Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal.
paper
Cited
Public
- Authors
- Aguirre, Adan; Rubio, Maria E; Gallo, Vittorio
- Year
- 2010
- Journal
- Nature
- PMID
- 20844536
- DOI
- 10.1038/nature09347
- PMCID
- PMC2941915
Specialized cellular microenvironments, or 'niches', modulate stem cell properties, including cell number, self-renewal and fate decisions. In the adult brain, niches that maintain a source of neural stem cells (NSCs) and neural progenitor cells (NPCs) are the subventricular zone (SVZ) of the lateral ventricle and the dentate gyrus of the hippocampus. The size of the NSC population of the SVZ at any time is the result of several ongoing processes, including self-renewal, cell differentiation, and cell death. Maintaining the balance between NSCs and NPCs in the SVZ niche is critical to supply the brain with specific neural populations, both under normal conditions or after injury. A fundamental question relevant to both normal development and to cell-based repair strategies in the central nervous system is how the balance of different NSC and NPC populations is maintained in the niche. EGFR (epidermal growth factor receptor) and Notch signalling pathways have fundamental roles during development of multicellular organisms. In Drosophila and in Caenorhabditis elegans these pathways may have either cooperative or antagonistic functions. In the SVZ, Notch regulates NSC identity and self-renewal, whereas EGFR specifically affects NPC proliferation and migration. This suggests that interplay of these two pathways may maintain the balance between NSC and NPC numbers. Here we show that functional cell-cell interaction between NPCs and NSCs through EGFR and Notch signalling has a crucial role in maintaining the balance between these cell populations in the SVZ. Enhanced EGFR signalling in vivo results in the expansion of the NPC pool, and reduces NSC number and self-renewal. This occurs through a non-cell-autonomous mechanism involving EGFR-mediated regulation of Notch signalling. Our findings define a novel interaction between EGFR and Notch pathways in the adult SVZ, and thus provide a mechanism for NSC and NPC pool maintenance.
EGFR overexpression reduces NSC proliferation and self renewal in the adult mouse SVZ(a) Decreased number of GFAP+BrdU+ and GFAP+Nestin+ NSCs, and increased number of NG2+ cells in the SVZ of the CNP-hEGFR mouse (*p<0.05). Means Β± SEM. (b) Decreased percentage of GFAP+Nestin+LeX+ NSCs and increased percentage of GFAP+S100b+ astrocytes in the SVZ of the CNP-hEGFR mouse (**p<0.02). (c) Neurospheres from WT (c1) and CNP-hEGFR (c2) cells. (d) Reduced neurosphere numbers (d1) and size (d2) in cultures from CNP-hEGFR mice (*p<0.02; **p<0.001).
EGFR overexpression downregulates Notch signaling in the SVZ, and NICD overexpression rescues proliferation and self-renewal of SVZ NSCs(a) Notch signaling is downregulated, but Numb is upregulated in the SVZ of CNP-hEGFR mice. (b) NICD, RBPjk, Hes1 are upregulated in the Wa2 SVZ, and Numb is downregulated. (c-d) High NICD levels were detected after in vivo electroporation by immunostaining. (eβf) GFAP-GFP+ neurosphere number (f1) and size (f2) increased after NICD electroporation. Means (n=3) Β± SEM (*p<0.01). Scale bars = 100ΞΌm. (g) High b-gal expression levels in the SVZ after viral infection in WT (g1) and CNP-hEGFR (g2) ventricles. (h) Ad-NICD transduction increased NICD, but reduced Numb expression. (i) Ad-NICD infection increased neurosphere formation in CNP-hEGFR mice, but not in WT. Means (n=3) Β± SEM (*p<0.02). Scale bars = 200ΞΌm.
EGFR-expressing NPCs regulate NSC properties through a non-autonomous cellular mechanism(a) Increased BrdU+ cells and reduced GFAP+ cells in CNP-hEGFR mice (**p<0.002). AraC: Increased GFAP+ cells compared with NaCl in CNP-hEGFR mice (**p<0.002; *p<0.05). (b1) AraC upregulates Hes1 and RBPjk mRNAs and downregulates Numb. (b2) AraC upregulates NICD protein and downregulates Numb. (c) CNP-hEGFR mice: AraC increases NSC proliferation and self-renewal (*p<0.001). Means (n=3) Β± SEM. (d) Reduced proliferation and self-renewal in WT NSCs cultured with CNP-hEGFR NPCs, as compared with WT cells. Ad-NICD overexpression rescued NSC proliferation. Means (n=3) Β± SEM (*p<0.02). (e) Higher proliferation and self-renewal of NSCs cultured with NPCs of the Wa2 mouse, as compared with WT cells. Means (n=3) Β± SEM (*p<0.05).
EGFR signaling reduces Notch1 expression through Numb(aβd) Hes1-dsRED-NICD co-electroporation in GFAP-GFP and GFAP-GFP/CNP-hEGFR mice. More Hes1-dsRED+GFAP-GFP+ cells are observed in GFAP-GFP mouse. NICD increases GFAP-GFP+Hes1-dsRED+ cell number. (e) WT cells infected with: i) LacZ or NICD, or ii) GFP retrovirus (CLE-GFP) or EGFR-GFP. NICD upregulates NICD and Notch1, but downregulates Numb. EGFR reduces Notch1 and NICD, but increases Numb. (f) DAPT upregulates Numb. (g) Increased Numb/Notch1 immunoprecipitation correlates with enhanced degradation. (h) Ad-NICD reduces Notch1/Numb interaction and Notch1 degradation in CNP-hEGFR SVZ. (i) EGFR increases Numb and reduces NICD; PD168393 prevents these effects. (j) EGFR increases Numb/Notch immunoprecipitation, and Notch1 degradation. (k) hEGFR siRNAs decrease Numb/Notch1 interaction and Notch1 degradation in CNP-hEGFR cells. (lβo) Numb siRNA knockdown enhances Notch signaling in CNP-hEGFR NSCs. Scrab=scrambled siRNA. (l) Numb siRNA downregulates Numb and upregulates Notch1. (m) Numb siRNA decreases Numb/Notch interaction and Notch1 degradation. (nβo) Co-electroporation of Scrab or Numb siRNA, and Hes1-dsRED constructs. Numb siRNA increases the number of Hes1-dsRED+CAG-GFP+ cells. Scale bar = 50ΞΌm.
| # | Section | Preview |
|---|---|---|
| 20 | METHODS β Plasmids, siRNAs, cell transfection and luciferase assays | Transient transfections and Luciferase assays were performed in 60% confluent SVZ cell culturesβ¦ |
| 21 | METHODS β Neural progenitor-neural stem cell co-cultures | NPCs were acutely dissociated from P8 CNP-hEGFR and WT SVZ mice and then processed for purificationβ¦ |
| 22 | METHODS β Microscopy and cell counting | A Bio-Rad MRC 1024 confocal laser-scanning microscope (Hercules, CA) equipped with a krypton-argonβ¦ |
| 23 | METHODS β Microscopy and cell counting | and tissue sections were matched across samples. The analysis of the SVZ was performed at differentβ¦ |
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| The Cellular Prion Protein Controls Notch Signaling in Neural Stem/Progenitor Cells. | Martin-LannerΓ©e S et al. | β | 2017 | β |
| The shedding protease ADAM17: Physiology and pathophysiology. | Zunke F et al. | β | 2017 | β |
| Thymosin Ξ²4 overexpression regulates neuron production and spatial distribution in the developing avian optic tectum. | Lever M et al. | β | 2017 | β |
| A CREB-Sirt1-Hes1 Circuitry Mediates Neural Stem Cell Response to Glucose Availability. | Fusco S et al. | β | 2016 | β |
| Alterations in cellular metabolome after pharmacological inhibition of Notch in glioblastoma cells. | Kahlert UD et al. | β | 2016 | β |
| A mosaic world: puzzles revealed by adult neural stem cell heterogeneity. | Chaker Z et al. | β | 2016 | β |
| Astrocyte-produced leukemia inhibitory factor expands the neural stem/progenitor pool following perinatal hypoxia-ischemia. | Felling RJ et al. | β | 2016 | β |
| Cell type-dependent Erk-Akt pathway crosstalk regulates the proliferation of fetal neural progenitor cells. | Rhim JH et al. | β | 2016 | β |
| Cellular Taxonomy of the Mouse Striatum as Revealed by Single-Cell RNA-Seq. | Gokce O et al. | β | 2016 | β |
| Central nervous system niche involvement in the leukemia. | Heidari N et al. | β | 2016 | β |
| Combined EGFR- and notch inhibition display additive inhibitory effect on glioblastoma cell viability and glioblastoma-induced endothelial cell sprouting in vitro. | Staberg M et al. | β | 2016 | β |
| Controversies in preterm brain injury. | Penn AA et al. | β | 2016 | β |
| CXCR7 Participates in CXCL12-mediated Cell Cycle and Proliferation Regulation in Mouse Neural Progenitor Cells. | Wang Y et al. | β | 2016 | β |
| Direct Reprogramming of Mouse Fibroblasts to Neural Stem Cells by Small Molecules. | Han YC et al. | β | 2016 | β |
| Elevation of Brain Magnesium Potentiates Neural Stem Cell Proliferation in the Hippocampus of Young and Aged Mice. | Jia S et al. | β | 2016 | β |
| ErbB Receptor Tyrosine Kinase: A Molecular Switch Between Cardiac and Neuroectoderm Specification in Human Pluripotent Stem Cells. | Ramachandra CJ et al. | β | 2016 | β |
| Expression and Function of the Epidermal Growth Factor Receptor in Physiology and Disease. | Chen J et al. | β | 2016 | β |
| Gene-based pleiotropy across migraine with aura and migraine without aura patient groups. | Zhao H et al. | β | 2016 | β |
| Heterocellular Contacts with Mouse Brain Endothelial Cells <i>Via</i> Laminin and Ξ±6Ξ²1 Integrin Sustain Subventricular Zone (SVZ) Stem/Progenitor Cells Properties. | Rosa AI et al. | β | 2016 | β |
| ID(ealizing) control of adult subventricular zone neural stem/precursor cell differentiation for CNS regeneration. | Bohrer C et al. | β | 2016 | β |
| Integrin signalling regulates the expansion of neuroepithelial progenitors and neurogenesis via Wnt7a and Decorin. | Long K et al. | β | 2016 | β |
| Isolation and characterization of neural stem cells from dystrophic mdx mouse. | Annese T et al. | β | 2016 | β |
| Mapping gene regulatory circuitry of Pax6 during neurogenesis. | Thakurela S et al. | β | 2016 | β |
| Neural stem cell heterogeneity through time and space in the ventricular-subventricular zone. | Rushing G et al. | β | 2016 | β |
| Neural Stem Cells and Nutrients: Poised Between Quiescence and Exhaustion. | Cavallucci V et al. | β | 2016 | β |
| Neurotrophin-3 promotes proliferation and cholinergic neuronal differentiation of bone marrow- derived neural stem cells via notch signaling pathway. | Yan YH et al. | β | 2016 | β |
| Notch-mediated lateral inhibition regulates proneural wave propagation when combined with EGF-mediated reaction diffusion. | Sato M et al. | β | 2016 | β |
| Notch signaling in cerebrovascular diseases (Review). | Cai Z et al. | β | 2016 | β |
| Physiological and pathological roles of the Ξ³-secretase complex. | Carroll CM et al. | β | 2016 | β |
| Potential Therapies by Stem Cell-Derived Exosomes in CNS Diseases: Focusing on the Neurogenic Niche. | Luarte A et al. | β | 2016 | β |
| Proliferation rates and gene expression profiles in human lymphoblastoid cell lines from patients with depression characterized in response to antidepressant drug therapy. | Breitfeld J et al. | β | 2016 | β |
| Temporal course of gene expression during motor memory formation in primary motor cortex of rats. | Hertler B et al. | β | 2016 | β |
| The Adult Ventricular-Subventricular Zone (V-SVZ) and Olfactory Bulb (OB) Neurogenesis. | Lim DA et al. | β | 2016 | β |
| The Crossroads of Neural Stem Cell Development and Tumorigenesis. | Yabut OR et al. | β | 2016 | β |
| The EGFR-HER2 module: a stem cell approach to understanding a prime target and driver of solid tumors. | Schneider MR et al. | β | 2016 | β |
| The EGFR signaling pathway controls gut progenitor differentiation during planarian regeneration and homeostasis. | BarberΓ‘n S et al. | β | 2016 | β |
| Thymosin beta 4 up-regulates miR-200a expression and induces differentiation and survival of rat brain progenitor cells. | Santra M et al. | β | 2016 | β |
| ZNF488 Enhances the Invasion and Tumorigenesis in Nasopharyngeal Carcinoma Via the Wnt Signaling Pathway Involving Epithelial Mesenchymal Transition. | Zong D et al. | β | 2016 | β |
| Activated k-ras, but not h-ras or N-ras, regulates brain neural stem cell proliferation in a raf/rb-dependent manner. | Bender RH et al. | β | 2015 | β |
| A Drosophila-centric view of protein tyrosine phosphatases. | Hatzihristidis T et al. | β | 2015 | β |
| Adult neurogenesis: Is it showtime for clinical translation? | Lai YJ et al. | β | 2015 | β |
| Are neural crest stem cells the missing link between hematopoietic and neurogenic niches? | Coste C et al. | β | 2015 | β |
| Bexarotene-Activated Retinoid X Receptors Regulate Neuronal Differentiation and Dendritic Complexity. | Mounier A et al. | β | 2015 | β |
| Correlation of Musashi-1, Lgr5, and pEGFR expressions in human small intestinal adenocarcinomas. | Wang Y et al. | β | 2015 | β |
| Crosstalk of EGFR signalling with Notch and Hippo pathways to regulate cell specification, migration and proliferation in cockroach panoistic ovaries. | Elshaer N et al. | β | 2015 | β |
| Differential expression of basal microRNAs' patterns in human dental pulp stem cells. | Vasanthan P et al. | β | 2015 | β |
| Effects of ADAM10 deletion on Notch-1 signaling pathway and neuronal maintenance in adult mouse brain. | Zhuang J et al. | β | 2015 | β |
| EGFR/MAPK signaling regulates the proliferation of Drosophila renal and nephric stem cells. | Li Z et al. | β | 2015 | β |
| EGFR signaling upregulates surface expression of the GluN2B-containing NMDA receptor and contributes to long-term potentiation in the hippocampus. | Tang Y et al. | β | 2015 | β |
| Ganglioside-Dependent Neural Stem Cell Proliferation in Alzheimer's Disease Model Mice. | Koon NA et al. | β | 2015 | β |
| Genetic and Stress-Induced Loss of NG2 Glia Triggers Emergence of Depressive-like Behaviors through Reduced Secretion of FGF2. | Birey F et al. | β | 2015 | β |
| Hedgehog and Resident Vascular Stem Cell Fate. | Mooney CJ et al. | β | 2015 | β |
| Heterogeneity of Notch signaling in astrocytes and the effects of GFAP and vimentin deficiency. | Lebkuechner I et al. | β | 2015 | β |
| Human Cytomegalovirus Infection Dysregulates the Localization and Stability of NICD1 and Jag1 in Neural Progenitor Cells. | Li XJ et al. | β | 2015 | β |
| IL-10 regulates adult neurogenesis by modulating ERK and STAT3 activity. | Pereira L et al. | β | 2015 | β |
| Morphological characteristics and identification of islet-like cells derived from rat adipose-derived stem cells cocultured with pancreas adult stem cells. | Hefei W et al. | β | 2015 | β |
| [Neural stem cells and Notch signalling]. | Traiffort E et al. | β | 2015 | β |
| Selective neuronal lineages derived from Dll4-expressing progenitors/precursors in the retina and spinal cord. | Zou M et al. | β | 2015 | β |
| SNAILs promote G1 phase in selected cancer cells. | Wu YL et al. | β | 2015 | β |
| The role of cannabinoids in adult neurogenesis. | Prenderville JA et al. | β | 2015 | β |
| The roles of nanocarriers on pigment epithelium-derived factor in the differentiation of human cardiac stem cells. | Liang H et al. | β | 2015 | β |
| Vascular endothelial growth factor receptor 3 controls neural stem cell activation in mice and humans. | Han J et al. | β | 2015 | β |
| Acute isolation and transcriptome characterization of cortical astrocytes and microglia from young and aged mice. | Orre M et al. | β | 2014 | β |
| A multi-resource data integration approach: identification of candidate genes regulating cell proliferation during neocortical development. | Vied CM et al. | β | 2014 | β |
| Angiogenesis in multiple sclerosis and experimental autoimmune encephalomyelitis. | Girolamo F et al. | β | 2014 | β |
| Cancer stem cell-specific scavenger receptor CD36 drives glioblastoma progression. | Hale JS et al. | β | 2014 | β |
| Cloning and expression characteristics of the notch-associated gene BmE(spl)mΞ³ from silkworm, Bombyx mori. | Liu M et al. | β | 2014 | β |
| Combined effect of nerve growth factor and brainβderived neurotrophic factor on neuronal differentiation of neural stem cells and the potential molecular mechanisms. | Liu F et al. | β | 2014 | β |
| Differential transcriptome profile of peripheral white cells to identify biomarkers involved in oxaliplatin induced neuropathy. | Morales M et al. | β | 2014 | β |
| Differentiation of glioblastoma multiforme stem-like cells leads to downregulation of EGFR and EGFRvIII and decreased tumorigenic and stem-like cell potential. | Stockhausen MT et al. | β | 2014 | β |
| EGFR blockade enriches for lung cancer stem-like cells through Notch3-dependent signaling. | Arasada RR et al. | β | 2014 | β |
| Epidermal growth factor-like domain-containing protein 7 (EGFL7) enhances EGF receptor-AKT signaling, epithelial-mesenchymal transition, and metastasis of gastric cancer cells. | Luo BH et al. | β | 2014 | β |
| ErbB expressing Schwann cells control lateral line progenitor cells via non-cell-autonomous regulation of Wnt/Ξ²-catenin. | Lush ME et al. | β | 2014 | β |
| Genetic activation of Hedgehog signaling unbalances the rate of neural stem cell renewal by increasing symmetric divisions. | Ferent J et al. | β | 2014 | β |
| Glial development: the crossroads of regeneration and repair in the CNS. | Gallo V et al. | β | 2014 | β |
| Glioma stem cells: turpis omen in nomen? (The evil in the name?). | Binda E et al. | β | 2014 | β |
| Inhibition of the Jagged/Notch pathway inhibits retinoblastoma cell proliferation via suppressing the PI3K/Akt, Src, p38MAPK and Wnt/Ξ²βcatenin signaling pathways. | Xiao W et al. | β | 2014 | β |
| Intranasal epidermal growth factor treatment rescues neonatal brain injury. | Scafidi J et al. | β | 2014 | β |
| Involvement of extracellular signal-regulated kinase (ERK1/2)-p53-p21 axis in mediating neural stem/progenitor cell cycle arrest in co-morbid HIV-drug abuse exposure. | Malik S et al. | β | 2014 | β |
| Jagged1 is necessary for postnatal and adult neurogenesis in the dentate gyrus. | Lavado A et al. | β | 2014 | β |
| Lineage-specific splicing of a brain-enriched alternative exon promotes glioblastoma progression. | Ferrarese R et al. | β | 2014 | β |
| Matrix regulators in neural stem cell functions. | Wade A et al. | β | 2014 | β |
| Molecular diversity subdivides the adult forebrain neural stem cell population. | Giachino C et al. | β | 2014 | β |
| N-cadherin promotes recruitment and migration of neural progenitor cells from the SVZ neural stem cell niche into demyelinated lesions. | Klingener M et al. | β | 2014 | β |
| Notching on Cancer's Door: Notch Signaling in Brain Tumors. | Teodorczyk M et al. | β | 2014 | β |
| Notching up neural stem cell homogeneity in homeostasis and disease. | Giachino C et al. | β | 2014 | β |
| Notch inhibition promotes fetal liver stem/progenitor cells differentiation into hepatocytes via the inhibition of HNF-1Ξ². | Wang T et al. | β | 2014 | β |
| Notch signaling induces retinal stem-like properties in perinatal neural retina progenitors and promotes symmetric divisions in adult retinal stem cells. | Balenci L et al. | β | 2014 | β |
| Physiological normoxia and absence of EGF is required for the long-term propagation of anterior neural precursors from human pluripotent cells. | Bilican B et al. | β | 2014 | β |
| Receptor tyrosine kinase (RTK) signalling in the control of neural stem and progenitor cell (NSPC) development. | Annenkov A | β | 2014 | β |
| Rostral-caudal distribution of Emx1-lineage stem/transit amplifying cells and lineage progression in embryonic cortex depend on Hedgehog signaling. | Lillien L | β | 2014 | β |
| SnapShot: adult neurogenesis in the V-SVZ. | Tong CK et al. | β | 2014 | β |
| Sox2 transcription network acts as a molecular switch to regulate properties of neural stem cells. | Shimozaki K | β | 2014 | β |
| TACE/ADAM17 is essential for oligodendrocyte development and CNS myelination. | Palazuelos J et al. | β | 2014 | β |
| Taking advantage of neural development to treat glioblastoma. | Zhang Z et al. | β | 2014 | β |
| TGFΞ² signaling regulates the timing of CNS myelination by modulating oligodendrocyte progenitor cell cycle exit through SMAD3/4/FoxO1/Sp1. | Palazuelos J et al. | β | 2014 | β |
| The nonlinear dynamics and fluctuations of mRNA levels in cross-talking pathway activated transcription. | Yu J et al. | β | 2014 | β |
| Tis21 is required for adult neurogenesis in the subventricular zone and for olfactory behavior regulating cyclins, BMP4, Hes1/5 and Ids. | Farioli-Vecchioli S et al. | β | 2014 | β |
| A Disintegrin and Metalloprotease 10 in neuronal maturation and gliogenesis during cortex development. | Ma Z et al. | β | 2013 | β |
| Adult neural stem cells and their niche: a dynamic duo during homeostasis, regeneration, and aging. | Silva-Vargas V et al. | β | 2013 | β |
| Aging results in molecular changes in an enriched population of undifferentiated rat spermatogonia. | Paul C et al. | β | 2013 | β |
| Cancer stem cells in glioma: challenges and opportunities. | Wang J et al. | β | 2013 | β |
| Cancer stem-like cell properties are regulated by EGFR/AKT/Ξ²-catenin signaling and preferentially inhibited by gefitinib in nasopharyngeal carcinoma. | Ma L et al. | β | 2013 | β |
| Common biological networks underlie genetic risk for alcoholism in African- and European-American populations. | Kos MZ et al. | β | 2013 | β |
| Comparative analysis of protein expression of three stem cell populations: models of cytokine delivery system in vivo. | Roche S et al. | β | 2013 | β |
| Current Understanding on EGFR and Wnt/Ξ²-Catenin Signaling in Glioma and Their Possible Crosstalk. | Paul I et al. | β | 2013 | β |
| Dll1 maintains quiescence of adult neural stem cells and segregates asymmetrically during mitosis. | Kawaguchi D et al. | β | 2013 | β |
| DNA-dependent protein kinase is a context dependent regulator of Lmx1a and midbrain specification. | Hunt CP et al. | β | 2013 | β |
| Epidermal growth factor receptor abnormalities in atypical teratoid/rhabdoid tumors and an unusual case with gene amplification. | Satomi K et al. | β | 2013 | β |
| Epidermal growth factor regulates hematopoietic regeneration after radiation injury. | Doan PL et al. | β | 2013 | β |
| Epidermal growth factor regulates NIKS keratinocyte proliferation through Notch signaling. | Roy M et al. | β | 2013 | β |
| ErbB1-4-dependent EGF/neuregulin signals and their cross talk in the central nervous system: pathological implications in schizophrenia and Parkinson's disease. | Iwakura Y et al. | β | 2013 | β |
| FOXO3 shares common targets with ASCL1 genome-wide and inhibits ASCL1-dependent neurogenesis. | Webb AE et al. | β | 2013 | β |
| Impaired neural differentiation of induced pluripotent stem cells generated from a mouse model of Sandhoff disease. | Ogawa Y et al. | β | 2013 | β |
| Interactions between VEGFR and Notch signaling pathways in endothelial and neural cells. | Thomas JL et al. | β | 2013 | β |
| Interleukin-10 regulates progenitor differentiation and modulates neurogenesis in adult brain. | Perez-Asensio FJ et al. | β | 2013 | β |
| Involvement of the Notch pathway in terminal astrocytic differentiation: role of PKA. | Angulo-Rojo C et al. | β | 2013 | β |
| Neural stem and progenitor cells in health and disease. | Ladran I et al. | β | 2013 | β |
| Neural stem cell survival factors. | Ramasamy S et al. | β | 2013 | β |
| Notch1 signaling modulates neuronal progenitor activity in the subventricular zone in response to aging and focal ischemia. | Sun F et al. | β | 2013 | β |
| Notch receptor expression in neurogenic regions of the adult zebrafish brain. | de Oliveira-Carlos V et al. | β | 2013 | β |
| Notch signaling imparts and preserves neural stem characteristics in the adult brain. | Piccin D et al. | β | 2013 | β |
| Notch signaling in mammalian hair cell regeneration. | Slowik AD et al. | β | 2013 | β |
| Nox4-generated superoxide drives angiotensin II-induced neural stem cell proliferation. | Topchiy E et al. | β | 2013 | β |
| Protection of neuronal diversity at the expense of neuronal numbers during nutrient restriction in the Drosophila visual system. | Lanet E et al. | β | 2013 | β |
| Protective astrogenesis from the SVZ niche after injury is controlled by Notch modulator Thbs4. | Benner EJ et al. | β | 2013 | β |
| Shades of gray: The delineation of marker expression within the adult rodent subventricular zone. | Mamber C et al. | β | 2013 | β |
| Signaling mechanisms regulating adult neural stem cells and neurogenesis. | Faigle R et al. | β | 2013 | β |
| Specific fate decisions in adult hepatic progenitor cells driven by MET and EGFR signaling. | Kitade M et al. | β | 2013 | β |
| Stem cells living with a Notch. | Koch U et al. | β | 2013 | β |
| The Jagged-1/Notch-1/Hes-1 pathway is involved in intestinal adaptation in a massive small bowel resection rat model. | Chen G et al. | β | 2013 | β |
| The role of EGFR and ErbB family related proteins in the oligodendrocyte specification in germinal niches of the adult mammalian brain. | Galvez-Contreras AY et al. | β | 2013 | β |
| Transforming growth factor-Ξ²1 primes proliferating adult neural progenitor cells to electrophysiological functionality. | Kraus S et al. | β | 2013 | β |
| Adult neural stem cells bridge their niche. | Fuentealba LC et al. | β | 2012 | β |
| Adult neurogenesis and brain regeneration in zebrafish. | Kizil C et al. | β | 2012 | β |
| Adult periventricular neural stem cells: outstanding progress and outstanding issues. | Chojnacki A et al. | β | 2012 | β |
| Astrocytes regulate adult hippocampal neurogenesis through ephrin-B signaling. | Ashton RS et al. | β | 2012 | β |
| Cancer stem cells in brain tumors and their lineage hierarchy. | Kong DS | β | 2012 | β |
| Cell-cycle regulation of NOTCH signaling during C. elegans vulval development. | Nusser-Stein S et al. | β | 2012 | β |
| Central role of the EGF receptor in neurometabolic aging. | Siddiqui S et al. | β | 2012 | β |
| Concise review: self-renewal in the central nervous system: neural stem cells from embryo to adult. | De Filippis L et al. | β | 2012 | β |
| Conditional deletion of Notch1 and Notch2 genes in excitatory neurons of postnatal forebrain does not cause neurodegeneration or reduction of Notch mRNAs and proteins. | Zheng J et al. | β | 2012 | β |
| Cyclopamine cooperates with EGFR inhibition to deplete stem-like cancer cells in glioblastoma-derived spheroid cultures. | Eimer S et al. | β | 2012 | β |
| Death receptor 5 and neuroproliferation. | Niu Y et al. | β | 2012 | β |
| Deciphering the Key Features of Malignant Tumor Microenvironment for Anti-cancer Therapy. | Shang B et al. | β | 2012 | β |
| Differential pathotropism of non-immortalized and immortalized human neural stem cell lines in a focal demyelination model. | Ferrari D et al. | β | 2012 | β |
| Diphenylhydantoin promotes proliferation in the subventricular zone and dentate gyrus. | Galvez-Contreras AY et al. | β | 2012 | β |
| Distinct roles of Nogo-a and Nogo receptor 1 in the homeostatic regulation of adult neural stem cell function and neuroblast migration. | Rolando C et al. | β | 2012 | β |
| Epidermal ADAM17 maintains the skin barrier by regulating EGFR ligand-dependent terminal keratinocyte differentiation. | Franzke CW et al. | β | 2012 | β |
| High-throughput clonal analysis of neural stem cells in microarrayed artificial niches. | Roccio M et al. | β | 2012 | β |
| Immunological characterization and transcription profiling of peripheral blood (PB) monocytes in children with autism spectrum disorders (ASD) and specific polysaccharide antibody deficiency (SPAD): case study. | Jyonouchi H et al. | β | 2012 | β |
| Indirect effects of Wnt3a/Ξ²-catenin signalling support mouse spermatogonial stem cells in vitro. | Yeh JR et al. | β | 2012 | β |
| Intrinsic regulation of adult subventricular zone neural progenitor cells and the effect of brain injury. | Jones KS et al. | β | 2012 | β |
| Mammalian target of rapamycin signaling is a key regulator of the transit-amplifying progenitor pool in the adult and aging forebrain. | Paliouras GN et al. | β | 2012 | β |
| Minocycline-preconditioned neural stem cells enhance neuroprotection after ischemic stroke in rats. | Sakata H et al. | β | 2012 | β |
| Morphological, molecular and functional differences of adult bone marrow- and adipose-derived stem cells isolated from rats of different ages. | Mantovani C et al. | β | 2012 | β |
| Neurogenic subventricular zone stem/progenitor cells are Notch1-dependent in their active but not quiescent state. | Basak O et al. | β | 2012 | β |
| Non-genetic modulation of Notch activity by artificial delivery of Notch intracellular domain into neural stem cells. | Haupt S et al. | β | 2012 | β |
| Notch is the key factor in the process of fetal liver stem/progenitor cells differentiation into hepatocytes. | Wang T et al. | β | 2012 | β |
| Nuclear factor kappa B signaling initiates early differentiation of neural stem cells. | Zhang Y et al. | β | 2012 | β |
| Numb regulates glioma stem cell fate and growth by altering epidermal growth factor receptor and Skp1-Cullin-F-box ubiquitin ligase activity. | Jiang X et al. | β | 2012 | β |
| PDGF in gliomas: more than just a growth factor? | Lindberg N et al. | β | 2012 | β |
| PEDF is a novel oligodendrogenic morphogen acting on the adult SVZ and corpus callosum. | Sohn J et al. | β | 2012 | β |
| Phosphoproteome of human glioblastoma initiating cells reveals novel signaling regulators encoded by the transcriptome. | Kozuka-Hata H et al. | β | 2012 | β |
| Spatiotemporal changes to the subventricular zone stem cell pool through aging. | Shook BA et al. | β | 2012 | β |
| Stemness of the organ of Corti relates to the epigenetic status of Sox2 enhancers. | Waldhaus J et al. | β | 2012 | β |
| Temporal profile of gene transcription noise modulated by cross-talking signal transduction pathways. | Sun Q et al. | β | 2012 | β |
| The adventitia: a progenitor cell niche for the vessel wall. | Majesky MW et al. | β | 2012 | β |
| The molecular profiles of neural stem cell niche in the adult subventricular zone. | Lee C et al. | β | 2012 | β |
| The voyage of stem cell toward terminal differentiation: a brief overview. | Bhattacharyya S et al. | β | 2012 | β |
| Thymosin Ξ²4 induces folding of the developing optic tectum in the chicken (Gallus domesticus). | Wirsching HG et al. | β | 2012 | β |
| Topographical analysis of the subependymal zone neurogenic niche. | FalcΓ£o AM et al. | β | 2012 | β |
| VCAM1 is essential to maintain the structure of the SVZ niche and acts as an environmental sensor to regulate SVZ lineage progression. | Kokovay E et al. | β | 2012 | β |
| An integrated inΒ vitro and inΒ vivo high-throughput screen identifies treatment leads for ependymoma. | Atkinson JM et al. | β | 2011 | β |
| BDNF promotes EGF-induced proliferation and migration of human fetal neural stem/progenitor cells via the PI3K/Akt pathway. | Zhang Q et al. | β | 2011 | β |
| Biology of the Mi-2/NuRD Complex in SLAC (Stemness, Longevity/Ageing, and Cancer). | Zhang Y | β | 2011 | β |
| Caveolin-1 inhibits oligodendroglial differentiation of neural stem/progenitor cells through modulating Ξ²-catenin expression. | Li Y et al. | β | 2011 | β |
| Construct and Compare Gene Coexpression Networks with DAPfinder and DAPview. | Skinner J et al. | β | 2011 | β |
| Lake-front property: a unique germinal niche by the lateral ventricles of the adult brain. | Ihrie RA et al. | β | 2011 | β |
| Maintaining tissue homeostasis: dynamic control of somatic stem cell activity. | Biteau B et al. | β | 2011 | β |
| Mediators of oligodendrocyte differentiation during remyelination. | Patel JR et al. | β | 2011 | β |
| Metalloprotease-disintegrin ADAM12 expression is regulated by Notch signaling via microRNA-29. | Li H et al. | β | 2011 | β |
| Neural stem cell biology in vertebrates and invertebrates: more alike than different? | Brand AH et al. | β | 2011 | β |
| Notch in the vertebrate nervous system: an old dog with new tricks. | Pierfelice T et al. | β | 2011 | β |
| Not(ch) just development: Notch signalling in the adult brain. | Ables JL et al. | β | 2011 | β |
| Notch signaling contributes to the maintenance of both normal neural stem cells and patient-derived glioma stem cells. | Hu YY et al. | β | 2011 | β |
| Ochratoxin A at nanomolar concentration perturbs the homeostasis of neural stem cells in highly differentiated but not in immature three-dimensional brain cell cultures. | Zurich MG et al. | β | 2011 | β |
| Oligodendrogenesis in the subventricular zone and the role of epidermal growth factor. | Gonzalez-Perez O et al. | β | 2011 | β |
| Pax6 regulates the epidermal growth factor-responsive neural stem cells of the subventricular zone. | Jia H et al. | β | 2011 | β |
| Promoting myelin repair and return of function in multiple sclerosis. | Zhang J et al. | β | 2011 | β |
| Regulation of neural stem cell in the human SVZ by trophic and morphogenic factors. | Alvarez-Palazuelos LE et al. | β | 2011 | β |
| Sustained activation of the HER1-ERK1/2-RSK signaling pathway controls myoepithelial cell fate in human mammary tissue. | Pasic L et al. | β | 2011 | β |
| Targeting oligodendrocyte protection and remyelination in multiple sclerosis. | Zhang J et al. | β | 2011 | β |
| The role of Notch signaling in adult neurogenesis. | Imayoshi I et al. | β | 2011 | β |
| Wnt signaling regulates symmetry of division of neural stem cells in the adult brain and in response to injury. | Piccin D et al. | β | 2011 | β |
| Neurogenesis: Pathways for population balance. | Walker D | β | 2010 | β |
| Stem cells: a balancing act. | Walker D | β | 2010 | β |