- -

Adult Neural Stem Cell Migration Is Impaired in a Mouse Model of Alzheimer's Disease

RiuNet: Institutional repository of the Polithecnic University of Valencia

Share/Send to

Cited by

Statistics

  • Estadisticas de Uso

Adult Neural Stem Cell Migration Is Impaired in a Mouse Model of Alzheimer's Disease

Show full item record

Esteve, D.; Molina-Navarro, MM.; Giraldo-Reboloso, E.; Martínez-Varea, N.; Blanco-Gandia, MC.; Rodríguez-Arias, M.; García-Verdugo, JM.... (2022). Adult Neural Stem Cell Migration Is Impaired in a Mouse Model of Alzheimer's Disease. Molecular Neurobiology. 59(2):1168-1182. https://doi.org/10.1007/s12035-021-02620-6

Por favor, use este identificador para citar o enlazar este ítem: http://hdl.handle.net/10251/195605

Files in this item

Item Metadata

Title: Adult Neural Stem Cell Migration Is Impaired in a Mouse Model of Alzheimer's Disease
Author: Esteve, Daniel Molina-Navarro, María Micaela Giraldo-Reboloso, Esther Martínez-Varea, Noelia Blanco-Gandia, Mari Carmen Rodríguez-Arias, Marta García-Verdugo, Jose Manuel Viña, José Lloret, Ana
UPV Unit: Universitat Politècnica de València. Escuela Técnica Superior de Ingeniería Agronómica y del Medio Natural - Escola Tècnica Superior d'Enginyeria Agronòmica i del Medi Natural
Issued date:
Abstract:
[EN] Neurogenesis in the adult brain takes place in two neurogenic niches: the ventricular-subventricular zone (V-SVZ) and the subgranular zone. After differentiation, neural precursor cells (neuroblasts) have to move to ...[+]
Subjects: Subventricular zone , Beta-amyloid toxicity , Neurogenesis , Senescence , Olfaction
Copyrigths: Reconocimiento (by)
Source:
Molecular Neurobiology. (issn: 0893-7648 )
DOI: 10.1007/s12035-021-02620-6
Publisher:
Springer-Verlag
Publisher version: https://doi.org/10.1007/s12035-021-02620-6
Project ID:
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-110906RB-I00/ES/NUEVAS INTERVENCIONES TERAPEUTICAS MULTIDOMINIO PARA RETRASAR LA FRAGILIDAD Y LA DISCAPACIDAD. IDENTIFICACION DE MECANISMOS MOLECULARES CON RELEVANCIA TRASLACIONAL/
...[+]
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-110906RB-I00/ES/NUEVAS INTERVENCIONES TERAPEUTICAS MULTIDOMINIO PARA RETRASAR LA FRAGILIDAD Y LA DISCAPACIDAD. IDENTIFICACION DE MECANISMOS MOLECULARES CON RELEVANCIA TRASLACIONAL/
info:eu-repo/grantAgreement/GVA//PROMETEO%2F2019%2F097/
info:eu-repo/grantAgreement/EC/H2020/696295/EU
info:eu-repo/grantAgreement/ISCIII//CB16%2F10%2F00435//CIBER-FES/
info:eu-repo/grantAgreement/EC/H2020/825546/EU
info:eu-repo/grantAgreement/UV//UV-INV-AE-1546096/
[-]
Thanks:
Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature. This work was supported by the following grants: Instituto de Salud Carlos III CB16/10/00435 (CIBER-FES), (PID2019-110906RB-I00/AEI/10. ...[+]
Type: Artículo

References

Alvarez-Buylla A, Garcia-Verdugo JM (2002) Neurogenesis in adult subventricular zone. J Neurosci 22(3):629–634

Christian KM, Song H, Ming GL (2014) Functions and dysfunctions of adult hippocampal neurogenesis. Annu Rev Neurosci 37:243–262

Fares J, Bou Diab Z, Nabha S, Fares Y (2019) Neurogenesis in the adult hippocampus: history, regulation, and prospective roles. Int J Neurosci 129(6):598–611 [+]
Alvarez-Buylla A, Garcia-Verdugo JM (2002) Neurogenesis in adult subventricular zone. J Neurosci 22(3):629–634

Christian KM, Song H, Ming GL (2014) Functions and dysfunctions of adult hippocampal neurogenesis. Annu Rev Neurosci 37:243–262

Fares J, Bou Diab Z, Nabha S, Fares Y (2019) Neurogenesis in the adult hippocampus: history, regulation, and prospective roles. Int J Neurosci 129(6):598–611

Obernier K, Alvarez-Buylla A (2019) Neural stem cells: origin, heterogeneity and regulation in the adult mammalian brain. Development. 146(4): dev156059.

Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A (2002) EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36(6):1021–1034

Doetsch F, García-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17(13):5046–5061

Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264(5162):1145–1148

Ernst A, Alkass K, Bernard S, Salehpour M, Perl S, Tisdale J et al (2014) Neurogenesis in the striatum of the adult human brain. Cell 156(5):1072–1083

García-González D, Dumitru I, Zuccotti A, Yen TY, Herranz-Pérez V, Tan, LL, et al (2020) Neurogenesis of medium spiny neurons in the nucleus accumbens continues into adulthood and is enhanced by pathological pain. Mol Psychiatry 26(9):4616-4632

Sohn J, Orosco L, Guo F, Chung SH, Bannerman P, Ko EM et al (2015) The subventricular zone continues to generate corpus callosum and rostral migratory stream astroglia in normal adult mice. J Neurosci 35(9):3756–3763

Muñoz-Espín D, Serrano M (2014) Cellular senescence: from physiology to pathology. Nat Rev Mol Cell Biol 15:482–496

Dimri GP, Campisi J (1994) Molecular and cell biology of replicative senescence. Cold Spring Harb Symp Quant Biol 59:67–73

Kurz DJ, Decary S, Hong Y, Erusalimsky JD (2000) Senescence-associated β-galactosidase reflects an increase in lysosomal mass during replicative ageing of human endothelial cells. J Cell Sci 113(20):3613–3622

Becker RE, Greig NH, Giacobini E (2008) Why do so many drugs for Alzheimer’s disease fail in development? Time for new methods and new practices? J Alzheimers Dis 15:303–325

Tobin MK, Musaraca K, Disouky A, Shetti A, Bheri A, Honer WG et al (2019) Human hippocampal neurogenesis persists in aged adults and Alzheimer’s disease patients. Cell Stem Cell. 24(6):974-982e3

Haughey NJ, Nath A, Chan SL, Borchard AC, Rao MS, Mattson MP (2002) Disruption of neurogenesis by amyloid β-peptide, and perturbed neural progenitor cell homeostasis, in models of Alzheimer’s disease. J Neurochem 83(6):1509–1524

He P, Shen Y (2009) Interruption of β-catenin signaling reduces neurogenesis in Alzheimer’s disease. J Neurosci 29(20):6545–6557

Rodríguez JJ, Jones VC, Verkhratsky A (2009) Impaired cell proliferation in the subventricular zone in an Alzheimer’s disease model. NeuroReport 20(10):907–912

Tang J, Song M, Wang Y, Fan X, Xu H, Bai Y (2009) Noggin and BMP4 co-modulate adult hippocampal neurogenesis in the APPswe/PS1ΔE9 transgenic mouse model of Alzheimer’s disease. Biochem Biophys Res Commun 385(3):341–345

Moreno-Jiménez EP, Flor-García M, Terreros-Roncal J, Rábano A, Cafini F, Pallas-Bazarra N et al (2019) Adult hippocampal neurogenesis is abundant in neurologically healthy subjects and drops sharply in patients with Alzheimer’s disease. Nat Med 25(4):554–560

Sorrells SF, Paredes MF, Cebrian-Silla A, Sandoval K, Qi D, Kelley KW et al (2018) Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults. Nature 555(7696):377–381

Teplow DB (2006) Preparation of amyloid β-protein for structural and functional studies. Methods Enzymol 413:20–33

ElAli A, Thériault P, Préfontaine P, Rivest S (2013) Mild chronic cerebral hypoperfusion induces neurovascular dysfunction, triggering peripheral beta-amyloid brain entry and aggregation. Acta Neuropathol Commun 1(1):75

Faucher P, Mons N, Micheau J, Louis C, Beracochea DJ (2016) Hippocampal injections of oligomeric amyloid β-peptide (1–42) induce selective working memory deficits and long-lasting alterations of ERK signaling pathway. Aging Neurosci 7:1–15

Harkany T, Ábrahám I, Timmerman W, Laskay G, Tóth B, Sasvári M et al (2000) β-Amyloid neurotoxicity is mediated by a glutamate-triggered excitotoxic cascade in rat nucleus basalis. Eur J Neurosci 12(8):2735–2745

Prediger RDS, Franco JL, Pandolfo P, Medeiros R, Duarte FS, Di Giunta G et al (2007) Differential susceptibility following β-amyloid peptide-(1–40) administration in C57BL/6 and Swiss albino mice: evidence for a dissociation between cognitive deficits and the glutathione system response. Behav Brain Res 177(2):205–213

Guo H, Aleyasin H, Howard SS, Dickinson BC, Lin VS, Haskew-Layton RE et al (2013) Two-photon fluorescence imaging of intracellular hydrogen peroxide with chemoselective fluorescent probes. J Biomed Opt 18(10):106002

Moser B, Hochreiter B, Herbst R, Schmid JA (2017) Fluorescence colocalization microscopy analysis can be improved by combining object-recognition with pixel-intensity-correlation. Biotechnol J. 12(1): 1600332

Wesson DW, Levy E, Nixon RA, Wilson DA (2010) Olfactory dysfunction correlates with amyloid-beta burden in an Alzheimer’s disease mouse model. J Neurosci 30:505–514

Sundberg H, Doving K, Novikov S, Ursin H (1982) A method for studying responses and habituation to odors in rats. Behav Neural Biol 34:113–119

Burma S, Chen BP, Murphy M, Kurimasa A, Chen DJ (2001) ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem 276(45):42462–42467

Kieroń M, Żekanowski C, Falk A, Wężyk M (2019) Oxidative DNA damage signalling in neural stem cells in Alzheimer’s disease. Oxid Med Cell Longev 2019:2149812

Sedelnikova OA, Pilch DR, Redon C, Bonner WM (2003) Histone H2AX in DNA damage and repair. Cancer Biol Ther 2:233–235

Myung NH, Zhu X, Kruman II, Castellani RJ, Petersen RB, Siedlak SL et al (2008) Evidence of DNA damage in Alzheimer disease: phosphorylation of histone H2AX in astrocytes. Age 30(4):209–215

Lloret A, Badía MC, Mora NJ, Ortega A, Pallardó FV, Alonso MD et al (2008) Gender and age-dependent differences in the mitochondrial apoptogenic pathway in Alzheimer’s disease. Free Radic Biol Med 44(12):2019–2025

He ZY, Wang WY, Hu WY, Yang L, Li Y, Zhang WY et al (2016) Gamma-H2AX upregulation caused by Wip1 deficiency increases depression-related cellular senescence in hippocampus. Sci Rep 6:34558

Hovest MG, Brüggenolte N, Hosseini KS, Krieg T (2006) Herrmann, G Senescence of human fibroblasts after psoralen photoactivation is mediated by ATR kinase and persistent DNA damage foci at telomeres. Mol Biol Cell 17(4):1758–1767

Pospelova TV, Demidenko ZN, Bukreeva EI, Pospelov VA, Gudkov AV (2009) Blagosklonny MV Pseudo-DNA damage response in senescent cells. Cell Cycle 8:4112–4118

Lim DA, Alvarez-buylla A (2016) The adult ventricular – subventricular zone. Cold Spring Harb Perspect Biol 8(5):a018820

Scopa C, Marrocco F, Latina V, Ruggeri F, Corvaglia V, La Regina F et al (2020) Impaired adult neurogenesis is an early event in Alzheimer’s disease neurodegeneration, mediated by intracellular Aβ oligomers. Cell Death Differ 27(3):934–948

da Cunha BR, Domingos C, Buzzo Stefanini AC, Henrique T, Polachini GM, Castelo-Branco P, Tajara EH (2019) Cellular interactions in the tumor microenvironment: the role of secretome. J Cancer 10:4574–4587

Rodier F, Campisi J (2011) Four faces of cellular senescence. J Cell Biol 192:547–556

Wilkinson HN, Hardman MJ (2020) Senescence in wound repair: emerging strategies to target chronic healing wounds. Front Cell Dev Biol 8:773

Kojima T, Hirota Y, Ema M, Takahashi S, Miyoshi I, Okano H, Sawamoto K (2010) Subventricular zone-derived neural progenitor cells migrate along a blood vessel scaffold toward the post-stroke striatum. Stem Cells. 28(3): 545-554

de Boer HR, Guerrero Llobet S, van Vugt MA (2016) Controlling the response to DNA damage by the APC/C-Cdh1. Cell Mol Life Sci 73(5):949–960

Ha K, Ma C, Lin H, Tang L, Lian Z, Zhao F et al (2017) The anaphase promoting complex impacts repair choice by protecting ubiquitin signalling at DNA damage sites. Nat Commun 8(1):15751

Lara-Gonzalez P, Kim T, Desai A (2017) Taming the beast: control of APC/CCdc20-dependent destruction. Cold Spring Harb Symp Quant Biol 82:111–121

Takahashi A, Imai Y, Yamakoshi K, Kuninaka S, Ohtani N, Yoshimoto S et al (2012) DNA damage signaling triggers degradation of histone methyltransferases through APC/C Cdh1 in senescent cells. Mol Cell 45(1):123–131

Feringa FM, Krenning L, Koch A, Van Den Berg J, Van Den Broek B, Jalink K, Medema RH (2016) Hypersensitivity to DNA damage in antephase as a safeguard for genome stability. Nat Commun 7:12618

Zhang J, Li H, Zhou T, Zhou J, Herrup K (2012) Cdk5 levels oscillate during the neuronal cell cycle: Cdh1 ubiquitination triggers proteosome-dependent degradation during S-phase. J Biol Chem 287(31):25985–25994

Almeida A, Bolaños JP, Moreno S (2005) Cdh1/Hct1-APC is essential for the survival of postmitotic neurons. J Neurosci 25(36):8115–8121

Maestre C, Delgado-Esteban M, Gomez-Sanchez JC, Bolaños JP, Almeida A (2008) Cdk5 phosphorylates Cdh1 and modulates cyclin B1 stability in excitotoxicity. EMBO J 27(20):2736–2745

Ayala R, Shu T, Tsai L-H (2007) Trekking across the brain: the journey of neuronal migration. Cell 128(1):29–43

Schneider L, Pellegatta S, Favaro R, Pisati F, Roncaglia P, Testa G et al (2013) DNA damage in mammalian neural stem cells leads to astrocytic differentiation mediated by BMP2 signaling through JAK-STAT. Stem Cell Rep 1(2):123–138

Schneider L (2014) Survival of neural stem cells undergoing dna damage-induced astrocytic differentiation in self-renewal-promoting conditions in vitro. PLoS ONE 9(1):e87228

Zhan JS, Gao K, Chai RC, Jia XH, Luo DP, Ge G et al (2017) Astrocytes in migration. Neurochem Res 42(1):272–282

Devanand DP, Michaels-Marston KS, Liu X, Pelton GH, Padilla M, Marder K et al (2000) Olfactory deficits in patients with mild cognitive impairment predict Alzheimer’s disease at follow-up. Am J Psychiatry 157(9):1399–1405

Velayudhan L, Pritchard M, Powell JF, Proitsi P, Lovestone S (2013) Smell identification function as a severity and progression marker in Alzheimer’s disease. Int Psychogeriatr 25(7):1157–1166

Yu Q, Guo P, Li D, Zuo L, Lian T, Yu S et al (2018) Olfactory dysfunction and its relationship with clinical symptoms of Alzheimer disease. Aging Dis 9(6):1084–1095

Wang C, Liu F, Liu Y-Y, Zhao C-H, You Y, Wang L et al (2011) Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain. Cell Res 21(11):1534–1550

Ardekani BA, Bachman AH, Figarsky K, Sidtis JJ (2014) Corpus callosum shape changes in early Alzheimer’s disease: an MRI study using the OASIS brain database. Brain Struct Funct 219(1):343–352

Benedicte M, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A (2006) Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 26:7907–7918

Mizrak D, Levitin HM, Delgado AC, Crotet V, Yuan J, Chaker Z et al (2019) Single-cell analysis of regional differences in adult V-SVZ neural stem cell lineages. Cell Rep 26(2):394-406e5

Selden N, Mesulam MM, Geula C (1994) Human striatum: the distribution of neurofibrillary tangles in Alzheimer’s disease. Brain Res 648(2):327–331

Pulakat L, Chen HH (2020) Pro-senescence and anti-senescence mechanisms of cardiovascular aging: cardiac MicroRNA regulation of longevity drug-induced autophagy. Front Pharmacol 11:774

Rodríguez-Matellán A, Alcazar N, Hernández F, Serrano M, Ávila J (2020) In vivo reprogramming ameliorates aging features in dentate gyrus cells and improves memory in mice. Stem Cell Rep 15(5):1056–1066

Zhang P, Kishimoto Y, Grammatikakis I, Gottimukkala K, Cutler RG, Zhang S et al (2019) Senolytic therapy alleviates Aβ-associated oligodendrocyte progenitor cell senescence and cognitive deficits in an Alzheimer’s disease model. Nat Neurosci 22(5):719–728

[-]

recommendations

 

This item appears in the following Collection(s)

Show full item record