Temporal dynamics of hippocampal neurogenesis in chronic neurodegeneration
Open accessAbstract
The study of neurogenesis during chronic neurodegeneration is crucial in order to understand the intrinsic repair mechanisms of the brain, and key to designing therapeutic strategies. In this study, using an experimental model of progressive chronic neurodegeneration, murine prion disease, we define the temporal dynamics of the generation, maturation and integration of new neurons in the hippocampal dentate gyrus, using dual pulse-chase, multicolour γ-retroviral tracing, transmission electron microscopy and patch-clamp. We found increased neurogenesis during the progression of prion disease, which partially counteracts the effects of chronic neurodegeneration, as evidenced by blocking neurogenesis with cytosine arabinoside, and helps to preserve the hippocampal function. Evidence obtained from human post-mortem samples, of both variant Creutzfeldt-Jakob disease and Alzheimer's disease patients, also suggests increased neurogenic activity. These results open a new avenue into the exploration of the effects and regulation of neurogenesis during chronic neurodegeneration, and offer a new model to reproduce the changes observed in human neurodegenerative diseases.
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?
An increase in hippocampal neurogenesis correlates with expansion of the microglia population.
“an increase in hippocampal neurogenesis was previously shown to correlate with the expansion of the microglia population [31]”
From Pharmacological modulation of TSPO in microglia/macrophages and neurons in a chronic neurodegenerative model of prion disease (2023) · cites this paper as [31]
The Results report increased hippocampal neurogenesis in prion-diseased mice, and the Discussion describes expansion of their microglial population. But the Discussion says the two responses *could* be related and that further analysis is needed; it does not show the correlation claimed. (LLM, conf=0.84)
Experimental — accuracy not yet measuredPrion disease experimental models are robust and tractable laboratory tools for studying these pathological processes.
“Prion disease experimental models are robust and tractable laboratory tools to study these pathological processes [31, 32].”
From Pharmacological modulation of TSPO in microglia/macrophages and neurons in a chronic neurodegenerative model of prion disease (2023) · cites this paper as [31]
Aberrant increased neurogenesis takes place during some neurodegenerative sequelae, including experimental prion disease.
“Our interest in the dentate gyrus was furthered by earlier discoveries that aberrant increased neurogenesis takes place during some neurodegenerative sequelae including that in experimental prion disease [31].”
From Pharmacological modulation of TSPO in microglia/macrophages and neurons in a chronic neurodegenerative model of prion disease (2023) · cites this paper as [31]
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
Kuhn, H., Dickinson-Anson, H., & Gage, F. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-06-02027.1996 · Cited by 3,139 · see citing works
Neuronal replacement from endogenous precursors in the adult brain after stroke
Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z., & Lindvall, O. (2002) · Nature Medicine · doi:10.1038/nm747 · Cited by 2,799 · see citing works
Dendritic organization in the neurons of the visual and motor cortices of the cat.
Sholl, D. A. (1953) · Europe PMC (PubMed Central) · Cited by 2,204 · see citing works
Plat-E: an efficient and stable system for transient packaging of retroviruses
MORITA, S., Kojima, T., & Kitamura, T. (2000) · Gene Therapy · doi:10.1038/sj.gt.3301206 · Cited by 1,660 · see citing works
Palop, J. J., Chin, J., Roberson, E. D., Wang, J., Thwin, M. T., Bien-Ly, N., Yoo, J., Ho, K. O., Yu, G.-Q., Kreitzer, A., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.07.025 · Cited by 1,653 · see citing works
Microglia Shape Adult Hippocampal Neurogenesis through Apoptosis-Coupled Phagocytosis
Sierra, A., Encinas, J. M., Deudero, J. J. P., Chancey, J. H., Enikolopov, G., Overstreet-Wadiche, L. S., Tsirka, S. E., & Maletic-Savatic, M. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.08.014 · Cited by 1,622 · see citing works
Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus
Schmidt-Hieber, C., Jonas, P., & Bischofberger, J. (2004) · Nature · doi:10.1038/nature02553 · Cited by 1,292 · see citing works
Rat forebrain neurogenesis and striatal neuron replacement after focal stroke
Parent, J. M., Vexler, Z. S., Gong, C., Derugin, N., & Ferriero, D. M. (2002) · Annals of Neurology · doi:10.1002/ana.10393 · Cited by 1,020 · see citing works
Increased hippocampal neurogenesis in Alzheimer's disease
Jin, K., Peel, A. L., Mao, X. O., Xie, L., Cottrell, B. A., Henshall, D. C., & Greenberg, D. A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2634794100 · Cited by 971 · 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 882 · see citing works
Nakashiba, T., Cushman, J. D., Pelkey, K. A., Renaudineau, S., Buhl, D. L., McHugh, T. J., Barrera, V. R., Chittajallu, R., Iwamoto, K. S., McBain, C. J., et al. (2012) · Cell · doi:10.1016/j.cell.2012.01.046 · Cited by 805 · see citing works
Brain inflammation and adult neurogenesis: The dual role of microglia
Ekdahl, C. T., Kokaia, Z., & Lindvall, O. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2008.06.052 · Cited by 801 · see citing works
Spatial selectivity of unit activity in the hippocampal granular layer
Jung, M. W., & McNaughton, B. L. (1993) · Hippocampus · doi:10.1002/hipo.450030209 · Cited by 789 · see citing works
GABAergic Excitation Promotes Neuronal Differentiation in Adult Hippocampal Progenitor Cells
Tozuka, Y., Fukuda, S., Namba, T., Seki, T., & Hisatsune, T. (2005) · Neuron · doi:10.1016/j.neuron.2005.08.023 · Cited by 741 · see citing works
Neurons born in the adult dentate gyrus form functional synapses with target cells
Toni, N., Laplagne, D. A., Zhao, C., Lombardi, G., Ribak, C. E., Gage, F. H., & Schinder, A. F. (2008) · Nature Neuroscience · doi:10.1038/nn.2156 · Cited by 741 · see citing works
Lugert, S., Basak, O., Knuckles, P., Haussler, U., Fabel, K., Götz, M., Haas, C. A., Kempermann, G., Taylor, V., & Giachino, C. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.03.017 · Cited by 704 · 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
NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus
Tashiro, A., Sandler, V. M., Toni, N., Zhao, C., & Gage, F. H. (2006) · Nature · doi:10.1038/nature05028 · Cited by 620 · see citing works
Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies
Veenman, C. L., Reiner, A. J., & Honig, M. G. (1992) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(92)90089-v · Cited by 613 · see citing works
Contribution of olfactory neural stem cells to tissue maintenance and regeneration
Leung, C. T., Coulombe, P. A., & Reed, R. R. (2007) · Nature Neuroscience · doi:10.1038/nn1882 · Cited by 466 · see citing works
Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke
Carlén, M., Meletis, K., Göritz, C., Darsalia, V., Evergren, E., Tanigaki, K., Amendola, M., Barnabé‐Heider, F., Yeung, M. S. Y., Naldini, L., et al. (2009) · Nature Neuroscience · doi:10.1038/nn.2268 · Cited by 453 · see citing works
Identification of neural stem cells in the adult vertebrate brain
Álvarez-Buylla, A., Seri, B., & Doetsch, F. K. (2002) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00770-5 · Cited by 413 · see citing works
Regulation of Microglial Proliferation during Chronic Neurodegeneration
Gómez-Nicola, D., Fransen, N. L., Suzzi, S., & Perry, V. H. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.4440-12.2013 · Cited by 407 · see citing works
Self-citationNeurodegenerative disease and adult neurogenesis
Winner, B., Kohl, Z., & Gage, F. H. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07613.x · Cited by 405 · see citing works
A Multicolor Panel of Novel Lentiviral “Gene Ontology” (LeGO) Vectors for Functional Gene Analysis
Riecken, K., Bartsch, U., Stocking, C., & Fehse, B. (2008) · Molecular Therapy · doi:10.1038/mt.2008.6 · Cited by 352 · see citing works
Self-citationBoekhoorn, K., Joëls, M., & Lucassen, P. (2006) · Neurobiology of Disease · doi:10.1016/j.nbd.2006.04.017 · Cited by 342 · 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
MASTERS, C. L., & RICHARDSON, E. P. (1978) · Brain · doi:10.1093/brain/101.2.333 · Cited by 310 · see citing works
Monosynaptic inputs to new neurons in the dentate gyrus
Vivar, C., Potter, M. C., Choi, J., Lee, J.-Y., Stringer, T. P., Callaway, E. M., Gage, F. H., Suh, H., & van Praag, H. (2012) · Nature Communications · doi:10.1038/ncomms2101 · Cited by 289 · see citing works
Li, G., Bien-Ly, N., Andrews-Zwilling, Y., Xu, Q., Bernardo, A., Ring, K., Halabisky, B., Deng, C., Mahley, R. W., & Huang, Y. (2009) · Cell Stem Cell · doi:10.1016/j.stem.2009.10.015 · Cited by 288 · see citing works
Contribution of systemic inflammation to chronic neurodegeneration
Perry, V. H. (2010) · Acta Neuropathologica · doi:10.1007/s00401-010-0722-x · Cited by 283 · see citing works
Self-citationSchmitz, C., Rutten, B. P. F., Pielen, A., Schäfer, S., Wirths, O., Tremp, G., Czech, C., Blanchard, V., Multhaup, G., Rezaie, P., et al. (2004) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)63235-x · Cited by 281 · see citing works
Steele, A. D., Emsley, J. G., Özdi̇nler, P. H., Lindquist, S. L., & Macklis, J. D. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511290103 · Cited by 271 · see citing works
Synaptic changes characterize early behavioural signs in the ME7 model of murine prion disease
Cunningham, C. M., Deacon, R. M. J., Wells, H., Boche, D., Waters, S., Diniz, C. W. P., Scott, H., Rawlins, J. N. P., & Perry, V. H. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02662.x · Cited by 266 · see citing works
Self-citationYoung and excitable: the function of new neurons in the adult mammalian brain
Doetsch, F. K., & Hen, R. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.01.018 · Cited by 236 · see citing works
Synaptic integration and plasticity of new neurons in the adult hippocampus
Ge, S., Sailor, K. A., Ming, G., & Song, H. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.155655 · Cited by 206 · see citing works
Sun, B., Halabisky, B., Zhou, Y., Palop, J. J., Yu, G., Mucke, L., & Gan, L. (2009) · Cell Stem Cell · doi:10.1016/j.stem.2009.10.003 · Cited by 205 · see citing works
PrP Deposition, Microglial Activation, and Neuronal Apoptosis in Murine Scrapie
Williams, A., Lucassen, P. J., Ritchie, D., & Bruce, M. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6424 · Cited by 204 · see citing works
Deshpande, A., Bergami, M., Ghanem, A., Conzelmann, K., Lepier, A., Götz, M., & Berninger, B. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218991110 · Cited by 198 · see citing works
Schambach, A., Bohne, J., Chandra, S., Will, E., Margison, G. P., Williams, D. A., & Baum, C. (2005) · Molecular Therapy · doi:10.1016/j.ymthe.2005.08.012 · Cited by 197 · 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
RGB marking facilitates multicolor clonal cell tracking
Riecken, K., Thomaschewski, M., Warlich, M., Volz, T., Cornils, K., Niebuhr, B., Täger, M., Lütgehetmann, M., Pollok, J., Stocking, C., et al. (2011) · Nature Medicine · doi:10.1038/nm.2338 · Cited by 174 · see citing works
Self-citationCracchiolo, J. R., Mori, T., Nazian, S., Tan, J., Potter, H., & Arendash, G. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.07.007 · Cited by 161 · see citing works
Depression, stress, epilepsy and adult neurogenesis
Danzer, S. C. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.05.023 · Cited by 157 · see citing works
Schambach, A., Mueller, D., Galla, M., Verstegen, M. M. A., Wagemaker, G., Loew, R., Baum, C., & Bohne, J. (2006) · Gene Therapy · doi:10.1038/sj.gt.3302807 · Cited by 143 · see citing works
Llorens-Martı́n, M., Fuster-Matanzo, A., Teixeira, C. M., Jurado‐Arjona, J., Ulloa, F., DeFelipe, J., Rábano, A., Hernández, F., Soriano, E., & Ávila, J. (2013) · Molecular Psychiatry · doi:10.1038/mp.2013.4 · Cited by 133 · see citing works
RGB marking with lentiviral vectors for multicolor clonal cell tracking
Riecken, K., Thomaschewski, M., Benten, D., & Fehse, B. (2012) · Nature Protocols · doi:10.1038/nprot.2012.026 · Cited by 103 · see citing works
Self-citationGebara, E., Sultan, S., Kocher-Braissant, J., & Toni, N. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00145 · Cited by 102 · see citing works
Valero, J., España, J., Parra‐Damas, A., Martín, E., Rodrı́guez-Álvarez, J., & Saura, C. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016832 · Cited by 100 · see citing works
Behavior of neural stem cells in the Alzheimer brain
Waldau, B., & Shetty, A. K. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8053-y · Cited by 99 · see citing works
Interleukin-15 regulates proliferation and self-renewal of adult neural stem cells
Gómez‐Nicola, D., Valle‐Argos, B., Pallas‐Bazarra, N., & Nieto‐Sampedro, M. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-01-0053 · Cited by 98 · see citing works
Marlatt, M. W., Potter, M. C., Bayer, T. A., van Praag, H., & Lucassen, P. J. (2013) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2012_237 · Cited by 92 · see citing works
Neurogenesis and Alzheimers Disease: Biology and Pathophysiology in Mice and Men
Marlatt, M. W., & Lucassen, P. J. (2010) · Current Alzheimer Research · doi:10.2174/156720510790691362 · Cited by 87 · see citing works
Rupp, N. J., Wegenast‐Braun, B. M., Radde, R., Calhoun, M. E., & Jucker, M. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.08.014 · Cited by 77 · see citing works
Morphologic and electrophysiologic maturation in developing dentate gyrus granule cells
Liu, X., Tilwalli, S., Ye, G.-L., Lio, P., Pasternak, J. F., & Trommer, B. L. (2000) · Brain Research · doi:10.1016/s0006-8993(99)02421-x · Cited by 74 · see citing works
Gómez‐Nicola, D., Valle‐Argos, B., Pita-Thomas, D. W., & Nieto‐Sampedro, M. (2008) · Glia · doi:10.1002/glia.20628 · Cited by 67 · see citing works
Behrens, A., Brandner, S., Genoud, N., & Aguzzi, A. (2001) · EMBO Reports · doi:10.1093/embo-reports/kve088 · Cited by 64 · see citing works
Gómez‐Nicola, D., Schetters, S. T. T., & Perry, V. H. (2014) · Glia · doi:10.1002/glia.22660 · Cited by 59 · see citing works
Self-citationBaum, C., Itoh, K., Meyer, J., Laker, C., Ito, Y., & Ostertag, W. (1997) · Journal of Virology · doi:10.1128/jvi.71.9.6323-6331.1997 · Cited by 49 · see citing works
Sporadic Creutzfeldt-Jakob disease mimicking nonconvulsive status epilepticus
Lapergue, B., Demeret, S., Denys, V., Laplanche, J., Damien Galanaud, E., Verny, M., Sazdovitch, V., Baulac, M., Haı̈k, S., Hauw, J., et al. (2010) · Neurology · doi:10.1212/wnl.0b013e3181e39703 · Cited by 44 · see citing works
Parvalbumin‐immunoreactive cortical neurons in Creutzfeldt‐Jakob disease
Ferrer, I., Casas, R., & Rivera, R. (1993) · Annals of Neurology · doi:10.1002/ana.410340617 · Cited by 43 · see citing works
Neural Injury Alters Proliferation and Integration of Adult-Generated Neurons in the Dentate Gyrus
Perederiy, J. V., Luikart, B. W., Washburn, E. K., Schnell, E., & Westbrook, G. L. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4785-12.2013 · Cited by 38 · see citing works
Jefferys, J. G. R., Empson, R. M., Whittington, M. A., & Prusiner, S. B. (1994) · Neurobiology of Disease · doi:10.1006/nbdi.1994.0004 · Cited by 33 · see citing works
Relaño-Ginés, A., Gabelle, A., Hamela, C., Bélondrade, M., Casanova, D., Mourton-Gilles, C., Lehmann, S., & Crozet, C. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003485 · Cited by 32 · see citing works
Experimental scrapie in rats: First electrophysiological observations
Bassant, M. H., Cathala, F., Court, L., Gourmelon, P., & Hauw, J. (1984) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(84)90090-7 · Cited by 27 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Choi, S. H., Bylykbashi, E., Chatila, Z. K., Lee, S. W., Pulli, B., Clemenson, G. D., Kim, E., Rompala, A., Oram, M. K., Asselin, C., et al. (2018) · Science · doi:10.1126/science.aan8821 · Cited by 802 · see citing works
Olmos-Alonso, A., Schetters, S. T. T., Sri, S., Askew, K., Mancuso, R., Vargas-Caballero, M., Holscher, C., Perry, V. H., & Gomez-Nicola, D. (2016) · Brain · doi:10.1093/brain/awv379 · Cited by 532 · see citing works
Self-citationEvidences for Adult Hippocampal Neurogenesis in Humans
Moreno-Jiménez, E. P., Terreros-Roncal, J., Flor-García, M., Rábano, A., & Llorens-Martín, M. (2021) · The Journal of Neuroscience · doi:10.1523/jneurosci.0675-20.2020 · Cited by 272 · see citing works
Neurogenesis in aging and age-related neurodegenerative diseases
Čulig, L., Chu, X., & Bohr, V. A. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101636 · Cited by 229 · see citing works
Adult Hippocampal Neurogenesis in Major Depressive Disorder and Alzheimer’s Disease
Berger, T., Lee, H. A., Young, A. H., Aarsland, D., & Thuret, S. (2020) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2020.03.010 · Cited by 203 · see citing works
Insights of 8-hydroxyquinolines: A novel target in medicinal chemistry
Gupta, R., Luxami, V., & Paul, K. (2021) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2021.104633 · Cited by 159 · see citing works
DNA methylation signature of human hippocampus in Alzheimer’s disease is linked to neurogenesis
Altuna, M., Urdánoz‐Casado, A., de Gordoa, J. S., Zelaya, M. V., Labarga, A., Lepesant, J. M. J., Roldán, M., Blanco‐Luquin, I., Perdones-Montero, Á., Larumbe, R., et al. (2019) · Clinical Epigenetics · doi:10.1186/s13148-019-0672-7 · Cited by 111 · see citing works
Microglia regulate hippocampal neurogenesis during chronic neurodegeneration
De Lucia, C., Rinchon, A., Olmos-Alonso, A., Riecken, K., Fehse, B., Boche, D., Perry, V. H., & Gomez-Nicola, D. (2016) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.11.001 · Cited by 110 · see citing works
Self-citationRichetin, K., Leclerc, C., Toni, N., Gallopin, T., Pech, S., Roybon, L., & Rampon, C. (2015) · Brain : a journal of neurology · doi:10.1093/brain/awu354 · Cited by 99 · see citing works
Kong, X., Gong, Z., Zhang, L., Sun, X., Ou, Z., Xu, B., Huang, J., Long, D., He, X., Lin, X.-H., et al. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.01.027 · Cited by 92 · see citing works
Bhattarai, P., Thomas, A. K., Zhang, Y., & Kızıl, Ç. (2017) · Neurogenesis · doi:10.1080/23262133.2017.1322666 · Cited by 76 · see citing works
Wnt/β-catenin signaling as a potential target for novel epilepsy therapies
Hodges, S. L., & Lugo, J. N. (2018) · Epilepsy Research · doi:10.1016/j.eplepsyres.2018.07.002 · Cited by 75 · see citing works
Retinoic Acid Is Required for Neural Stem and Progenitor Cell Proliferation in the Adult Hippocampus
Mishra, S., Kelly, K. K., Rumian, N. L., & Siegenthaler, J. A. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.04.024 · Cited by 69 · see citing works
Neuropeptides Modulate Local Astrocytes to Regulate Adult Hippocampal Neural Stem Cells
Asrican, B., Wooten, J., Li, Y., Quintanilla, L., Zhang, F., Wander, C. M., Bao, H., Yeh, C., Luo, Y., Olsen, R. H. J., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.07.039 · Cited by 70 · see citing works
The role of NADPH oxidases in neuronal development
Terzi, A., & Suter, D. M. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.04.027 · Cited by 65 · see citing works
The Ever-Changing Morphology of Hippocampal Granule Neurons in Physiology and Pathology
Llorens-Martı́n, M., Rábano, A., & Ávila, J. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00526 · Cited by 61 · see citing works
Zeng, Q., Zheng, M., Zhang, T., & He, G. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.11.054 · Cited by 64 · see citing works
Katsouri, L., Ashraf, A., Birch, A. M., Lee, K. K. L., Mirzaei, N., & Sastre, M. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.10.004 · Cited by 59 · see citing works
Targeting Alzheimer's disease with gene and cell therapies
Loera‐Valencia, R., Piras, A., Ismail, M.-A.-M., Manchanda, S., Eyjolfsdottir, H., Saido, T. C., Johansson, J., Eriksdotter, M., Winblad, B. G., & Nilsson, P. (2018) · Journal of Internal Medicine · doi:10.1111/joim.12759 · Cited by 57 · see citing works
Huang, C. Y., Fu, X., Zhou, D., & Li, J. (2015) · Neurochemical Research · doi:10.1007/s11064-015-1614-1 · Cited by 54 · see citing works
Adult neurogenesis in Alzheimer's disease
Choi, S. H., & Tanzi, R. E. (2023) · Hippocampus · doi:10.1002/hipo.23504 · Cited by 54 · see citing works
Fingolimod induces neurogenesis in adult mouse hippocampus and improves contextual fear memory
Efstathopoulos, P., Kourgiantaki, A., Karali, K., Sidiropoulou, K., Margioris, A. N., Gravanis, A., & Charalampopoulos, I. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.179 · Cited by 49 · see citing works
Soluble Tau has devastating effects on the structural plasticity of hippocampal granule neurons
Bolós, M., Pallas‐Bazarra, N., Terreros‐Roncal, J., Perea, J. R., Jurado‐Arjona, J., Ávila, J., & Llorens-Martı́n, M. (2017) · Translational Psychiatry · doi:10.1038/s41398-017-0013-6 · Cited by 51 · see citing works
Methods to study adult hippocampal neurogenesis in humans and across the phylogeny
Terreros‐Roncal, J., Flor‐García, M., Moreno‐Jiménez, E. P., Rodríguez-Moreno, C. B., Márquez‐Valadez, B., Gallardo‐Caballero, M., Rábano, A., & Llorens-Martı́n, M. (2022) · Hippocampus · doi:10.1002/hipo.23474 · Cited by 51 · see citing works
In-vivo RGB marking and multicolour single-cell tracking in the adult brain
Gómez‐Nicola, D., Riecken, K., Fehse, B., & Perry, V. H. (2014) · Scientific Reports · doi:10.1038/srep07520 · Cited by 47 · see citing works
Self-citationUnified theory of Alzheimer’s disease (UTAD): implications for prevention and curative therapy
Nehls, M. (2016) · Journal of Molecular Psychiatry · doi:10.1186/s40303-016-0018-8 · Cited by 41 · see citing works
Jiang, P., Zhu, T., Xia, Z., Gao, F., Gu, W., Chen, X., Yuan, T., & Yu, H. (2015) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-015-0588-y · Cited by 41 · see citing works
Coşacak, M. İ., Bhattarai, P., Jager, P. L. D., Menon, V., Tosto, G., & Kızıl, Ç. (2022) · Cells · doi:10.3390/cells11111807 · Cited by 38 · see citing works
Regeneration, Plasticity, and Induced Molecular Programs in Adult Zebrafish Brain
Coşacak, M. İ., Papadimitriou, C., & Kızıl, Ç. (2015) · BioMed Research International · doi:10.1155/2015/769763 · Cited by 40 · see citing works
Ghoneim, F. M., Khalaf, H. A., Elsamanoudy, A. Z., El‐khair, S. M. A., Helaly, A. M. N., Mahmoud, E.-H. M., & Elshafey, S. H. (2015) · PubMed Central · Cited by 37 · see citing works
Richetin, K., Petsophonsakul, P., Roybon, L., Guiard, B. P., & Rampon, C. (2017) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2017.05.025 · Cited by 35 · see citing works
Dard, R. F., Dahan, L., & Rampon, C. (2018) · Hippocampus · doi:10.1002/hipo.23052 · Cited by 27 · see citing works
Stupack, J., Xiong, X.-P., Jiang, L.-L., Zhang, T., Zhou, L., Campos, A. R., Ranscht, B., Mobley, W. C., Pasquale, E. B., Xu, H., et al. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0723-20.2020 · Cited by 32 · see citing works
Sefiani, A., & Geoffroy, C. G. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.682259 · Cited by 31 · see citing works
Corrêa-Velloso, J. C., Gonçalves, M. C., Naaldijk, Y., Oliveira‐Giacomelli, Á., Pillat, M. M., & Ulrich, H. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.04.033 · Cited by 31 · see citing works
Neil3 induced neurogenesis protects against prion disease during the clinical phase
Jalland, C. M. O., Scheffler, K., Benestad, S. L., Moldal, T., Ersdal, C., Gunnes, G., Suganthan, R., Bjørås, M., & Tranulis, M. A. (2016) · Scientific Reports · doi:10.1038/srep37844 · Cited by 30 · see citing works
Collins, S. J., Tumpach, C., Groveman, B. R., Drew, S. C., & Haigh, C. L. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2790-3 · Cited by 28 · see citing works
Slota, J. A., Sajesh, B. V., Frost, K. F., Medina, S. J., & Booth, S. A. (2022) · Acta Neuropathologica Communications · doi:10.1186/s40478-022-01450-4 · Cited by 26 · see citing works
Gatt, A. P., Lee, H. A., Williams, G. H., Thuret, S., & Ballard, C. G. (2019) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2018.12.016 · Cited by 28 · see citing works
Migraine Pharmacological Treatment and Cognitive Impairment: Risks and Benefits
Russo, M., Rosa, M. A. D., Calisi, D., Consoli, S., Evangelista, G., Dono, F., Santilli, M., Granzotto, A., ONOFRJ, M. C., & Sensi, S. L. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231911418 · Cited by 29 · see citing works
Exercising New Neurons to Vanquish Alzheimer Disease
Llorens-Martı́n, M. (2018) · Brain Plasticity · doi:10.3233/bpl-180065 · Cited by 24 · see citing works
Pierucci, F., Garcia‐Gil, M., Frati, A., Bini, F., Martinesi, M., Vannini, E., Mainardi, M., Luzzati, F., Peretto, P. M., Caleo, M., et al. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.01.003 · Cited by 23 · see citing works
A brain boost to fight Alzheimer's disease
Spires‐Jones, T. L., & Ritchie, C. W. (2018) · Science · doi:10.1126/science.aau8060 · Cited by 21 · see citing works
Immunohistochemical evidence for adult human neurogenesis in health and disease.
Gault, N., & Szele, F. G. (2021) · WIREs Mechanisms of Disease · doi:10.1002/wsbm.1526 · Cited by 16 · see citing works
Untold New Beginnings: Adult Hippocampal Neurogenesis and Alzheimer’s Disease
Teixeira, C. M., Pallas‐Bazarra, N., Bolós, M., Terreros‐Roncal, J., Ávila, J., & Llorens-Martı́n, M. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-179918 · Cited by 20 · see citing works
Is Alzheimer’s Also a Stem Cell Disease? – The Zebrafish Perspective
Kızıl, Ç., & Bhattarai, P. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00159 · Cited by 19 · see citing works
Vassal, M., Martins, F., Monteiro, B., Tambaro, S., Martínez‐Murillo, R., & Rebelo, S. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04246-w · Cited by 22 · see citing works
Vicente-Rodríguez, M., Mancuso, R., Peris-Yague, A., Simmons, C., NIMA Consortium, Wlazly, D., Dickinson, A., Foster, A., Knight, C., Leckey, C., et al. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02769-y · Cited by 17 · see citing works
“by earlier discoveries that aberrant increased neurogenesis takes place during some neurodegenerative sequelae including that in experimental prion disease [31].”
BackgroundResultInfluentialImportance of being Nernst: Synaptic activity and functional relevance in stem cell-derived neurons
Bradford, A. B. (2015) · World Journal of Stem Cells · doi:10.4252/wjsc.v7.i6.899 · Cited by 17 · see citing works
Chronic Progressive Neurodegeneration in a Transgenic Mouse Model of Prion Disease
Fainstein, N., Dori, D., Frid, K., Fritz, A. T., Shapiro, I., Gabizon, R., & Ben‐Hur, T. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00510 · Cited by 16 · see citing works
Parrie, L. E., Crowell, J. A. E., Telling, G. C., & Bessen, R. A. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2018.03.012 · Cited by 16 · see citing works
Effects of circadian rhythm disorder on the hippocampus of SHR and WKY rats
Wang, Y., Zhang, Y., Wang, W., Liu, X., Chi, Y., Lei, J., Zhang, B., & Zhang, T. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107141 · Cited by 16 · see citing works
Ghibaudi, M., Amenta, A., Agosti, M., Riva, M., Graïc, J., Bifari, F., & Bonfanti, L. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032514 · Cited by 16 · see citing works
The prion protein regulates beta-amyloid-mediated self-renewal of neural stem cells in vitro
Collins, S. J., Tumpach, C., Li, Q., Lewis, V., Ryan, T. M., Roberts, B. R., Drew, S. C., Lawson, V., & Haigh, C. L. (2015) · Stem Cell Research & Therapy · doi:10.1186/s13287-015-0067-4 · Cited by 16 · see citing works
Llorens-Martı́n, M., Teixeira, C. M., Jurado‐Arjona, J., Rakwal, R., Shibato, J., Soya, H., & Ávila, J. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2181-6 · Cited by 16 · see citing works
Linking adult hippocampal neurogenesis with human physiology and disease
Bowers, M., & Jessberger, S. (2016) · Developmental Dynamics · doi:10.1002/dvdy.24396 · Cited by 15 · see citing works
Haigh, C. L., Tumpach, C., Collins, S. J., & Drew, S. C. (2016) · Cell Biochemistry and Biophysics · doi:10.1007/s12013-016-0747-4 · Cited by 15 · see citing works
Emerging Molecular Pathways Governing Dietary Regulation of Neural Stem Cells during Aging
de Lucia, C., Murphy, T., & Thuret, S. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00017 · Cited by 15 · see citing works
Hayes, D. M., Geil, C., Chen, K. Y., McClain, J. A., Heath, M. M., Deeny, M. A., & Nixon, K. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.01.032 · Cited by 14 · see citing works
Gil, L., Chi-Ahumada, É., Niño, S. A., Capdeville, G., Méndez-Torres, A. M., Guerrero, C., Poves, A. B. R., Olazabal, I. M., & Jiménez-Capdeville, M. E. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232112873 · Cited by 10 · see citing works
Preparation of human formalin-fixed brain slices for electron microscopic investigations
Krause, M., Brüne, M., & Theiß, C. (2016) · Annals of Anatomy - Anatomischer Anzeiger · doi:10.1016/j.aanat.2016.04.030 · Cited by 9 · see citing works
The cellular prion protein promotes neuronal regeneration after acute nasotoxic injury
Parrie, L. E., Crowell, J. A. E., Moreno, J. A., Suinn, S. S., Telling, G. C., & Bessen, R. A. (2020) · Prion · doi:10.1080/19336896.2020.1714373 · Cited by 9 · see citing works
Frid, K., Binyamin, O., Usman, A., & Gabizon, R. (2020) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2020.07.030 · Cited by 9 · see citing works
Human adult hippocampal neurogenesis in health and disease
Alonso-Moreno, M. C., Gallardo‐Caballero, M., Prádanos-Senén, A. V., & Llorens-Martı́n, M. (2025) · Aging Brain · doi:10.1016/j.nbas.2025.100145 · Cited by 10 · see citing works
Functional Activation of Newborn Neurons Following Alcohol-Induced Reactive Neurogenesis
Nawarawong, N. N., Geil, C., Hopkins, D. M., Pauly, J. R., & Nixon, K. (2021) · Brain Sciences · doi:10.3390/brainsci11040499 · Cited by 8 · see citing works
Hoeijmakers, L., Meerhoff, G., de Vries, J. W., Ruigrok, S., van Dam, A., Leuven, F. V., Korosi, A., & Lucassen, P. (2018) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2017.09.013 · Cited by 13 · see citing works
Reviving through human hippocampal newborn neurons
Mendez‐David, I., Schofield, R. M., Tritschler, L., Colle, R., Guilloux, J., Gardier, A. M., Corruble, E., Hen, R., & David, D. J. P. (2021) · L Encéphale · doi:10.1016/j.encep.2021.09.001 · Cited by 6 · see citing works
Pastor-Alonso, O., Zahra, A. S., Kaske, B., García‐Moreno, F., Tetzlaff, F., Bockelmann, E., Grunwald, V., Martín‐Suárez, S., Riecken, K., Witte, O. W., et al. (2023) · The EMBO Journal · doi:10.1038/s44318-023-00011-2 · Cited by 5 · see citing works
Self-citationCell-based therapy against prion diseases
Relaño-Ginés, A., Lehmann, S., & Crozet, C. (2018) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2018.11.001 · Cited by 5 · see citing works
Yan, Y., Su, J., Xie, M., Kong, Y., Wang, C., Yuan, G., Fang, Y., Hwang, K., Kim, C., Han, H. S., et al. (2025) · Brain stimulation · doi:10.1016/j.brs.2025.103015 · Cited by 4 · see citing works
Exploring the triad: VPS35 , neurogenesis, and neurodegenerative diseases
Qiu, Z., Deng, X., Fu, Y., Jiang, M., & Cui, X. (2024) · Journal of Neurochemistry · doi:10.1111/jnc.16184 · Cited by 3 · see citing works
Liang, Z., Li, Z., Zhang, D., Luo, X., Liu, Q., Qin, D., Wang, M., Xu, Z., Feng, J., He, J., et al. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-02937-x · Cited by 3 · see citing works
The intrigue is infectious: Impacts of prion protein during neural development
Allison, W. T. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2018.05.019 · Cited by 3 · see citing works
How can we exploit the brain’s ability to repair itself?
Miller, V., & Gómez‐Nicola, D. (2014) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.2014.985659 · Cited by 2 · see citing works
Carpanini, S. M., Bradford, B. M., Alfieri, A., Piccardo, P., Monzón‐Sandoval, J., Brown, D., Boyle, A., Pokrovskaya, A., Mabbott, N. A., Manson, J. C., et al. (2025) · Frontiers in Neuroscience · doi:10.3389/fnins.2025.1525017 · Cited by 1 · see citing works
Stem Cells and Neurogenesis in Relation to Dementia and Alzheimer’s Disease Mouse Models
Lucassen, P., Jacobs, E. H., Hoeijmakers, L., Lesuis, S. L., Krugers, H., Korosi, A., Kuhn, H., & Boekhoorn, K. (2015) · Stem cell biology and regenerative medicine · doi:10.1007/978-1-4939-1908-6_4 · Cited by 1 · see citing works
Stem cell-based therapeutic strategy in delaying prion disease
Metkar, S. K., Girigoswami, K., & Girigoswami, A. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-820071-1.00014-1 · Cited by 1 · see citing works
Gómez‐Nicola, D., Riecken, K., Perry, V. H., & Fehse, B. (2015) · Human Gene Therapy · doi:10.1089/hum.2015.010 · Cited by 1 · see citing works
Self-citationMatrix signalling and hippocampal neurogenesis
Rooney, A. G. (2018) · ERA
Kempermann, G. (2025) · Oxford University Press eBooks · doi:10.1093/med/9780197519233.003.0012
Slota, J. A., Sajesh, B. V., Frost, K. F., Medina, S. J., & Booth, S. A. (2022) · Figshare · doi:10.6084/m9.figshare.21532645
Vicente‐Rodríguez, M., Mancuso, R., Peris-Yague, A., Simmons, C., Gómez‐Nicola, D., Perry, V. H., Turkheimer, F., Lovestone, S., Parker, C. A., & Cash, D. (2024) · Figshare · doi:10.6084/m9.figshare.26581280
Self-citationİnsan Beyninde Erişkin Hipokampal Nörogenez
Ozturk, A. H., & Öztürk, N. C. (2026) · Akdeniz Medical Journal · doi:10.53394/akd.1617398
Prádanos-Senén, A. V., Rodríguez-Moreno, C. B., & Llorens-Martı́n, M. (2026) · Glia · doi:10.1002/glia.70248
- Authors
- Gomez-Nicola, D., Suzzi, S., Vargas-Caballero, M., Fransen, N. L., Al-Malki, H., Cebrian-Silla, A., Garcia-Verdugo, J. M., Riecken, K., Fehse, B., & Perry, V. H.
- Affiliations
- University of Southampton (GB)
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-06-18
- Volume
- 137
- Issue
- 8
- Pages
- 2312-2328
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- PMC
- PMC4107745
- OpenAlex
- W2093987055
- Cited by
- 84
- References
- 66
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 3 · 2023: 4 · 2022: 7 · 2021: 7 · 2020: 6 · 2019: 4 · 2018: 15 · 2017: 7 · 2016: 9 · 2015: 10 · 2014: 5
- FWCI
- 3.60
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Brain (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- ePrints Soton (University of Southampton) (acceptedVersion)
- Funders
- European Commission
- Ministerio de Economía y Competitividad
- Medical Research Council (MR/K022687/1)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- hippocampal neurogenesis, chronic neurodegeneration, prion disease, dentate gyrus, neural integration, variant Creutzfeldt-Jakob disease, Alzheimer's disease, cytarabine
- MeSH terms
- Adult, Aged, Alzheimer Disease, Animals, Antimetabolites, Antineoplastic, Chronic Disease, Cytarabine, Disease Models, Animal, Female, Genetic Vectors, Hippocampus, Humans, Creutzfeldt-Jakob Syndrome, Male, Mice, Inbred C57BL, Middle Aged, Neural Pathways, Prions, Time Factors, Tissue Banks, Prion Diseases, Patch-Clamp Techniques, Disease Progression, Dentate Gyrus, Mossy Fibers, Hippocampal, Neurodegenerative Diseases, Cell Proliferation, Mice, Neurogenesis, Young Adult, Neuroanatomical Tract-Tracing Techniques, 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