[en] Harmonic mechanisms orchestrate neurogenesis in the healthy brain within specific neurogenic niches, which generate neurons from neural stem cells as a homeostatic mechanism. These newly generated neurons integrate into existing neuronal circuits to participate in different brain tasks. Despite the mechanisms that protect the mammalian brain, this organ is susceptible to many different types of damage that result in the loss of neuronal tissue and therefore in alterations in the functionality of the affected regions. Nevertheless, the mammalian brain has developed mechanisms to respond to these injuries, potentiating its capacity to generate new neurons from neural stem cells and altering the homeostatic processes that occur in neurogenic niches. These alterations may lead to the generation of new neurons within the damaged brain regions. Notwithstanding, the activation of these repair mechanisms, regeneration of neuronal tissue within brain injuries does not naturally occur. In this review, we discuss how the different neurogenic niches respond to different types of brain injuries, focusing on the capacity of the progenitors generated in these niches to migrate to the injured regions and activate repair mechanisms. We conclude that the search for pharmacological drugs that stimulate the migration of newly generated neurons to brain injuries may result in the development of therapies to repair the damaged brain tissue.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Geribaldi-Doldán, Noelia ; Departamento de Anatomía y Embriología Humanas, Facultad de Medicina, Universidad de Cádiz, 11003 Cádiz, Spain ; Instituto de Investigación e Innovación Biomédica de Cádiz (INiBICA), 11009 Cádiz, Spain
Carrascal, Livia ; Instituto de Investigación e Innovación Biomédica de Cádiz (INiBICA), 11009 Cádiz, Spain ; Departamento de Fisiología, Facultad de Farmacia, Universidad de Sevilla, 41012 Sevilla, Spain
Pérez-García, Patricia; Instituto de Investigación e Innovación Biomédica de Cádiz (INiBICA), 11009 Cádiz, Spain ; Departamento de Biomedicina, Biotecnología y Salud Pública, Área de Fisiología, Facultad de Medicina, Universidad de Cádiz, 11003 Cádiz, Spain
Oliva-Montero, José M; Instituto de Investigación e Innovación Biomédica de Cádiz (INiBICA), 11009 Cádiz, Spain ; Departamento de Biomedicina, Biotecnología y Salud Pública, Área de Fisiología, Facultad de Medicina, Universidad de Cádiz, 11003 Cádiz, Spain
Pardillo-Díaz, Ricardo; Instituto de Investigación e Innovación Biomédica de Cádiz (INiBICA), 11009 Cádiz, Spain ; Departamento de Biomedicina, Biotecnología y Salud Pública, Área de Fisiología, Facultad de Medicina, Universidad de Cádiz, 11003 Cádiz, Spain
Domínguez-García, Samuel ; Instituto de Investigación e Innovación Biomédica de Cádiz (INiBICA), 11009 Cádiz, Spain ; Departamento de Biomedicina, Biotecnología y Salud Pública, Área de Fisiología, Facultad de Medicina, Universidad de Cádiz, 11003 Cádiz, Spain ; Department of Neuroscience, Karolinska Institutet, Biomedicum, 17177 Stockholm, Sweden
Bernal-Utrera, Carlos ; Instituto de Investigación e Innovación Biomédica de Cádiz (INiBICA), 11009 Cádiz, Spain ; Departamento de Fisioterapia, Facultad de Enfermería, Fisioterapia y Podología, Universidad de Sevilla, 41009 Sevilla, Spain
Gómez Oliva, Ricardo ; Université de Liège - ULiège > GIGA > GIGA Neurosciences - Molecular Regulation of Neurogenesis ; Instituto de Investigación e Innovación Biomédica de Cádiz (INiBICA), 11009 Cádiz, Spain ; Departamento de Biomedicina, Biotecnología y Salud Pública, Área de Fisiología, Facultad de Medicina, Universidad de Cádiz, 11003 Cádiz, Spain
Martínez-Ortega, Sergio; Instituto de Investigación e Innovación Biomédica de Cádiz (INiBICA), 11009 Cádiz, Spain ; Departamento de Biomedicina, Biotecnología y Salud Pública, Área de Fisiología, Facultad de Medicina, Universidad de Cádiz, 11003 Cádiz, Spain
Verástegui, Cristina ; Departamento de Anatomía y Embriología Humanas, Facultad de Medicina, Universidad de Cádiz, 11003 Cádiz, Spain ; Instituto de Investigación e Innovación Biomédica de Cádiz (INiBICA), 11009 Cádiz, Spain
Nunez-Abades, Pedro ; Instituto de Investigación e Innovación Biomédica de Cádiz (INiBICA), 11009 Cádiz, Spain ; Departamento de Fisiología, Facultad de Farmacia, Universidad de Sevilla, 41012 Sevilla, Spain
Castro, Carmen ; Instituto de Investigación e Innovación Biomédica de Cádiz (INiBICA), 11009 Cádiz, Spain ; Departamento de Biomedicina, Biotecnología y Salud Pública, Área de Fisiología, Facultad de Medicina, Universidad de Cádiz, 11003 Cádiz, Spain
Language :
English
Title :
Migratory Response of Cells in Neurogenic Niches to Neuronal Death: The Onset of Harmonic Repair?
Publication date :
01 April 2023
Journal title :
International Journal of Molecular Sciences
ISSN :
1661-6596
eISSN :
1422-0067
Publisher :
Multidisciplinary Digital Publishing Institute (MDPI), Switzerland
AEI - Agencia Estatal de Investigación EU - European Union Regional Government of Andalusia Consejería de Salud y Familias
Funding text :
This work was supported by the Spanish Agencia Estatal de Investigación (grant number RTI-2018-099908-B-C21 and RTI-2018-099908-B-C22 granted to C.C.). This work has been co-financed by the European Union under the 2014-2020 ERDF Operational Programme and by the Department of Economic Transformation, Industry, Knowledge, and Universities of the Regional Government of Andalusia. Project reference: (grant number FEDER-UCA18-106647 granted to C.C.). This work has been co-financed and by the Consejería de Salud y Familias and by EDRF ITI regional funds (80%) (Grant number: ITI-Cadiz-0042-2019 granted to C.C.).
Wingo T.S. Liu Y. Gerasimov E.S. Vattathil S.M. Wynne M.E. Liu J. Lori A. Faundez V. Bennett D.A. Seyfried N.T. et al. Shared mechanisms across the major psychiatric and neurodegenerative diseases Nat. Commun. 2022 13 4314 10.1038/s41467-022-31873-5 35882878
Wang H. Yang F. Zhang S. Xin R. Sun Y. Genetic and environmental factors in Alzheimer’s and Parkinson’s diseases and promising therapeutic intervention via fecal microbiota transplantation NPJ Park. Dis. 2021 7 70 10.1038/s41531-021-00213-7 34381040
Golde T.E. The therapeutic importance of understanding mechanisms of neuronal cell death in neurodegenerative disease Mol. Neurodegener. 2009 4 8 10.1186/1750-1326-4-8 19193222
Pardillo-Díaz R. Carrascal L. Ayala A. Nunez-Abades P. Oxidative stress induced by cumene hydroperoxide evokes changes in neuronal excitability of rat motor cortex neurons Neuroscience 2015 289 85 98 10.1016/j.neuroscience.2014.12.055
Pardillo-Díaz R. Pérez-García P. Castro C. Nunez-Abades P. Carrascal L. Oxidative Stress as a Potential Mechanism Underlying Membrane Hyperexcitability in Neurodegenerative Diseases Antioxidants 2022 11 1511 10.3390/antiox11081511
Qin C. Yang S. Chu Y.-H. Zhang H. Pang X.-W. Chen L. Zhou L.-Q. Chen M. Tian D.-S. Wang W. Signaling pathways involved in ischemic stroke: Molecular mechanisms and therapeutic interventions Signal. Transduct. Target. Ther. 2022 7 215 10.1038/s41392-022-01064-1
Tuo Q.-Z. Zhang S.-T. Lei P. Mechanisms of neuronal cell death in ischemic stroke and their therapeutic implications Med. Res. Rev. 2022 42 259 305 10.1002/med.21817
Morrison S.J. Kimble J. Asymmetric and symmetric stem-cell divisions in development and cancer Nature 2006 441 1068 1074 10.1038/nature04956
Obernier K. Alvarez-Buylla A. Neural stem cells: Origin, heterogeneity and regulation in the adult mammalian brain Development 2019 146 dev156059 10.1242/dev.156059
Gould E. Reeves A.J. Graziano M.S. Gross C.G. Neurogenesis in the neocortex of adult primates Science 1999 286 548 552 10.1126/science.286.5439.548
Gould E. Vail N. Wagers M. Gross C.G. Adult-generated hippocampal and neocortical neurons in macaques have a transient existence Proc. Natl. Acad. Sci. USA 2001 98 10910 10917 10.1073/pnas.181354698 11526209
Doetsch F. Garcia-Verdugo J.M. Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain J. Neurosci. 1997 17 5046 5061 10.1523/JNEUROSCI.17-13-05046.1997 9185542
Suh H. Consiglio A. Ray J. Sawai T. D’Amour K.A. Gage F.H. In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus Cell Stem Cell 2007 1 515 528 10.1016/j.stem.2007.09.002
Alvarez-Buylla A. Lim D.A. For the long run: Maintaining germinal niches in the adult brain Neuron 2004 41 683 686 10.1016/S0896-6273(04)00111-4
Bond A.M. Ming G.L. Song H. Adult Mammalian Neural Stem Cells and Neurogenesis: Five Decades Later Cell Stem Cell 2015 17 385 395 10.1016/j.stem.2015.09.003
Abrous D.N. Koehl M. Le Moal M. Adult neurogenesis: From precursors to network and physiology Physiol. Rev. 2005 85 523 569 10.1152/physrev.00055.2003 15788705
Alvarez-Buylla A. Garcia-Verdugo J.M. Neurogenesis in adult subventricular zone J. Neurosci. 2002 22 629 634 10.1523/JNEUROSCI.22-03-00629.2002
Lim D.A. Alvarez-Buylla A. The Adult Ventricular-Subventricular Zone (V-SVZ) and Olfactory Bulb (OB) Neurogenesis Cold Spring Harb. Perspect. Biol. 2016 8 a018820 10.1101/cshperspect.a018820
Lledo P.M. Saghatelyan A. Integrating new neurons into the adult olfactory bulb: Joining the network, life-death decisions, and the effects of sensory experience Trends Neurosci. 2005 28 248 254 10.1016/j.tins.2005.03.005
Defterali C. Moreno-Estelles M. Crespo C. Diaz-Guerra E. Diaz-Moreno M. Vergano-Vera E. Nieto-Estevez V. Hurtado-Chong A. Consiglio A. Mira H. et al. Neural stem cells in the adult olfactory bulb core generate mature neurons in vivo Stem Cells 2021 39 1253 1269 10.1002/stem.3393
Menn B. Garcia-Verdugo J.M. Yaschine C. Gonzalez-Perez O. Rowitch D. Alvarez-Buylla A. Origin of oligodendrocytes in the subventricular zone of the adult brain J. Neurosci. 2006 26 7907 7918 10.1523/JNEUROSCI.1299-06.2006
van Praag H. Schinder A.F. Christie B.R. Toni N. Palmer T.D. Gage F.H. Functional neurogenesis in the adult hippocampus Nature 2002 415 1030 1034 10.1038/4151030a 11875571
Seri B. Garcia-Verdugo J.M. McEwen B.S. Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus J. Neurosci. 2001 21 7153 7160 10.1523/JNEUROSCI.21-18-07153.2001
Butti E. Cusimano M. Bacigaluppi M. Martino G. Neurogenic and non-neurogenic functions of endogenous neural stem cells Front. Neurosci. 2014 8 92 10.3389/fnins.2014.00092 24808821
Sun G.J. Zhou Y. Stadel R.P. Moss J. Yong J.H. Ito S. Kawasaki N.K. Phan A.T. Oh J.H. Modak N. et al. Tangential migration of neuronal precursors of glutamatergic neurons in the adult mammalian brain Proc. Natl. Acad. Sci. USA 2015 112 9484 9489 10.1073/pnas.1508545112 26170290
Dayer A.G. Cleaver K.M. Abouantoun T. Cameron H.A. New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors J. Cell. Biol. 2005 168 415 427 10.1083/jcb.200407053
Luzzati F. Nato G. Oboti L. Vigna E. Rolando C. Armentano M. Bonfanti L. Fasolo A. Peretto P. Quiescent neuronal progenitors are activated in the juvenile guinea pig lateral striatum and give rise to transient neurons Development 2014 141 4065 4075 10.1242/dev.107987
Ernst A. Alkass K. Bernard S. Salehpour M. Perl S. Tisdale J. Possnert G. Druid H. Frisen J. Neurogenesis in the striatum of the adult human brain Cell 2014 156 1072 1083 10.1016/j.cell.2014.01.044
Recabal A. Caprile T. Garcia-Robles M.L.A. Hypothalamic Neurogenesis as an Adaptive Metabolic Mechanism Front. Neurosci. 2017 11 190 10.3389/fnins.2017.00190
Bergmann O. Spalding K.L. Frisen J. Adult Neurogenesis in Humans Cold Spring Harb. Perspect. Biol. 2015 7 a018994 10.1101/cshperspect.a018994
Bergmann O. Liebl J. Bernard S. Alkass K. Yeung M.S. Steier P. Kutschera W. Johnson L. Landen M. Druid H. et al. The age of olfactory bulb neurons in humans Neuron 2012 74 634 639 10.1016/j.neuron.2012.03.030
Leuner B. Kozorovitskiy Y. Gross C.G. Gould E. Diminished adult neurogenesis in the marmoset brain precedes old age Proc. Natl. Acad. Sci. USA 2007 104 17169 17173 10.1073/pnas.0708228104
Ben Abdallah N.M. Slomianka L. Lipp H.P. Reversible effect of X-irradiation on proliferation, neurogenesis, and cell death in the dentate gyrus of adult mice Hippocampus 2007 17 1230 1240 10.1002/hipo.20358
Boldrini M. Fulmore C.A. Tartt A.N. Simeon L.R. Pavlova I. Poposka V. Rosoklija G.B. Stankov A. Arango V. Dwork A.J. et al. Human Hippocampal Neurogenesis Persists throughout Aging Cell Stem Cell 2018 22 589 599 e585 10.1016/j.stem.2018.03.015
Sorrells S.F. Paredes M.F. Cebrian-Silla A. Sandoval K. Qi D. Kelley K.W. James D. Mayer S. Chang J. Auguste K.I. et al. Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults Nature 2018 555 377 381 10.1038/nature25975 29513649
Flor-Garcia M. Terreros-Roncal J. Moreno-Jimenez E.P. Avila J. Rabano A. Llorens-Martin M. Unraveling human adult hippocampal neurogenesis Nat. Protoc. 2020 15 668 693 10.1038/s41596-019-0267-y 31915385
Carrasco M. Rabaneda L.G. Murillo-Carretero M. Ortega-Martinez S. Martinez-Chantar M.L. Woodhoo A. Luka Z. Wagner C. Lu S.C. Mato J.M. et al. Glycine N-methyltransferase expression in the hippocampus and its role in neurogenesis and cognitive performance Hippocampus 2014 24 840 852 10.1002/hipo.22274
Rabaneda L.G. Geribaldi-Doldan N. Murillo-Carretero M. Carrasco M. Martinez-Salas J.M. Verastegui C. Castro C. Altered regulation of the Spry2/Dyrk1A/PP2A triad by homocysteine impairs neural progenitor cell proliferation Biochim. Biophys. Acta 2016 1863 3015 3026 10.1016/j.bbamcr.2016.09.018
Gomez-Oliva R. Geribaldi-Doldan N. Dominguez-Garcia S. Carrascal L. Verastegui C. Nunez-Abades P. Castro C. Vitamin D deficiency as a potential risk factor for accelerated aging, impaired hippocampal neurogenesis and cognitive decline: A role for Wnt/beta-catenin signaling Aging (Albany N. Y.) 2020 12 13824 13844 10.18632/aging.103510 32554862
Cuartero M.I. de la Parra J. Pérez-Ruiz A. Bravo-Ferrer I. Durán-Laforet V. García-Culebras A. García-Segura J.M. Dhaliwal J. Frankland P.W. Lizasoain I. et al. Abolition of aberrant neurogenesis ameliorates cognitive impairment after stroke in mice J. Clin. Investig. 2019 129 1536 1550 10.1172/JCI120412 30676325
Berdugo-Vega G. Arias-Gil G. López-Fernández A. Artegiani B. Wasielewska J.M. Lee C.C. Lippert M.T. Kempermann G. Takagaki K. Calegari F. Increasing neurogenesis refines hippocampal activity rejuvenating navigational learning strategies and contextual memory throughout life Nat. Commun. 2020 11 135 10.1038/s41467-019-14026-z
Terreros-Roncal J. Moreno-Jimenez E.P. Flor-Garcia M. Rodriguez-Moreno C.B. Trinchero M.F. Cafini F. Rabano A. Llorens-Martin M. Impact of neurodegenerative diseases on human adult hippocampal neurogenesis Science 2021 374 1106 1113 10.1126/science.abl5163
Moreno-Jiménez E.P. Flor-García M. Terreros-Roncal J. Rábano A. Cafini F. Pallas-Bazarra N. Ávila J. Llorens-Martín M. Adult hippocampal neurogenesis is abundant in neurologically healthy subjects and drops sharply in patients with Alzheimer’s disease Nat. Med. 2019 25 554 560 10.1038/s41591-019-0375-9 30911133
Blennow K. Hardy J. Zetterberg H. The neuropathology and neurobiology of traumatic brain injury Neuron 2012 76 886 899 10.1016/j.neuron.2012.11.021 23217738
Altmann C. Keller S. Schmidt M.H.H. The Role of SVZ Stem Cells in Glioblastoma Cancers 2019 11 448 10.3390/cancers11040448
Fabel K. Kempermann G. Physical activity and the regulation of neurogenesis in the adult and aging brain Neuromolecular Med. 2008 10 59 66 10.1007/s12017-008-8031-4
Ding W.Y. Huang J. Wang H. Waking up quiescent neural stem cells: Molecular mechanisms and implications in neurodevelopmental disorders PLoS Genet. 2020 16 e1008653 10.1371/journal.pgen.1008653
Fontan-Lozano A. Morcuende S. Davis-Lopez de Carrizosa M.A. Benitez-Temino B. Mejias R. Matarredona E.R. To Become or Not to Become Tumorigenic: Subventricular Zone Versus Hippocampal Neural Stem Cells Front. Oncol. 2020 10 602217 10.3389/fonc.2020.602217
Kempermann G. Song H. Gage F.H. Neurogenesis in the Adult Hippocampus Cold Spring Harb. Perspect. Biol. 2015 7 a018812 10.1101/cshperspect.a018812 26330519
Young C.C. Brooks K.J. Buchan A.M. Szele F.G. Cellular and molecular determinants of stroke-induced changes in subventricular zone cell migration Antioxid. Redox Signal. 2011 14 1877 1888 10.1089/ars.2010.3435 20673127
Bressan C. Saghatelyan A. Intrinsic Mechanisms Regulating Neuronal Migration in the Postnatal Brain Front. Cell. Neurosci. 2020 14 620379 10.3389/fncel.2020.620379 33519385
Kaneko N. Sawada M. Sawamoto K. Mechanisms of neuronal migration in the adult brain J. Neurochem. 2017 141 835 847 10.1111/jnc.14002
Bellion A. Baudoin J.P. Alvarez C. Bornens M. Metin C. Nucleokinesis in tangentially migrating neurons comprises two alternating phases: Forward migration of the Golgi/centrosome associated with centrosome splitting and myosin contraction at the rear J. Neurosci. 2005 25 5691 5699 10.1523/JNEUROSCI.1030-05.2005
Schaar B.T. McConnell S.K. Cytoskeletal coordination during neuronal migration Proc. Natl. Acad. Sci. USA 2005 102 13652 13657 10.1073/pnas.0506008102 16174753
Tsai J.W. Bremner K.H. Vallee R.B. Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue Nat. Neurosci. 2007 10 970 979 10.1038/nn1934 17618279
Shinohara R. Thumkeo D. Kamijo H. Kaneko N. Sawamoto K. Watanabe K. Takebayashi H. Kiyonari H. Ishizaki T. Furuyashiki T. et al. A role for mDia, a Rho-regulated actin nucleator, in tangential migration of interneuron precursors Nat. Neurosci. 2012 15 373 380 10.1038/nn.3020
Lois C. Garcia-Verdugo J.M. Alvarez-Buylla A. Chain migration of neuronal precursors Science 1996 271 978 981 10.1126/science.271.5251.978 8584933
Zhang R.L. Chopp M. Gregg S.R. Toh Y. Roberts C. Letourneau Y. Buller B. Jia L. Siamak P.N.D. Zhang Z.G. Patterns and dynamics of subventricular zone neuroblast migration in the ischemic striatum of the adult mouse J. Cereb. Blood Flow. Metab. 2009 29 1240 1250 10.1038/jcbfm.2009.55
Fujioka T. Kaneko N. Ajioka I. Nakaguchi K. Omata T. Ohba H. Fassler R. Garcia-Verdugo J.M. Sekiguchi K. Matsukawa N. et al. beta1 integrin signaling promotes neuronal migration along vascular scaffolds in the post-stroke brain EBioMedicine 2017 16 195 203 10.1016/j.ebiom.2017.01.005 28153772
Barkho B.Z. Munoz A.E. Li X. Li L. Cunningham L.A. Zhao X. Endogenous matrix metalloproteinase (MMP)-3 and MMP-9 promote the differentiation and migration of adult neural progenitor cells in response to chemokines Stem Cells 2008 26 3139 3149 10.1634/stemcells.2008-0519 18818437
Geribaldi-Doldan N. Carrasco M. Murillo-Carretero M. Dominguez-Garcia S. Garcia-Cozar F.J. Munoz-Miranda J.P. Del Rio-Garcia V. Verastegui C. Castro C. Specific inhibition of ADAM17/TACE promotes neurogenesis in the injured motor cortex Cell Death Dis. 2018 9 862 10.1038/s41419-018-0913-2
Yagita Y. Sakurai T. Tanaka H. Kitagawa K. Colman D.R. Shan W. N-cadherin mediates interaction between precursor cells in the subventricular zone and regulates further differentiation J. Neurosci. Res. 2009 87 3331 3342 10.1002/jnr.22044 19301425
Belvindrah R. Hankel S. Walker J. Patton B.L. Muller U. Beta1 integrins control the formation of cell chains in the adult rostral migratory stream J. Neurosci. 2007 27 2704 2717 10.1523/JNEUROSCI.2991-06.2007 17344408
Anton E.S. Ghashghaei H.T. Weber J.L. McCann C. Fischer T.M. Cheung I.D. Gassmann M. Messing A. Klein R. Schwab M.H. et al. Receptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain Nat. Neurosci. 2004 7 1319 1328 10.1038/nn1345 15543145
Ghashghaei H.T. Weber J. Pevny L. Schmid R. Schwab M.H. Lloyd K.C. Eisenstat D.D. Lai C. Anton E.S. The role of neuregulin-ErbB4 interactions on the proliferation and organization of cells in the subventricular zone Proc. Natl. Acad. Sci. USA 2006 103 1930 1935 10.1073/pnas.0510410103
Kaneko N. Marin O. Koike M. Hirota Y. Uchiyama Y. Wu J.Y. Lu Q. Tessier-Lavigne M. Alvarez-Buylla A. Okano H. et al. New neurons clear the path of astrocytic processes for their rapid migration in the adult brain Neuron 2010 67 213 223 10.1016/j.neuron.2010.06.018
Snapyan M. Lemasson M. Brill M.S. Blais M. Massouh M. Ninkovic J. Gravel C. Berthod F. Gotz M. Barker P.A. et al. Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling J. Neurosci. 2009 29 4172 4188 10.1523/JNEUROSCI.4956-08.2009
Bovetti S. Hsieh Y.C. Bovolin P. Perroteau I. Kazunori T. Puche A.C. Blood vessels form a scaffold for neuroblast migration in the adult olfactory bulb J. Neurosci. 2007 27 5976 5980 10.1523/JNEUROSCI.0678-07.2007
Whitman M.C. Fan W. Rela L. Rodriguez-Gil D.J. Greer C.A. Blood vessels form a migratory scaffold in the rostral migratory stream J. Comp. Neurol. 2009 516 94 104 10.1002/cne.22093
Wittko I.M. Schanzer A. Kuzmichev A. Schneider F.T. Shibuya M. Raab S. Plate K.H. VEGFR-1 regulates adult olfactory bulb neurogenesis and migration of neural progenitors in the rostral migratory stream in vivo J. Neurosci. 2009 29 8704 8714 10.1523/JNEUROSCI.5527-08.2009 19587277
Bozoyan L. Khlghatyan J. Saghatelyan A. Astrocytes control the development of the migration-promoting vasculature scaffold in the postnatal brain via VEGF signaling J. Neurosci. 2012 32 1687 1704 10.1523/JNEUROSCI.5531-11.2012 22302810
Kaneko N. Herranz-Perez V. Otsuka T. Sano H. Ohno N. Omata T. Nguyen H.B. Thai T.Q. Nambu A. Kawaguchi Y. et al. New neurons use Slit-Robo signaling to migrate through the glial meshwork and approach a lesion for functional regeneration Sci. Adv. 2018 4 eaav0618 10.1126/sciadv.aav0618 30547091
Ohab J.J. Fleming S. Blesch A. Carmichael S.T. A neurovascular niche for neurogenesis after stroke J. Neurosci. 2006 26 13007 13016 10.1523/JNEUROSCI.4323-06.2006 17167090
Robin A.M. Zhang Z.G. Wang L. Zhang R.L. Katakowski M. Zhang L. Wang Y. Zhang C. Chopp M. Stromal cell-derived factor 1alpha mediates neural progenitor cell motility after focal cerebral ischemia J. Cereb. Blood Flow. Metab. 2006 26 125 134 10.1038/sj.jcbfm.9600172
Thored P. Arvidsson A. Cacci E. Ahlenius H. Kallur T. Darsalia V. Ekdahl C.T. Kokaia Z. Lindvall O. Persistent production of neurons from adult brain stem cells during recovery after stroke Stem Cells 2006 24 739 747 10.1634/stemcells.2005-0281
Grade S. Weng Y.C. Snapyan M. Kriz J. Malva J.O. Saghatelyan A. Brain-derived neurotrophic factor promotes vasculature-associated migration of neuronal precursors toward the ischemic striatum PLoS ONE 2013 8 e55039 10.1371/journal.pone.0055039
Ng K.L. Li J.D. Cheng M.Y. Leslie F.M. Lee A.G. Zhou Q.Y. Dependence of olfactory bulb neurogenesis on prokineticin 2 signaling Science 2005 308 1923 1927 10.1126/science.1112103
Murase S. Horwitz A.F. Deleted in colorectal carcinoma and differentially expressed integrins mediate the directional migration of neural precursors in the rostral migratory stream J. Neurosci. 2002 22 3568 3579 10.1523/JNEUROSCI.22-09-03568.2002
Paratcha G. Ibanez C.F. Ledda F. GDNF is a chemoattractant factor for neuronal precursor cells in the rostral migratory stream Mol. Cell. Neurosci. 2006 31 505 514 10.1016/j.mcn.2005.11.007
Garzotto D. Giacobini P. Crepaldi T. Fasolo A. De Marchis S. Hepatocyte growth factor regulates migration of olfactory interneuron precursors in the rostral migratory stream through Met-Grb2 coupling J. Neurosci. 2008 28 5901 5909 10.1523/JNEUROSCI.1083-08.2008 18524894
Wang T.W. Zhang H. Gyetko M.R. Parent J.M. Hepatocyte growth factor acts as a mitogen and chemoattractant for postnatal subventricular zone-olfactory bulb neurogenesis Mol. Cell. Neurosci. 2011 48 38 50 10.1016/j.mcn.2011.06.003
Yan Y.P. Lang B.T. Vemuganti R. Dempsey R.J. Osteopontin is a mediator of the lateral migration of neuroblasts from the subventricular zone after focal cerebral ischemia Neurochem. Int. 2009 55 826 832 10.1016/j.neuint.2009.08.007 19686792
Yan Y.P. Sailor K.A. Lang B.T. Park S.W. Vemuganti R. Dempsey R.J. Monocyte chemoattractant protein-1 plays a critical role in neuroblast migration after focal cerebral ischemia J. Cereb. Blood Flow. Metab. 2007 27 1213 1224 10.1038/sj.jcbfm.9600432 17191078
Gotz M. Stricker S.H. Go with the flow: Signaling from the ventricle directs neuroblast migration Nat. Neurosci. 2006 9 470 472 10.1038/nn0406-470
Nguyen-Ba-Charvet K.T. Picard-Riera N. Tessier-Lavigne M. Baron-Van Evercooren A. Sotelo C. Chedotal A. Multiple roles for slits in the control of cell migration in the rostral migratory stream J. Neurosci. 2004 24 1497 1506 10.1523/JNEUROSCI.4729-03.2004
Hurtado-Chong A. Yusta-Boyo M.J. Vergano-Vera E. Bulfone A. de Pablo F. Vicario-Abejon C. IGF-I promotes neuronal migration and positioning in the olfactory bulb and the exit of neuroblasts from the subventricular zone Eur. J. Neurosci. 2009 30 742 755 10.1111/j.1460-9568.2009.06870.x
Bolteus A.J. Bordey A. GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone J. Neurosci. 2004 24 7623 7631 10.1523/JNEUROSCI.1999-04.2004
Sawamoto K. Wichterle H. Gonzalez-Perez O. Cholfin J.A. Yamada M. Spassky N. Murcia N.S. Garcia-Verdugo J.M. Marin O. Rubenstein J.L. et al. New neurons follow the flow of cerebrospinal fluid in the adult brain Science 2006 311 629 632 10.1126/science.1119133
Wu N. Sun X. Zhou C. Yan J. Cheng C. Neuroblasts migration under control of reactive astrocyte-derived BDNF: A promising therapy in late neurogenesis after traumatic brain injury Stem Cell. Res. 2023 14 2 10.1186/s13287-022-03232-0
Battista D. Rutishauser U. Removal of polysialic acid triggers dispersion of subventricularly derived neuroblasts into surrounding CNS tissues J. Neurosci. 2010 30 3995 4003 10.1523/JNEUROSCI.4382-09.2010
Collaborators G.D.F. Estimation of the global prevalence of dementia in 2019 and forecasted prevalence in 2050: An analysis for the Global Burden of Disease Study 2019 Lancet Public Health 2022 7 e105 e125 10.1016/S2468-2667(21)00249-8
Hohman T.J. Dumitrescu L. Barnes L.L. Thambisetty M. Beecham G. Kunkle B. Gifford K.A. Bush W.S. Chibnik L.B. Mukherjee S. et al. Sex-Specific Association of Apolipoprotein E With Cerebrospinal Fluid Levels of Tau JAMA Neurol. 2018 75 989 998 10.1001/jamaneurol.2018.0821 29801024
Lane C.A. Hardy J. Schott J.M. Alzheimer’s disease Eur. J. Neurol. 2018 25 59 70 10.1111/ene.13439
Serrano-Pozo A. Frosch M.P. Masliah E. Hyman B.T. Neuropathological alterations in Alzheimer disease Cold Spring Harb. Perspect. Med. 2011 1 a006189 10.1101/cshperspect.a006189
Rodríguez-Iglesias N. Sierra A. Valero J. Rewiring of Memory Circuits: Connecting Adult Newborn Neurons With the Help of Microglia Front. Cell. Dev. Biol. 2019 7 24 10.3389/fcell.2019.00024 30891446
Tobin M.K. Musaraca K. Disouky A. Shetti A. Bheri A. Honer W.G. Kim N. Dawe R.J. Bennett D.A. Arfanakis K. et al. Human Hippocampal Neurogenesis Persists in Aged Adults and Alzheimer’s Disease Patients Cell Stem Cell 2019 24 974 982.e3 10.1016/j.stem.2019.05.003
Jin K. Peel A.L. Mao X.O. Xie L. Cottrell B.A. Henshall D.C. Greenberg D.A. Increased hippocampal neurogenesis in Alzheimer’s disease Proc. Natl. Acad. Sci. USA 2004 101 343 347 10.1073/pnas.2634794100 14660786
Boekhoorn K. Joels M. Lucassen P.J. Increased proliferation reflects glial and vascular-associated changes, but not neurogenesis in the presenile Alzheimer hippocampus Neurobiol. Dis. 2006 24 1 14 10.1016/j.nbd.2006.04.017
Moser M.B. Moser E.I. Forrest E. Andersen P. Morris R.G. Spatial learning with a minislab in the dorsal hippocampus Proc. Natl. Acad. Sci. USA 1995 92 9697 9701 10.1073/pnas.92.21.9697
Henke P.G. Hippocampal pathway to the amygdala and stress ulcer development Brain Res. Bull. 1990 25 691 695 10.1016/0361-9230(90)90044-Z 2289157
Marquez-Valadez B. Rabano A. Llorens-Martin M. Progression of Alzheimer’s disease parallels unusual structural plasticity of human dentate granule cells Acta Neuropathol. Commun. 2022 10 125 10.1186/s40478-022-01431-7
Haughey N.J. Nath A. Chan S.L. Borchard A.C. Rao M.S. Mattson M.P. Disruption of neurogenesis by amyloid beta-peptide, and perturbed neural progenitor cell homeostasis, in models of Alzheimer’s disease J. Neurochem. 2002 83 1509 1524 10.1046/j.1471-4159.2002.01267.x
Ermini F.V. Grathwohl S. Radde R. Yamaguchi M. Staufenbiel M. Palmer T.D. Jucker M. Neurogenesis and alterations of neural stem cells in mouse models of cerebral amyloidosis Am. J. Pathol. 2008 172 1520 1528 10.2353/ajpath.2008.060520 18467698
Donovan M.H. Yazdani U. Norris R.D. Games D. German D.C. Eisch A.J. Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer’s disease J. Comp. Neurol. 2006 495 70 83 10.1002/cne.20840 16432899
Fuster-Matanzo A. de Barreda E.G. Dawson H.N. Vitek M.P. Avila J. Hernandez F. Function of tau protein in adult newborn neurons FEBS Lett. 2009 583 3063 3068 10.1016/j.febslet.2009.08.017 19695252
Pallas-Bazarra N. Jurado-Arjona J. Navarrete M. Esteban J.A. Hernandez F. Avila J. Llorens-Martin M. Novel function of Tau in regulating the effects of external stimuli on adult hippocampal neurogenesis EMBO J. 2016 35 1417 1436 10.15252/embj.201593518
Esteve D. Molina-Navarro M.M. Giraldo E. Martinez-Varea N. Blanco-Gandia M.C. Rodriguez-Arias M. Garcia-Verdugo J.M. Vina J. Lloret A. Adult Neural Stem Cell Migration Is Impaired in a Mouse Model of Alzheimer’s Disease Mol. Neurobiol. 2022 59 1168 1182 10.1007/s12035-021-02620-6
Poewe W. Seppi K. Tanner C.M. Halliday G.M. Brundin P. Volkmann J. Schrag A.E. Lang A.E. Parkinson disease Nat. Rev. Dis. Prim. 2017 3 17013 10.1038/nrdp.2017.13
Mortality G.B.D. Causes of Death C. Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990-2013: A systematic analysis for the Global Burden of Disease Study 2013 Lancet 2015 385 117 171 10.1016/S0140-6736(14)61682-2
Blauwendraat C. Heilbron K. Vallerga C.L. Bandres-Ciga S. von Coelln R. Pihlstrom L. Simon-Sanchez J. Schulte C. Sharma M. Krohn L. et al. Parkinson’s disease age at onset genome-wide association study: Defining heritability, genetic loci, and alpha-synuclein mechanisms Mov. Disord. 2019 34 866 875 10.1002/mds.27659 30957308
Schapira A.H. Olanow C.W. Greenamyre J.T. Bezard E. Slowing of neurodegeneration in Parkinson’s disease and Huntington’s disease: Future therapeutic perspectives Lancet 2014 384 545 555 10.1016/S0140-6736(14)61010-2
Obeso J.A. Stamelou M. Goetz C.G. Poewe W. Lang A.E. Weintraub D. Burn D. Halliday G.M. Bezard E. Przedborski S. et al. Past, present, and future of Parkinson’s disease: A special essay on the 200th Anniversary of the Shaking Palsy Mov. Disord. 2017 32 1264 1310 10.1002/mds.27115
Bezard E. Gross C.E. Compensatory mechanisms in experimental and human parkinsonism: Towards a dynamic approach Prog. Neurobiol. 1998 55 93 116 10.1016/S0301-0082(98)00006-9 9618745
Surmeier D.J. Determinants of dopaminergic neuron loss in Parkinson’s disease FEBS J. 2018 285 3657 3668 10.1111/febs.14607
Boger H.A. Granholm A.C. McGinty J.F. Middaugh L.D. A dual-hit animal model for age-related parkinsonism Prog. Neurobiol. 2010 90 217 229 10.1016/j.pneurobio.2009.10.013 19853012
Sturm E. Stefanova N. Multiple system atrophy: Genetic or epigenetic? Exp. Neurobiol. 2014 23 277 291 10.5607/en.2014.23.4.277
Hope A.D. Myhre R. Kachergus J. Lincoln S. Bisceglio G. Hulihan M. Farrer M.J. Alpha-synuclein missense and multiplication mutations in autosomal dominant Parkinson’s disease Neurosci. Lett. 2004 367 97 100 10.1016/j.neulet.2004.05.100
Salmina A.B. Kapkaeva M.R. Vetchinova A.S. Illarioshkin S.N. Novel Approaches Used to Examine and Control Neurogenesis in Parkinson’s Disease Int. J. Mol. Sci. 2021 22 9608 10.3390/ijms22179608 34502516
Novosadova E.V. Nenasheva V.V. Makarova I.V. Dolotov O.V. Inozemtseva L.S. Arsenyeva E.L. Chernyshenko S.V. Sultanov R.I. Illarioshkin S.N. Grivennikov I.A. et al. Parkinson’s Disease-Associated Changes in the Expression of Neurotrophic Factors and their Receptors upon Neuronal Differentiation of Human Induced Pluripotent Stem Cells J. Mol. Neurosci. 2020 70 514 521 10.1007/s12031-019-01450-5
Jellinger K.A. Multiple System Atrophy: An Oligodendroglioneural Synucleinopathy1 J. Alzheimers Dis. 2018 62 1141 1179 10.3233/JAD-170397
Arzate D.M. Guerra-Crespo M. Covarrubias L. Induction of typical and atypical neurogenesis in the adult substantia nigra after mouse embryonic stem cells transplantation Neuroscience 2019 408 308 326 10.1016/j.neuroscience.2019.03.042 31034794
Baker S.A. Baker K.A. Hagg T. Dopaminergic nigrostriatal projections regulate neural precursor proliferation in the adult mouse subventricular zone Eur. J. Neurosci. 2004 20 575 579 10.1111/j.1460-9568.2004.03486.x 15233767
Farzanehfar P. Comparative review of adult midbrain and striatum neurogenesis with classical neurogenesis Neurosci. Res. 2018 134 1 9 10.1016/j.neures.2018.01.002
Hermann A. Storch A. Endogenous regeneration in Parkinson’s disease: Do we need orthotopic dopaminergic neurogenesis? Stem Cells 2008 26 2749 2752 10.1634/stemcells.2008-0567 18719222
L’Episcopo F. Tirolo C. Testa N. Caniglia S. Morale M.C. Cossetti C. D’Adamo P. Zardini E. Andreoni L. Ihekwaba A.E. et al. Reactive astrocytes and Wnt/beta-catenin signaling link nigrostriatal injury to repair in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson’s disease Neurobiol. Dis. 2011 41 508 527 10.1016/j.nbd.2010.10.023
Bender H. Fietz S.A. Richter F. Stanojlovic M. Alpha-Synuclein Pathology Coincides With Increased Number of Early Stage Neural Progenitors in the Adult Hippocampus Front. Cell. Dev. Biol. 2021 9 691560 10.3389/fcell.2021.691560
Farzanehfar P. Towards a Better Treatment Option for Parkinson’s Disease: A Review of Adult Neurogenesis Neurochem. Res. 2016 41 3161 3170 10.1007/s11064-016-2053-3
Ermine C.M. Wright J.L. Frausin S. Kauhausen J.A. Parish C.L. Stanic D. Thompson L.H. Modelling the dopamine and noradrenergic cell loss that occurs in Parkinson’s disease and the impact on hippocampal neurogenesis Hippocampus 2018 28 327 337 10.1002/hipo.22835
Aponso P.M. Faull R.L. Connor B. Increased progenitor cell proliferation and astrogenesis in the partial progressive 6-hydroxydopamine model of Parkinson’s disease Neuroscience 2008 151 1142 1153 10.1016/j.neuroscience.2007.11.036
Brown S.J. Boussaad I. Jarazo J. Fitzgerald J.C. Antony P. Keatinge M. Blechman J. Schwamborn J.C. Kruger R. Placzek M. et al. PINK1 deficiency impairs adult neurogenesis of dopaminergic neurons Sci. Rep. 2021 11 6617 10.1038/s41598-021-84278-7 33758225
Agnihotri S.K. Shen R. Li J. Gao X. Bueler H. Loss of PINK1 leads to metabolic deficits in adult neural stem cells and impedes differentiation of newborn neurons in the mouse hippocampus FASEB J. 2017 31 2839 2853 10.1096/fj.201600960RR 28325755
Brodski C. Blaess S. Partanen J. Prakash N. Crosstalk of Intercellular Signaling Pathways in the Generation of Midbrain Dopaminergic Neurons In Vivo and from Stem Cells J. Dev. Biol. 2019 7 3 10.3390/jdb7010003 30650592
Inestrosa N.C. Arenas E. Emerging roles of Wnts in the adult nervous system Nat. Rev. Neurosci. 2010 11 77 86 10.1038/nrn2755
Maiese K. Novel applications of trophic factors, Wnt and WISP for neuronal repair and regeneration in metabolic disease Neural Regen. Res. 2015 10 518 528 10.4103/1673-5374.155427
Marchetti B. Wnt/beta-Catenin Signaling Pathway Governs a Full Program for Dopaminergic Neuron Survival, Neurorescue and Regeneration in the MPTP Mouse Model of Parkinson’s Disease Int. J. Mol. Sci. 2018 19 3743 10.3390/ijms19123743
L’Episcopo F. Tirolo C. Testa N. Caniglia S. Morale M.C. Deleidi M. Serapide M.F. Pluchino S. Marchetti B. Plasticity of subventricular zone neuroprogenitors in MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) mouse model of Parkinson’s disease involves cross talk between inflammatory and Wnt/beta-catenin signaling pathways: Functional consequences for neuroprotection and repair J. Neurosci. 2012 32 2062 2085 10.1523/JNEUROSCI.5259-11.2012
L’Episcopo F. Tirolo C. Testa N. Caniglia S. Morale M.C. Impagnatiello F. Pluchino S. Marchetti B. Aging-induced Nrf2-ARE pathway disruption in the subventricular zone drives neurogenic impairment in parkinsonian mice via PI3K-Wnt/beta-catenin dysregulation J. Neurosci. 2013 33 1462 1485 10.1523/JNEUROSCI.3206-12.2013
L’Episcopo F. Tirolo C. Testa N. Caniglia S. Morale M.C. Serapide M.F. Pluchino S. Marchetti B. Wnt/beta-catenin signaling is required to rescue midbrain dopaminergic progenitors and promote neurorepair in ageing mouse model of Parkinson’s disease Stem Cells 2014 32 2147 2163 10.1002/stem.1708
Bjugstad K.B. Teng Y.D. Redmond D.E. Jr. Elsworth J.D. Roth R.H. Cornelius S.K. Sladek J.R. Jr. Human neural stem cells migrate along the nigrostriatal pathway in a primate model of Parkinson’s disease Exp. Neurol. 2008 211 362 369 10.1016/j.expneurol.2008.01.025
Van den Berge S.A. van Strien M.E. Hol E.M. Resident adult neural stem cells in Parkinson’s disease—The brain’s own repair system? Eur. J. Pharm. 2013 719 117 127 10.1016/j.ejphar.2013.04.058
Jiang M. Tu H.T. Zhang K. Zhang W. Yu W.P. Xu J. Tan E.K. Guo K.H. Zeng L. Impaired neurogenesis in the hippocampus of an adult VPS35 mutant mouse model of Parkinson’s disease through interaction with APP Neurobiol. Dis. 2021 153 105313 10.1016/j.nbd.2021.105313 33636388
Gusella J.F. Wexler N.S. Conneally P.M. Naylor S.L. Anderson M.A. Tanzi R.E. Watkins P.C. Ottina K. Wallace M.R. Sakaguchi A.Y. et al. A polymorphic DNA marker genetically linked to Huntington’s disease Nature 1983 306 234 238 10.1038/306234a0 6316146
Bates G. Huntingtin aggregation and toxicity in Huntington’s disease Lancet 2003 361 1642 1644 10.1016/S0140-6736(03)13304-1 12747895
Moily N.S. Kota L.N. Anjanappa R.M. Venugopal S. Vaidyanathan R. Pal P. Purushottam M. Jain S. Kandasamy M. Trinucleotide repeats and haplotypes at the huntingtin locus in an Indian sample overlaps with European haplogroup a PLoS Curr. 2014 6 10.1371/currents.hd.a3ad1a381ab1eed117675145318c9a80
Bates G.P. History of genetic disease: The molecular genetics of Huntington disease—A history Nat. Rev. Genet. 2005 6 766 773 10.1038/nrg1686 16136077
Poirier M.A. Jiang H. Ross C.A. A structure-based analysis of huntingtin mutant polyglutamine aggregation and toxicity: Evidence for a compact beta-sheet structure Hum. Mol. Genet. 2005 14 765 774 10.1093/hmg/ddi071
Graveland G.A. Williams R.S. DiFiglia M. Evidence for degenerative and regenerative changes in neostriatal spiny neurons in Huntington’s disease Science 1985 227 770 773 10.1126/science.3155875
Kandasamy M. Aigner L. Reactive Neuroblastosis in Huntington’s Disease: A Putative Therapeutic Target for Striatal Regeneration in the Adult Brain Front. Cell. Neurosci. 2018 12 37 10.3389/fncel.2018.00037 29593498
Crowell V. Houghton R. Tomar A. Fernandes T. Squitieri F. Modeling Manifest Huntington’s Disease Prevalence Using Diagnosed Incidence and Survival Time Neuroepidemiology 2021 55 361 368 10.1159/000516767 34350853
Curtis M.A. Connor B. Faull R.L. Neurogenesis in the diseased adult human brain—New therapeutic strategies for neurodegenerative diseases Cell. Cycle 2003 2 428 430 10.4161/cc.2.5.526 12963834
Kohl Z. Regensburger M. Aigner R. Kandasamy M. Winner B. Aigner L. Winkler J. Impaired adult olfactory bulb neurogenesis in the R6/2 mouse model of Huntington’s disease BMC Neurosci. 2010 11 114 10.1186/1471-2202-11-114 20836877
Kandasamy M. Rosskopf M. Wagner K. Klein B. Couillard-Despres S. Reitsamer H.A. Stephan M. Nguyen H.P. Riess O. Bogdahn U. et al. Reduction in subventricular zone-derived olfactory bulb neurogenesis in a rat model of Huntington’s disease is accompanied by striatal invasion of neuroblasts PLoS ONE 2015 10 e0116069 10.1371/journal.pone.0116069
Kandasamy M. Couillard-Despres S. Raber K.A. Stephan M. Lehner B. Winner B. Kohl Z. Rivera F.J. Nguyen H.P. Riess O. et al. Stem cell quiescence in the hippocampal neurogenic niche is associated with elevated transforming growth factor-beta signaling in an animal model of Huntington disease J. Neuropathol. Exp. Neurol. 2010 69 717 728 10.1097/NEN.0b013e3181e4f733 20535034
Lazic S.E. Grote H. Armstrong R.J. Blakemore C. Hannan A.J. van Dellen A. Barker R.A. Decreased hippocampal cell proliferation in R6/1 Huntington’s mice Neuroreport 2004 15 811 813 10.1097/00001756-200404090-00014
Lazic S.E. Grote H.E. Blakemore C. Hannan A.J. van Dellen A. Phillips W. Barker R.A. Neurogenesis in the R6/1 transgenic mouse model of Huntington’s disease: Effects of environmental enrichment Eur. J. Neurosci. 2006 23 1829 1838 10.1111/j.1460-9568.2006.04715.x
Gil J.M. Mohapel P. Araujo I.M. Popovic N. Li J.Y. Brundin P. Petersen A. Reduced hippocampal neurogenesis in R6/2 transgenic Huntington’s disease mice Neurobiol. Dis. 2005 20 744 751 10.1016/j.nbd.2005.05.006
Aigner L. Bogdahn U. TGF-beta in neural stem cells and in tumors of the central nervous system Cell. Tissue Res. 2008 331 225 241 10.1007/s00441-007-0466-7
Pitkanen A. Lukasiuk K. Molecular and cellular basis of epileptogenesis in symptomatic epilepsy Epilepsy Behav. 2009 14 (Suppl. 1) 16 25 10.1016/j.yebeh.2008.09.023
Kuruba R. Hattiangady B. Shetty A.K. Hippocampal neurogenesis and neural stem cells in temporal lobe epilepsy Epilepsy Behav. 2009 14 (Suppl. 1) 65 73 10.1016/j.yebeh.2008.08.020
Cho K.O. Lybrand Z.R. Ito N. Brulet R. Tafacory F. Zhang L. Good L. Ure K. Kernie S.G. Birnbaum S.G. et al. Aberrant hippocampal neurogenesis contributes to epilepsy and associated cognitive decline Nat. Commun. 2015 6 6606 10.1038/ncomms7606
Parent J.M. Yu T.W. Leibowitz R.T. Geschwind D.H. Sloviter R.S. Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus J. Neurosci. 1997 17 3727 3738 10.1523/JNEUROSCI.17-10-03727.1997
Luo C. Koyama R. Ikegaya Y. Microglia engulf viable newborn cells in the epileptic dentate gyrus Glia 2016 64 1508 1517 10.1002/glia.23018 27301702
Sierra A. Martin-Suarez S. Valcarcel-Martin R. Pascual-Brazo J. Aelvoet S.A. Abiega O. Deudero J.J. Brewster A.L. Bernales I. Anderson A.E. et al. Neuronal hyperactivity accelerates depletion of neural stem cells and impairs hippocampal neurogenesis Cell Stem Cell 2015 16 488 503 10.1016/j.stem.2015.04.003 25957904
Chen P. Chen F. Wu Y. Zhou B. New Insights Into the Role of Aberrant Hippocampal Neurogenesis in Epilepsy Front. Neurol. 2021 12 727065 10.3389/fneur.2021.727065 34975709
Chan E.C. Lue M.Y. Hsu K.C. Fan H.A. Identification of novel genes that are differentially expressed in human colorectal carcinoma Biochim. Biophys. Acta 1998 1407 200 204 10.1016/S0925-4439(98)00041-6
Huttmann K. Sadgrove M. Wallraff A. Hinterkeuser S. Kirchhoff F. Steinhauser C. Gray W.P. Seizures preferentially stimulate proliferation of radial glia-like astrocytes in the adult dentate gyrus: Functional and immunocytochemical analysis Eur. J. Neurosci. 2003 18 2769 2778 10.1111/j.1460-9568.2003.03002.x
Jessberger S. Romer B. Babu H. Kempermann G. Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells Exp. Neurol. 2005 196 342 351 10.1016/j.expneurol.2005.08.010
Deisseroth K. Singla S. Toda H. Monje M. Palmer T.D. Malenka R.C. Excitation-neurogenesis coupling in adult neural stem/progenitor cells Neuron 2004 42 535 552 10.1016/S0896-6273(04)00266-1
Lugert S. Basak O. Knuckles P. Haussler U. Fabel K. Gotz M. Haas C.A. Kempermann G. Taylor V. Giachino C. Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging Cell Stem Cell 2010 6 445 456 10.1016/j.stem.2010.03.017
Blumcke I. Schewe J.C. Normann S. Brustle O. Schramm J. Elger C.E. Wiestler O.D. Increase of nestin-immunoreactive neural precursor cells in the dentate gyrus of pediatric patients with early-onset temporal lobe epilepsy Hippocampus 2001 11 311 321 10.1002/hipo.1045 11769312
Scharfman H.E. Sollas A.L. Smith K.L. Jackson M.B. Goodman J.H. Structural and functional asymmetry in the normal and epileptic rat dentate gyrus J. Comp. Neurol. 2002 454 424 439 10.1002/cne.10449 12455007
Scharfman H.E. Gray W.P. Relevance of seizure-induced neurogenesis in animal models of epilepsy to the etiology of temporal lobe epilepsy Epilepsia 2007 48 (Suppl. 2) 33 41 10.1111/j.1528-1167.2007.01065.x 17571351
Gong C. Wang T.W. Huang H.S. Parent J.M. Reelin regulates neuronal progenitor migration in intact and epileptic hippocampus J. Neurosci. 2007 27 1803 1811 10.1523/JNEUROSCI.3111-06.2007
Bielefeld P. Dura I. Danielewicz J. Lucassen P.J. Baekelandt V. Abrous D.N. Encinas J.M. Fitzsimons C.P. Insult-induced aberrant hippocampal neurogenesis: Functional consequences and possible therapeutic strategies Behav. Brain Res. 2019 372 112032 10.1016/j.bbr.2019.112032 31199935
Scharfman H.E. Goodman J.H. Sollas A.L. Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: Functional implications of seizure-induced neurogenesis J. Neurosci. 2000 20 6144 6158 10.1523/JNEUROSCI.20-16-06144.2000
Ribak C.E. Tran P.H. Spigelman I. Okazaki M.M. Nadler J.V. Status epilepticus-induced hilar basal dendrites on rodent granule cells contribute to recurrent excitatory circuitry J. Comp. Neurol. 2000 428 240 253 10.1002/1096-9861(20001211)428:2<240::AID-CNE4>3.0.CO;2-Q
Dashtipour K. Tran P.H. Okazaki M.M. Nadler J.V. Ribak C.E. Ultrastructural features and synaptic connections of hilar ectopic granule cells in the rat dentate gyrus are different from those of granule cells in the granule cell layer Brain Res. 2001 890 261 271 10.1016/S0006-8993(00)03119-X
Jung K.H. Chu K. Kim M. Jeong S.W. Song Y.M. Lee S.T. Kim J.Y. Lee S.K. Roh J.K. Continuous cytosine-b-D-arabinofuranoside infusion reduces ectopic granule cells in adult rat hippocampus with attenuation of spontaneous recurrent seizures following pilocarpine-induced status epilepticus Eur. J. Neurosci. 2004 19 3219 3226 10.1111/j.0953-816X.2004.03412.x
Teixeira C.M. Kron M.M. Masachs N. Zhang H. Lagace D.C. Martinez A. Reillo I. Duan X. Bosch C. Pujadas L. et al. Cell-autonomous inactivation of the reelin pathway impairs adult neurogenesis in the hippocampus J. Neurosci. 2012 32 12051 12065 10.1523/JNEUROSCI.1857-12.2012 22933789
Pun R.Y. Rolle I.J. Lasarge C.L. Hosford B.E. Rosen J.M. Uhl J.D. Schmeltzer S.N. Faulkner C. Bronson S.L. Murphy B.L. et al. Excessive activation of mTOR in postnatally generated granule cells is sufficient to cause epilepsy Neuron 2012 75 1022 1034 10.1016/j.neuron.2012.08.002 22998871
Parent J.M. Valentin V.V. Lowenstein D.H. Prolonged seizures increase proliferating neuroblasts in the adult rat subventricular zone-olfactory bulb pathway J. Neurosci. 2002 22 3174 3188 10.1523/JNEUROSCI.22-08-03174.2002
Jessberger S. Parent J.M. Epilepsy and Adult Neurogenesis Cold Spring Harb. Perspect. Biol. 2015 7 a020677 10.1101/cshperspect.a020677
Araki T. Ikegaya Y. Koyama R. The effects of microglia- and astrocyte-derived factors on neurogenesis in health and disease Eur. J. Neurosci. 2021 54 5880 5901 10.1111/ejn.14969 32920880
Lybrand Z.R. Goswami S. Zhu J. Jarzabek V. Merlock N. Aktar M. Smith C. Zhang L. Varma P. Cho K.O. et al. A critical period of neuronal activity results in aberrant neurogenesis rewiring hippocampal circuitry in a mouse model of epilepsy Nat. Commun. 2021 12 1423 10.1038/s41467-021-21649-8
Zhou Q.G. Nemes A.D. Lee D. Ro E.J. Zhang J. Nowacki A.S. Dymecki S.M. Najm I.M. Suh H. Chemogenetic silencing of hippocampal neurons suppresses epileptic neural circuits J. Clin. Investig. 2019 129 310 323 10.1172/JCI95731
Varma P. Brulet R. Zhang L. Hsieh J. Targeting Seizure-Induced Neurogenesis in a Clinically Relevant Time Period Leads to Transient But Not Persistent Seizure Reduction J. Neurosci. 2019 39 7019 7028 10.1523/JNEUROSCI.0920-19.2019
Hattiangady B. Rao M.S. Shetty A.K. Chronic temporal lobe epilepsy is associated with severely declined dentate neurogenesis in the adult hippocampus Neurobiol. Dis. 2004 17 473 490 10.1016/j.nbd.2004.08.008
Bonde S. Ekdahl C.T. Lindvall O. Long-term neuronal replacement in adult rat hippocampus after status epilepticus despite chronic inflammation Eur. J. Neurosci. 2006 23 965 974 10.1111/j.1460-9568.2006.04635.x
Pineda J.R. Encinas J.M. The Contradictory Effects of Neuronal Hyperexcitation on Adult Hippocampal Neurogenesis Front. Neurosci. 2016 10 74 10.3389/fnins.2016.00074 26973452
Kralic J.E. Ledergerber D.A. Fritschy J.M. Disruption of the neurogenic potential of the dentate gyrus in a mouse model of temporal lobe epilepsy with focal seizures Eur. J. Neurosci. 2005 22 1916 1927 10.1111/j.1460-9568.2005.04386.x 16262631
Hattiangady B. Shetty A.K. Decreased neuronal differentiation of newly generated cells underlies reduced hippocampal neurogenesis in chronic temporal lobe epilepsy Hippocampus 2010 20 97 112 10.1002/hipo.20594 19309040
Muro-Garcia T. Martin-Suarez S. Espinosa N. Valcarcel-Martin R. Marinas A. Zaldumbide L. Galbarriatu L. Sierra A. Fuentealba P. Encinas J.M. Reactive Disruption of the Hippocampal Neurogenic Niche After Induction of Seizures by Injection of Kainic Acid in the Amygdala Front. Cell. Dev. Biol. 2019 7 158 10.3389/fcell.2019.00158
Mathern G.W. Leiphart J.L. De Vera A. Adelson P.D. Seki T. Neder L. Leite J.P. Seizures decrease postnatal neurogenesis and granule cell development in the human fascia dentata Epilepsia 2002 43 (Suppl. 5) 68 73 10.1046/j.1528-1157.43.s.5.28.x 12121298
Fahrner A. Kann G. Flubacher A. Heinrich C. Freiman T.M. Zentner J. Frotscher M. Haas C.A. Granule cell dispersion is not accompanied by enhanced neurogenesis in temporal lobe epilepsy patients Exp. Neurol. 2007 203 320 332 10.1016/j.expneurol.2006.08.023
Ammothumkandy A. Ravina K. Wolseley V. Tartt A.N. Yu P.N. Corona L. Zhang N. Nune G. Kalayjian L. Mann J.J. et al. Altered adult neurogenesis and gliogenesis in patients with mesial temporal lobe epilepsy Nat. Neurosci. 2022 25 493 503 10.1038/s41593-022-01044-2 35383330
Martin-Suarez S. Abiega O. Ricobaraza A. Hernandez-Alcoceba R. Encinas J.M. Alterations of the Hippocampal Neurogenic Niche in a Mouse Model of Dravet Syndrome Front. Cell. Dev. Biol. 2020 8 654 10.3389/fcell.2020.00654
Dirnagl U. Iadecola C. Moskowitz M.A. Pathobiology of ischaemic stroke: An integrated view Trends Neurosci. 1999 22 391 397 10.1016/S0166-2236(99)01401-0
Murphy T.H. Corbett D. Plasticity during stroke recovery: From synapse to behaviour Nat. Rev. Neurosci. 2009 10 861 872 10.1038/nrn2735
Johnson W. Onuma O. Owolabi M. Sachdev S. Stroke: A global response is needed Bull. World Health Organ. 2016 94 634A 10.2471/BLT.16.181636 27708464
Nakagomi T. Molnar Z. Nakano-Doi A. Taguchi A. Saino O. Kubo S. Clausen M. Yoshikawa H. Nakagomi N. Matsuyama T. Ischemia-induced neural stem/progenitor cells in the pia mater following cortical infarction Stem Cells Dev. 2011 20 2037 2051 10.1089/scd.2011.0279 21838536
Yu T.S. Washington P.M. Kernie S.G. Injury-Induced Neurogenesis: Mechanisms and Relevance Neuroscientist 2016 22 61 71 10.1177/1073858414563616
Rahman A.A. Amruta N. Pinteaux E. Bix G.J. Neurogenesis After Stroke: A Therapeutic Perspective Transl. Stroke Res. 2021 12 1 14 10.1007/s12975-020-00841-w
Jones T.A. Adkins D.L. Motor System Reorganization After Stroke: Stimulating and Training Toward Perfection Physiology 2015 30 358 370 10.1152/physiol.00014.2015
Arvidsson A. Collin T. Kirik D. Kokaia Z. Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke Nat. Med. 2002 8 963 970 10.1038/nm747 12161747
Kojima T. Hirota Y. Ema M. Takahashi S. Miyoshi I. Okano H. Sawamoto K. Subventricular zone-derived neural progenitor cells migrate along a blood vessel scaffold toward the post-stroke striatum Stem Cells 2010 28 545 554 10.1002/stem.306
Nakatomi H. Kuriu T. Okabe S. Yamamoto S. Hatano O. Kawahara N. Tamura A. Kirino T. Nakafuku M. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors Cell 2002 110 429 441 10.1016/S0092-8674(02)00862-0
Komitova M. Mattsson B. Johansson B.B. Eriksson P.S. Enriched environment increases neural stem/progenitor cell proliferation and neurogenesis in the subventricular zone of stroke-lesioned adult rats Stroke 2005 36 1278 1282 10.1161/01.STR.0000166197.94147.59
Marlier Q. Verteneuil S. Vandenbosch R. Malgrange B. Mechanisms and Functional Significance of Stroke-Induced Neurogenesis Front. Neurosci. 2015 9 458 10.3389/fnins.2015.00458
Zhang R.L. Zhang Z.G. Lu M. Wang Y. Yang J.J. Chopp M. Reduction of the cell cycle length by decreasing G1 phase and cell cycle reentry expand neuronal progenitor cells in the subventricular zone of adult rat after stroke J. Cereb. Blood Flow. Metab. 2006 26 857 863 10.1038/sj.jcbfm.9600237 16251885
Zhang R.L. Zhang Z.G. Roberts C. LeTourneau Y. Lu M. Zhang L. Wang Y. Chopp M. Lengthening the G(1) phase of neural progenitor cells is concurrent with an increase of symmetric neuron generating division after stroke J. Cereb. Blood Flow. Metab. 2008 28 602 611 10.1038/sj.jcbfm.9600556 17928800
Zhang R.L. Zhang Z.G. Chopp M. Ischemic stroke and neurogenesis in the subventricular zone Neuropharmacology 2008 55 345 352 10.1016/j.neuropharm.2008.05.027 18632119
Lichtenwalner R.J. Parent J.M. Adult neurogenesis and the ischemic forebrain J. Cereb. Blood Flow. Metab. 2006 26 1 20 10.1038/sj.jcbfm.9600170
Woitke F. Ceanga M. Rudolph M. Niv F. Witte O.W. Redecker C. Kunze A. Keiner S. Adult hippocampal neurogenesis poststroke: More new granule cells but aberrant morphology and impaired spatial memory PLoS ONE 2017 12 e0183463 10.1371/journal.pone.0183463
Niv F. Keiner S. Krishna Witte O.W. Lie D.C. Redecker C. Aberrant neurogenesis after stroke: A retroviral cell labeling study Stroke 2012 43 2468 2475 10.1161/STROKEAHA.112.660977
Faiz M. Sachewsky N. Gascon S. Bang K.W. Morshead C.M. Nagy A. Adult Neural Stem Cells from the Subventricular Zone Give Rise to Reactive Astrocytes in the Cortex after Stroke Cell Stem Cell 2015 17 624 634 10.1016/j.stem.2015.08.002
He T. Yang G.Y. Zhang Z. Crosstalk of Astrocytes and Other Cells during Ischemic Stroke Life 2022 12 910 10.3390/life12060910
Patabendige A. Singh A. Jenkins S. Sen J. Chen R. Astrocyte Activation in Neurovascular Damage and Repair Following Ischaemic Stroke Int. J. Mol. Sci. 2021 22 4280 10.3390/ijms22084280
Wang L. Chopp M. Zhang R.L. Zhang L. Letourneau Y. Feng Y.F. Jiang A. Morris D.C. Zhang Z.G. The Notch pathway mediates expansion of a progenitor pool and neuronal differentiation in adult neural progenitor cells after stroke Neuroscience 2009 158 1356 1363 10.1016/j.neuroscience.2008.10.064
Carlen M. Meletis K. Goritz C. Darsalia V. Evergren E. Tanigaki K. Amendola M. Barnabe-Heider F. Yeung M.S. Naldini L. et al. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke Nat. Neurosci. 2009 12 259 267 10.1038/nn.2268
Xiao M.J. Han Z. Shao B. Jin K. Notch signaling and neurogenesis in normal and stroke brain Int. J. Physiol. Pathophysiol. Pharm. 2009 1 192 202
Li Z. Wang J. Zhao C. Ren K. Xia Z. Yu H. Jiang K. Acute Blockage of Notch Signaling by DAPT Induces Neuroprotection and Neurogenesis in the Neonatal Rat Brain After Stroke Transl. Stroke Res. 2016 7 132 140 10.1007/s12975-015-0441-7 26691164
Santopolo G. Magnusson J.P. Lindvall O. Kokaia Z. Frisen J. Blocking Notch-Signaling Increases Neurogenesis in the Striatum after Stroke Cells 2020 9 1732 10.3390/cells9071732 32698472
Falcon-Urrutia P. Carrasco C.M. Lois P. Palma V. Roth A.D. Shh Signaling through the Primary Cilium Modulates Rat Oligodendrocyte Differentiation PLoS ONE 2015 10 e0133567 10.1371/journal.pone.0133567 26218245
Liu L. Zhao B. Xiong X. Xia Z. The Neuroprotective Roles of Sonic Hedgehog Signaling Pathway in Ischemic Stroke Neurochem. Res. 2018 43 2199 2211 10.1007/s11064-018-2645-1
Dai R.L. Zhu S.Y. Xia Y.P. Mao L. Mei Y.W. Yao Y.F. Xue Y.M. Hu B. Sonic hedgehog protects cortical neurons against oxidative stress Neurochem. Res. 2011 36 67 75 10.1007/s11064-010-0264-6
Jin Y. Raviv N. Barnett A. Bambakidis N.C. Filichia E. Luo Y. The shh signaling pathway is upregulated in multiple cell types in cortical ischemia and influences the outcome of stroke in an animal model PLoS ONE 2015 10 e0124657 10.1371/journal.pone.0124657
Macas J. Nern C. Plate K.H. Momma S. Increased generation of neuronal progenitors after ischemic injury in the aged adult human forebrain J. Neurosci. 2006 26 13114 13119 10.1523/JNEUROSCI.4667-06.2006
Carroll L.J. Cassidy J.D. Holm L. Kraus J. Coronado V.G. WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury Methodological issues and research recommendations for mild traumatic brain injury: The WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury J. Rehabil. Med. 2004 43 113 125 10.1080/16501960410023877
Menon D.K. Schwab K. Wright D.W. Maas A.I. Position statement: Definition of traumatic brain injury Arch. Phys. Med. Rehabil. 2010 91 1637 1640 10.1016/j.apmr.2010.05.017 21044706
Maas A.I. Traumatic brain injury in India: A big problem in need of data Neurol. India 2017 65 257 258 10.4103/0028-3886.201848 28290383
Mendez M.F. What is the Relationship of Traumatic Brain Injury to Dementia? J. Alzheimers Dis. 2017 57 667 681 10.3233/JAD-161002 28269777
van Gils A. Stone J. Welch K. Davidson L.R. Kerslake D. Caesar D. McWhirter L. Carson A. Management of mild traumatic brain injury Pr. Neurol. 2020 20 213 221 10.1136/practneurol-2018-002087
Wilson L. Stewart W. Dams-O’Connor K. Diaz-Arrastia R. Horton L. Menon D.K. Polinder S. The chronic and evolving neurological consequences of traumatic brain injury Lancet Neurol. 2017 16 813 825 10.1016/S1474-4422(17)30279-X
Rosenfeld J.V. Maas A.I. Bragge P. Morganti-Kossmann M.C. Manley G.T. Gruen R.L. Early management of severe traumatic brain injury Lancet 2012 380 1088 1098 10.1016/S0140-6736(12)60864-2
Badner A. Cummings B.J. The endogenous progenitor response following traumatic brain injury: A target for cell therapy paradigms Neural Regen. Res. 2022 17 2351 2354 10.4103/1673-5374.335833
Sun D. Endogenous neurogenic cell response in the mature mammalian brain following traumatic injury Exp. Neurol. 2016 275 405 410 10.1016/j.expneurol.2015.04.017
Fallon J. Reid S. Kinyamu R. Opole I. Opole R. Baratta J. Korc M. Endo T.L. Duong A. Nguyen G. et al. In vivo induction of massive proliferation, directed migration, and differentiation of neural cells in the adult mammalian brain Proc. Natl. Acad. Sci. USA 2000 97 14686 14691 10.1073/pnas.97.26.14686
Jin K. Minami M. Lan J.Q. Mao X.O. Batteur S. Simon R.P. Greenberg D.A. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat Proc. Natl. Acad. Sci. USA 2001 98 4710 4715 10.1073/pnas.081011098
Liu J. Solway K. Messing R.O. Sharp F.R. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils J. Neurosci. 1998 18 7768 7778 10.1523/JNEUROSCI.18-19-07768.1998 9742147
Romero-Grimaldi C. Murillo-Carretero M. Lopez-Toledano M.A. Carrasco M. Castro C. Estrada C. ADAM-17/tumor necrosis factor-alpha-converting enzyme inhibits neurogenesis and promotes gliogenesis from neural stem cells Stem Cells 2011 29 1628 1639 10.1002/stem.710
Buffo A. Rite I. Tripathi P. Lepier A. Colak D. Horn A.P. Mori T. Gotz M. Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain Proc. Natl. Acad. Sci. USA 2008 105 3581 3586 10.1073/pnas.0709002105 18299565
Dominguez-Garcia S. Geribaldi-Doldan N. Gomez-Oliva R. Ruiz F.A. Carrascal L. Bolivar J. Verastegui C. Garcia-Alloza M. Macias-Sanchez A.J. Hernandez-Galan R. et al. A novel PKC activating molecule promotes neuroblast differentiation and delivery of newborn neurons in brain injuries Cell. Death Dis. 2020 11 262 10.1038/s41419-020-2453-9 32321920
Villasana L.E. Kim K.N. Westbrook G.L. Schnell E. Functional Integration of Adult-Born Hippocampal Neurons after Traumatic Brain Injury(1,2,3) eNeuro 2015 2 10.1523/ENEURO.0056-15.2015 26478908
Blaiss C.A. Yu T.S. Zhang G. Chen J. Dimchev G. Parada L.F. Powell C.M. Kernie S.G. Temporally specified genetic ablation of neurogenesis impairs cognitive recovery after traumatic brain injury J. Neurosci. 2011 31 4906 4916 10.1523/JNEUROSCI.5265-10.2011 21451029
Richardson R.M. Sun D. Bullock M.R. Neurogenesis after traumatic brain injury Neurosurg. Clin. N. Am. 2007 18 169 181 10.1016/j.nec.2006.10.007
Gao X. Chen J. Moderate traumatic brain injury promotes neural precursor proliferation without increasing neurogenesis in the adult hippocampus Exp. Neurol. 2013 239 38 48 10.1016/j.expneurol.2012.09.012
Ortiz-Lopez L. Vega-Rivera N.M. Babu H. Ramirez-Rodriguez G.B. Brain-Derived Neurotrophic Factor Induces Cell Survival and the Migration of Murine Adult Hippocampal Precursor Cells During Differentiation In Vitro Neurotox. Res. 2017 31 122 135 10.1007/s12640-016-9673-x
Wang Y. Teng H.L. Gao Y. Zhang F. Ding Y.Q. Huang Z.H. Brain-derived Neurotrophic Factor Promotes the Migration of Olfactory Ensheathing Cells Through TRPC Channels Glia 2016 64 2154 2165 10.1002/glia.23049
Carabalona A. Hu D.J. Vallee R.B. KIF1A inhibition immortalizes brain stem cells but blocks BDNF-mediated neuronal migration Nat. Neurosci. 2016 19 253 262 10.1038/nn.4213 26752160
Zhou Y. Oudin M.J. Gajendra S. Sonego M. Falenta K. Williams G. Lalli G. Doherty P. Regional effects of endocannabinoid, BDNF and FGF receptor signalling on neuroblast motility and guidance along the rostral migratory stream Mol. Cell. Neurosci. 2015 64 32 43 10.1016/j.mcn.2014.12.001 25481343
Manivannan S. Marei O. Elalfy O. Zaben M. Neurogenesis after traumatic brain injury—The complex role of HMGB1 and neuroinflammation Neuropharmacology 2021 183 108400 10.1016/j.neuropharm.2020.108400 33189765
Braun H. Schafer K. Hollt V. BetaIII tubulin-expressing neurons reveal enhanced neurogenesis in hippocampal and cortical structures after a contusion trauma in rats J. Neurotrauma 2002 19 975 983 10.1089/089771502320317122
Itoh T. Satou T. Hashimoto S. Ito H. Isolation of neural stem cells from damaged rat cerebral cortex after traumatic brain injury Neuroreport 2005 16 1687 1691 10.1097/01.wnr.0000183330.44112.ab
Grade S. Götz M. Neuronal replacement therapy: Previous achievements and challenges ahead NPJ Regen. Med. 2017 2 29 10.1038/s41536-017-0033-0
Sivandzade F. Cucullo L. Regenerative stem cell therapy for neurodegenerative diseases: An overview Int. J. Mol. Sci. 2021 22 2153 10.3390/ijms22042153
Guo Z. Zhang L. Wu Z. Chen Y. Wang F. Chen G. In vivo direct reprogramming of reactive glial cells into functional neurons after brain injury and in an Alzheimer’s disease model Cell Stem Cell 2014 14 188 202 10.1016/j.stem.2013.12.001
Niu W. Zang T. Smith D.K. Vue T.Y. Zou Y. Bachoo R. Johnson J.E. Zhang C.L. SOX2 reprograms resident astrocytes into neural progenitors in the adult brain Stem Cell Rep. 2015 4 780 794 10.1016/j.stemcr.2015.03.006
Fon D. Al-Abboodi A. Chan P.P. Zhou K. Crack P. Finkelstein D.I. Forsythe J.S. Effects of GDNF-loaded injectable gelatin-based hydrogels on endogenous neural progenitor cell migration Adv. Heal. Mater. 2014 3 761 774 10.1002/adhm.201300287
Fon D. Zhou K. Ercole F. Fehr F. Marchesan S. Minter M.R. Crack P.J. Finkelstein D.I. Forsythe J.S. Nanofibrous scaffolds releasing a small molecule BDNF-mimetic for the re-direction of endogenous neuroblast migration in the brain Biomaterials 2014 35 2692 2712 10.1016/j.biomaterials.2013.12.016 24406218
Cook D.J. Nguyen C. Chun H.N. Llorente I.L. Chiu A.S. Machnicki M. Zarembinski T.I. Carmichael S.T. Hydrogel-delivered brain-derived neurotrophic factor promotes tissue repair and recovery after stroke J. Cereb. Blood Flow. Metab. 2017 37 1030 1045 10.1177/0271678X16649964 27174996
Nakaguchi K. Jinnou H. Kaneko N. Sawada M. Hikita T. Saitoh S. Tabata Y. Sawamoto K. Growth factors released from gelatin hydrogel microspheres increase new neurons in the adult mouse brain Stem Cells Int. 2012 2012 915160 10.1155/2012/915160 23093979
Kobayashi T. Ahlenius H. Thored P. Kobayashi R. Kokaia Z. Lindvall O. Intracerebral infusion of glial cell line-derived neurotrophic factor promotes striatal neurogenesis after stroke in adult rats Stroke 2006 37 2361 2367 10.1161/01.STR.0000236025.44089.e1 16873711
Teramoto T. Qiu J. Plumier J.C. Moskowitz M.A. EGF amplifies the replacement of parvalbumin-expressing striatal interneurons after ischemia J. Clin. Investig. 2003 111 1125 1132 10.1172/JCI200317170 12697732
Sun Y. Jin K. Xie L. Childs J. Mao X.O. Logvinova A. Greenberg D.A. VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia J. Clin. Investig. 2003 111 1843 1851 10.1172/JCI200317977
Filippo T.R. Galindo L.T. Barnabe G.F. Ariza C.B. Mello L.E. Juliano M.A. Juliano L. Porcionatto M.A. CXCL12 N-terminal end is sufficient to induce chemotaxis and proliferation of neural stem/progenitor cells Stem Cell Res. 2013 11 913 925 10.1016/j.scr.2013.06.003
Lim D.A. Tramontin A.D. Fau–Trevejo J.M. Herrera D.G. García-Verdugo J.M. Alvarez-Buylla A. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis Neuron 2000 28 713 726 10.1016/S0896-6273(00)00148-3
Tang J. Song M. Wang Y. Fan X. Xu H. Bai Y. Noggin and BMP4 co-modulate adult hippocampal neurogenesis in the APP(swe)/PS1(DeltaE9) transgenic mouse model of Alzheimer’s disease Biochem. Biophys. Res. Commun. 2009 385 341 345 10.1016/j.bbrc.2009.05.067
Zhang C. Chopp M. Cui Y. Wang L. Zhang R. Zhang L. Lu M. Szalad A. Doppler E. Hitzl M. et al. Cerebrolysin enhances neurogenesis in the ischemic brain and improves functional outcome after stroke J. Neurosci. Res. 2010 88 3275 3281 10.1002/jnr.22495
Cui X. Chen J. Zacharek A. Roberts C. Yang Y. Chopp M. Nitric oxide donor up-regulation of SDF1/CXCR4 and Ang1/Tie2 promotes neuroblast cell migration after stroke J. Neurosci. Res. 2009 87 86 95 10.1002/jnr.21836
Calio M.L. Mosini A.C. Marinho D.S. Salles G.N. Massinhani F.H. Ko G.M. Porcionatto M.A. Leptin enhances adult neurogenesis and reduces pathological features in a transgenic mouse model of Alzheimer’s disease Neurobiol. Dis. 2021 148 105219 10.1016/j.nbd.2020.105219 33301880
Ge W. Ren C. Xing L. Guan L. Zhang C. Sun X. Wang G. Niu H. Qun S. Ginkgo biloba extract improves cognitive function and increases neurogenesis by reducing Abeta pathology in 5xFAD mice Am. J. Transl. Res. 2021 13 1471 1482 33841671
Han J. Pollak J. Yang T. Siddiqui M.R. Doyle K.P. Taravosh-Lahn K. Cekanaviciute E. Han A. Goodman J.Z. Jones B. et al. Delayed administration of a small molecule tropomyosin-related kinase B ligand promotes recovery after hypoxic-ischemic stroke Stroke 2012 43 1918 1924 10.1161/STROKEAHA.111.641878
Chen D. Wei L. Liu Z.R. Yang J.J. Gu X. Wei Z.Z. Liu L.P. Yu S.P. Pyruvate Kinase M2 Increases Angiogenesis, Neurogenesis, and Functional Recovery Mediated by Upregulation of STAT3 and Focal Adhesion Kinase Activities After Ischemic Stroke in Adult Mice Neurotherapeutics 2018 15 770 784 10.1007/s13311-018-0635-2
Dominguez-Garcia S. Gomez-Oliva R. Geribaldi-Doldan N. Hierro-Bujalance C. Sendra M. Ruiz F.A. Carrascal L. Macias-Sanchez A.J. Verastegui C. Hernandez-Galan R. et al. Effects of classical PKC activation on hippocampal neurogenesis and cognitive performance: Mechanism of action Neuropsychopharmacology 2021 46 1207 1219 10.1038/s41386-020-00934-y
Geribaldi-Doldan N. Gomez-Oliva R. Dominguez-Garcia S. Nunez-Abades P. Castro C. Protein Kinase C: Targets to Regenerate Brain Injuries? Front. Cell. Dev. Biol. 2019 7 39 10.3389/fcell.2019.00039
Garcia-Bernal F. Geribaldi-Doldan N. Dominguez-Garcia S. Carrasco M. Murillo-Carretero M. Delgado-Ariza A. Diez-Salguero M. Verastegui C. Castro C. Protein Kinase C Inhibition Mediates Neuroblast Enrichment in Mechanical Brain Injuries Front. Cell. Neurosci. 2018 12 462 10.3389/fncel.2018.00462 30542270
Geribaldi-Doldan N. Flores-Giubi E. Murillo-Carretero M. Garcia-Bernal F. Carrasco M. Macias-Sanchez A.J. Dominguez-Riscart J. Verastegui C. Hernandez-Galan R. Castro C. 12-Deoxyphorbols Promote Adult Neurogenesis by Inducing Neural Progenitor Cell Proliferation via PKC Activation Int. J. Neuropsychopharmacol. 2015 19 pyv085 10.1093/ijnp/pyv085 26224011
Murillo-Carretero M. Geribaldi-Doldan N. Flores-Giubi E. Garcia-Bernal F. Navarro-Quiroz E.A. Carrasco M. Macias-Sanchez A.J. Herrero-Foncubierta P. Delgado-Ariza A. Verastegui C. et al. ELAC (3,12-di-O-acetyl-8-O-tigloilingol), a plant-derived lathyrane diterpene, induces subventricular zone neural progenitor cell proliferation through PKCbeta activation Br. J. Pharm. 2017 174 2373 2392 10.1111/bph.13846
Gómez-Oliva R. Martínez-Ortega S. Atienza-Navarro I. Domínguez-García S. Bernal C. Geribaldi-Doldán N. Verástegui C. Ezzanad A. Hernández-Galán R. Núnez-Abades P. et al. Rescue of neurogenesis and age-associated cognitive decline in SAMP8 mouse: Role of transforming growth factor alpha bioRxiv 2023 10.1101/2023.01.14.524036