Vascular‐derived TGF‐β increases in the stem cell niche and perturbs neurogenesis during aging and following irradiation in the adult mouse brain

Neurogenesis decreases during aging and following cranial radiotherapy, causing a progressive cognitive decline that is currently untreatable. However, functional neural stem cells remained present in the subventricular zone of high dose‐irradiated and aged mouse brains. We therefore investigated wh...

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Published inEMBO molecular medicine Vol. 5; no. 4; pp. 548 - 562
Main Authors Pineda, Jose R., Daynac, Mathieu, Chicheportiche, Alexandra, Cebrian‐Silla, Arantxa, Sii Felice, Karine, Garcia‐Verdugo, Jose Manuel, Boussin, François D., Mouthon, Marc‐André
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.04.2013
WILEY‐VCH Verlag
EMBO Press
WILEY-VCH Verlag
Springer Nature
Subjects
Aging
Aging - metabolism
Aging - radiation effects
Alzheimer's disease
Animals
Apoptosis
Brain - cytology
Brain - growth & development
Brain - metabolism
Brain - radiation effects
Brain cancer
Cell Proliferation
Cognitive ability
Endothelial cells
Endothelial Cells - metabolism
Experiments
Humans
irradiation
Male
Mice
Mice, Inbred C57BL
Neural stem cells
Neural Stem Cells - cytology
Neural Stem Cells - metabolism
Neural Stem Cells - radiation effects
Neurogenesis
Neurogenesis - radiation effects
Progenitor cells
Radiation therapy
Research Article
Signal Transduction - radiation effects
Smad3 protein
Stem Cell Niche
Stem cell transplantation
Stem cells
Subventricular zone
TGF‐beta
Transforming Growth Factor beta - metabolism
Transforming growth factor-b
Transforming growth factor-b1
France
endothelial cells
aging
neural stem cells
TGF‐beta
irradiation
Online AccessGet full text
ISSN1757-4676
1757-4684
1757-4684
DOI10.1002/emmm.201202197

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Abstract Neurogenesis decreases during aging and following cranial radiotherapy, causing a progressive cognitive decline that is currently untreatable. However, functional neural stem cells remained present in the subventricular zone of high dose‐irradiated and aged mouse brains. We therefore investigated whether alterations in the neurogenic niches are perhaps responsible for the neurogenesis decline. This hypothesis was supported by the absence of proliferation of neural stem cells that were engrafted into the vascular niches of irradiated host brains. Moreover, we observed a marked increase in TGF‐β1 production by endothelial cells in the stem cell niche in both middle‐aged and irradiated mice. In co‐cultures, irradiated brain endothelial cells induced the apoptosis of neural stem/progenitor cells via TGF‐β/Smad3 signalling. Strikingly, the blockade of TGF‐β signalling in vivo using a neutralizing antibody or the selective inhibitor SB‐505124 significantly improved neurogenesis in aged and irradiated mice, prevented apoptosis and increased the proliferation of neural stem/progenitor cells. These findings suggest that anti‐TGF‐β‐based therapy may be used for future interventions to prevent neurogenic collapse following radiotherapy or during aging. Graphical Abstract In aged or irradiated mice, the neural stem cell vascular niche expresses increased levels of TGFbeta1, which induces apoptosis of neural stem cells via Smad3. Treatment with TGFbeta signaling blockers restores neurogenesis in these mice.
AbstractList Neurogenesis decreases during aging and following cranial radiotherapy, causing a progressive cognitive decline that is currently untreatable. However, functional neural stem cells remained present in the subventricular zone of high dose‐irradiated and aged mouse brains. We therefore investigated whether alterations in the neurogenic niches are perhaps responsible for the neurogenesis decline. This hypothesis was supported by the absence of proliferation of neural stem cells that were engrafted into the vascular niches of irradiated host brains. Moreover, we observed a marked increase in TGF‐β1 production by endothelial cells in the stem cell niche in both middle‐aged and irradiated mice. In co‐cultures, irradiated brain endothelial cells induced the apoptosis of neural stem/progenitor cells via TGF‐β/Smad3 signalling. Strikingly, the blockade of TGF‐β signalling in vivo using a neutralizing antibody or the selective inhibitor SB‐505124 significantly improved neurogenesis in aged and irradiated mice, prevented apoptosis and increased the proliferation of neural stem/progenitor cells. These findings suggest that anti‐TGF‐β‐based therapy may be used for future interventions to prevent neurogenic collapse following radiotherapy or during aging.
Abstract Neurogenesis decreases during aging and following cranial radiotherapy, causing a progressive cognitive decline that is currently untreatable. However, functional neural stem cells remained present in the subventricular zone of high dose‐irradiated and aged mouse brains. We therefore investigated whether alterations in the neurogenic niches are perhaps responsible for the neurogenesis decline. This hypothesis was supported by the absence of proliferation of neural stem cells that were engrafted into the vascular niches of irradiated host brains. Moreover, we observed a marked increase in TGF‐β1 production by endothelial cells in the stem cell niche in both middle‐aged and irradiated mice. In co‐cultures, irradiated brain endothelial cells induced the apoptosis of neural stem/progenitor cells via TGF‐β/Smad3 signalling. Strikingly, the blockade of TGF‐β signalling in vivo using a neutralizing antibody or the selective inhibitor SB‐505124 significantly improved neurogenesis in aged and irradiated mice, prevented apoptosis and increased the proliferation of neural stem/progenitor cells. These findings suggest that anti‐TGF‐β‐based therapy may be used for future interventions to prevent neurogenic collapse following radiotherapy or during aging.
Neurogenesis decreases during aging and following cranial radiotherapy, causing a progressive cognitive decline that is currently untreatable. However, functional neural stem cells remained present in the subventricular zone of high dose‐irradiated and aged mouse brains. We therefore investigated whether alterations in the neurogenic niches are perhaps responsible for the neurogenesis decline. This hypothesis was supported by the absence of proliferation of neural stem cells that were engrafted into the vascular niches of irradiated host brains. Moreover, we observed a marked increase in TGF‐β1 production by endothelial cells in the stem cell niche in both middle‐aged and irradiated mice. In co‐cultures, irradiated brain endothelial cells induced the apoptosis of neural stem/progenitor cells via TGF‐β/Smad3 signalling. Strikingly, the blockade of TGF‐β signalling in vivo using a neutralizing antibody or the selective inhibitor SB‐505124 significantly improved neurogenesis in aged and irradiated mice, prevented apoptosis and increased the proliferation of neural stem/progenitor cells. These findings suggest that anti‐TGF‐β‐based therapy may be used for future interventions to prevent neurogenic collapse following radiotherapy or during aging. Graphical Abstract In aged or irradiated mice, the neural stem cell vascular niche expresses increased levels of TGFbeta1, which induces apoptosis of neural stem cells via Smad3. Treatment with TGFbeta signaling blockers restores neurogenesis in these mice.
Neurogenesis decreases during aging and following cranial radiotherapy, causing a progressive cognitive decline that is currently untreatable. However, functional neural stem cells remained present in the subventricular zone of high dose-irradiated and aged mouse brains. We therefore investigated whether alterations in the neurogenic niches are perhaps responsible for the neurogenesis decline. This hypothesis was supported by the absence of proliferation of neural stem cells that were engrafted into the vascular niches of irradiated host brains. Moreover, we observed a marked increase in TGF-β1 production by endothelial cells in the stem cell niche in both middle-aged and irradiated mice. In co-cultures, irradiated brain endothelial cells induced the apoptosis of neural stem/progenitor cells via TGF-β/Smad3 signalling. Strikingly, the blockade of TGF-β signalling in vivo using a neutralizing antibody or the selective inhibitor SB-505124 significantly improved neurogenesis in aged and irradiated mice, prevented apoptosis and increased the proliferation of neural stem/progenitor cells. These findings suggest that anti-TGF-β-based therapy may be used for future interventions to prevent neurogenic collapse following radiotherapy or during aging.
Neurogenesis decreases during aging and following cranial radiotherapy, causing a progressive cognitive decline that is currently untreatable. However, functional neural stem cells remained present in the subventricular zone of high dose‐irradiated and aged mouse brains. We therefore investigated whether alterations in the neurogenic niches are perhaps responsible for the neurogenesis decline. This hypothesis was supported by the absence of proliferation of neural stem cells that were engrafted into the vascular niches of irradiated host brains. Moreover, we observed a marked increase in TGF‐β1 production by endothelial cells in the stem cell niche in both middle‐aged and irradiated mice. In co‐cultures, irradiated brain endothelial cells induced the apoptosis of neural stem/progenitor cells via TGF‐β/Smad3 signalling. Strikingly, the blockade of TGF‐β signalling in vivo using a neutralizing antibody or the selective inhibitor SB‐505124 significantly improved neurogenesis in aged and irradiated mice, prevented apoptosis and increased the proliferation of neural stem/progenitor cells. These findings suggest that anti‐TGF‐β‐based therapy may be used for future interventions to prevent neurogenic collapse following radiotherapy or during aging. In aged or irradiated mice, the neural stem cell vascular niche expresses increased levels of TGFbeta1, which induces apoptosis of neural stem cells via Smad3. Treatment with TGFbeta signaling blockers restores neurogenesis in these mice.
Neurogenesis decreases during aging and following cranial radiotherapy, causing a progressive cognitive decline that is currently untreatable. However, functional neural stem cells remained present in the subventricular zone of high dose-irradiated and aged mouse brains. We therefore investigated whether alterations in the neurogenic niches are perhaps responsible for the neurogenesis decline. This hypothesis was supported by the absence of proliferation of neural stem cells that were engrafted into the vascular niches of irradiated host brains. Moreover, we observed a marked increase in TGF-β1 production by endothelial cells in the stem cell niche in both middle-aged and irradiated mice. In co-cultures, irradiated brain endothelial cells induced the apoptosis of neural stem/progenitor cells via TGF-β/Smad3 signalling. Strikingly, the blockade of TGF-β signalling in vivo using a neutralizing antibody or the selective inhibitor SB-505124 significantly improved neurogenesis in aged and irradiated mice, prevented apoptosis and increased the proliferation of neural stem/progenitor cells. These findings suggest that anti-TGF-β-based therapy may be used for future interventions to prevent neurogenic collapse following radiotherapy or during aging.Neurogenesis decreases during aging and following cranial radiotherapy, causing a progressive cognitive decline that is currently untreatable. However, functional neural stem cells remained present in the subventricular zone of high dose-irradiated and aged mouse brains. We therefore investigated whether alterations in the neurogenic niches are perhaps responsible for the neurogenesis decline. This hypothesis was supported by the absence of proliferation of neural stem cells that were engrafted into the vascular niches of irradiated host brains. Moreover, we observed a marked increase in TGF-β1 production by endothelial cells in the stem cell niche in both middle-aged and irradiated mice. In co-cultures, irradiated brain endothelial cells induced the apoptosis of neural stem/progenitor cells via TGF-β/Smad3 signalling. Strikingly, the blockade of TGF-β signalling in vivo using a neutralizing antibody or the selective inhibitor SB-505124 significantly improved neurogenesis in aged and irradiated mice, prevented apoptosis and increased the proliferation of neural stem/progenitor cells. These findings suggest that anti-TGF-β-based therapy may be used for future interventions to prevent neurogenic collapse following radiotherapy or during aging.
Author Chicheportiche, Alexandra
Garcia‐Verdugo, Jose Manuel
Sii Felice, Karine
Pineda, Jose R.
Daynac, Mathieu
Boussin, François D.
Mouthon, Marc‐André
Cebrian‐Silla, Arantxa
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/23526803$$D View this record in MEDLINE/PubMed
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Issue 4
Keywords endothelial cells
aging
neural stem cells
TGF‐beta
irradiation
Language English
License Attribution
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Copyright © 2013 The Authors. Published by John Wiley and Sons, Ltd on behalf of EMBO.
This is an open access article under the terms of the Creative Commons Attribution License (CC BY 3.0), which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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SSID ssj0065618
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Snippet Neurogenesis decreases during aging and following cranial radiotherapy, causing a progressive cognitive decline that is currently untreatable. However,...
Abstract Neurogenesis decreases during aging and following cranial radiotherapy, causing a progressive cognitive decline that is currently untreatable....
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SourceType Open Website
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StartPage 548
SubjectTerms Aging
Aging - metabolism
Aging - radiation effects
Alzheimer's disease
Animals
Apoptosis
Brain - cytology
Brain - growth & development
Brain - metabolism
Brain - radiation effects
Brain cancer
Cell Proliferation
Cognitive ability
Endothelial cells
Endothelial Cells - metabolism
Experiments
Humans
irradiation
Male
Mice
Mice, Inbred C57BL
Neural stem cells
Neural Stem Cells - cytology
Neural Stem Cells - metabolism
Neural Stem Cells - radiation effects
Neurogenesis
Neurogenesis - radiation effects
Progenitor cells
Radiation therapy
Research Article
Signal Transduction - radiation effects
Smad3 protein
Stem Cell Niche
Stem cell transplantation
Stem cells
Subventricular zone
TGF‐beta
Transforming Growth Factor beta - metabolism
Transforming growth factor-b
Transforming growth factor-b1
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Title Vascular‐derived TGF‐β increases in the stem cell niche and perturbs neurogenesis during aging and following irradiation in the adult mouse brain
URI https://link.springer.com/article/10.1002/emmm.201202197
https://onlinelibrary.wiley.com/doi/abs/10.1002%2Femmm.201202197
https://www.ncbi.nlm.nih.gov/pubmed/23526803
https://www.proquest.com/docview/2299119686
https://www.proquest.com/docview/1324385522
https://pubmed.ncbi.nlm.nih.gov/PMC3628106
https://doaj.org/article/5705b7354b2b44e29a1c2a687c53a99c
Volume 5
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