An Autism-Associated Variant of Epac2 Reveals a Role for Ras/Epac2 Signaling in Controlling Basal Dendrite Maintenance in Mice
The architecture of dendritic arbors determines circuit connectivity, receptive fields, and computational properties of neurons, and dendritic structure is impaired in several psychiatric disorders. While apical and basal dendritic compartments of pyramidal neurons are functionally specialized and d...
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| Published in | PLoS biology Vol. 10; no. 6; p. e1001350 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.06.2012
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1545-7885 1544-9173 1545-7885 |
| DOI | 10.1371/journal.pbio.1001350 |
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| Abstract | The architecture of dendritic arbors determines circuit connectivity, receptive fields, and computational properties of neurons, and dendritic structure is impaired in several psychiatric disorders. While apical and basal dendritic compartments of pyramidal neurons are functionally specialized and differentially regulated, little is known about mechanisms that selectively maintain basal dendrites. Here we identified a role for the Ras/Epac2 pathway in maintaining basal dendrite complexity of cortical neurons. Epac2 is a guanine nucleotide exchange factor (GEF) for the Ras-like small GTPase Rap, and it is highly enriched in the adult mouse brain. We found that in vivo Epac2 knockdown in layer 2/3 cortical neurons via in utero electroporation reduced basal dendritic architecture, and that Epac2 knockdown in mature cortical neurons in vitro mimicked this effect. Overexpression of an Epac2 rare coding variant, found in human subjects diagnosed with autism, also impaired basal dendritic morphology. This mutation disrupted Epac2's interaction with Ras, and inhibition of Ras selectively interfered with basal dendrite maintenance. Finally, we observed that components of the Ras/Epac2/Rap pathway exhibited differential abundance in the basal versus apical dendritic compartments. These findings define a role for Epac2 in enabling crosstalk between Ras and Rap signaling in maintaining basal dendrite complexity, and exemplify how rare coding variants, in addition to their disease relevance, can provide insight into cellular mechanisms relevant for brain connectivity. |
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| AbstractList | The architecture of dendritic arbors determines circuit connectivity, receptive fields, and computational properties of neurons, and dendritic structure is impaired in several psychiatric disorders. While apical and basal dendritic compartments of pyramidal neurons are functionally specialized and differentially regulated, little is known about mechanisms that selectively maintain basal dendrites. Here we identified a role for the Ras/Epac2 pathway in maintaining basal dendrite complexity of cortical neurons. Epac2 is a guanine nucleotide exchange factor (GEF) for the Ras-like small GTPase Rap, and it is highly enriched in the adult mouse brain. We found that in vivo Epac2 knockdown in layer 2/3 cortical neurons via in utero electroporation reduced basal dendritic architecture, and that Epac2 knockdown in mature cortical neurons in vitro mimicked this effect. Overexpression of an Epac2 rare coding variant, found in human subjects diagnosed with autism, also impaired basal dendritic morphology. This mutation disrupted Epac2's interaction with Ras, and inhibition of Ras selectively interfered with basal dendrite maintenance. Finally, we observed that components of the Ras/Epac2/Rap pathway exhibited differential abundance in the basal versus apical dendritic compartments. These findings define a role for Epac2 in enabling crosstalk between Ras and Rap signaling in maintaining basal dendrite complexity, and exemplify how rare coding variants, in addition to their disease relevance, can provide insight into cellular mechanisms relevant for brain connectivity. The architecture of dendritic arbors determines circuit connectivity, receptive fields, and computational properties of neurons, and dendritic structure is impaired in several psychiatric disorders. While apical and basal dendritic compartments of pyramidal neurons are functionally specialized and differentially regulated, little is known about mechanisms that selectively maintain basal dendrites. Here we identified a role for the Ras/Epac2 pathway in maintaining basal dendrite complexity of cortical neurons. Epac2 is a guanine nucleotide exchange factor (GEF) for the Ras-like small GTPase Rap, and it is highly enriched in the adult mouse brain. We found that in vivo Epac2 knockdown in layer 2/3 cortical neurons via in utero electroporation reduced basal dendritic architecture, and that Epac2 knockdown in mature cortical neurons in vitro mimicked this effect. Over expression of an Epac2 rare coding variant, found in human subjects diagnosed with autism, also impaired basal dendritic morphology. This mutation disrupted Epac2's interaction with Ras, and inhibition of Ras selectively interfered with basal dendrite maintenance. Finally, we observed that components of the Ras/Epac2/Rap pathway exhibited differential abundance in the basal versus apical dendritic compartments. These findings define a role for Epac2 in enabling crosstalk between Ras and Rap signaling in maintaining basal dendrite complexity, and exemplify how rare coding variants, in addition to their disease relevance, can provide insight into cellular mechanisms relevant for brain connectivity. Epac2 disruption impairs basal (but not apical) dendrite complexity in cortical neurons, and an autism-associated mutation in Epac2 implicates a Ras/Epac2 signaling pathway in the active maintenance of basal dendritic arbors. The architecture of dendritic arbors determines circuit connectivity, receptive fields, and computational properties of neurons, and dendritic structure is impaired in several psychiatric disorders. While apical and basal dendritic compartments of pyramidal neurons are functionally specialized and differentially regulated, little is known about mechanisms that selectively maintain basal dendrites. Here we identified a role for the Ras/Epac2 pathway in maintaining basal dendrite complexity of cortical neurons. Epac2 is a guanine nucleotide exchange factor (GEF) for the Ras-like small GTPase Rap, and it is highly enriched in the adult mouse brain. We found that in vivo Epac2 knockdown in layer 2/3 cortical neurons via in utero electroporation reduced basal dendritic architecture, and that Epac2 knockdown in mature cortical neurons in vitro mimicked this effect. Overexpression of an Epac2 rare coding variant, found in human subjects diagnosed with autism, also impaired basal dendritic morphology. This mutation disrupted Epac2's interaction with Ras, and inhibition of Ras selectively interfered with basal dendrite maintenance. Finally, we observed that components of the Ras/Epac2/Rap pathway exhibited differential abundance in the basal versus apical dendritic compartments. These findings define a role for Epac2 in enabling crosstalk between Ras and Rap signaling in maintaining basal dendrite complexity, and exemplify how rare coding variants, in addition to their disease relevance, can provide insight into cellular mechanisms relevant for brain connectivity. A fundamental feature of a neuron is the morphology of its dendrites, which are the processes that receive and integrate synaptic signals from other neurons. Neurons in the mammalian cortex exhibit two distinct dendritic arbors: apical dendrites, which extend far from the cell body, and basal dendrites, which elaborate locally around the cell body. After development, neurons must actively maintain each of these dendritic arbors to sustain their specific connectivity. Because several neurological and neurodevelopmental disorders are associated with disruptions in dendritic morphology, it is crucial to understand the molecular mechanisms that regulate the process of active maintenance of dendritic arbors. We find that disruption of a particular molecular pathway, the Ras-Epac2 pathway, can result in dramatic simplification of basal, but not apical, dendritic arbors in both cultured neurons and in the intact mouse brain. We show that a mutant form of Epac2, identified in patients with autism, also impairs basal dendrite maintenance and disrupts its interaction with Ras. Our findings suggest that specific molecular pathways can regulate distinct dendritic regions, and that disease-related mutations can inform our understanding of the molecules that regulate important biological processes. The architecture of dendritic arbors determines circuit connectivity, receptive fields, and computational properties of neurons, and dendritic structure is impaired in several psychiatric disorders. While apical and basal dendritic compartments of pyramidal neurons are functionally specialized and differentially regulated, little is known about mechanisms that selectively maintain basal dendrites. Here we identified a role for the Ras/Epac2 pathway in maintaining basal dendrite complexity of cortical neurons. Epac2 is a guanine nucleotide exchange factor (GEF) for the Ras-like small GTPase Rap, and it is highly enriched in the adult mouse brain. We found that in vivo Epac2 knockdown in layer 2/3 cortical neurons via in utero electroporation reduced basal dendritic architecture, and that Epac2 knockdown in mature cortical neurons in vitro mimicked this effect. Overexpression of an Epac2 rare coding variant, found in human subjects diagnosed with autism, also impaired basal dendritic morphology. This mutation disrupted Epac2's interaction with Ras, and inhibition of Ras selectively interfered with basal dendrite maintenance. Finally, we observed that components of the Ras/Epac2/Rap pathway exhibited differential abundance in the basal versus apical dendritic compartments. These findings define a role for Epac2 in enabling crosstalk between Ras and Rap signaling in maintaining basal dendrite complexity, and exemplify how rare coding variants, in addition to their disease relevance, can provide insight into cellular mechanisms relevant for brain connectivity. The architecture of dendritic arbors determines circuit connectivity, receptive fields, and computational properties of neurons, and dendritic structure is impaired in several psychiatric disorders. While apical and basal dendritic compartments of pyramidal neurons are functionally specialized and differentially regulated, little is known about mechanisms that selectively maintain basal dendrites. Here we identified a role for the Ras/Epac2 pathway in maintaining basal dendrite complexity of cortical neurons. Epac2 is a guanine nucleotide exchange factor (GEF) for the Ras-like small GTPase Rap, and it is highly enriched in the adult mouse brain. We found that in vivo Epac2 knockdown in layer 2/3 cortical neurons via in utero electroporation reduced basal dendritic architecture, and that Epac2 knockdown in mature cortical neurons in vitro mimicked this effect. Overexpression of an Epac2 rare coding variant, found in human subjects diagnosed with autism, also impaired basal dendritic morphology. This mutation disrupted Epac2's interaction with Ras, and inhibition of Ras selectively interfered with basal dendrite maintenance. Finally, we observed that components of the Ras/Epac2/Rap pathway exhibited differential abundance in the basal versus apical dendritic compartments. These findings define a role for Epac2 in enabling crosstalk between Ras and Rap signaling in maintaining basal dendrite complexity, and exemplify how rare coding variants, in addition to their disease relevance, can provide insight into cellular mechanisms relevant for brain connectivity.The architecture of dendritic arbors determines circuit connectivity, receptive fields, and computational properties of neurons, and dendritic structure is impaired in several psychiatric disorders. While apical and basal dendritic compartments of pyramidal neurons are functionally specialized and differentially regulated, little is known about mechanisms that selectively maintain basal dendrites. Here we identified a role for the Ras/Epac2 pathway in maintaining basal dendrite complexity of cortical neurons. Epac2 is a guanine nucleotide exchange factor (GEF) for the Ras-like small GTPase Rap, and it is highly enriched in the adult mouse brain. We found that in vivo Epac2 knockdown in layer 2/3 cortical neurons via in utero electroporation reduced basal dendritic architecture, and that Epac2 knockdown in mature cortical neurons in vitro mimicked this effect. Overexpression of an Epac2 rare coding variant, found in human subjects diagnosed with autism, also impaired basal dendritic morphology. This mutation disrupted Epac2's interaction with Ras, and inhibition of Ras selectively interfered with basal dendrite maintenance. Finally, we observed that components of the Ras/Epac2/Rap pathway exhibited differential abundance in the basal versus apical dendritic compartments. These findings define a role for Epac2 in enabling crosstalk between Ras and Rap signaling in maintaining basal dendrite complexity, and exemplify how rare coding variants, in addition to their disease relevance, can provide insight into cellular mechanisms relevant for brain connectivity. |
| Audience | Academic |
| Author | Penzes, Peter Russell, Theron A. Shepherd, Gordon M. G. Smith, Katharine R. Woolfrey, Kevin M. Yasvoina, Marina V. Srivastava, Deepak P. Lee, Hyerin Wokosin, David L. Jones, Kelly A. Anderson, Charles T. Ozdinler, P. Hande |
| AuthorAffiliation | 3 Weinberg College of Arts and Sciences, Northwestern University, Evanston, Illinois, United States of America University of Cambridge, United Kingdom 4 Davee Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, Illinois, United States of America 7 Department of Psychiatry and Behavioral Sciences, Northwestern University Feinberg School of Medicine, Chicago, Illinois, United States of America 1 Department of Physiology, Northwestern University Feinberg School of Medicine, Chicago, Illinois, United States of America 2 Department of Neuroscience & Centre for the Cellular Basis of Behaviour, The James Black Centre, King's College London, Institute of Psychiatry, London, United Kingdom 6 Lurie Cancer Research Center, Northwestern University Feinberg School of Medicine, Chicago, Illinois, United States of America 5 Cognitive Neurology and Disease Center, Northwestern University Feinberg School of Medicine, Chicago, Illinois, United States of America |
| AuthorAffiliation_xml | – name: 6 Lurie Cancer Research Center, Northwestern University Feinberg School of Medicine, Chicago, Illinois, United States of America – name: 7 Department of Psychiatry and Behavioral Sciences, Northwestern University Feinberg School of Medicine, Chicago, Illinois, United States of America – name: University of Cambridge, United Kingdom – name: 2 Department of Neuroscience & Centre for the Cellular Basis of Behaviour, The James Black Centre, King's College London, Institute of Psychiatry, London, United Kingdom – name: 3 Weinberg College of Arts and Sciences, Northwestern University, Evanston, Illinois, United States of America – name: 1 Department of Physiology, Northwestern University Feinberg School of Medicine, Chicago, Illinois, United States of America – name: 5 Cognitive Neurology and Disease Center, Northwestern University Feinberg School of Medicine, Chicago, Illinois, United States of America – name: 4 Davee Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, Illinois, United States of America |
| Author_xml | – sequence: 1 givenname: Deepak P. surname: Srivastava fullname: Srivastava, Deepak P. – sequence: 2 givenname: Kevin M. surname: Woolfrey fullname: Woolfrey, Kevin M. – sequence: 3 givenname: Kelly A. surname: Jones fullname: Jones, Kelly A. – sequence: 4 givenname: Charles T. surname: Anderson fullname: Anderson, Charles T. – sequence: 5 givenname: Katharine R. surname: Smith fullname: Smith, Katharine R. – sequence: 6 givenname: Theron A. surname: Russell fullname: Russell, Theron A. – sequence: 7 givenname: Hyerin surname: Lee fullname: Lee, Hyerin – sequence: 8 givenname: Marina V. surname: Yasvoina fullname: Yasvoina, Marina V. – sequence: 9 givenname: David L. surname: Wokosin fullname: Wokosin, David L. – sequence: 10 givenname: P. Hande surname: Ozdinler fullname: Ozdinler, P. Hande – sequence: 11 givenname: Gordon M. G. surname: Shepherd fullname: Shepherd, Gordon M. G. – sequence: 12 givenname: Peter surname: Penzes fullname: Penzes, Peter |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22745599$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2012 Public Library of Science 2012 Srivastava et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Srivastava DP, Woolfrey KM, Jones KA, Anderson CT, Smith KR, et al. (2012) An Autism-Associated Variant of Epac2 Reveals a Role for Ras/Epac2 Signaling in Controlling Basal Dendrite Maintenance in Mice. PLoS Biol 10(6): e1001350. doi:10.1371/journal.pbio.1001350 Srivastava et al. 2012 |
| Copyright_xml | – notice: COPYRIGHT 2012 Public Library of Science – notice: 2012 Srivastava et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Srivastava DP, Woolfrey KM, Jones KA, Anderson CT, Smith KR, et al. (2012) An Autism-Associated Variant of Epac2 Reveals a Role for Ras/Epac2 Signaling in Controlling Basal Dendrite Maintenance in Mice. PLoS Biol 10(6): e1001350. doi:10.1371/journal.pbio.1001350 – notice: Srivastava et al. 2012 |
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| Issue | 6 |
| Keywords | ras Proteins Signal Transduction Autistic Disorder Neurons Humans Mice, Inbred C57BL Cell Communication Rats Rats, Sprague-Dawley Guanine Nucleotide Exchange Factors Animals HEK293 Cells Female Dendrites Mice |
| Language | English |
| License | This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. Creative Commons Attribution License |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: DPS KMW PHO GMGS PP. Performed the experiments: DPS KMW KAJ CTA TAR HL MVY KRS. Analyzed the data: DPS KMW CTA KRS DLW PHO GMGS PP. Contributed reagents/materials/analysis tools: DLW PHO GMGS. Wrote the paper: DPS KMW KAJ PP. |
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| Snippet | The architecture of dendritic arbors determines circuit connectivity, receptive fields, and computational properties of neurons, and dendritic structure is... Epac2 disruption impairs basal (but not apical) dendrite complexity in cortical neurons, and an autism-associated mutation in Epac2 implicates a Ras/Epac2... The architecture of dendritic arbors determines circuit connectivity, receptive fields, and computational properties of neurons, and dendritic structure is... |
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| SubjectTerms | Alliances Animals Autism Autistic Disorder - genetics Autistic Disorder - metabolism Biology Brain research Cell Communication Dendrites Dendrites - metabolism Development and progression Experiments Female Guanine Nucleotide Exchange Factors - genetics Guanine Nucleotide Exchange Factors - metabolism Health aspects HEK293 Cells Humans Mental disorders Mice Mice, Inbred C57BL Mutation Neural circuitry Neurons Neurons - metabolism Physiological aspects Proteins ras Proteins Rats Rats, Sprague-Dawley Schizophrenia Signal Transduction |
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| Title | An Autism-Associated Variant of Epac2 Reveals a Role for Ras/Epac2 Signaling in Controlling Basal Dendrite Maintenance in Mice |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/22745599 https://www.proquest.com/docview/1303654235 https://www.proquest.com/docview/1022864919 https://pubmed.ncbi.nlm.nih.gov/PMC3383751 https://doaj.org/article/82bebeeb8c44423d9a906dbfb32001e3 http://dx.doi.org/10.1371/journal.pbio.1001350 |
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