The enhancement of activity rescues the establishment of Mecp2 null neuronal phenotypes

Abstract MECP2 mutations cause Rett syndrome (RTT), a severe and progressive neurodevelopmental disorder mainly affecting females. Although RTT patients exhibit delayed onset of symptoms, several evidences demonstrate that MeCP2 deficiency alters early development of the brain. Indeed, during early...

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Main Authors: Linda Scaramuzza, Giuseppina De Rocco, Genni Desiato, Clementina Cobolli Gigli, Martina Chiacchiaretta, Filippo Mirabella, Davide Pozzi, Marco De Simone, Paola Conforti, Massimiliano Pagani, Fabio Benfenati, Fabrizia Cesca, Francesco Bedogni, Nicoletta Landsberger
Format: Article
Language:English
Published: Springer Nature 2021-03-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.202012433
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author Linda Scaramuzza
Giuseppina De Rocco
Genni Desiato
Clementina Cobolli Gigli
Martina Chiacchiaretta
Filippo Mirabella
Davide Pozzi
Marco De Simone
Paola Conforti
Massimiliano Pagani
Fabio Benfenati
Fabrizia Cesca
Francesco Bedogni
Nicoletta Landsberger
author_facet Linda Scaramuzza
Giuseppina De Rocco
Genni Desiato
Clementina Cobolli Gigli
Martina Chiacchiaretta
Filippo Mirabella
Davide Pozzi
Marco De Simone
Paola Conforti
Massimiliano Pagani
Fabio Benfenati
Fabrizia Cesca
Francesco Bedogni
Nicoletta Landsberger
author_sort Linda Scaramuzza
collection DOAJ
description Abstract MECP2 mutations cause Rett syndrome (RTT), a severe and progressive neurodevelopmental disorder mainly affecting females. Although RTT patients exhibit delayed onset of symptoms, several evidences demonstrate that MeCP2 deficiency alters early development of the brain. Indeed, during early maturation, Mecp2 null cortical neurons display widespread transcriptional changes, reduced activity, and defective morphology. It has been proposed that during brain development these elements are linked in a feed‐forward cycle where neuronal activity drives transcriptional and morphological changes that further increase network maturity. We hypothesized that the enhancement of neuronal activity during early maturation might prevent the onset of RTT‐typical molecular and cellular phenotypes. Accordingly, we show that the enhancement of excitability, obtained by adding to neuronal cultures Ampakine CX546, rescues transcription of several genes, neuronal morphology, and responsiveness to stimuli. Greater effects are achieved in response to earlier treatments. In vivo, short and early administration of CX546 to Mecp2 null mice prolongs lifespan, delays the disease progression, and rescues motor abilities and spatial memory, thus confirming the value for RTT of an early restoration of neuronal activity.
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spelling doaj-art-2bd801b819f54039b58d0e6634ff886c2025-08-20T03:42:52ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842021-03-0113411810.15252/emmm.202012433The enhancement of activity rescues the establishment of Mecp2 null neuronal phenotypesLinda Scaramuzza0Giuseppina De Rocco1Genni Desiato2Clementina Cobolli Gigli3Martina Chiacchiaretta4Filippo Mirabella5Davide Pozzi6Marco De Simone7Paola Conforti8Massimiliano Pagani9Fabio Benfenati10Fabrizia Cesca11Francesco Bedogni12Nicoletta Landsberger13Division of Neuroscience, IRCCS San Raffaele Scientific InstituteDivision of Neuroscience, IRCCS San Raffaele Scientific InstituteIRCCS Humanitas Research HospitalDivision of Neuroscience, IRCCS San Raffaele Scientific InstituteCenter for Synaptic Neuroscience and Technology, Istituto Italiano di TecnologiaIRCCS Humanitas Research HospitalIRCCS Humanitas Research HospitalIstituto Nazionale Genetica Molecolare “Romeo ed Enrica Invernizzi”Istituto Nazionale Genetica Molecolare “Romeo ed Enrica Invernizzi”Department of Medical Biotechnology and Translational Medicine, University of MilanCenter for Synaptic Neuroscience and Technology, Istituto Italiano di TecnologiaCenter for Synaptic Neuroscience and Technology, Istituto Italiano di TecnologiaDivision of Neuroscience, IRCCS San Raffaele Scientific InstituteDivision of Neuroscience, IRCCS San Raffaele Scientific InstituteAbstract MECP2 mutations cause Rett syndrome (RTT), a severe and progressive neurodevelopmental disorder mainly affecting females. Although RTT patients exhibit delayed onset of symptoms, several evidences demonstrate that MeCP2 deficiency alters early development of the brain. Indeed, during early maturation, Mecp2 null cortical neurons display widespread transcriptional changes, reduced activity, and defective morphology. It has been proposed that during brain development these elements are linked in a feed‐forward cycle where neuronal activity drives transcriptional and morphological changes that further increase network maturity. We hypothesized that the enhancement of neuronal activity during early maturation might prevent the onset of RTT‐typical molecular and cellular phenotypes. Accordingly, we show that the enhancement of excitability, obtained by adding to neuronal cultures Ampakine CX546, rescues transcription of several genes, neuronal morphology, and responsiveness to stimuli. Greater effects are achieved in response to earlier treatments. In vivo, short and early administration of CX546 to Mecp2 null mice prolongs lifespan, delays the disease progression, and rescues motor abilities and spatial memory, thus confirming the value for RTT of an early restoration of neuronal activity.https://doi.org/10.15252/emmm.202012433AmpakineMecp2neuronal activityneuronal maturationRett syndrome
spellingShingle Linda Scaramuzza
Giuseppina De Rocco
Genni Desiato
Clementina Cobolli Gigli
Martina Chiacchiaretta
Filippo Mirabella
Davide Pozzi
Marco De Simone
Paola Conforti
Massimiliano Pagani
Fabio Benfenati
Fabrizia Cesca
Francesco Bedogni
Nicoletta Landsberger
The enhancement of activity rescues the establishment of Mecp2 null neuronal phenotypes
EMBO Molecular Medicine
Ampakine
Mecp2
neuronal activity
neuronal maturation
Rett syndrome
title The enhancement of activity rescues the establishment of Mecp2 null neuronal phenotypes
title_full The enhancement of activity rescues the establishment of Mecp2 null neuronal phenotypes
title_fullStr The enhancement of activity rescues the establishment of Mecp2 null neuronal phenotypes
title_full_unstemmed The enhancement of activity rescues the establishment of Mecp2 null neuronal phenotypes
title_short The enhancement of activity rescues the establishment of Mecp2 null neuronal phenotypes
title_sort enhancement of activity rescues the establishment of mecp2 null neuronal phenotypes
topic Ampakine
Mecp2
neuronal activity
neuronal maturation
Rett syndrome
url https://doi.org/10.15252/emmm.202012433
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