements, M., Quadrato, G., Pitulescu, M. E., Adams, R. H., & Parrinello, S. (2014) · Nature Cell Biology · doi:10.1038/ncb3045 · Cited by 279 · see citing works
Neuronal Differentiation of Precursors in the Neocortical Ventricular Zone Is Triggered by BMP
Li, W., Cogswell, C. A., & LoTurco, J. J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-21-08853.1998 · Cited by 277 · see citing works
Adult neural stem cells in distinct microdomains generate previously unknown interneuron types
Merkle, F. T., Fuentealba, L. C., Sanders, T. A., Magno, L., Kessaris, N., & Álvarez-Buylla, A. (2013) · Nature Neuroscience · doi:10.1038/nn.3610 · Cited by 277 · see citing works
High Levels of Id1 Expression Define B1 Type Adult Neural Stem Cells
Nam, H.-S., & Benezra, R. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.08.017 · Cited by 272 · 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
LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells
Bonaguidi, M. A., McGuire, T. L., Hu, M., Kan, L., Samanta, J., & Kessler, J. A. (2005) · Development · doi:10.1242/dev.02166 · Cited by 268 · see citing works
Neural precursor cell chain migration and division are regulated through different β1 integrins
Jacques, T. S., Relvas, J. B., Nishimura, S. L., Pytela, R., Edwards, G. M., Streuli, C. H., & ffrench‐Constant, C. (1998) · Development · doi:10.1242/dev.125.16.3167 · Cited by 265 · see citing works
Adult Neurogenesis Requires Smad4-Mediated Bone Morphogenic Protein Signaling in Stem Cells
Colak, D., Mori, T., Brill, M. S., Pfeifer, A., Falk, S., Deng, C., Monteiro, R. M., Mummery, C. L., Sommer, L., & Götz, M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4374-07.2008 · Cited by 264 · 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
Self-citationChemorepulsion of Neuronal Migration by Slit2 in the Developing Mammalian Forebrain
Hu, H. (1999) · Neuron · doi:10.1016/s0896-6273(01)80029-5 · Cited by 249 · see citing works
Olig2 Directs Astrocyte and Oligodendrocyte Formation in Postnatal Subventricular Zone Cells
Marshall, C. A. G., Novitch, B. G., & Goldman, J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1924-05.2005 · Cited by 249 · see citing works
Stump, G., Durrer, A., Klein, A.-L., Lütolf, S., Suter, U., & Taylor, V. (2002) · Mechanisms of Development · doi:10.1016/s0925-4773(02)00043-6 · Cited by 248 · 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
Murase, S., & Horwitz, A. F. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03568.2002 · Cited by 245 · 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
Sun, G., Yu, R. T., Evans, R. M., & Shi, Y. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704089104 · Cited by 241 · see citing works
Ramos, A. D., Diaz, A. A., Nellore, A., Delgado, R. N., Park, K.-Y., Gonzales-Roybal, G., Oldham, M. C., Song, J. S., & Lim, D. A. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.03.003 · Cited by 240 · see citing works
Self-citationWaclaw, R. R., Allen, Z. J., Bell, S. M., Erdélyi, F., Szabó, G., Potter, S. S., & Campbell, K. (2006) · Neuron · doi:10.1016/j.neuron.2006.01.018 · Cited by 237 · see citing works
Leukemia Inhibitory Factor Promotes Neural Stem Cell Self-Renewal in the Adult Brain
Bauer, Š., & Patterson, P. H. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3047-06.2006 · Cited by 234 · see citing works
Moreno‐López, B., Romero‐Grimaldi, C., Noval, J. A., Murillo‐Carretero, M., Matarredona, E. R., & Estrada, C. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1574-03.2004 · Cited by 230 · see citing works
Tenascin-R mediates activity-dependent recruitment of neuroblasts in the adult mouse forebrain
Saghatelyan, A., de Chevigny, A., Schachner, M., & Lledo, P. (2004) · Nature Neuroscience · doi:10.1038/nn1211 · Cited by 229 · see citing works
Kirschenbaum, B., Doetsch, F. K., Lois, C., & Álvarez-Buylla, A. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-06-02171.1999 · Cited by 224 · see citing works
Roegiers, F., & Jan, Y. N. (2004) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2004.02.010 · Cited by 223 · see citing works
Vascular niche factor PEDF modulates Notch-dependent stemness in the adult subependymal zone
Andreu-Agulló, C., Morante‐Redolat, J. M., Delgado, A. C., & Fariñas, I. (2009) · Nature Neuroscience · doi:10.1038/nn.2437 · Cited by 218 · see citing works
Neurogenesis at the Brain–Cerebrospinal Fluid Interface
Lehtinen, M. K., & Walsh, C. A. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-092910-154026 · Cited by 213 · see citing works
New Neurons Clear the Path of Astrocytic Processes for Their Rapid Migration in the Adult Brain
Kaneko, N., Marín, O., Koike, M., Hirota, Y., Uchiyama, Y., Wu, J. Y., Lu, Q., Tessier-Lavigne, M., Alvarez-Buylla, A., Okano, H., et al. (2010) · Neuron · doi:10.1016/j.neuron.2010.06.018 · Cited by 212 · see citing works
Self-citationKuo, C. T., Mirzadeh, Z., Soriano‐Navarro, M., Rašin, M. R., Wang, D., Shen, J., Šestan, N., García‐Verdugo, J. M., Álvarez-Buylla, A., Jan, L. Y., et al. (2006) · Cell · doi:10.1016/j.cell.2006.10.041 · Cited by 211 · see citing works
Ephrin-A2 reverse signaling negatively regulates neural progenitor proliferation and neurogenesisPreprint
Holmberg, J., Armulik, A., Senti, K.-A., Edoff, K., Spalding, K. L., Momma, S., Cassidy, R. M., Flanagan, J. G., & Frisén, J. (2005) · Genes & Development · doi:10.1101/gad.326905 · Cited by 209 · see citing works
Kosaka, K., Aika, Y., Toida, K., Heizmann, C. W., Hunziker, W. H., Jacobowitz, D. M., Nagatsu, I., Streit, P., Visser, T. J., & Kosaka, T. (1995) · Neuroscience Research · doi:10.1016/0168-0102(95)90017-9 · Cited by 208 · see citing works
Ninkovic, J., Steiner-Mezzadri, A., Jawerka, M., Akinci, U., Masserdotti, G., Petricca, S., Fischer, J., von Holst, A., Beckers, J., Lie, D. C., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.07.002 · Cited by 208 · see citing works
Jin, K., Mao, X. O., Sun, Y., Xie, L., Jin, L., Nishi, E., Klagsbrun, M., & Greenberg, D. A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-13-05365.2002 · Cited by 207 · see citing works
O’Keeffe, G. C., Tyers, P., Aarsland, D., Dalley, J. W., Barker, R. A., & Caldwell, M. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803955106 · Cited by 207 · see citing works
Kosaka, K., Toida, K., Aika, Y., & Kosaka, T. (1998) · Neuroscience Research · doi:10.1016/s0168-0102(98)00002-9 · Cited by 202 · see citing works
The Subventricular Zone En-face: Wholemount Staining and Ependymal Flow
Mirzadeh, Z., Doetsch, F. K., Sawamoto, K., Wichterle, H., & Álvarez-Buylla, A. (2010) · Journal of Visualized Experiments · doi:10.3791/1938 · Cited by 199 · see citing works
Kokovay, E., Wang, Y., Kusek, G., Wurster, R., Lederman, P. L., Lowry, N. A., Shen, Q., & Temple, S. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.06.016 · Cited by 199 · see citing works
Wong, S. Y., & Reiter, J. F. (2008) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(08)00809-0 · Cited by 194 · see citing works
Jagged1 signals in the postnatal subventricular zone are required for neural stem cell self‐renewal
Nyfeler, Y., Kirch, R. D., Mantei, N., Leone, D. P., Radtke, F., Suter, U., & Taylor, V. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600816 · Cited by 191 · see citing works
Zheng, W., Nowakowski, R. S., & Vaccarino, F. M. (2004) · Developmental Neuroscience · doi:10.1159/000082136 · Cited by 191 · see citing works
Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors
Chambers, C. B., Peng, Y., Nguyen, H., Gaiano, N., Fishell, G., & Nye, J. S. (2001) · Development · doi:10.1242/dev.128.5.689 · Cited by 184 · see citing works
Delgado, A. C., Ferrón, S. R., Vicente, D., Porlan, E., Pérez‐Villalba, A., Trujillo, C. M., D’Ocón, P., & Fariñas, I. (2014) · Neuron · doi:10.1016/j.neuron.2014.06.015 · Cited by 182 · see citing works
The Heterogeneity of Adult Neural Stem Cells and the Emerging Complexity of Their NichePreprint
Álvarez-Buylla, A., Kohwi, M., Nguyen, T. M., & Merkle, F. T. (2008) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2008.73.019 · Cited by 180 · see citing works
Wnt signaling: multiple functions in neural development
Ille, F., & Sommer, L. (2005) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-005-4552-2 · Cited by 177 · see citing works
Chmielnicki, E., Benraiss, A., Economides, A. N., & Goldman, S. A. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1554-03.2004 · Cited by 171 · see citing works
NeuroD1 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
Transventricular delivery of Sonic hedgehog is essential to cerebellar ventricular zone development
Huang, X., Liu, J., Ketova, T., Fleming, J. T., Grover, V. K., Cooper, M. K., Litingtung, Y., & Chiang, C. C. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911838107 · Cited by 167 · see citing works
Structure and function of the Smoothened extracellular domain in vertebrate Hedgehog signaling
Nachtergaele, S., Whalen, D. M., Mydock, L. K., Zhao, Z., Malinauskas, T., Krishnan, K., Ingham, P. W., Covey, D. F., Siebold, C., & Rohatgi, R. (2013) · eLife · doi:10.7554/elife.01340 · Cited by 167 · see citing works
Histone deacetylases 1 and 2 are expressed at distinct stages of neuro‐glial development
MacDonald, J. L., & Roskams, A. J. (2008) · Developmental Dynamics · doi:10.1002/dvdy.21626 · Cited by 166 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain
Yao, Z., van Velthoven, C. T. J., Kunst, M., Zhang, M., McMillen, D., Lee, C., Jung, W., Goldy, J., Abdelhak, A., Aitken, M., et al. (2023) · Nature · doi:10.1038/s41586-023-06812-z · Cited by 1,194 · see citing works
Challenges to curing primary brain tumours
Aldape, K., Brindle, K. M., Chesler, L., Chopra, R., Gajjar, A., Gilbert, M. R., Gottardo, N., Gutmann, D. H., Hargrave, D., Holland, E. C., et al. (2019) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-019-0177-5 · Cited by 959 · see citing works
Leeman, D. S., Hebestreit, K., Ruetz, T., Webb, A. E., McKay, A., Pollina, E. A., Dulken, B. W., Zhao, X., Yeo, R. W., Ho, T. T., et al. (2018) · Science · doi:10.1126/science.aag3048 · Cited by 528 · see citing works
Neural stem cells: origin, heterogeneity and regulation in the adult mammalian brain
Obernier, K., & Alvarez-Buylla, A. (2019) · Development · doi:10.1242/dev.156059 · Cited by 578 · see citing works
Quiescence Modulates Stem Cell Maintenance and Regenerative Capacity in the Aging Brain
Kalamakis, G., Brüne, D., Ravichandran, S., Bolz, J., Fan, W., Ziebell, F., Stiehl, T., Catalá-Martinez, F., Kupke, J., Zhao, S., et al. (2019) · Cell · doi:10.1016/j.cell.2019.01.040 · Cited by 399 · see citing works
Micheli, L., Ceccarelli, M., D’Andrea, G., & Tirone, F. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.09.002 · Cited by 288 · see citing works
Shah, P. T., Stratton, J. A., Stykel, M. G., Abbasi, S., Sharma, S., Mayr, K. A., Koblinger, K., Whelan, P. J., & Biernaskie, J. (2018) · Cell · doi:10.1016/j.cell.2018.03.063 · Cited by 221 · see citing works
Single cell molecular alterations reveal target cells and pathways of concussive brain injury
Arneson, D., Zhang, G., Ying, Z., Zhuang, Y., Byun, H. R., Ahn, I. S., Gomez-Pinilla, F., & Yang, X. (2018) · Nature Communications · doi:10.1038/s41467-018-06222-0 · Cited by 193 · see citing works
Defining the Adult Neural Stem Cell Niche Proteome Identifies Key Regulators of Adult Neurogenesis
Kjell, J., Fischer-Sternjak, J., Thompson, A. J., Friess, C., Sticco, M. J., Salinas, F., Cox, J., Martinelli, D. C., Ninkovic, J., Franze, K., et al. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.01.002 · Cited by 163 · see citing works
P2X7 Receptor Signaling in Stress and Depression
Ribeiro, D. E., Roncalho, A. L., Glaser, T., Ulrich, H., Wegener, G., & Joca, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20112778 · Cited by 129 · see citing works
Ojala, D. S., Sun, S., Santiago-Ortiz, J. L., Shapiro, M. G., Romero, P. A., & Schaffer, D. V. (2018) · Molecular Therapy · doi:10.1016/j.ymthe.2017.09.006 · Cited by 97 · see citing works
Epithelial Sodium Channel Regulates Adult Neural Stem Cell Proliferation in a Flow-Dependent Manner
Petrik, D., Myoga, M. H., Grade, S., Gerkau, N. J., Pusch, M., Rose, C. R., Grothe, B., & Götz, M. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2018.04.016 · Cited by 104 · see citing works
A New Hypothesis for Alzheimer’s Disease: The Lipid Invasion Model
Rudge, J. D. (2022) · Journal of Alzheimer's Disease Reports · doi:10.3233/adr-210299 · Cited by 58 · see citing works
Mastrorilli, V., Scopa, C., Saraulli, D., Costanzi, M., Scardigli, R., Rouault, J.-P., Farioli-Vecchioli, S., & Tirone, F. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1376-4 · Cited by 33 · see citing works
Tuberous sclerosis complex–associated CNS abnormalities depend on hyperactivation of mTORC1 and Akt
Zordan, P., Cominelli, M., Cascino, F., Tratta, E., Poliani, P. L., & Galli, R. (2018) · Journal of Clinical Investigation · doi:10.1172/jci96342 · Cited by 28 · see citing works
Neurogenesis and Neuroinflammation in Dialogue: Mapping Gaps, Modulating Microglia, Rewiring Aging
Tanaka, M. (2026) · Cells · doi:10.3390/cells15010078 · Cited by 11 · see citing works
Yoo, Y.-E., Mandal, P., Tang, Z., Zhang, Z., Zhang, J., Chen, X., Robinson, M., Eaton, M., Deming, B., Halurkar, M., et al. (2025) · doi:10.1101/2025.09.16.676420 · Cited by 1 · see citing works
- Authors
- Lim, D. A., & Alvarez-Buylla, A.
- Affiliations
- University of California, San Francisco (US)
- ORCID
- Lim, Daniel A.
- Venue
- Cold Spring Harbor Perspectives in Biology
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2016-04-05
- Volume
- 8
- Issue
- 5
- Pages
- a018820
- ISSN
- 1943-0264 (ISSN-L)
- PMC
- PMC4852803
- OpenAlex
- W2319605272
- Cited by
- 571
- References
- 280
- Citations by year
- 2026: 28 · 2025: 48 · 2024: 54 · 2023: 79 · 2022: 58 · 2021: 71 · 2020: 70 · 2019: 58 · 2018: 55 · 2017: 43 · 2016: 6 · 2015: 1
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Cold Spring Harbor Perspectives in Biology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- 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
- adult neurogenesis, ventricular-subventricular zone, olfactory bulb, neural stem cells, neuroblast migration, olfactory bulb interneurons, neural stem cell proliferation, neural stem cell migration, brain tumors, regenerative therapy
- MeSH terms
- Animals, Cell Differentiation, Humans, Interneurons, Models, Biological, Olfactory Bulb, Signal Transduction, Cell Lineage, Epigenesis, Genetic, Mice, Neurogenesis, Neural Stem Cells
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
