MEF2 negatively regulates learning-induced structural plasticity and memory formation
The authors report that endogenous myocyte enhance factor 2 (MEF2) levels affect spatial and fear memory formation in adult mice. MEF2-induced memory disruption was rescued by interfering with AMPA receptor endocytosis. Memory formation is thought to be mediated by dendritic-spine growth and restruc...
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| Veröffentlicht in: | Nature neuroscience 2012-09, Vol.15 (9), p.1255-1264 |
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| creator | Cole, Christina J Mercaldo, Valentina Restivo, Leonardo Yiu, Adelaide P Sekeres, Melanie J Han, Jin-Hee Vetere, Gisella Pekar, Tetyana Ross, P Joel Neve, Rachael L Frankland, Paul W Josselyn, Sheena A |
| description | The authors report that endogenous myocyte enhance factor 2 (MEF2) levels affect spatial and fear memory formation in adult mice. MEF2-induced memory disruption was rescued by interfering with AMPA receptor endocytosis.
Memory formation is thought to be mediated by dendritic-spine growth and restructuring. Myocyte enhancer factor 2 (MEF2) restricts spine growth
in vitro
, suggesting that this transcription factor negatively regulates the spine remodeling necessary for memory formation. Here we show that memory formation in adult mice was associated with changes in endogenous MEF2 levels and function. Locally and acutely increasing MEF2 function in the dentate gyrus blocked both learning-induced increases in spine density and spatial-memory formation. Increasing MEF2 function in amygdala disrupted fear-memory formation. We rescued MEF2-induced memory disruption by interfering with AMPA receptor endocytosis, suggesting that AMPA receptor trafficking is a key mechanism underlying the effects of MEF2. In contrast, decreasing MEF2 function in dentate gyrus and amygdala facilitated the formation of spatial and fear memory, respectively. These bidirectional effects indicate that MEF2 is a key regulator of plasticity and that relieving the suppressive effects of MEF2-mediated transcription permits memory formation. |
| doi_str_mv | 10.1038/nn.3189 |
| format | Article |
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Memory formation is thought to be mediated by dendritic-spine growth and restructuring. Myocyte enhancer factor 2 (MEF2) restricts spine growth
in vitro
, suggesting that this transcription factor negatively regulates the spine remodeling necessary for memory formation. Here we show that memory formation in adult mice was associated with changes in endogenous MEF2 levels and function. Locally and acutely increasing MEF2 function in the dentate gyrus blocked both learning-induced increases in spine density and spatial-memory formation. Increasing MEF2 function in amygdala disrupted fear-memory formation. We rescued MEF2-induced memory disruption by interfering with AMPA receptor endocytosis, suggesting that AMPA receptor trafficking is a key mechanism underlying the effects of MEF2. In contrast, decreasing MEF2 function in dentate gyrus and amygdala facilitated the formation of spatial and fear memory, respectively. These bidirectional effects indicate that MEF2 is a key regulator of plasticity and that relieving the suppressive effects of MEF2-mediated transcription permits memory formation.</description><identifier>ISSN: 1097-6256</identifier><identifier>EISSN: 1546-1726</identifier><identifier>DOI: 10.1038/nn.3189</identifier><identifier>PMID: 22885849</identifier><identifier>CODEN: NANEFN</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>631/208/200 ; 631/378/1595 ; 631/378/2591 ; Amygdala - metabolism ; Amygdala - physiology ; Animal Genetics and Genomics ; Animals ; Behavioral Sciences ; Biological Techniques ; Biomedical and Life Sciences ; Biomedicine ; Blotting, Western ; Conditioning (Psychology) - physiology ; Dendritic Spines - physiology ; Dependovirus ; Endocytosis - physiology ; Fear ; Female ; Genetic Vectors ; Hippocampus - cytology ; Hippocampus - physiology ; Immunohistochemistry ; In Situ Hybridization, Fluorescence ; Learning - physiology ; Luciferases - genetics ; Male ; Maze Learning - physiology ; MEF2 Transcription Factors ; Memory ; Memory - physiology ; Mice ; Mice, Inbred C57BL ; Myogenic Regulatory Factors - genetics ; Myogenic Regulatory Factors - physiology ; Neurobiology ; Neuronal Plasticity - physiology ; Neurons - physiology ; Neuroplasticity ; Neurosciences ; Physiological aspects ; Proteins ; Receptors, AMPA - physiology ; Simplexvirus - genetics ; Transcription factors</subject><ispartof>Nature neuroscience, 2012-09, Vol.15 (9), p.1255-1264</ispartof><rights>Springer Nature America, Inc. 2012</rights><rights>COPYRIGHT 2012 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Sep 2012</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c542t-27d475d09bb76420689305c02d9428bc2684c3ca8678815588718b189fe79f503</citedby><cites>FETCH-LOGICAL-c542t-27d475d09bb76420689305c02d9428bc2684c3ca8678815588718b189fe79f503</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/nn.3189$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/nn.3189$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22885849$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Cole, Christina J</creatorcontrib><creatorcontrib>Mercaldo, Valentina</creatorcontrib><creatorcontrib>Restivo, Leonardo</creatorcontrib><creatorcontrib>Yiu, Adelaide P</creatorcontrib><creatorcontrib>Sekeres, Melanie J</creatorcontrib><creatorcontrib>Han, Jin-Hee</creatorcontrib><creatorcontrib>Vetere, Gisella</creatorcontrib><creatorcontrib>Pekar, Tetyana</creatorcontrib><creatorcontrib>Ross, P Joel</creatorcontrib><creatorcontrib>Neve, Rachael L</creatorcontrib><creatorcontrib>Frankland, Paul W</creatorcontrib><creatorcontrib>Josselyn, Sheena A</creatorcontrib><title>MEF2 negatively regulates learning-induced structural plasticity and memory formation</title><title>Nature neuroscience</title><addtitle>Nat Neurosci</addtitle><addtitle>Nat Neurosci</addtitle><description>The authors report that endogenous myocyte enhance factor 2 (MEF2) levels affect spatial and fear memory formation in adult mice. MEF2-induced memory disruption was rescued by interfering with AMPA receptor endocytosis.
Memory formation is thought to be mediated by dendritic-spine growth and restructuring. Myocyte enhancer factor 2 (MEF2) restricts spine growth
in vitro
, suggesting that this transcription factor negatively regulates the spine remodeling necessary for memory formation. Here we show that memory formation in adult mice was associated with changes in endogenous MEF2 levels and function. Locally and acutely increasing MEF2 function in the dentate gyrus blocked both learning-induced increases in spine density and spatial-memory formation. Increasing MEF2 function in amygdala disrupted fear-memory formation. We rescued MEF2-induced memory disruption by interfering with AMPA receptor endocytosis, suggesting that AMPA receptor trafficking is a key mechanism underlying the effects of MEF2. In contrast, decreasing MEF2 function in dentate gyrus and amygdala facilitated the formation of spatial and fear memory, respectively. These bidirectional effects indicate that MEF2 is a key regulator of plasticity and that relieving the suppressive effects of MEF2-mediated transcription permits memory formation.</description><subject>631/208/200</subject><subject>631/378/1595</subject><subject>631/378/2591</subject><subject>Amygdala - metabolism</subject><subject>Amygdala - physiology</subject><subject>Animal Genetics and Genomics</subject><subject>Animals</subject><subject>Behavioral Sciences</subject><subject>Biological Techniques</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Blotting, Western</subject><subject>Conditioning (Psychology) - physiology</subject><subject>Dendritic Spines - physiology</subject><subject>Dependovirus</subject><subject>Endocytosis - physiology</subject><subject>Fear</subject><subject>Female</subject><subject>Genetic Vectors</subject><subject>Hippocampus - cytology</subject><subject>Hippocampus - physiology</subject><subject>Immunohistochemistry</subject><subject>In Situ Hybridization, Fluorescence</subject><subject>Learning - physiology</subject><subject>Luciferases - genetics</subject><subject>Male</subject><subject>Maze Learning - physiology</subject><subject>MEF2 Transcription Factors</subject><subject>Memory</subject><subject>Memory - physiology</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Myogenic Regulatory Factors - genetics</subject><subject>Myogenic Regulatory Factors - physiology</subject><subject>Neurobiology</subject><subject>Neuronal Plasticity - physiology</subject><subject>Neurons - physiology</subject><subject>Neuroplasticity</subject><subject>Neurosciences</subject><subject>Physiological aspects</subject><subject>Proteins</subject><subject>Receptors, AMPA - physiology</subject><subject>Simplexvirus - genetics</subject><subject>Transcription factors</subject><issn>1097-6256</issn><issn>1546-1726</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqNkl1rFTEQhoMotlbxH8iCF-rFHrPZfEwuS2m1UBHUXi_Z7OySsps95qN4_r05tFqPeCG5SJg88_K-wxDysqGbhrbw3vtN24B-RI4bwWXdKCYflzfVqpZMyCPyLMYbSqkSoJ-SI8YABHB9TK4_nV-wyuNkkrvFeVcFnPJsEsZqRhO881Pt_JAtDlVMIduUg5mr7WxictalXWX8UC24rGFXjWtYis7qn5Mno5kjvri_T8j1xfm3s4_11ecPl2enV7UVnKWaqYErMVDd90pyRiXolgpL2aA5g94yCdy21oBUAI0QAKqBvuQcUelR0PaEvL3T3Yb1e8aYusVFi_NsPK45dmUALZegQPwH2iopKRO6oK__Qm_WHHwJsqeKNUUlf6AmM2Pn_LimYOxetDttKWsa3oIs1OYfVDkDLs6uHkdX6gcN7w4aCpPwR5pMjrG7_PrlkH1zx9qwxhhw7LbBLSbsis-9Vei87_Z7UchX95Fyv-Dwm_u1CA_jieXLTxj-zHyo9RNltrtq</recordid><startdate>20120901</startdate><enddate>20120901</enddate><creator>Cole, Christina J</creator><creator>Mercaldo, Valentina</creator><creator>Restivo, Leonardo</creator><creator>Yiu, Adelaide P</creator><creator>Sekeres, Melanie J</creator><creator>Han, Jin-Hee</creator><creator>Vetere, Gisella</creator><creator>Pekar, Tetyana</creator><creator>Ross, P Joel</creator><creator>Neve, Rachael L</creator><creator>Frankland, Paul W</creator><creator>Josselyn, Sheena A</creator><general>Nature Publishing Group US</general><general>Nature Publishing Group</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U7</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20120901</creationdate><title>MEF2 negatively regulates learning-induced structural plasticity and memory formation</title><author>Cole, Christina J ; Mercaldo, Valentina ; Restivo, Leonardo ; Yiu, Adelaide P ; Sekeres, Melanie J ; Han, Jin-Hee ; Vetere, Gisella ; Pekar, Tetyana ; Ross, P Joel ; Neve, Rachael L ; Frankland, Paul W ; Josselyn, Sheena A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c542t-27d475d09bb76420689305c02d9428bc2684c3ca8678815588718b189fe79f503</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>631/208/200</topic><topic>631/378/1595</topic><topic>631/378/2591</topic><topic>Amygdala - metabolism</topic><topic>Amygdala - physiology</topic><topic>Animal Genetics and Genomics</topic><topic>Animals</topic><topic>Behavioral Sciences</topic><topic>Biological Techniques</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Blotting, Western</topic><topic>Conditioning (Psychology) - physiology</topic><topic>Dendritic Spines - physiology</topic><topic>Dependovirus</topic><topic>Endocytosis - physiology</topic><topic>Fear</topic><topic>Female</topic><topic>Genetic Vectors</topic><topic>Hippocampus - cytology</topic><topic>Hippocampus - physiology</topic><topic>Immunohistochemistry</topic><topic>In Situ Hybridization, Fluorescence</topic><topic>Learning - physiology</topic><topic>Luciferases - genetics</topic><topic>Male</topic><topic>Maze Learning - physiology</topic><topic>MEF2 Transcription Factors</topic><topic>Memory</topic><topic>Memory - physiology</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Myogenic Regulatory Factors - genetics</topic><topic>Myogenic Regulatory Factors - physiology</topic><topic>Neurobiology</topic><topic>Neuronal Plasticity - physiology</topic><topic>Neurons - physiology</topic><topic>Neuroplasticity</topic><topic>Neurosciences</topic><topic>Physiological aspects</topic><topic>Proteins</topic><topic>Receptors, AMPA - physiology</topic><topic>Simplexvirus - genetics</topic><topic>Transcription factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Cole, Christina J</creatorcontrib><creatorcontrib>Mercaldo, Valentina</creatorcontrib><creatorcontrib>Restivo, Leonardo</creatorcontrib><creatorcontrib>Yiu, Adelaide P</creatorcontrib><creatorcontrib>Sekeres, Melanie J</creatorcontrib><creatorcontrib>Han, Jin-Hee</creatorcontrib><creatorcontrib>Vetere, Gisella</creatorcontrib><creatorcontrib>Pekar, Tetyana</creatorcontrib><creatorcontrib>Ross, P Joel</creatorcontrib><creatorcontrib>Neve, Rachael L</creatorcontrib><creatorcontrib>Frankland, Paul W</creatorcontrib><creatorcontrib>Josselyn, Sheena A</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Science in Context</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Psychology Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Nature neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cole, Christina J</au><au>Mercaldo, Valentina</au><au>Restivo, Leonardo</au><au>Yiu, Adelaide P</au><au>Sekeres, Melanie J</au><au>Han, Jin-Hee</au><au>Vetere, Gisella</au><au>Pekar, Tetyana</au><au>Ross, P Joel</au><au>Neve, Rachael L</au><au>Frankland, Paul W</au><au>Josselyn, Sheena A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>MEF2 negatively regulates learning-induced structural plasticity and memory formation</atitle><jtitle>Nature neuroscience</jtitle><stitle>Nat Neurosci</stitle><addtitle>Nat Neurosci</addtitle><date>2012-09-01</date><risdate>2012</risdate><volume>15</volume><issue>9</issue><spage>1255</spage><epage>1264</epage><pages>1255-1264</pages><issn>1097-6256</issn><eissn>1546-1726</eissn><coden>NANEFN</coden><abstract>The authors report that endogenous myocyte enhance factor 2 (MEF2) levels affect spatial and fear memory formation in adult mice. MEF2-induced memory disruption was rescued by interfering with AMPA receptor endocytosis.
Memory formation is thought to be mediated by dendritic-spine growth and restructuring. Myocyte enhancer factor 2 (MEF2) restricts spine growth
in vitro
, suggesting that this transcription factor negatively regulates the spine remodeling necessary for memory formation. Here we show that memory formation in adult mice was associated with changes in endogenous MEF2 levels and function. Locally and acutely increasing MEF2 function in the dentate gyrus blocked both learning-induced increases in spine density and spatial-memory formation. Increasing MEF2 function in amygdala disrupted fear-memory formation. We rescued MEF2-induced memory disruption by interfering with AMPA receptor endocytosis, suggesting that AMPA receptor trafficking is a key mechanism underlying the effects of MEF2. In contrast, decreasing MEF2 function in dentate gyrus and amygdala facilitated the formation of spatial and fear memory, respectively. These bidirectional effects indicate that MEF2 is a key regulator of plasticity and that relieving the suppressive effects of MEF2-mediated transcription permits memory formation.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>22885849</pmid><doi>10.1038/nn.3189</doi><tpages>10</tpages></addata></record> |
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| subjects | 631/208/200 631/378/1595 631/378/2591 Amygdala - metabolism Amygdala - physiology Animal Genetics and Genomics Animals Behavioral Sciences Biological Techniques Biomedical and Life Sciences Biomedicine Blotting, Western Conditioning (Psychology) - physiology Dendritic Spines - physiology Dependovirus Endocytosis - physiology Fear Female Genetic Vectors Hippocampus - cytology Hippocampus - physiology Immunohistochemistry In Situ Hybridization, Fluorescence Learning - physiology Luciferases - genetics Male Maze Learning - physiology MEF2 Transcription Factors Memory Memory - physiology Mice Mice, Inbred C57BL Myogenic Regulatory Factors - genetics Myogenic Regulatory Factors - physiology Neurobiology Neuronal Plasticity - physiology Neurons - physiology Neuroplasticity Neurosciences Physiological aspects Proteins Receptors, AMPA - physiology Simplexvirus - genetics Transcription factors |
| title | MEF2 negatively regulates learning-induced structural plasticity and memory formation |
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