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Neurogenesis and aging: FGF‐2 and HB‐EGF restore neurogenesis in hippocampus and subventricular zone of aged mice
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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.
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“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
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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
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
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
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
Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo
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
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 1,418
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 1,365
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
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 1,214
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
Research works printed but not linked: 1
- 10.1002/(SICI)1097-4695(199808)36:2<267::AID-NEU12>3.0.CO;2-B · DOI
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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
“Although infusion of FGF2 does not affect SGZ proliferation in young mice, deletion of fgfr1 in the CNS decreases SGZ neurogenesis (Jin et al., 2003; Zhao et al., 2007).”
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
“, 2001) and epidermal and fibroblast growth factor (Jin et al., 2003), reduction of corticosterone levels by adrenalectomy (Cameron and McKay, 1999), and environmental enrichment (Kempermann et al.”
BackgroundADULT 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 1,891
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 1,425
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
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
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
“For example, FGF2 enhances dentate neurogenesis in both neonatal and adult brain [247,209,222,273,48,49,282,85], and intracerebroventricular (ICV) infusions of FGF-2 upregulate dentate neurogenesis in the aged brain [159,85,132,141,160].”
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 700
“…approach has been demonstrated by studies showing that restoring the levels of neurotrophic factors such as FGF2 and IGF-1 in the hippocampus by direct infusion or by overexpression increases hippocampal neurogenesis in aged rats (Jin et al., 2003; Lichtenwalner et al., 2001; Pardo et al., 2016).”
Schmidt, H. D., & Duman, R. S. (2007) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e3282ee2aa8 · Cited by 662
“In contrast, another study found that infusion of FGF-2 into the lateral ventricles increased neurogenesis in the hippocampus of adult mice (Jin et al., 2003).”
ResultFoxOs 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
“…growth factor (FGF), epidermal growth factor (EGF), and the transforming growth factor (TGFb), all of which have been shown to affect self-renewal capacity both c. in vivo and in vitro (Battista et al., 2006; Doetsch et al., 2002a; Jin et al., 2003; Palma et al., 2005; Reya et al., 2003).”
BackgroundEnhanced 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 444
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 363
“Interestingly, these decreases may be reversible, and many of the stimuli that promote neurogenesis also promote dendritic growth and increased arbor complexity (9).”
BackgroundMunoz, 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 421
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
“Neurotrophic factors have been suggested to correlate with age-dependent decline of neurogenesis ( 12 , 23).”
BackgroundEndocannabinoid signalling and the deteriorating brain
Marzo, V. D., Stella, N., & Zimmer, A. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3876 · Cited by 395
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 388
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 392
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 352
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 336
“1), 43–56 49 (Butt & Dinsdale 2005; Jin et al. 2003; Tatebayashi et al. 1999,”
BackgroundShetty, A. K., Hattiangady, B., & Shetty, G. A. (2005) · Glia · doi:10.1002/glia.20187 · Cited by 325
“Scale bar ¼ 100 mm. studies show that subcutaneous injections or ICV infusions of FGF-2 can increase dentate neurogenesis in both adult and aged hippocampus (Wagner et al., 1999; Cheng et al., 2002; Jin et al., 2003).”
BackgroundNeurotrophic 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
“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
Ratey, J. J., & Loehr, J. E. (2011) · Reviews in the Neurosciences · doi:10.1515/rns.2011.017 · Cited by 342
“Fibroblast growth factor-2 (FGF-2) is another growth factor with effects on neurogenesis; animal studies have shown that FGF-2 increases neurogenesis in the hippocampus of adult and aged animals (Jin et al. , 2003 ; Mud ò et al., 2009 ).”
BackgroundSomatotropic 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 296
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 299
“However, it is unclear which cells are targeted by the growth factors and it is unknown if this level of neurogenesis can be sustained past the 1-week observation period reported (Jin et al., 2003).”
BackgroundInfluentialAdult 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 283
“…heparin-binding EGF-like growth factor (HB-EGF), basic fibroblast growth factor (bFGF, also known as FGF-2), and insulin-like growth factor-1 (IGF-1), into the senescent brain reverses the age-related decline in neurogenesis in the dentate gyrus (Lichtenwalner et al, 2001; Jin et al, 2003a).”
BackgroundInfluentialDefective 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
“We noted that the effects of SR141716A were more prominent in SVZ than DG. Prior examples exist of inter-regional differences in neurogenesis, including the finding that several growth factors stimulate neurogenesis in DG and SVZ to different extents (Jin et al., 2002b, 2003b; Kuhn et al., 1997).”
BackgroundResultSelf-citationStein, L. R., & Imai, S. (2014) · The EMBO Journal · doi:10.1002/embj.201386917 · Cited by 265
“In mice, the number of proliferating NSPCs in the SGZ declines exponentially in the first 9 months of life (Ben Abdallah et al, 2010), and they are almost completely absent by 24 months of age (Jin et al, 2003; Lugert et al, 2010; Encinas et al, 2011).”
BackgroundFibroblast 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
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 267
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 255
“Recent results showed 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 [67].”
BackgroundHattiangady, B., & Shetty, A. K. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.09.015 · Cited by 258
“This possibility is also supported by the observations that increased levels of VEGF, IGF-1, BDNF, and erythropoietin enhance neurogenesis via stimulation of angiogenesis and increased density of vascular niches [40,65,80,88].”
BackgroundInfluentialRao, M. S., Hattiangady, B., & Shetty, A. K. (2006) · Aging Cell · doi:10.1111/j.1474-9726.2006.00243.x · Cited by 241
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
“, 2002), aged mice (Jin et al., 2003), and after traumatic brain injury (Yoshimura et al.”
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
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 240
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 242
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 237
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
“Despite this natural decline with age, previous studies have shown that the adult brain remains responsive to therapeutic interventions that enhance neurogenesis (Jin et al., 2003; Wise, 2003).”
BackgroundRao, 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 233
“Nevertheless, addition of new neurons to the DG from stem or progenitor cells declines drastically during ageing (Seki & Arai, 1995; Kuhn et al., 1996; Cameron&McKay, 1999; Lichtenwalner et al., 2001; Kempermann et al., 2002; Jin et al., 2003;Nacheret al., 2003).”
BackgroundInfluentialDynamics 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 228
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 227
Zhang, C., McNeil, E. M., Dressler, L., & Siman, R. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2006.09.018 · Cited by 217
“…is long-lasting in the APP/PS-1 double knock-in mouse hippocampus During aging, there is a substantial decline in neurogenesis in the hippocampal dentate gyrus, as evidenced both by doublecortin immunostaining and bromodeoxyuridine incorporation (Cameron and McKay, 1999;Jin et al., 2003).”
BackgroundWalker, M., Patel, K., & Stappenbeck, T. (2008) · The Journal of Pathology · doi:10.1002/path.2474 · Cited by 223
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
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 220
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 217
Ahlenius, H., Visan, V., Kokaia, M., Lindvall, O., & Kokaia, Z. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.6003-08.2009 · Cited by 217
“, 2002), infusion of growth factors (Jin et al., 2003), or stroke (Jin et al.”
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 208
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 210
“Neurotrophic factors have been suggested to correlate with age-dependent decline of neurogenesis (12, 23).”
Adult neurogenesis in non‐mammalian vertebrates
Chapouton, P., Jagasia, R., & Bally‐Cuif, L. (2007) · BioEssays · doi:10.1002/bies.20615 · Cited by 201
“An age-related decrease in proliferation (as revealed by BrdU labeling) and in the survival of newborn neurons has been observed in both the SEZ((44,45)) and SGZ((1,46)) (and references therein), suggesting that NSCs do not actually renew indefinitely, as is the case for hematopoietic stem cells.”
BackgroundVEGF‐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 192
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 189
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
“It has been proposed that recruitment strategies could be viable in the treatment of neurodegeneration because aged neurogenic areas of the brain can respond to growth factors with increased proliferation (Jin et al., 2003).”
BackgroundInfluentialSegovia, G., Yagüe, A. G., García‐Verdugo, J. M., & Mora, F. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2005.11.005 · Cited by 181
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
“Increasing age decreases the number of new neurons in the dentate gyrus and the SVZ.(90) Sildenafil not only enhances angiogenesis and neurogenesis in young adults, but also augments angiogenesis and neurogenesis in aged ischemic rats.”
BackgroundInfluentialZhao, 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
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 172
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
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
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 161
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 159
“Two separate studies demonstrated that ultrasound treatment in vitro and in vivo significantly up-regulated vascular endothelial growth factor (VEGF) and basic fibroblast growth factor (bFGF) (17,27), two trophic factors that promote hippocampal neurogenesis (19,20).”
BackgroundTsai, C., Ukropec, J., Ukropcová, B., & Pai, M. (2017) · NeuroImage Clinical · doi:10.1016/j.nicl.2017.10.028 · Cited by 162
“Indeed, intracerebroventricular or subcutaneous injections of FGF-2 can significantly enhance neurogenesis in the dentate gyrus in the aged brain (Jin et al., 2003).”
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 158
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
“Basic FGF can also restore neurogenesis in the hippocampus and subventricular zone in aged animals (Jin et al., 2003; Rai et al., 2007).”
BackgroundConover, J. C., & Notti, R. Q. (2007) · Cell and Tissue Research · doi:10.1007/s00441-007-0503-6 · Cited by 158
“However, with increased age, SVZ progenitor proliferation has been reported to decrease by more than 50% (elderly 22- to 25-month-old mice compared with younger 2- to 3-month-old mice; Jin et al. 2003; Maslov et al. 2004; Tropepe et al. 1997).”
BackgroundFunctional 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 156
“VEGF-A has also been reported to suppress the transmembrane tight junction proteins claudin-5 and occludin in brain microvascular endothelial cultures.”
BackgroundInfluentialFunctional 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 153
“Type I cells likely give rise to Type II progenitor cells under the influence of additional local niche factors [fibroblast growth factor-2 (Jin et al., 2003), sonic hedgehog (Lai et al.”
BackgroundPieper, 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 150
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 149
“Overall, it appears that age-related reductions in stem cell mitogenic factors, microvasculature and cerebral blood flow, and low-grade inflammation influence reduced neurogenesis in aging because increased neurogenesis could be obtained through interventional strategies that upregulate the concentration of NSC mitoge…”
BackgroundBorn 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 155
“…(FGF‐2) and EGF re‐ sulted in not only a reversal in age‐related decrease in neurogenesis, but also an enhancement of the number of adult‐born neurons in the aged hippocampus, illustrating that the aged brain is still suscepti‐ ble to the influence of exogenous growth factors (Jin et al., 2003).”
BackgroundKiyota, 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 154
“In the central nervous system, FGF2 is expressed in neurogenic regions and has been implicated in the control of adult neurogenesis based on changes in proliferation and fate choice of adult neural progenitor cells (19, 22).”
BackgroundGivogri, 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 144
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
“, 1995), and infusions of FGF-2 into the brain increase adult neurogenesis (Kuhn et al., 1997; Tao et al., 1997; Jin et al., 2003).”
BackgroundInfluentialHippocampal 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 144
“While no studies are currently available on the effects of administration of these factors into the chronically epileptic hippocampus, this approach has promise based on their ability to enhance neurogenesis in both intact and injured aged hippocampus [122–126].”
Buckwalter, M. S., Yamane, M., Coleman, B. S., Ormerod, B. K., Chin, J. T., Palmer, T., & Wyss-Coray, T. (2006) · The American Journal of Pathology · doi:10.2353/ajpath.2006.051272 · Cited by 127
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 152
“…[72] Mice (C57BL/6) 20 months Exposure to an enriched environment from age 10 months to 20 months maintained adult neurogenesis at an elevated level Jin et al. 2003 [66] Mice (CD1) 3, 20 months Relative effect of intracerebroventricular infusion of fibroblast growth factor 2 and heparin binding…”
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 151
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
“Focal cerebral ischemia increases neurogenesis in the SVZ of young adult rats, and newly generated neurons migrate toward ischemic boundary regions (Arvidsson et al., 2002; Parent et al., 2002; Jin et al., 2003a; Zhang et al., 2004a,b).”
BackgroundInfluentialNeurogenesis 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 140
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 145
“a non-linear decline in neurogenesis with age [56,57], with final numbers of in vivo proliferating progenitors about 75% lower at mid age to aged (12–24 months) compared with young (2 month old) mice [58].”
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
Tandé, D., Höglinger, G. U., Debeir, T., Freundlieb, N., Hirsch, É. C., & François, C. (2006) · Brain · doi:10.1093/brain/awl041 · Cited by 136
“…in the study of Bedard et al. (2002b), a condition known to induce an increase in neurogenesis (Kempermann et al., 1997), or differences in age, since ageing has been shown to affect neurogenesis in hippocampus and subventricular zone (Gould et al., 1999; Jin et al., 2003; Bondolfi et al., 2004).”
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 148
“2), for example, a decreased number of proliferating cells or limited proliferation potential resulting from increased quiescence.”
BackgroundMethodInfluentialOlariu, A., Cleaver, K. M., & Cameron, H. A. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21268 · Cited by 145
“Specific staining of dividing cells in the adult rat dentate gyrus by this antibody has been demonstrated previously (Kee et al., 2002), and in the current study all Ki67-labeled cells were found to be colabeled with cumulatively injected BrdU at short timepoints, as expected for specific staining…”
BackgroundSpatiotemporal 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
“Jin et al. (2003) were able to demonstrate that, after infusions of FGF or EGF, the level of total proliferation in the aged SVZ was comparable with the young adult, and aged NSCs isolated using a nestin–GFP mouse can generate the same number of neurospheres as young NSCs (Ahlenius et al., 2009).”
BackgroundResultSun, 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 137
“…et al., 1999; Yoshimura et al., 2001,2003), epidermal growth factor (EGF) (Craig et al., 1996), brain-derived neurotrophic factor (BDNF) (Pencea et al., 2001), heparin-binding epidermal growth factor (HP-EGF) (Jin et al., 2002, 2003) and vascular endothelial growth factor (VEGF) (Sun et al., 2003).”
Duce, J. A., Podvin, S., Hollander, W., Kipling, D., Rosene, D. L., & Abraham, C. R. (2007) · Glia · doi:10.1002/glia.20593 · Cited by 134
“…in aging white matter has already been suggested to reflect remyelination in the rhesus monkey (Peters and Sethares, 2004) and results have previously GLIA DOI 10.1002/glia demonstrated that the aged brain still retains the capacity to respond to exogenous growth factors (Jin et al., 2003).”
InfluentialDistinct 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
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
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 126
“neuroblasts [102], have also been observed [48,88], further”
BackgroundNeurogenesis 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 126
“This possibility is supported by the reported enhancement of neurogenesis in aged rodent brains following exogenous delivery of IGF-I (37), or of FGF-2 or heparinbinding EGF-like growth factor (38).”
BackgroundActivity 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 120
“1995), is another key candidate for mediating activity-dependent effects across the life span (Jin et al. 2003), because FGF-2 can act systemically (Wagner et al.”
BackgroundRoles 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
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
“However, during chronic epilepsy, the microenvironment of hippocampus exhibits further alterations in the form of decreased levels of multiple neurotrophic factors (e.g., BDNF, FGF-2, and IGF-1), reduced expression of reelin, and increased levels of cystatin C. Inflammation also persists, though it is reduced compared…”
BackgroundInfluentialRadiation 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
Brinton, R. D., & Wang, J. M. (2006) · Current Alzheimer Research · doi:10.2174/156720506777632817 · Cited by 115
“The efficacy of AP α as a neurogenic factor is comparable to that induced by bFGF + heparin from our own study and also in agreement with previously published results [62] after 3 days treatment and a 25 % increase of BrdU incorporation in 3 month old rat brain [ 44 ].”
BackgroundResultGene 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
Исаев, Н. К., Stelmashook, E. V., & Генрихс, Е. Е. (2019) · Reviews in the Neurosciences · doi:10.1515/revneuro-2018-0084 · Cited by 119
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
Metadata
- 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
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