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Article

Environmental Enrichment Induces Meningeal Niche Remodeling through TrkB-Mediated Signaling

1
Section of Pharmacology, Department of Diagnostic and Public Health, University of Verona, 37134 Verona, Italy
2
Department of Surgical Sciences, Dentistry, Gynecology and Pediatrics, University of Verona, 37134 Verona, Italy
3
Laboratory of Cell Metabolism and Regenerative Medicine, Department of Medical Biotechnology and Translational Medicine, University of Milan, 20129 Milan, Italy
*
Author to whom correspondence should be addressed.
Academic Editors: Luca Bonfanti and Sebastien Couillard-Despres
Int. J. Mol. Sci. 2021, 22(19), 10657; https://doi.org/10.3390/ijms221910657
Received: 5 June 2021 / Revised: 22 September 2021 / Accepted: 26 September 2021 / Published: 1 October 2021
(This article belongs to the Special Issue Neuron and Brain Maturation)
Neural precursors (NPs) present in the hippocampus can be modulated by several neurogenic stimuli, including environmental enrichment (EE) acting through BDNF-TrkB signaling. We have recently identified NPs in meninges; however, the meningeal niche response to pro-neurogenic stimuli has never been investigated. To this aim, we analyzed the effects of EE exposure on NP distribution in mouse brain meninges. Following neurogenic stimuli, although we did not detect modification of the meningeal cell number and proliferation, we observed an increased number of neural precursors in the meninges. A lineage tracing experiment suggested that EE-induced β3-Tubulin+ immature neuronal cells present in the meninges originated, at least in part, from GLAST+ radial glia cells. To investigate the molecular mechanism responsible for meningeal reaction to EE exposure, we studied the BDNF-TrkB interaction. Treatment with ANA-12, a TrkB non-competitive inhibitor, abolished the EE-induced meningeal niche changes. Overall, these data showed, for the first time, that EE exposure induced meningeal niche remodeling through TrkB-mediated signaling. Fluoxetine treatment further confirmed the meningeal niche response, suggesting it may also respond to other pharmacological neurogenic stimuli. A better understanding of the neurogenic stimuli modulation for meninges may be useful to improve the effectiveness of neurodegenerative and neuropsychiatric treatments. View Full-Text
Keywords: neurogenesis; TrkB; BDNF; meninges; ANA-12; meningeal niche; radial glia cell; neural precursor; enriched environment; EE; ENR neurogenesis; TrkB; BDNF; meninges; ANA-12; meningeal niche; radial glia cell; neural precursor; enriched environment; EE; ENR
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MDPI and ACS Style

Zorzin, S.; Corsi, A.; Ciarpella, F.; Bottani, E.; Dolci, S.; Malpeli, G.; Pino, A.; Amenta, A.; Fumagalli, G.F.; Chiamulera, C.; Bifari, F.; Decimo, I. Environmental Enrichment Induces Meningeal Niche Remodeling through TrkB-Mediated Signaling. Int. J. Mol. Sci. 2021, 22, 10657. https://doi.org/10.3390/ijms221910657

AMA Style

Zorzin S, Corsi A, Ciarpella F, Bottani E, Dolci S, Malpeli G, Pino A, Amenta A, Fumagalli GF, Chiamulera C, Bifari F, Decimo I. Environmental Enrichment Induces Meningeal Niche Remodeling through TrkB-Mediated Signaling. International Journal of Molecular Sciences. 2021; 22(19):10657. https://doi.org/10.3390/ijms221910657

Chicago/Turabian Style

Zorzin, Stefania, Andrea Corsi, Francesca Ciarpella, Emanuela Bottani, Sissi Dolci, Giorgio Malpeli, Annachiara Pino, Alessia Amenta, Guido Franceso Fumagalli, Cristiano Chiamulera, Francesco Bifari, and Ilaria Decimo. 2021. "Environmental Enrichment Induces Meningeal Niche Remodeling through TrkB-Mediated Signaling" International Journal of Molecular Sciences 22, no. 19: 10657. https://doi.org/10.3390/ijms221910657

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