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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.
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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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“The age-related decline in nestin expression levels observed in this study was not surprising in light of evidence showing age-related declines in SVZ cell proliferation and neurogenesis (Jin et al., 2003).”
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“According to the following facts: (1) oligodendrocyte degeneration and myelin breakdown or white matter damage are important events in the pathogenesis of AD [6–8,10,17] (2) FGF2 infusion or gene transfer restores neurogenesis in subventricular zone and hippocampal functions in aged mice and mouse models of AD and has…”
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BackgroundInfluentialImpact of β-hydroxy β-methylbutyrate (HMB) on age-related functional deficits in mice
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“neurogenesis include amphiregulin (AREG) (Falk and Frisén, 2002), FGF2 (Douet et al., 2013; Hayamizu et al., 2001; Jin et al., 2003), and TGF-α (Tropepe et al.”
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“IN FGF2 increased neurogenesis in the subventricular zone of the mouse brain [49] and improved spatial memory as well as decreased hippocampal degeneration in an AD rat model [50].”
BackgroundA mathematical model of adult subventricular neurogenesis
Ashbourn, J. M. A., Miller, J. J. J. J., Reumers, V., Baekelandt, V., & Geris, L. (2012) · Journal of The Royal Society Interface · doi:10.1098/rsif.2012.0193 · Cited by 17
Neurogenesis in Diseases of the Central Nervous System
Phillips, W., Michell, A. W., & Barker, R. A. (2006) · Stem Cells and Development · doi:10.1089/scd.2006.15.359 · Cited by 16
“Infusion of EGF and FGF2 increases neurogenesis further, with appropriate integration and function of newborn neurons and a functional improvement of the animal in the Morris water maze.”
InfluentialBaumann, G. K., Travieso, L. G., Liebl, D. J., & Theus, M. H. (2013) · Experimental Biology and Medicine · doi:10.1177/1535370213494558 · Cited by 14
Kang, W., Nguyen, K. C. Q., & Hébert, J. M. (2019) · Stem Cell Reports · doi:10.1016/j.stemcr.2019.05.006 · Cited by 14
“Note that the SVZ of loss-of-function Nestin-CreER; Fgfr1flox/flox;Fgfr2flox/flox;Fgfr3flox/floxmutants, inwhich all expressed FGFR genes are deleted with TM (and for which we previously described a strong phenotype in the hippocampal SGZ; Kang and Hébert, 2015), were also examined.”
BackgroundInfluentialDesigning neuroreparative strategies using aged regenerating animal models
Vanhunsel, S., Beckers, A. M., & Moons, L. (2020) · Ageing Research Reviews · doi:10.1016/j.arr.2020.101086 · Cited by 14
Lee, C. H., Choi, J. H., Yoo, K., Park, O. K., Moon, J. B., Sohn, Y., Cho, J. H., Hwang, I. K., & Won, M. (2010) · Brain Research · doi:10.1016/j.brainres.2010.03.027 · Cited by 14
Evaluation of Disease Lesions in the Developing Canine MPS IIIA Brain
Winner, L. K., Marshall, N. R., Jolly, R. D., Trim, P. J., Duplock, S. K., Snel, M. F., & Hemsley, K. M. (2018) · JIMD Reports · doi:10.1007/8904_2018_110 · Cited by 13
“2011), as infusion of this molecule increases neurogenesis in both young and older mice (Jin et al. 2003).”
BackgroundAge-dependent changes in the subcallosal zone neurogenesis of mice
Kim, H. J., Kim, J. Y., & Sun, W. (2012) · Neurochemistry International · doi:10.1016/j.neuint.2012.02.027 · Cited by 13
“Reduced EGF receptor (EGFR) signaling elements were found in aged animals (Enwere et al., 2004), and FGF-2 restores proliferation in the SVZ and SGZ of aged mice (Doetsch et al., 2002; Jin et al., 2003).”
BackgroundLuo, F., Zhang, Z., Barnett, A., Bellinger, T. J., Turcato, F. C., Schmidt, K., & Luo, Y. (2020) · Experimental Neurology · doi:10.1016/j.expneurol.2019.113168 · Cited by 12
del Puerto, A., López-Fonseca, C., Simón‐García, A., Martí-Prado, B., Barrios-Muñoz, A. L., Pose‐Utrilla, J., López‐Menéndez, C., Alcover‐Sanchez, B., Cesca, F., Schiavo, G., et al. (2023) · Cell Death and Disease · doi:10.1038/s41419-023-05995-7 · Cited by 11
“M Representative phase contrast micrographs of Kidins220 Gfap Δ / Δ SEZ neurospheres in both conditions, scale bar: 50 μ m. Data represent mean ± s.e.m.”
BackgroundMethodEffects of FGF receptor peptide agonists on animal behavior under normal and pathological conditions
Rudenko, O., Tkach, V., Berezin, V., & Bock, E. (2010) · Neuroscience Research · doi:10.1016/j.neures.2010.05.002 · Cited by 11
Cerebellar stem cells do not produce neurons and astrocytes in adult mouse
Su, X., Guan, W., Yu, Y., & Fu, Y. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2014.05.131 · Cited by 11
Zhao, X., Wang, Y., Wait, E. C., Mankowski, W. C., Bjornsson, C. S., Cohen, A. R., Zuloaga, K. L., & Temple, S. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.03.012 · Cited by 13
Bauer, H., Tempfer, H., Bernroider, G., & Bauer, H. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.10.008 · Cited by 11
“…environmental changes such as an increase in the glucocorticoid level or treatment with growth factors like FGF- 2 or EGF can elevate neurogenesis in the hippocampal area of old rats and improve their neurological status (Cameron and McKay, 1999; Lichtenwalner et al., 2001; Jin et al., 2003).”
Ganglioside-Dependent Neural Stem Cell Proliferation in Alzheimer’s Disease Model Mice
Koon, N. A., Itokazu, Y., & Yu, R. K. (2015) · ASN NEURO · doi:10.1177/1759091415618916 · Cited by 11
“Although adult neurogenesis is gradually diminished with the onset of aging in mice, a significant number of NSCs still exists in aged brains (Jin et al., 2003).”
BackgroundPetrović, D. J., Jagečić, D., Krasić, J., Sinčić, N., & Mitrečić, D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241814161 · Cited by 10
Trimpe, D. M., & Byrd-Jacobs, C. A. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.06.026 · Cited by 10
“In mice, age induces a reduction in formation of newly formed cells in the subventricular zone and, subsequently, in the olfactory bulbs in 2- to 4-month-old vs. 20- to 24-month-old mice (Tropepe et al., 1997; Jin et al., 2003).”
BackgroundAge-dependent changes in Fibroblast Growth Factor 2 (FGF-2) expression in mouse cerebellar neurons
Reynolds, J., Logan, A., Berry, M., Dent, R. G., Gonzales, A. M., & Toescu, E. C. (2005) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2005.tb00365.x · Cited by 10
“Alternative splicing generates a range of FGF2 isoforms.”
BackgroundInfluentialChanges of cell proliferation and differentiation in the developing brain of mouse
Qiu, L., Zhu, C., Wang, X., & Xu, F. (2007) · Neuroscience Bulletin · doi:10.1007/s12264-007-0007-0 · Cited by 10
“[24] Jin K, Sun Y, Xie L, Batteur S, Mao XO, Smelick C, et al.”
BackgroundAre Alzheimer's and coronary artery diseases genetically related to longevity?
Bellou, E., & Escott‐Price, V. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.1102347 · Cited by 10
Age‐related changes in Ki‐67 and DCX expression in the BALB/ c mouse (Mus Musculus) brain
Nkomozepi, P., Mazengenya, P., & Ihunwo, A. O. (2018) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2018.11.005 · Cited by 9
“Intracerebral infusions of FGF 2 or heparin binding EGF in aged rodents was reported to restore SVZ and RMS neurogenesis to levels found in young rodents (Jin et al., 2003).”
BackgroundInfluentialIn vivo serial MRI of age-dependent neural progenitor cell migration in the rat brain
Shuboni‐Mulligan, D. D., Chakravarty, S., Mallett, C. L., Wolf, A. M., Dmitriev, P., Forton, S. M., & Shapiro, E. M. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.05.073 · Cited by 9
Mesenchymal stem cells for treatment of neurological disorders: a paracrine effect
Kim, M., Kim, K. H., Park, S. R., & Choi, B. H. (2013) · Tissue Engineering and Regenerative Medicine · doi:10.1007/s13770-013-1087-8 · Cited by 9
“NSCs are self-renewing multipotent cells that generate neuronal and glial cells of the nervous system.55 Infusion of VEGF into the lateral ventricle increases neurogenesis by promoting survival of newborn neurons.56 In addition, mice over-expressing VEGF show enhanced neurogenesis and migration of the newly generated…”
BackgroundInfluentialMicroglia: The Bodyguard and the Hunter of the Adult Neurogenic Niche
Valero, J., Eiriz, M. F., Santos, T., Neiva, I., Ferreira, R., & Malva, J. O. (2012) · Humana Press eBooks · doi:10.1007/978-1-61779-940-2_14 · Cited by 9
Phillipps, H. R., Rand, C. J., Brown, R. S. E., Kokay, I. C., Stanton, J. L., & Grattan, D. R. (2019) · The FASEB Journal · doi:10.1096/fj.201802262r · Cited by 9
Choroid plexus trophic factors in the developing and adult brain
Arnaud, K., & Nardo, A. A. D. (2016) · Frontiers in Biology · doi:10.1007/s11515-016-1401-7 · Cited by 9
“FGF2 and EGF also maintain neural niche architecture and cell lineage progression (Jin et al., 2003).”
Epidermal growth factor-induced cell proliferation in the adult rat striatum
McGinn, M. J., Sun, D., Schneider, S. L., Alexander, J. K., & Colello, R. J. (2004) · Brain Research · doi:10.1016/j.brainres.2003.12.054 · Cited by 9
Hwang, I. K., Yoo, K., Park, O. K., Choi, J. H., Lee, C. H., & Won, M. (2009) · Journal of Veterinary Medical Science · doi:10.1292/jvms.71.211 · Cited by 9
“Doublecortin (DCX) has been used as a marker of neuronal differentiation in the brain of various animals such as mice [14], rats [3, 15, 18, 20–22], gerbils [12], monkeys [26], dogs [11, 24] and humans [13].”
MethodNeurogenesis in the Damaged Mammalian Brain
Nakafuku, M., & Grande, A. W. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397265-1.00074-5 · Cited by 8
Meunier, A., Sawamoto, K., & Spassky, N. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814405-3.00042-4 · Cited by 8
In vitro characterization on the role of APOE polymorphism in human hippocampal neurogenesis
Lee, H.-A., Price, J., Srivastava, D. P., & Thuret, S. (2023) · Hippocampus · doi:10.1002/hipo.23502 · Cited by 6
“…or radial glia-like stem cells expressing markers like Paired Box 6 [PAX6], Maekawa et al., 2005, Hes family BHLH transcription factor 5 [HES5], Jin et al., 2003, and achaete-scute family BHLH transcription factor 1 [ASCL1], Andersen et al., 2014), first need to become “transient…”
BackgroundNeural Stem Cells: Exogenous and Endogenous Promising Therapies for Stroke
Guerra‐Crespo, M., la Herrán-Arita, A. K. D., Boronat-Garca, A., Maya-Espinosa, G., Garca-Montes, J. R., Fallon, J. H., & Drucker-Col, R. (2012) · InTech eBooks · doi:10.5772/31400 · Cited by 8
“, 1999) and restores the proliferative rates in aging rats (Fluxe et al., 2008; Jin et al., 2003).”
Background
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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