Female-specific dysfunction of sensory neocortical circuits in a mouse model of autism mediated by mGluR5 and estrogen receptor α
Little is known of the brain mechanisms that mediate sex-specific autism symptoms. Here, we demonstrate that deletion of the autism spectrum disorder (ASD)-risk gene, Pten, in neocortical pyramidal neurons (NSEPten knockout [KO]) results in robust cortical circuit hyperexcitability selectively in fe...
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| Published in: | Cell reports (Cambridge) Vol. 43; no. 4; p. 114056 |
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| Main Authors: | , , , , , , , , |
| Format: | Journal Article |
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| Abstract | Little is known of the brain mechanisms that mediate sex-specific autism symptoms. Here, we demonstrate that deletion of the autism spectrum disorder (ASD)-risk gene, Pten, in neocortical pyramidal neurons (NSEPten knockout [KO]) results in robust cortical circuit hyperexcitability selectively in female mice observed as prolonged spontaneous persistent activity states. Circuit hyperexcitability in females is mediated by metabotropic glutamate receptor 5 (mGluR5) and estrogen receptor α (ERα) signaling to mitogen-activated protein kinases (Erk1/2) and de novo protein synthesis. Pten KO layer 5 neurons have a female-specific increase in mGluR5 and mGluR5-dependent protein synthesis. Furthermore, mGluR5-ERα complexes are generally elevated in female cortices, and genetic reduction of ERα rescues enhanced circuit excitability, protein synthesis, and neuron size selectively in NSEPten KO females. Female NSEPten KO mice display deficits in sensory processing and social behaviors as well as mGluR5-dependent seizures. These results reveal mechanisms by which sex and a high-confidence ASD-risk gene interact to affect brain function and behavior.
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•Sex and a high-confidence ASD-risk gene, Pten, interact to affect brain function and behavior•Deletion of Pten causes robust hyperexcitability of neocortical circuits in female mice•Circuit hyperexcitability is driven by mGluR5 and ERα signaling to ERK and protein synthesis•Female Pten KO neurons have enhanced mGluR5 and ERα-dependent protein synthesis
Molinaro et al. report enhanced cortical circuit excitability, selectively in females, in mouse models of Pten deletion. Hyperexcitability is driven by mGluR5 and ERα signaling to ERK and protein synthesis. Enhanced mGluR5-ERα interactions and enhanced mGluR5-dependent protein synthesis in Pten KO neurons may drive female-specific circuit effects. |
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| AbstractList | Little is known of the brain mechanisms that mediate sex-specific autism symptoms. Here, we demonstrate that deletion of the autism spectrum disorder (ASD)-risk gene, Pten, in neocortical pyramidal neurons (NSEPten knockout [KO]) results in robust cortical circuit hyperexcitability selectively in female mice observed as prolonged spontaneous persistent activity states. Circuit hyperexcitability in females is mediated by metabotropic glutamate receptor 5 (mGluR5) and estrogen receptor α (ERα) signaling to mitogen-activated protein kinases (Erk1/2) and de novo protein synthesis. Pten KO layer 5 neurons have a female-specific increase in mGluR5 and mGluR5-dependent protein synthesis. Furthermore, mGluR5-ERα complexes are generally elevated in female cortices, and genetic reduction of ERα rescues enhanced circuit excitability, protein synthesis, and neuron size selectively in NSEPten KO females. Female NSEPten KO mice display deficits in sensory processing and social behaviors as well as mGluR5-dependent seizures. These results reveal mechanisms by which sex and a high-confidence ASD-risk gene interact to affect brain function and behavior. Little is known of the brain mechanisms that mediate sex-specific autism symptoms. Here, we demonstrate that deletion of the autism spectrum disorder (ASD)-risk gene, Pten, in neocortical pyramidal neurons ( Pten knockout [KO]) results in robust cortical circuit hyperexcitability selectively in female mice observed as prolonged spontaneous persistent activity states. Circuit hyperexcitability in females is mediated by metabotropic glutamate receptor 5 (mGluR5) and estrogen receptor α (ERα) signaling to mitogen-activated protein kinases (Erk1/2) and de novo protein synthesis. Pten KO layer 5 neurons have a female-specific increase in mGluR5 and mGluR5-dependent protein synthesis. Furthermore, mGluR5-ERα complexes are generally elevated in female cortices, and genetic reduction of ERα rescues enhanced circuit excitability, protein synthesis, and neuron size selectively in Pten KO females. Female Pten KO mice display deficits in sensory processing and social behaviors as well as mGluR5-dependent seizures. These results reveal mechanisms by which sex and a high-confidence ASD-risk gene interact to affect brain function and behavior. Little is known of the brain mechanisms that mediate sex-specific autism symptoms. Here, we demonstrate that deletion of the autism spectrum disorder (ASD)-risk gene, Pten, in neocortical pyramidal neurons (NSEPten knockout [KO]) results in robust cortical circuit hyperexcitability selectively in female mice observed as prolonged spontaneous persistent activity states. Circuit hyperexcitability in females is mediated by metabotropic glutamate receptor 5 (mGluR5) and estrogen receptor α (ERα) signaling to mitogen-activated protein kinases (Erk1/2) and de novo protein synthesis. Pten KO layer 5 neurons have a female-specific increase in mGluR5 and mGluR5-dependent protein synthesis. Furthermore, mGluR5-ERα complexes are generally elevated in female cortices, and genetic reduction of ERα rescues enhanced circuit excitability, protein synthesis, and neuron size selectively in NSEPten KO females. Female NSEPten KO mice display deficits in sensory processing and social behaviors as well as mGluR5-dependent seizures. These results reveal mechanisms by which sex and a high-confidence ASD-risk gene interact to affect brain function and behavior. [Display omitted] •Sex and a high-confidence ASD-risk gene, Pten, interact to affect brain function and behavior•Deletion of Pten causes robust hyperexcitability of neocortical circuits in female mice•Circuit hyperexcitability is driven by mGluR5 and ERα signaling to ERK and protein synthesis•Female Pten KO neurons have enhanced mGluR5 and ERα-dependent protein synthesis Molinaro et al. report enhanced cortical circuit excitability, selectively in females, in mouse models of Pten deletion. Hyperexcitability is driven by mGluR5 and ERα signaling to ERK and protein synthesis. Enhanced mGluR5-ERα interactions and enhanced mGluR5-dependent protein synthesis in Pten KO neurons may drive female-specific circuit effects. Little is known of the brain mechanisms that mediate sex-specific autism symptoms. Here, we demonstrate that deletion of the autism spectrum disorder (ASD)-risk gene, Pten , in neocortical pyramidal neurons ( NSE Pten knockout [KO]) results in robust cortical circuit hyperexcitability selectively in female mice observed as prolonged spontaneous persistent activity states. Circuit hyperexcitability in females is mediated by metabotropic glutamate receptor 5 (mGluR5) and estrogen receptor α (ERα) signaling to mitogen-activated protein kinases (Erk1/2) and de novo protein synthesis. Pten KO layer 5 neurons have a female-specific increase in mGluR5 and mGluR5-dependent protein synthesis. Furthermore, mGluR5-ERα complexes are generally elevated in female cortices, and genetic reduction of ERα rescues enhanced circuit excitability, protein synthesis, and neuron size selectively in NSE Pten KO females. Female NSE Pten KO mice display deficits in sensory processing and social behaviors as well as mGluR5-dependent seizures. These results reveal mechanisms by which sex and a high-confidence ASD-risk gene interact to affect brain function and behavior. Molinaro et al. report enhanced cortical circuit excitability, selectively in females, in mouse models of Pten deletion. Hyperexcitability is driven by mGluR5 and ERα signaling to ERK and protein synthesis. Enhanced mGluR5-ERα interactions and enhanced mGluR5-dependent protein synthesis in Pten KO neurons may drive female-specific circuit effects. |
| ArticleNumber | 114056 |
| Author | Huber, Kimberly M. Gonzalez, Darya Bowles, Jacob E. Molinaro, Gemma Birnbaum, Shari G. Razak, Khaleel A. Croom, Katilynne Mirjafary, Saba Gibson, Jay R. |
| AuthorAffiliation | 5 Lead contact 2 Department of Psychiatry, O’Donnell Brain Institute, UT Southwestern Medical Center, Dallas, TX, USA 3 Graduate Neuroscience Program, University of California, Riverside, Riverside, CA, USA 4 Department of Psychology, University of California, Riverside, Riverside, CA, USA 1 Department of Neuroscience, O’Donnell Brain Institute, UT Southwestern Medical Center, Dallas, TX, USA |
| AuthorAffiliation_xml | – name: 1 Department of Neuroscience, O’Donnell Brain Institute, UT Southwestern Medical Center, Dallas, TX, USA – name: 3 Graduate Neuroscience Program, University of California, Riverside, Riverside, CA, USA – name: 2 Department of Psychiatry, O’Donnell Brain Institute, UT Southwestern Medical Center, Dallas, TX, USA – name: 5 Lead contact – name: 4 Department of Psychology, University of California, Riverside, Riverside, CA, USA |
| Author_xml | – sequence: 1 givenname: Gemma surname: Molinaro fullname: Molinaro, Gemma organization: Department of Neuroscience, O’Donnell Brain Institute, UT Southwestern Medical Center, Dallas, TX, USA – sequence: 2 givenname: Jacob E. surname: Bowles fullname: Bowles, Jacob E. organization: Department of Neuroscience, O’Donnell Brain Institute, UT Southwestern Medical Center, Dallas, TX, USA – sequence: 3 givenname: Katilynne surname: Croom fullname: Croom, Katilynne organization: Graduate Neuroscience Program, University of California, Riverside, Riverside, CA, USA – sequence: 4 givenname: Darya surname: Gonzalez fullname: Gonzalez, Darya organization: Department of Neuroscience, O’Donnell Brain Institute, UT Southwestern Medical Center, Dallas, TX, USA – sequence: 5 givenname: Saba surname: Mirjafary fullname: Mirjafary, Saba organization: Department of Neuroscience, O’Donnell Brain Institute, UT Southwestern Medical Center, Dallas, TX, USA – sequence: 6 givenname: Shari G. surname: Birnbaum fullname: Birnbaum, Shari G. organization: Department of Psychiatry, O’Donnell Brain Institute, UT Southwestern Medical Center, Dallas, TX, USA – sequence: 7 givenname: Khaleel A. surname: Razak fullname: Razak, Khaleel A. organization: Graduate Neuroscience Program, University of California, Riverside, Riverside, CA, USA – sequence: 8 givenname: Jay R. surname: Gibson fullname: Gibson, Jay R. organization: Department of Neuroscience, O’Donnell Brain Institute, UT Southwestern Medical Center, Dallas, TX, USA – sequence: 9 givenname: Kimberly M. orcidid: 0000-0002-7479-0661 surname: Huber fullname: Huber, Kimberly M. email: kimberly.huber@utsouthwestern.edu organization: Department of Neuroscience, O’Donnell Brain Institute, UT Southwestern Medical Center, Dallas, TX, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38581678$$D View this record in MEDLINE/PubMed |
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| Copyright | 2024 The Authors Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved. |
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| Keywords | UP state circuit excitability CP: Cell biology ERα signal transduction CP: Neuroscience PTEN protein synthesis somatosensory cortex mGluR5 cell size autism |
| Language | English |
| License | This is an open access article under the CC BY-NC-ND license. Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS G.M.: conceptualization, investigation, formal analysis, writing – original draft. J.E.B.: investigation. K.C.: investigation, formal analysis. D.G.: investigation. S.M.: investigation. S.G.B.: conceptualization, supervision. K.A.R.: conceptualization, supervision, formal analysis. J.R.G.: conceptualization, supervision, validation. K.M.H.: conceptualization, formal analysis, writing, supervision, funding acquisition. |
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| Title | Female-specific dysfunction of sensory neocortical circuits in a mouse model of autism mediated by mGluR5 and estrogen receptor α |
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