Coordinated changes in cellular behavior ensure the lifelong maintenance of the hippocampal stem cell population
Open accessPublished version of a preprint
Abstract
Neural stem cell numbers fall rapidly in the hippocampus of juvenile mice but stabilize during adulthood, ensuring lifelong hippocampal neurogenesis. We show that this stabilization of stem cell numbers in young adults is the result of coordinated changes in stem cell behavior. Although proliferating neural stem cells in juveniles differentiate rapidly, they increasingly return to a resting state of shallow quiescence and progress through additional self-renewing divisions in adulthood. Single-cell transcriptomics, modeling, and label retention analyses indicate that resting cells have a higher activation rate and greater contribution to neurogenesis than dormant cells, which have not left quiescence. These changes in stem cell behavior result from a progressive reduction in expression of the pro-activation protein ASCL1 because of increased post-translational degradation. These cellular mechanisms help reconcile current contradictory models of hippocampal neural stem cell (NSC) dynamics and may contribute to the different rates of decline of hippocampal neurogenesis in mammalian species, including humans.
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?
With increasing age, a subset of NSCs enter deep quiescence instead of a shallower, reversible quiescence characteristic of young NSCs.
“With increasing age, a subset of NSCs enter deep quiescence instead of a shallower, reversible quiescence, which is characteristic of young NSCs29.”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [29]
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
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890 · see citing works
Model selection and multimodel inference: a practical information-theoretic approach.
Guthery, F. S., Burnham, K. P., & Anderson, D. R. (2003) · The Journal of Wildlife Management · doi:10.2307/3802723 · Cited by 41,495 · see citing works
clusterProfiler: an R Package for Comparing Biological Themes Among Gene Clusters
Yu, G., Wang, L.-G., Han, Y., & He, Q.-Y. (2012) · OMICS: A Journal of Integrative Biology · doi:10.1089/omi.2011.0118 · Cited by 36,259 · see citing works
Comprehensive Integration of Single-Cell Data
Stuart, T., Butler, A., Hoffman, P., Hafemeister, C., Papalexi, E., Mauck, W. M., Hao, Y., Stoeckius, M., Smibert, P., & Satija, R. (2019) · Cell · doi:10.1016/j.cell.2019.05.031 · Cited by 15,453 · see citing works
López-Otín, C., Blasco, M. A., Partridge, L., Serrano, M., & Kroemer, G. (2013) · Cell · doi:10.1016/j.cell.2013.05.039 · Cited by 14,982 · see citing works
Integrating single-cell transcriptomic data across different conditions, technologies, and species
Butler, A., Hoffman, P., Smibert, P., Papalexi, E., & Satija, R. (2018) · Nature Biotechnology · doi:10.1038/nbt.4096 · Cited by 13,174 · see citing works
A robust and high-throughput Cre reporting and characterization system for the whole mouse brain
Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2467 · Cited by 6,907 · see citing works
Dimensionality reduction for visualizing single-cell data using UMAP
Becht, E., McInnes, L., Healy, J., Dutertre, C.-A., Kwok, I. W. H., Ng, L. G., Ginhoux, F., & Newell, E. W. (2019) · Nature Biotechnology · doi:10.1038/nbt.4314 · Cited by 5,358 · see citing works
A guided tour into subcellular colocalization analysis in light microscopy
Bolte, S., & Cordelières, F. (2006) · Journal of Microscopy · doi:10.1111/j.1365-2818.2006.01706.x · Cited by 5,238 · see citing works
Hafemeister, C., & Satija, R. (2019) · Genome Biology · doi:10.1186/s13059-019-1874-1 · Cited by 4,479 · see citing works
Slingshot: cell lineage and pseudotime inference for single-cell transcriptomics
Street, K., Risso, D., Fletcher, R. B., Das, D., Ngai, J., Yosef, N., Purdom, E., & Dudoit, S. (2018) · BMC Genomics · doi:10.1186/s12864-018-4772-0 · Cited by 3,159 · see citing works
Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus
Srinivas, S., Watanabe, T., Lin, C.-S., William, C. M., Tanabe, Y., Jessell, T. M., & Costantini, F. (2001) · BMC Developmental Biology · doi:10.1186/1471-213x-1-4 · Cited by 3,121 · see citing works
Defining the Epithelial Stem Cell Niche in Skin
Tumbar, T., Guasch, G., Greco, V., Blanpain, C., Lowry, W. E., Rendl, M., & Fuchs, E. (2004) · Science · doi:10.1126/science.1092436 · Cited by 2,031 · see citing works
Dynamics of hippocampal neurogenesis in adult humans
Spalding, K. L., Bergmann, O., Alkass, K., Bernard, S., Salehpour, M., Huttner, H. B., Boström, E., Westerlund, I., Vial, C., Buchholz, B. A., et al. (2013) · Cell · doi:10.1016/j.cell.2013.05.002 · Cited by 1,841 · see citing works
Moreno-Jiménez, E. P., Flor-García, M., Terreros-Roncal, J., Rábano, A., Cafini, F., Pallas-Bazarra, N., Ávila, J., & Llorens-Martín, M. (2019) · Nature Medicine · doi:10.1038/s41591-019-0375-9 · Cited by 1,577 · see citing works
Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults
Sorrells, S. F., Paredes, M. F., Cebrian-Silla, A., Sandoval, K., Qi, D., Kelley, K. W., James, D., Mayer, S., Chang, J., Auguste, K. I., et al. (2018) · Nature · doi:10.1038/nature25975 · Cited by 1,422 · see citing works
Human Hippocampal Neurogenesis Persists throughout Aging
Boldrini, M., Fulmore, C. A., Tartt, A. N., Simeon, L. R., Pavlova, I., Poposka, V., Rosoklija, G. B., Stankov, A., Arango, V., Dwork, A. J., et al. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2018.03.015 · Cited by 1,345 · see citing works
Kanda, T., Sullivan, K., & Wahl, G. (1998) · Current Biology · doi:10.1016/s0960-9822(98)70156-3 · Cited by 1,040 · see citing works
Encinas, J. M., Michurina, T. V., Peunova, N. I., Park, J.-H., Tordo, J., Peterson, D. A., Fishell, G., Koulakov, A. A., & Enikolopov, G. (2011) · Cell stem cell · doi:10.1016/j.stem.2011.03.010 · Cited by 891 · see citing works
Oligodendrocyte Dynamics in the Healthy Adult CNS: Evidence for Myelin Remodeling
Young, K. M., Psachoulia, K., Tripathi, R. B., Dunn, S.-J., Cossell, L., Attwell, D., Tohyama, K., & Richardson, W. D. (2013) · Neuron · doi:10.1016/j.neuron.2013.01.006 · Cited by 872 · see citing works
In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics
Bonaguidi, M. A., Wheeler, M. A., Shapiro, J. S., Stadel, R. P., Sun, G. J., Ming, G.-L., & Song, H. (2011) · Cell · doi:10.1016/j.cell.2011.05.024 · Cited by 831 · see citing works
Human Adult Neurogenesis: Evidence and Remaining Questions
Kempermann, G., Gage, F. H., Aigner, L., Song, H., Curtis, M. A., Thuret, S., Kuhn, H. G., Jessberger, S., Frankland, P. W., Cameron, H. A., et al. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2018.04.004 · Cited by 790 · see citing works
Single-Cell RNA-Seq with Waterfall Reveals Molecular Cascades underlying Adult Neurogenesis
Shin, J., Berg, D. A., Zhu, Y., Shin, J. Y., Song, J., Bonaguidi, M. A., Enikolopov, G., Nauen, D. W., Christian, K. M., Ming, G.-L., et al. (2015) · Cell Stem Cell · doi:10.1016/j.stem.2015.07.013 · Cited by 784 · see citing works
Llorens-Bobadilla, E., Zhao, S., Baser, A., Saiz-Castro, G., Zwadlo, K., & Martin-Villalba, A. (2015) · Cell Stem Cell · doi:10.1016/j.stem.2015.07.002 · Cited by 778 · see citing works
Neural stem and progenitor cells in nestin‐GFP transgenic mice
Mignone, J., Kukekov, V. G., Chiang, A., Steindler, D. A., & Enikolopov, G. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.10964 · Cited by 705 · see citing works
Ki67 is a Graded Rather than a Binary Marker of Proliferation versus Quiescence
Miller, I., Min, M., Yang, C., Tian, C., Gookin, S. E., Carter, D., & Spencer, S. L. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.06.110 · Cited by 637 · see citing works
A New Description of Cellular Quiescence
Coller, H. A., Sang, L., & Roberts, J. M. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040083 · Cited by 548 · see citing works
The dynamics of gene expression in vertebrate embryogenesis at single-cell resolution
Briggs, J., Weinreb, C., Wagner, D. E., Megason, S. G., Peshkin, L., Kirschner, M. W., & Klein, A. M. (2018) · Science · doi:10.1126/science.aar5780 · Cited by 548 · 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
Oscillatory Control of Factors Determining Multipotency and Fate in Mouse Neural Progenitors
Imayoshi, I., Isomura, A., Harima, Y., Kawaguchi, K., Kori, H., Miyachi, H., Fujiwara, T., Ishidate, F., & Kageyama, R. (2013) · Science · doi:10.1126/science.1242366 · Cited by 509 · see citing works
Metabolic control of adult neural stem cell activity by Fasn-dependent lipogenesis
Knobloch, M., Braun, S., Zurkirchen, L., Schoultz, C., Zamboni, N., Araúzo-Bravo, M., Kovacs, W. J., Karalay, Ö., Suter, U., Machado, R. A. C., et al. (2012) · Nature · doi:10.1038/nature11689 · Cited by 503 · see citing works
Hochgerner, H., Zeisel, A., Lönnerberg, P., & Linnarsson, S. (2018) · Nature Neuroscience · doi:10.1038/s41593-017-0056-2 · Cited by 482 · see citing works
Vitamin A-Retinoic Acid Signaling Regulates Hematopoietic Stem Cell Dormancy
Cabezas-Wallscheid, N., Buettner, F., Sommerkamp, P., Klimmeck, D., Ladel, L., Thalheimer, F. B., Pastor-Flores, D., Roma, L. P., Renders, S., Zeisberger, P., et al. (2017) · Cell · doi:10.1016/j.cell.2017.04.018 · Cited by 454 · 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
Self-citationMori, T., Tanaka, K., Buffo, A., Wurst, W., Kühn, R., & Götz, M. (2006) · Glia · doi:10.1002/glia.20350 · Cited by 398 · see citing works
Early age-related changes in adult hippocampal neurogenesis in C57 mice
Abdallah, N. M. ‐. B., Slomianka, L., Vyssotski, A. L., & Lipp, H. (2008) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2008.03.002 · Cited by 368 · see citing works
Tissue-Resident Adult Stem Cell Populations of Rapidly Self-Renewing Organs
Barker, N., Bartfeld, S., & Clevers, H. C. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.11.016 · Cited by 352 · see citing works
Copley, M. R., Babovic, S., Benz, C., Knapp, D. J. H. F., Beer, P. A., Kent, D. G., Wöhrer, S., Treloar, D. Q., Day, C. W., Rowe, K. M., et al. (2013) · Nature Cell Biology · doi:10.1038/ncb2783 · Cited by 330 · see citing works
Stem Cell Quiescence: Dynamism, Restraint, and Cellular Idling
van Velthoven, C. T. J., & Rando, T. A. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.01.001 · Cited by 313 · see citing works
Live imaging of neurogenesis in the adult mouse hippocampus
Pilz, G.-A., Bottes, S., Betizeau, M., Jörg, D. J., Carta, S., April-Monn, S., Simons, B. D., Helmchen, F., & Jessberger, S. (2018) · Science · doi:10.1126/science.aao5056 · Cited by 306 · see citing works
Loss of Dickkopf-1 Restores Neurogenesis in Old Age and Counteracts Cognitive Decline
Seib, D. R., Corsini, N. S., Ellwanger, K., Plaas, C., Mateos, Á., Pitzer, C., Niehrs, C., Celikel, T., & Martín-Villalba, A. (2013) · Cell stem cell · doi:10.1016/j.stem.2012.11.010 · Cited by 294 · see citing works
EdU, a new thymidine analogue for labelling proliferating cells in the nervous system
Chehrehasa, F., Meedeniya, A. C. B., Dwyer, P. K., Abrahamsen, G., & Mackay‐Sim, A. (2008) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2008.10.006 · Cited by 281 · see citing works
Zhao, X., Heng, J. I., Guardavaccaro, D., Jiang, R., Pagano, M., Guillemot, F., Iavarone, A., & Lasorella, A. (2008) · Nature Cell Biology · doi:10.1038/ncb1727 · Cited by 269 · see citing works
Self-citationA Common Embryonic Origin of Stem Cells Drives Developmental and Adult Neurogenesis
Berg, D. A., Su, Y., Jimenez-Cyrus, D., Patel, A., Huang, N., Morizet, D., Lee, S., Shah, R., Ringeling, F. R., Jain, R., et al. (2019) · Cell · doi:10.1016/j.cell.2019.02.010 · Cited by 267 · see citing works
Ponti, G., Obernier, K., Guinto, C. D., Jose, L., Bonfanti, L., & Álvarez-Buylla, A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219563110 · Cited by 260 · see citing works
Marciniak-Czochra, A. K., Stiehl, T., Ho, A. D., Jäger, W., & Wagner, W. (2008) · Stem Cells and Development · doi:10.1089/scd.2008.0143 · Cited by 255 · see citing works
Self-citationReturn to quiescence of mouse neural stem cells by degradation of a proactivation protein
Urbán, N., van den Berg, D. L. C., Forget, A., Andersen, J., Demmers, J., Hunt, C., Ayrault, O., & Guillemot, F. (2016) · Science · doi:10.1126/science.aaf4802 · Cited by 254 · see citing works
Self-citationAndersen, J., Urbán, N., Achimastou, A., Ito, A., Simic, M., Ullom, K., Martynoga, B., Lebel, M., Göritz, C., Frisén, J., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.08.004 · Cited by 212 · see citing works
Self-citationDissection of Hippocampal Dentate Gyrus from Adult Mouse
Hagihara, H., Toyama, K., Yamasaki, N., & Miyakawa, T. (2009) · Journal of Visualized Experiments · doi:10.3791/1543 · Cited by 203 · see citing works
Gontier, G., Iyer, M., Shea, J. M., Bieri, G., Wheatley, E. G., Ramalho-Santos, M., & Villeda, S. A. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.02.001 · Cited by 197 · see citing works
Ascl1 Coordinately Regulates Gene Expression and the Chromatin Landscape during Neurogenesis
Raposo, A. A. S. F., Vasconcelos, F. F., Drechsel, D., Marie, C., Johnston, C., Dolle, D. D., Bithell, A., Gillotin, S., van den Berg, D. L. C., Ettwiller, L. M., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.02.025 · Cited by 186 · see citing works
Self-citationTroy+ brain stem cells cycle through quiescence and regulate their number by sensing niche occupancy
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
Recalibrating the Relevance of Adult Neurogenesis
Snyder, J. S. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2018.12.001 · Cited by 183 · see citing works
A unifying hypothesis on mammalian neural stem cell properties in the adult hippocampus
Bonaguidi, M. A., Song, J., Ming, G., & Song, H. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.03.013 · Cited by 176 · see citing works
The Ventral Hippocampus Is the Embryonic Origin for Adult Neural Stem Cells in the Dentate Gyrus
Li, G., Fang, L., Fernández, G., & Pleasure, S. J. (2013) · Neuron · doi:10.1016/j.neuron.2013.03.019 · Cited by 171 · see citing works
Development of the adult neurogenic niche in the hippocampus of mice
Nicola, Z., Fabel, K. S., & Kempermann, G. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00053 · Cited by 159 · see citing works
Miranda, C. J., Braun, L., Jiang, Y., Hester, M. E., Zhang, L., Riolo, M., Wang, H., Rao, M., Altura, R. A., & Kaspar, B. K. (2012) · Aging Cell · doi:10.1111/j.1474-9726.2012.00816.x · Cited by 153 · see citing works
Walker, T., & Kempermann, G. (2014) · Journal of Visualized Experiments · doi:10.3791/51225 · Cited by 152 · see citing works
Controlling Depth of Cellular Quiescence by an Rb-E2F Network Switch
Kwon, J. S., Everetts, N. J., Wang, X., Wang, W., Croce, K. D., Xing, J., & Yao, G. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.09.007 · Cited by 132 · see citing works
Notch2 signaling maintains NSC quiescence in the murine ventricular-subventricular zone
Engler, A., Rolando, C., Giachino, C., Saotome, I., Erni, A., Brien, C., Zhang, R., Zimber-Strobl, U., Radtke, F., Artavanis-Tsakonas, S., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2017.12.094 · Cited by 125 · see citing works
Characterization of stem cells using mathematical models of multistage cell lineages
Stiehl, T., & Marciniak-Czochra, A. K. (2010) · Mathematical and Computer Modelling · doi:10.1016/j.mcm.2010.03.057 · Cited by 123 · see citing works
Self-citationDoes Adult Neurogenesis Persist in the Human Hippocampus?
Paredes, M. F., Sorrells, S. F., Cebrián‐Silla, A., Sandoval, K., Qi, D., Kelley, K. W., James, D., Mayer, S., Chang, J. W., Auguste, K. I., et al. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.11.006 · Cited by 115 · see citing works
Age-Associated Increase in BMP Signaling Inhibits Hippocampal Neurogenesis
Yousef, H., Morgenthaler, A., Schlesinger, C., Bugaj, L. J., Conboy, I. M., & Schaffer, D. V. (2014) · Stem Cells · doi:10.1002/stem.1943 · Cited by 109 · see citing works
Encinas, J. M., & Sierra, A. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.10.010 · Cited by 102 · see citing works
Wang, L., Sharma, K., Deng, H., Siddique, T., Grisotti, G., Liu, E., & Roos, R. P. (2007) · Neurobiology of Disease · doi:10.1016/j.nbd.2007.10.004 · Cited by 101 · see citing works
Ali, F. R., Cheng, K., Kirwan, P., Metcalfe, S. M., Livesey, F. J., Barker, R. A., & Philpott, A. (2014) · Development · doi:10.1242/dev.106377 · Cited by 101 · see citing works
Adult Hippocampal Neurogenesis in Natural Populations of MammalsPreprint
Amrein, I. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021295 · Cited by 96 · see citing works
Blomfield, I. M., Rocamonde, B., Masdeu, M., Mulugeta, E., Vaga, S., van den Berg, D. L. C., Huillard, E., Guillemot, F., & Urbán, N. (2019) · eLife · doi:10.7554/elife.48561 · Cited by 90 · see citing works
Self-citationForget, A., Bihannic, L., Cigna, S. M., Lefevre, C., Remke, M., Barnat, M., Dodier, S., Shirvani, H., Mercier, A. L., Mensah, A., et al. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.05.014 · Cited by 84 · see citing works
Young, M. R., & Tye, B. (1997) · Molecular Biology of the Cell · doi:10.1091/mbc.8.8.1587 · Cited by 70 · see citing works
Bechard, M. E., Bankaitis, E. D., Hipkens, S. B., et al. (2016) · Genes & Development · doi:10.1101/gad.284729.116 · Cited by 67 · see citing works
Dissection of Hippocampal Dentate Gyrus from Adult Mouse
Hagihara, H., Toyama, K., Yamasaki, N., & Miyakawa, T. (2009) · Journal of Visualized Experiments · doi:10.3791/1543-v · Cited by 65 · see citing works
Revealing age-related changes of adult hippocampal neurogenesis using mathematical models
Ziebell, F., Dehler, S., Martín-Villalba, A., & Marciniak-Czochra, A. K. (2018) · Development · doi:10.1242/dev.153544 · Cited by 59 · see citing works
Self-citationPhenotypical and functional heterogeneity of neural stem cells in the aged hippocampus
Martín‐Suárez, S., Valero, J., Muro‐García, T., & Encinas, J. M. (2019) · Aging Cell · doi:10.1111/acel.12958 · Cited by 58 · see citing works
Modes of division and differentiation of neural stem cells
Lazutkin, A. A., Podgorny, O. V., & Enikolopov, G. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112118 · Cited by 58 · see citing works
Expression, Nuclear Localization and Interactions of Human MCM/P1 Proteins
Tsuruga, H., Yabuta, N., Hashizume, K., et al. (1997) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1997.6865 · Cited by 54 · see citing works
Nakamura, K., Kameda, H., Koshimizu, Y., et al. (2008) · Journal of Histochemistry & Cytochemistry · doi:10.1369/jhc.2008.950915 · Cited by 54 · see citing works
Brandt, M., Hübner, M., & Storch, A. (2012) · Stem Cells · doi:10.1002/stem.1244 · Cited by 53 · see citing works
Bast, L., Calzolari, F., Strasser, M. K., Hasenauer, J., Theis, F. J., Ninkovic, J., & Marr, C. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.11.088 · Cited by 50 · see citing works
Stem cell self-renewal in regeneration and cancer: Insights from mathematical modeling
Stiehl, T., & Marciniak‐Czochra, A. (2017) · Current Opinion in Systems Biology · doi:10.1016/j.coisb.2017.09.006 · Cited by 47 · see citing works
Self-citationWalker, T. L., & Kempermann, G. (2014) · Journal of Visualized Experiments · doi:10.3791/51225-v · Cited by 44 · see citing works
Braun, K. A., & Breeden, L. L. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-09-0792 · Cited by 38 · see citing works
Ziebell, F., Martín-Villalba, A., & Marciniak-Czochra, A. K. (2014) · Journal of The Royal Society Interface · doi:10.1098/rsif.2014.0144 · Cited by 34 · see citing works
Self-citationNoguchi, H., Castillo, J. G., Nakashima, K., & Pleasure, S. J. (2019) · eLife · doi:10.7554/elife.42918 · Cited by 34 · see citing works
Knobloch, M., von Schoultz, C., Zurkirchen, L., Braun, S. M. G., Vidmar, M., & Jessberger, S. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.08.013 · Cited by 32 · see citing works
Soprano, K. J. (1994) · Journal of Cellular Biochemistry · doi:10.1002/jcb.240540407 · Cited by 30 · see citing works
Multimode: An R Package for Mode AssessmentPreprint
Ameijeiras‐Alonso, J., Crujeiras, R. M., & Rodríguez‐Casal, A. (2018) · arXiv (Cornell University) · doi:10.48550/arxiv.1803.00472 · Cited by 25 · see citing works
Early Stem Cell Aging in the Mature BrainPreprint
Ibrayeva, A., Bay, M., Pu, E., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/654608 · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Ageing and rejuvenation of tissue stem cells and their niches
Brunet, A., Goodell, M. A., & Rando, T. A. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00510-w · Cited by 407 · see citing works
Impact of neurodegenerative diseases on human adult hippocampal neurogenesis
Terreros-Roncal, J., Moreno-Jiménez, E. P., Flor-García, M., Rodríguez-Moreno, C. B., Trinchero, M. F., Cafini, F., Rábano, A., & Llorens-Martín, M. (2021) · Science · doi:10.1126/science.abl5163 · Cited by 289 · see citing works
Early stem cell aging in the mature brain
Ibrayeva, A., Bay, M., Pu, E., Jörg, D. J., Peng, L., Jun, H., Zhang, N., Aaron, D., Lin, C., Resler, G., et al. (2021) · Cell Stem Cell · doi:10.1016/j.stem.2021.03.018 · Cited by 137 · see citing works
Familial Alzheimer’s disease mutations in PSEN1 lead to premature human stem cell neurogenesis
Arber, C., Lovejoy, C., Harris, L., Willumsen, N., Alatza, A., Casey, J. M., Lines, G., Kerins, C., Mueller, A. K., Zetterberg, H., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2020.108615 · Cited by 116 · see citing works
Self-citation
- Authors
- Harris, L., Rigo, P., Stiehl, T., Gaber, Z. B., Austin, S. H. L., Masdeu, M. D. M., Edwards, A., Urbán, N., Marciniak-Czochra, A., & Guillemot, F.
- Affiliations
- The Francis Crick Institute (GB)
- Heidelberg University (DE)
- Corresponding author
- Guillemot, François
- ORCID
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2021-05
- Volume
- 28
- Issue
- 5
- Pages
- 863-876.e6
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- PMC
- PMC8110946
- OpenAlex
- W3130856386
- Cited by
- 173
- References
- 88
- Citations by year
- 2026: 16 · 2025: 34 · 2024: 24 · 2023: 39 · 2022: 40 · 2021: 20
- FWCI
- 11.07
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell stem cell (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Figshare (submittedVersion, cc-by)
- RWTH Publications (RWTH Aachen)
- Funders
- Wellcome Trust (106187/Z/14/Z, U117570528)
- Francis Crick Institute
- Cancer Research UK
- Medical Research Council (U117570528, FC0010089)
- Deutsche Forschungsgemeinschaft (SFB 873)
- 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 › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- hippocampal neural stem cells, stem cell quiescence, stem cell self-renewal, stem cell activation, ASCL1, stem cell differentiation, hippocampal neurogenesis, stem cell dynamics, label retention, single-cell transcriptomics
- MeSH terms
- Animals, Hippocampus, Cell Proliferation, Mice, Adult Stem Cells, 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
