Neurogenesis and aging: FGF‐2 and HB‐EGF restore neurogenesis in hippocampus and subventricular zone of aged mice
Open accessAbstract
Summary: Neurogenesis, which may contribute to the ability of the adult brain to function normally and adapt to disease, nevertheless declines with advancing age. Adult neurogenesis can be enhanced by administration of growth factors, but whether the aged brain remains responsive to these factors is unknown. We compared the effects of intracerebroventricular fibroblast growth factor (FGF)‐2 and heparin‐binding epidermal growth factor‐like growth factor (HB‐EGF) on neurogenesis in the hippocampal dentate subgranular zone (SGZ) and the subventricular zone (SVZ) of young adult (3‐month) and aged (20‐month) mice. Neurogenesis, measured by labelling with bromodeoxyuridine (BrdU) and by expression of doublecortin, was reduced by ∼90% in SGZ and by ∼50% in SVZ of aged mice. HB‐EGF increased BrdU labelling in SGZ at 3 months by ∼60% and at 20 months by ∼450%, which increased the number of BrdU‐labelled cells in SGZ of aged mice to ∼25% of that in young adults. FGF‐2 also stimulated BrdU labelling in SGZ, by ∼25% at 3 months and by ∼250% at 20 months, increasing the number of newborn neurones in older mice to ∼20% of that in younger mice. In SVZ, HB‐EGF and FGF‐2 increased BrdU incorporation by ∼140% at 3 months and ∼170% at 20 months, so the number of BrdU‐labelled cells was comparable in untreated 3‐month‐old and growth factor‐treated 20‐month‐old mice. These results demonstrate that the aged brain retains the capacity to respond to exogenous growth factors with increased neurogenesis, which may have implications for the therapeutic potential of neurogenesis enhancement in age‐associated neurological disorders.
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?
ICV injection of FGF2 induces neurogenesis in both the SVZ and SGZ.
“Intracerebroventricular (ICV) injection of FGF2 induced neurogenesis in both the SVZ and SGZ (Jin et al. 2003; Mudo et al. 2009; Rai et al. 2007).”
From Neurotrophic factors and neuroplasticity pathways in the pathophysiology and treatment of depression (2018) · cites this paper as Jin et al. 2003
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
Neurogenesis in the adult is involved in the formation of trace memories
Shors, T. J., Miesegaes, G. R., Beylin, A. V., Zhao, M., Rydel, T. A., & Gould, E. (2001) · Nature · doi:10.1038/35066584 · Cited by 2,014 · see citing works
Lewy body–like pathology in long-term embryonic nigral transplants in Parkinson's disease
Kordower, J. H., Chu, Y., Hauser, R. A., Freeman, T. B., & Olanow, C. W. (2008) · Nature Medicine · doi:10.1038/nm1747 · Cited by 1,722 · 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
Self-citationNakatomi, H., Kuriu, T., Okabe, S., Yamamoto, S.-I., Hatano, O., Kawahara, N., Tamura, A., Kirino, T., & Nakafuku, M. (2002) · Cell · doi:10.1016/s0092-8674(02)00862-0 · Cited by 1,416 · see citing works
Doublecortin Is a Microtubule-Associated Protein and Is Expressed Widely by Migrating Neurons
Gleeson, J. G., Lin, P. T., Flanagan, L. A., & Walsh, C. A. (1999) · Neuron · doi:10.1016/s0896-6273(00)80778-3 · Cited by 1,341 · see citing works
Induction of neurogenesis in the neocortex of adult mice
Magavi, S. S. P., Leavitt, B. R., & Macklis, J. D. (2000) · Nature · doi:10.1038/35016083 · Cited by 1,217 · see citing works
Kuhn, H. G., Winkler, J., Kempermann, G., Thal, L. J., & Gage, F. H. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-15-05820.1997 · Cited by 1,208 · see citing works
Experience-Induced Neurogenesis in the Senescent Dentate Gyrus
Kempermann, G., Kuhn, H. G., & Gage, F. H. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-09-03206.1998 · Cited by 1,150 · see citing works
Jin, K., Minami, M., Lan, J., Mao, X., Batteur, S., Simon, R., & Greenberg, D. A. (2001) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.081011098 · Cited by 1,117 · see citing works
Self-citationIncreased Neurogenesis in the Dentate Gyrus After Transient Global Ischemia in Gerbils
Liu, J., Solway, K., Messing, R. O., & Sharp, F. R. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-19-07768.1998 · Cited by 1,025 · see citing works
Conversion of <i>Xenopus</i> Ectoderm into Neurons by NeuroD, a Basic Helix-Loop-Helix Protein
Lee, J. E., Hollenberg, S. M., Snider, L., Turner, D. L., Lipnick, N., & Weintraub, H. (1995) · Science · doi:10.1126/science.7754368 · Cited by 1,023 · see citing works
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
Kempermann, G., Gast, D., & Gage, F. H. (2002) · Annals of Neurology · doi:10.1002/ana.10262 · Cited by 889 · see citing works
Peripheral Infusion of IGF-I Selectively Induces Neurogenesis in the Adult Rat Hippocampus
Åberg, M. A. I., Åberg, N. D., Hedbäcker, H., Oscarsson, J., & Eriksson, P. S. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-08-02896.2000 · Cited by 852 · see citing works
Hippocampal neurogenesis in adult Old World primates
Gould, E., Reeves, A. J., Fallah, M., Tanapat, P., Gross, C. G., & Fuchs, E. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.9.5263 · Cited by 815 · see citing works
Restoring production of hippocampal neurons in old age
Cameron, H. A., & McKay, R. D. G. (1999) · Nature Neuroscience · doi:10.1038/13197 · Cited by 710 · see citing works
Kukekov, V. G., Laywell, E. D., Suslov, O. N., Davies, K. G., Scheffler, B., Thomas, L. B., O'Brien, T. J., Kusakabe, M., & Steindler, D. A. (1999) · Experimental Neurology · doi:10.1006/exnr.1999.7028 · Cited by 522 · see citing works
Musashi1: An Evolutionally Conserved Marker for CNS Progenitor Cells Including Neural Stem Cells
Kaneko, Y., Sakakibara, S., Imai, T., Suzuki, A., Nakamura, Y., Sawamoto, K., Ogawa, Y., Toyama, Y., Miyata, T., & Okano, H. (2000) · Developmental Neuroscience · doi:10.1159/000017435 · Cited by 519 · see citing works
Debus, E. S., Weber, K. K., & Osborn, M. (1984) · Differentiation · doi:10.1111/j.1432-0436.1984.tb01355.x · Cited by 487 · see citing works
FGF-2 regulation of neurogenesis in adult hippocampus after brain injury
Yoshimura, S., Takagi, Y., Harada, J., Teramoto, T., Thomas, S. S., Waeber, C., Bakowska, J. C., Breakefield, X. O., & Moskowitz, M. A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.101034998 · Cited by 455 · see citing works
The Adult Substantia Nigra Contains Progenitor Cells with Neurogenic Potential
Lie, D. C., Dziewczapolski, G., Willhoite, A. R., Kaspar, B. K., Shults, C. W., & Gage, F. H. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06639.2002 · Cited by 449 · see citing works
Lichtenwalner, R. J., Forbes, M. E., Bennett, S. A., Lynch, C. D., Sonntag, W. E., & Riddle, D. R. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00378-5 · Cited by 428 · see citing works
Wagner, J. P., Black, I. B., & DiCicco-Bloom, E. M. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-14-06006.1999 · Cited by 373 · see citing works
O'Kusky, J. R., Ye, P., & D'Ercole, A. J. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-22-08435.2000 · Cited by 358 · see citing works
Stem cell factor stimulates neurogenesis in vitro and in vivo
Jin, K., Mao, X. O., Sun, Y., Xie, L., & Greenberg, D. A. (2002) · Journal of Clinical Investigation · doi:10.1172/jci15251 · Cited by 263 · see citing works
Self-citationJin, 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
Self-citationStem cell factor stimulates neurogenesis in vitro and in vivo
Jin, K., Mao, X. O., Sun, Y., Xie, L., & Greenberg, D. A. (2002) · Journal of Clinical Investigation · doi:10.1172/jci0215251 · Cited by 200 · see citing works
Self-citationAdult neurogenesis: from canaries to the clinic.
Goldman, S. A. (1998) · PubMed · Cited by 169 · see citing works
Yazaki, N., Hosoi, Y., Kawabata, K., Miyake, A., Minami, M., Satoh, M., Ohta, M., Kawasaki, T., & Itoh, N. (1994) · Journal of Neuroscience Research · doi:10.1002/jnr.490370403 · Cited by 145 · see citing works
Wen, P. H., Shao, X., Shao, Z., Hof, P. R., Wısnıewskı, T., Kelley, K. A., Friedrich, V. L., Ho, L., Pasinetti, G. M., Shioi, J., et al. (2002) · Neurobiology of Disease · doi:10.1006/nbdi.2002.0490 · Cited by 112 · see citing works
The aged mouse as a model of cognitive decline with special emphasis on studies in NMRI mice
Gower, A. J., & Lamberty, Y. (1993) · Behavioural Brain Research · doi:10.1016/0166-4328(93)90132-a · Cited by 110 · see citing works
Neural stem cells: From fly to vertebrates
Doe, C. Q., Fuerstenberg, S., & Peng, C. (1998) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199808)36:2 · Cited by 85 · see citing works
Hematopoietic stem cells and aging
Globerson, A. (1999) · Experimental Gerontology · doi:10.1016/s0531-5565(98)00069-2 · Cited by 66 · see citing works
Sato, K., Hayashi, T., Sasaki, C., Iwai, M., Li, F., Manabe, Y., Seki, T., & Abe, K. (2001) · Brain Research · doi:10.1016/s0006-8993(01)03137-7 · Cited by 38 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Mechanisms and Functional Implications of Adult Neurogenesis
Zhao, C., Deng, W., & Gage, F. H. (2008) · Cell · doi:10.1016/j.cell.2008.01.033 · Cited by 3,007 · see citing works
Exercise enhances learning and hippocampal neurogenesis in aged mice
van Praag, H., Shubert, T., Zhao, C., & Gage, F. H. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1731-05.2005 · Cited by 2,078 · see citing works
ADULT NEUROGENESIS IN THE MAMMALIAN CENTRAL NERVOUS SYSTEM
Ming, G., & Song, H. (2005) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.051804.101459 · Cited by 1,829 · 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
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
Self-citationAdult neurogenesis: from precursors to network and physiology
Abrous, D. N., Koehl, M., & Le Moal, M. (2005) · Physiological Reviews · doi:10.1152/physrev.00055.2003 · Cited by 971 · see citing works
Progesterone receptors: form and function in brain
Brinton, R. D., Thompson, R. F., Foy, M. R., Baudry, M., Wang, J., Finch, C. E., Morgan, T. E., Pike, C. J., Mack, W. J., Stanczyk, F. Z., et al. (2008) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.02.001 · Cited by 675 · see citing works
The effects of aging in the hippocampus and cognitive decline
Bettio, L. E. B., Rajendran, L., & Gil‐Mohapel, J. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.04.030 · Cited by 654 · see citing works
Schmidt, H. D., & Duman, R. S. (2007) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e3282ee2aa8 · Cited by 649 · see citing works
FoxOs Cooperatively Regulate Diverse Pathways Governing Neural Stem Cell Homeostasis
Paik, J.-H., Ding, Z., Narurkar, R., Ramkissoon, S., Muller, F., Kamoun, W. S., Chae, S.-S., Zheng, H., Ying, H., Mahoney, J., et al. (2009) · Cell Stem Cell · doi:10.1016/j.stem.2009.09.013 · Cited by 459 · see citing works
Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APP Sw,Ind ) mice
Jin, K., Galván, V., Xie, L., Mao, X. O., Gorostiza, O. F., Bredesen, D. E., & Greenberg, D. A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403678101 · Cited by 433 · see citing works
Self-citationmicroRNA-132 regulates dendritic growth and arborization of newborn neurons in the adult hippocampus
Magill, S. T., Cambronne, X. A., Luikart, B. W., Lioy, D. T., Leighton, B. H., Westbrook, G. L., Mandel, G., & Goodman, R. H. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1015691107 · Cited by 431 · see citing works
Munoz, J. R., Stoutenger, B. R., Robinson, A. P., Spees, J. L., & Prockop, D. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508945102 · Cited by 416 · see citing works
Cardiovascular fitness is associated with cognition in young adulthood
Åberg, M. A. I., Pedersen, N. L., Torén, K., Svartengren, M., Bäckstrand, B., Johnsson, T., Cooper-Kuhn, C. M., Åberg, N. D., Nilsson, M., & Kuhn, H. G. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905307106 · Cited by 382 · see citing works
Endocannabinoid signalling and the deteriorating brain
Marzo, V. D., Stella, N., & Zimmer, A. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3876 · Cited by 381 · see citing works
Signaling in Adult Neurogenesis
Suh, H., Deng, W., & Gage, F. H. (2009) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.042308.113256 · Cited by 373 · 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
The Choroid Plexus‐Cerebrospinal Fluid System: From Development to Aging
Redzic, Z. B., Preston, J. E., Duncan, J. A., Chodobski, A., & Szmydynger‐Chodobska, J. (2005) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(05)71001-2 · Cited by 343 · see citing works
Neurotrophic factors in Alzheimer’s disease: role of axonal transport
Schindowski, K., Bélarbi, K., & Buée, L. (2008) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2007.00378.x · Cited by 335 · see citing works
Shetty, A. K., Hattiangady, B., & Shetty, G. A. (2005) · Glia · doi:10.1002/glia.20187 · Cited by 316 · see citing works
Neurotrophic factors and neuroplasticity pathways in the pathophysiology and treatment of depression
Levy, M. J. F., Boulle, F., Steinbusch, H. W., van den Hove, D. L. A., Kenis, G., & Lanfumey, L. (2018) · Psychopharmacology · doi:10.1007/s00213-018-4950-4 · Cited by 308 · see citing works
“Chronic imipramine and desipramine treatment increased cell proliferation in the SGZ (Pechnick et al. 2011; Santarelli et al. 2003; Schiavon et al. 2010).”
BackgroundInfluentialProgramming of neural cells by (endo)cannabinoids: from physiological rules to emerging therapies
Maccarrone, M., Guzmán, M., Mackie, K., Doherty, P., & Harkany, T. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3846 · Cited by 298 · see citing works
Ratey, J. J., & Loehr, J. E. (2011) · Reviews in the Neurosciences · doi:10.1515/rns.2011.017 · Cited by 308 · see citing works
Somatotropic Signaling: Trade-Offs Between Growth, Reproductive Development, and Longevity
Bartke, A., Sun, L. Y., & Longo, V. D. (2013) · Physiological Reviews · doi:10.1152/physrev.00006.2012 · Cited by 286 · see citing works
The aging neurogenic subventricular zone
Luo, J., Daniels, S. B., Lennington, J. B., Notti, R. Q., & Conover, J. C. (2006) · Aging Cell · doi:10.1111/j.1474-9726.2006.00197.x · Cited by 285 · see citing works
Adult Neurogenesis and the Ischemic Forebrain
Lichtenwalner, R. J., & Parent, J. M. (2005) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600170 · Cited by 281 · see citing works
Defective Adult Neurogenesis in CB1 Cannabinoid Receptor Knockout Mice
Jin, K., Xie, L., Kim, S. H., Parmentier‐Batteur, S., Sun, Y., Mao, X. O., Childs, J., & Greenberg, D. A. (2004) · Molecular Pharmacology · doi:10.1124/mol.66.2.204 · Cited by 271 · see citing works
Self-citationStein, L. R., & Imai, S. (2014) · The EMBO Journal · doi:10.1002/embj.201386917 · Cited by 265 · see citing works
Fibroblast Growth Factor-2 Signaling in Neurogenesis and Neurodegeneration
Woodbury, M. E., & Ikezu, T. (2014) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-013-9501-5 · Cited by 266 · see citing works
Wang, J. M., Johnston, P. B., Ball, B. G., & Brinton, R. D. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4520-04.2005 · Cited by 261 · see citing works
The role of epidermal growth factor and its receptors in mammalian CNS
Wong, R. W.-C., & Guillaud, L. (2004) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2004.01.004 · Cited by 250 · see citing works
Hattiangady, B., & Shetty, A. K. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.09.015 · Cited by 247 · see citing works
Rao, M. S., Hattiangady, B., & Shetty, A. K. (2006) · Aging Cell · doi:10.1111/j.1474-9726.2006.00243.x · Cited by 241 · see citing works
The Adult Mouse Hippocampal Progenitor Is Neurogenic But Not a Stem Cell
Bull, N. D., & Bartlett, P. F. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3249-05.2005 · Cited by 242 · see citing works
Stroke-induced neurogenesis in aged brain
Darsalia, V., Heldmann, U., Lindvall, O., & Kokaia, Z. (2005) · Stroke · doi:10.1161/01.str.0000173151.36031.be · Cited by 240 · see citing works
Diminished adult neurogenesis in the marmoset brain precedes old age
Leuner, B., Kozorovitskiy, Y., Gross, C. G., & Gould, E. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708228104 · Cited by 234 · see citing works
The aging hippocampus: A multi-level analysis in the rat
Driscoll, I. F., Howard, S. R., Stone, J. C., Monfils, M., Tomanek, B., Brooks, W. M., & Sutherland, R. J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.01.040 · Cited by 223 · see citing works
Predictable chronic mild stress improves mood, hippocampal neurogenesis and memory
Parihar, V. K., Hattiangady, B., Kuruba, R., Shuai, B., & Shetty, A. K. (2009) · Molecular Psychiatry · doi:10.1038/mp.2009.130 · Cited by 225 · see citing works
Crews, L., Adame, A., Patrick, C., DeLaney, A., Pham, E., Rockenstein, E., Hansen, L., & Masliah, E. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1305-10.2010 · Cited by 222 · see citing works
Rao, M. S. R., Hattiangady, B., Abdel‐Rahman, A., Stanley, D. P., & Shetty, A. K. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03853.x · Cited by 220 · see citing works
Dynamics of neurogenesis in the dentate gyrus of adult rats
Kinkaid, H. Y. M., & Wojtowicz, J. M. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2005.05.022 · Cited by 219 · see citing works
Signaling in adult neurogenesis
Mu, Y., Lee, S. W., & Gage, F. H. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.04.010 · Cited by 217 · see citing works
Zhang, C., McNeil, E. M., Dressler, L., & Siman, R. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2006.09.018 · Cited by 217 · see citing works
Walker, M., Patel, K., & Stappenbeck, T. (2008) · The Journal of Pathology · doi:10.1002/path.2474 · Cited by 215 · see citing works
Jin, K., LaFevre-Bernt, M. A., Sun, Y., Chen, S., Gafni, J., Crippen, D., Logvinova, A. V., Ross, C. A., Greenberg, D. A., & Ellerby, L. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506375102 · Cited by 212 · see citing works
Self-citationA comparative framework for understanding the biological principles of adult neurogenesis
Lindsey, B. W., & Tropepe, V. (2006) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2006.11.007 · Cited by 212 · see citing works
Astrocytes regulate adult hippocampal neurogenesis through ephrin-B signaling
Ashton, R. S., Conway, A., Pangarkar, C., Bergen, J., Lim, K., Shah, P. S., Bissell, M. J., & Schaffer, D. V. (2012) · Nature Neuroscience · doi:10.1038/nn.3212 · Cited by 212 · see citing works
Ahlenius, H., Visan, V., Kokaia, M., Lindvall, O., & Kokaia, Z. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.6003-08.2009 · Cited by 208 · see citing works
Stem cells for ischemic brain injury: A critical review
Burns, T. C., Verfaillie, C. M., & Low, W. C. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22038 · Cited by 207 · see citing works
Wu, C.-W. J., Chang, Y.-T., Yu, L., Chen, H., Jen, C. J., Wu, S.-Y., Lo, C., & Kuo, Y. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.90775.2008 · Cited by 204 · see citing works
Adult neurogenesis in non‐mammalian vertebrates
Chapouton, P., Jagasia, R., & Bally‐Cuif, L. (2007) · BioEssays · doi:10.1002/bies.20615 · Cited by 201 · see citing works
VEGF‐overexpressing transgenic mice show enhanced post‐ischemic neurogenesis and neuromigration
Wang, Y., Jin, K., Mao, X. O., Xie, L., Banwait, S., Marti, H. H., & Greenberg, D. A. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21169 · Cited by 189 · see citing works
Self-citationAdult neurogenesis in the intact and epileptic dentate gyrus
Parent, J. M. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63028-3 · Cited by 182 · see citing works
Telomere Shortening in Neural Stem Cells Disrupts Neuronal Differentiation and Neuritogenesis
Ferrón, S. R., Marqués-Torrejón, M. Á., Mira, H., Flores, I., Taylor, K., Blasco, M. A., & Fariñas, I. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.3836-09.2009 · Cited by 179 · see citing works
Segovia, G., Yagüe, A. G., García‐Verdugo, J. M., & Mora, F. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2005.11.005 · Cited by 173 · see citing works
Neurorestorative treatment of stroke: Cell and pharmacological approaches
Chen, J., & Chopp, M. (2006) · NeuroRx · doi:10.1016/j.nurx.2006.07.007 · Cited by 169 · see citing works
Zhao, M., Li, D., Shimazu, K., Zhou, Y.-X., Lu, B., & Deng, C.-X. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.10.019 · Cited by 171 · see citing works
Reduction in paracrine Wnt3 factors during aging causes impaired adult neurogenesis
Okamoto, M., Inoue, K., Iwamura, H., Terashima, K., Soya, H., Asashima, M., & Kuwabara, T. (2011) · The FASEB Journal · doi:10.1096/fj.11-184697 · Cited by 162 · see citing works
The FGF-2/FGFRs neurotrophic system promotes neurogenesis in the adult brain
Mudò, G., Bonomo, A., Di Liberto, V., Frinchi, M., Fuxe, K., & Belluardo, N. (2009) · Journal of Neural Transmission · doi:10.1007/s00702-009-0207-z · Cited by 158 · see citing works
Adult neural stem cells and their niche: a dynamic duo during homeostasis, regeneration, and aging
Silva-Vargas, V., Crouch, E. E., & Doetsch, F. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.09.004 · Cited by 157 · see citing works
Roles of FGF signaling in stem cell self-renewal, senescence and aging
Coutu, D. L., & Galipeau, J. (2011) · Aging · doi:10.18632/aging.100369 · Cited by 156 · see citing works
Scarcelli, T., Jordão, J. F., O’Reilly, M. A., Ellens, N. P. K., Hynynen, K., & Aubert, I. (2014) · Brain stimulation · doi:10.1016/j.brs.2013.12.012 · Cited by 156 · see citing works
Tsai, C., Ukropec, J., Ukropcová, B., & Pai, M. (2017) · NeuroImage Clinical · doi:10.1016/j.nicl.2017.10.028 · Cited by 156 · see citing works
The current clinical management of Huntington's disease
Phillips, W., Shannon, K. M., & Barker, R. A. (2008) · Movement Disorders · doi:10.1002/mds.21971 · Cited by 156 · see citing works
Sun, D., Bullock, M. R., McGinn, M. J., Zhou, Z., Altememi, N., Hagood, S., Hamm, R. J., & Colello, R. J. (2008) · Experimental Neurology · doi:10.1016/j.expneurol.2008.11.011 · Cited by 154 · see citing works
Conover, J. C., & Notti, R. Q. (2007) · Cell and Tissue Research · doi:10.1007/s00441-007-0503-6 · Cited by 150 · see citing works
Functional dissection of astrocyte-secreted proteins: Implications in brain health and diseases
Jha, M. K., Kim, J.-H., Song, G. J., Lee, W., Lee, I. K., Lee, H., An, S. S. A., Kim, S., & Suk, K. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.12.003 · Cited by 149 · see citing works
Functional circuits of new neurons in the dentate gyrus
Vivar, C., & van Praag, H. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00015 · Cited by 150 · see citing works
Pieper, A. A., Wu, X., Han, T. W., Estill, S. J., Dang, Q. T., Wu, L. C., Reece-Fincanon, S., Dudley, C. A., Richardson, J. A., Brat, D. J., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506713102 · Cited by 149 · see citing works
Emerging Anti-Aging Strategies - Scientific Basis and Efficacy
Shetty, A. K., Kodali, M., Upadhya, R., & Madhu, L. N. (2018) · Aging and Disease · doi:10.14336/ad.2018.1026 · Cited by 148 · see citing works
Born this way: Hippocampal neurogenesis across the lifespan
Kozareva, D. A., Cryan, J. F., & Nolan, Y. M. (2019) · Aging Cell · doi:10.1111/acel.13007 · Cited by 148 · see citing works
Kiyota, T., Dixie, K. L. I., Jacobsen, M. T., Xiong, H., & Ikezu, T. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102349108 · Cited by 145 · see citing works
Givogri, M. I., de Planell, M., Galbiati, F., Superchi, D., Gritti, A., Vescovi, A. L., de Vellis, J., & Bongarzone, E. R. (2006) · Developmental Neuroscience · doi:10.1159/000090755 · Cited by 145 · see citing works
Rai, K. S., Hattiangady, B., & Shetty, A. K. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05820.x · Cited by 144 · see citing works
Hippocampal neurogenesis and neural stem cells in temporal lobe epilepsy
Kuruba, R., Hattiangady, B., & Shetty, A. K. (2008) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2008.08.020 · Cited by 143 · see citing works
Buckwalter, M. S., Yamane, M., Coleman, B. S., Ormerod, B. K., Chin, J. T., Palmer, T. D., & Wyss‐Coray, T. (2006) · American Journal Of Pathology · doi:10.2353/ajpath.2006.051272 · Cited by 141 · see citing works
Adult hippocampal neurogenesis and aging
Klempin, F., & Kempermann, G. (2007) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-007-0731-5 · Cited by 139 · see citing works
Mobley, A. S., Rodriguez‐Gil, D. J., Imamura, F., & Greer, C. A. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.11.004 · Cited by 140 · see citing works
Zhang, R. L., Zhang, Z., Zhang, L., Wang, Y., Zhang, C., & Chopp, M. (2006) · Journal of Neuroscience Research · doi:10.1002/jnr.20813 · Cited by 138 · see citing works
Neurogenesis decreases with age in the canine hippocampus and correlates with cognitive function
Siwak, C. T., Head, E., Muggenburg, B. A., Milgram, N. W., & Cotman, C. W. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.05.001 · Cited by 138 · see citing works
Neurogenesis in the aging brain
Apple, D. M., Fonseca, R. S., & Kokovay, E. (2017) · Biochemical Pharmacology · doi:10.1016/j.bcp.2017.06.116 · Cited by 140 · see citing works
Shimabukuro, M. K., Langhi, L. G. P., Cordeiro, I., Brito, J. M., Batista, C. M. D. C., Mattson, M. P., & de Mello Coelho, V. (2016) · Scientific Reports · doi:10.1038/srep23795 · Cited by 136 · see citing works
Tandé, D., Höglinger, G. U., Debeir, T., Freundlieb, N., Hirsch, É. C., & François, C. (2006) · Brain · doi:10.1093/brain/awl041 · Cited by 136 · see citing works
Stem Cell Review Series: Role of neurogenesis in age‐related memory disorders
Drapeau, E., & Abrous, D. N. (2008) · Aging Cell · doi:10.1111/j.1474-9726.2008.00369.x · Cited by 136 · see citing works
Olariu, A., Cleaver, K. M., & Cameron, H. A. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21268 · Cited by 135 · see citing works
Spatiotemporal Changes to the Subventricular Zone Stem Cell Pool through Aging
Shook, B. A., Manz, D. H., Peters, J. J., Kang, S., & Conover, J. C. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5987-11.2012 · Cited by 136 · see citing works
Sun, D., Colello, R. J., Daugherty, W. P., Kwon, T. H., McGinn, M. J., Harvey, H. B., & Bullock, M. R. (2005) · Journal of Neurotrauma · doi:10.1089/neu.2005.22.95 · Cited by 134 · see citing works
Duce, J. A., Podvin, S., Hollander, W., Kipling, D., Rosene, D. L., & Abraham, C. R. (2007) · Glia · doi:10.1002/glia.20593 · Cited by 131 · see citing works
Distinct cytokine profiles in human brains resilient to Alzheimer's pathology
Barroeta-Espar, I., Weinstock, L. D., Perez-Nievas, B. G., Meltzer, A. C., Siao Tick Chong, M., Amaral, A. C., Murray, M. E., Moulder, K. L., Morris, J. C., Cairns, N. J., et al. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.10.009 · Cited by 133 · see citing works
Ischemia‐induced neurogenesis is preserved but reduced in the aged rodent brain
Jin, K., Minami, M., Xie, L., Sun, Y., Mao, X. O., Wang, Y., Simon, R. P., & Greenberg, D. A. (2004) · Aging Cell · doi:10.1111/j.1474-9728.2004.00131.x · Cited by 121 · see citing works
Self-citationHippocampal Neurogenesis Levels Predict WATERMAZE Search Strategies in the Aging Brain
Gil‐Mohapel, J., Brocardo, P. S., Choquette, W., Gothard, R., Simpson, J. M., & Christie, B. R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0075125 · Cited by 119 · see citing works
Neurogenesis and brain injury: managing a renewable resource for repair
Hallbergson, A. F., Gnatenco, C., & Peterson, D. A. (2003) · Journal of Clinical Investigation · doi:10.1172/jci20098 · Cited by 125 · see citing works
Activity Dependency and Aging in the Regulation of Adult NeurogenesisPreprint
Kempermann, G. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018929 · Cited by 113 · see citing works
Roles of the mammalian subventricular zone in cell replacement after brain injury
Romanko, M. J. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.07.001 · Cited by 114 · see citing works
Implications of decreased hippocampal neurogenesis in chronic temporal lobe epilepsy
Hattiangady, B., & Shetty, A. K. (2008) · Epilepsia · doi:10.1111/j.1528-1167.2008.01635.x · Cited by 116 · see citing works
Radiation Response of Neural Precursor Cells
Fike, J. R., Rola, R., & Limoli, C. L. (2007) · Neurosurgery Clinics of North America · doi:10.1016/j.nec.2006.10.010 · Cited by 112 · see citing works
Brinton, R. D., & Wang, J. M. (2006) · Current Alzheimer Research · doi:10.2174/156720506777632817 · Cited by 113 · see citing works
Gene Expression Changes in the Course of Neural Progenitor Cell Differentiation
Gurok, U., Steinhoff, C., Lipkowitz, B., Ropers, H., Scharff, C., & Nuber, U. A. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0809-04.2004 · Cited by 112 · see citing works
Исаев, Н. К., Stelmashook, E. V., & Генрихс, Е. Е. (2019) · Reviews in the Neurosciences · doi:10.1515/revneuro-2018-0084 · Cited by 110 · see citing works
Liu, L., Wang, J., Zhao, L., Nilsen, J., McClure, K., Wong, K., & Brinton, R. D. (2009) · Endocrinology · doi:10.1210/en.2008-1447 · Cited by 108 · see citing works
- Authors
- Jin, K., Sun, Y., Xie, L., Batteur, S., Mao, X. O., Smelick, C., Logvinova, A., & Greenberg, D. A.
- Affiliations
- Buck Institute for Research on Aging (US)
- Corresponding author
- Greenberg, David A.
- Venue
- Aging Cell
- Publisher
- Wiley
- Published
- 2003-05-28
- Volume
- 2
- Issue
- 3
- Pages
- 175-183
- ISSN
- 1474-9718 (ISSN-L)
- 1474-9726
- OpenAlex
- W2091535724
- Cited by
- 396
- References
- 36
- Citations by year
- 2026: 1 · 2025: 7 · 2024: 6 · 2023: 6 · 2022: 4 · 2021: 14 · 2020: 13 · 2019: 15 · 2018: 8 · 2017: 19 · 2016: 20 · 2015: 19 · 2014: 19 · 2013: 38 · 2012: 22
- FWCI
- 5.36
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Aging Cell (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (NS44110)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Keywords
- adult neurogenesis, aging, FGF2, HB-EGF, dentate gyrus, subventricular zone, growth factor responsiveness, brain aging
- MeSH terms
- Aging, Animals, Cerebral Ventricles, Epidermal Growth Factor, Heparin, Hippocampus, Male, Mice, Inbred Strains, Neurons, Fibroblast Growth Factor 2, Dentate Gyrus, Intercellular Signaling Peptides and Proteins, Mice, Heparin-binding EGF-like Growth Factor
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
