Postsynaptic adhesion GPCR latrophilin-2 mediates target recognition in entorhinal-hippocampal synapse assembly
Synapse assembly likely requires postsynaptic target recognition by incoming presynaptic afferents. Using newly generated conditional knock-in and knockout mice, we show in this study that latrophilin-2 (Lphn2), a cell-adhesion G protein-coupled receptor and presumptive α-latrotoxin receptor, contro...
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| Veröffentlicht in: | The Journal of cell biology 2017-11, Vol.216 (11), p.3831-3846 |
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| creator | Anderson, Garret R Maxeiner, Stephan Sando, Richard Tsetsenis, Theodoros Malenka, Robert C Südhof, Thomas C |
| description | Synapse assembly likely requires postsynaptic target recognition by incoming presynaptic afferents. Using newly generated conditional knock-in and knockout mice, we show in this study that latrophilin-2 (Lphn2), a cell-adhesion G protein-coupled receptor and presumptive α-latrotoxin receptor, controls the numbers of a specific subset of synapses in CA1-region hippocampal neurons, suggesting that Lphn2 acts as a synaptic target-recognition molecule. In cultured hippocampal neurons, Lphn2 maintained synapse numbers via a postsynaptic instead of a presynaptic mechanism, which was surprising given its presumptive role as an α-latrotoxin receptor. In CA1-region neurons in vivo, Lphn2 was specifically targeted to dendritic spines in the stratum lacunosum-moleculare, which form synapses with presynaptic entorhinal cortex afferents. In this study, postsynaptic deletion of Lphn2 selectively decreased spine numbers and impaired synaptic inputs from entorhinal but not Schaffer-collateral afferents. Behaviorally, loss of Lphn2 from the CA1 region increased spatial memory retention but decreased learning of sequential spatial memory tasks. Thus, Lphn2 appears to control synapse numbers in the entorhinal cortex/CA1 region circuit by acting as a domain-specific postsynaptic target-recognition molecule. |
| doi_str_mv | 10.1083/jcb.201703042 |
| format | Article |
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Using newly generated conditional knock-in and knockout mice, we show in this study that latrophilin-2 (Lphn2), a cell-adhesion G protein-coupled receptor and presumptive α-latrotoxin receptor, controls the numbers of a specific subset of synapses in CA1-region hippocampal neurons, suggesting that Lphn2 acts as a synaptic target-recognition molecule. In cultured hippocampal neurons, Lphn2 maintained synapse numbers via a postsynaptic instead of a presynaptic mechanism, which was surprising given its presumptive role as an α-latrotoxin receptor. In CA1-region neurons in vivo, Lphn2 was specifically targeted to dendritic spines in the stratum lacunosum-moleculare, which form synapses with presynaptic entorhinal cortex afferents. In this study, postsynaptic deletion of Lphn2 selectively decreased spine numbers and impaired synaptic inputs from entorhinal but not Schaffer-collateral afferents. Behaviorally, loss of Lphn2 from the CA1 region increased spatial memory retention but decreased learning of sequential spatial memory tasks. Thus, Lphn2 appears to control synapse numbers in the entorhinal cortex/CA1 region circuit by acting as a domain-specific postsynaptic target-recognition molecule.</description><identifier>ISSN: 0021-9525</identifier><identifier>EISSN: 1540-8140</identifier><identifier>DOI: 10.1083/jcb.201703042</identifier><identifier>PMID: 28972101</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Adhesion ; Animals ; Assembly ; Behavior, Animal ; CA1 Region, Hippocampal - metabolism ; CA1 Region, Hippocampal - pathology ; CA1 Region, Hippocampal - physiopathology ; Cell adhesion & migration ; Cells, Cultured ; Clonal deletion ; Cortex (entorhinal) ; Dendritic spines ; Dendritic Spines - metabolism ; Dendritic Spines - pathology ; Entorhinal Cortex - metabolism ; Entorhinal Cortex - pathology ; Entorhinal Cortex - physiopathology ; Fear ; G protein-coupled receptors ; Genotype ; Hippocampus ; Latrotoxin ; Maze Learning ; Memory ; Memory tasks ; Mental task performance ; Mice, Mutant Strains ; Motor Activity ; Neurons ; Neurons - metabolism ; Neurons - pathology ; Neurosciences ; Phenotype ; Presynaptic Terminals - metabolism ; Presynaptic Terminals - pathology ; Receptors, G-Protein-Coupled - genetics ; Receptors, G-Protein-Coupled - metabolism ; Receptors, Peptide - genetics ; Receptors, Peptide - metabolism ; Rotarod Performance Test ; Smell ; Spatial analysis ; Spatial discrimination learning ; Spatial memory ; Spine ; Synapses ; Synaptic Membranes - metabolism ; Synaptic Membranes - pathology ; Synaptic Potentials ; Synaptogenesis ; Target recognition ; Time Factors ; Transfection</subject><ispartof>The Journal of cell biology, 2017-11, Vol.216 (11), p.3831-3846</ispartof><rights>2017 Anderson et al.</rights><rights>Copyright Rockefeller University Press Nov 2017</rights><rights>2017 Anderson et al. 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c415t-d657af45d5c653e86bb8b68d55c9aa374ee010bd428beb0e812c31365d0c6eee3</citedby><cites>FETCH-LOGICAL-c415t-d657af45d5c653e86bb8b68d55c9aa374ee010bd428beb0e812c31365d0c6eee3</cites><orcidid>0000-0002-4472-695X ; 0000-0003-4866-4255</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28972101$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Anderson, Garret R</creatorcontrib><creatorcontrib>Maxeiner, Stephan</creatorcontrib><creatorcontrib>Sando, Richard</creatorcontrib><creatorcontrib>Tsetsenis, Theodoros</creatorcontrib><creatorcontrib>Malenka, Robert C</creatorcontrib><creatorcontrib>Südhof, Thomas C</creatorcontrib><title>Postsynaptic adhesion GPCR latrophilin-2 mediates target recognition in entorhinal-hippocampal synapse assembly</title><title>The Journal of cell biology</title><addtitle>J Cell Biol</addtitle><description>Synapse assembly likely requires postsynaptic target recognition by incoming presynaptic afferents. Using newly generated conditional knock-in and knockout mice, we show in this study that latrophilin-2 (Lphn2), a cell-adhesion G protein-coupled receptor and presumptive α-latrotoxin receptor, controls the numbers of a specific subset of synapses in CA1-region hippocampal neurons, suggesting that Lphn2 acts as a synaptic target-recognition molecule. In cultured hippocampal neurons, Lphn2 maintained synapse numbers via a postsynaptic instead of a presynaptic mechanism, which was surprising given its presumptive role as an α-latrotoxin receptor. In CA1-region neurons in vivo, Lphn2 was specifically targeted to dendritic spines in the stratum lacunosum-moleculare, which form synapses with presynaptic entorhinal cortex afferents. In this study, postsynaptic deletion of Lphn2 selectively decreased spine numbers and impaired synaptic inputs from entorhinal but not Schaffer-collateral afferents. Behaviorally, loss of Lphn2 from the CA1 region increased spatial memory retention but decreased learning of sequential spatial memory tasks. Thus, Lphn2 appears to control synapse numbers in the entorhinal cortex/CA1 region circuit by acting as a domain-specific postsynaptic target-recognition molecule.</description><subject>Adhesion</subject><subject>Animals</subject><subject>Assembly</subject><subject>Behavior, Animal</subject><subject>CA1 Region, Hippocampal - metabolism</subject><subject>CA1 Region, Hippocampal - pathology</subject><subject>CA1 Region, Hippocampal - physiopathology</subject><subject>Cell adhesion & migration</subject><subject>Cells, Cultured</subject><subject>Clonal deletion</subject><subject>Cortex (entorhinal)</subject><subject>Dendritic spines</subject><subject>Dendritic Spines - metabolism</subject><subject>Dendritic Spines - pathology</subject><subject>Entorhinal Cortex - metabolism</subject><subject>Entorhinal Cortex - pathology</subject><subject>Entorhinal Cortex - physiopathology</subject><subject>Fear</subject><subject>G protein-coupled receptors</subject><subject>Genotype</subject><subject>Hippocampus</subject><subject>Latrotoxin</subject><subject>Maze Learning</subject><subject>Memory</subject><subject>Memory tasks</subject><subject>Mental task performance</subject><subject>Mice, Mutant Strains</subject><subject>Motor Activity</subject><subject>Neurons</subject><subject>Neurons - metabolism</subject><subject>Neurons - pathology</subject><subject>Neurosciences</subject><subject>Phenotype</subject><subject>Presynaptic Terminals - metabolism</subject><subject>Presynaptic Terminals - pathology</subject><subject>Receptors, G-Protein-Coupled - genetics</subject><subject>Receptors, G-Protein-Coupled - metabolism</subject><subject>Receptors, Peptide - genetics</subject><subject>Receptors, Peptide - metabolism</subject><subject>Rotarod Performance Test</subject><subject>Smell</subject><subject>Spatial analysis</subject><subject>Spatial discrimination learning</subject><subject>Spatial memory</subject><subject>Spine</subject><subject>Synapses</subject><subject>Synaptic Membranes - metabolism</subject><subject>Synaptic Membranes - pathology</subject><subject>Synaptic Potentials</subject><subject>Synaptogenesis</subject><subject>Target recognition</subject><subject>Time Factors</subject><subject>Transfection</subject><issn>0021-9525</issn><issn>1540-8140</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkU1v1DAQhi0EokvhyBVF4tJLyvgrcS5IaEVbpEpUVTlbtjO78cqJg-1F2n9PlpZV4TSHefTonXkJeU_hkoLin3bOXjKgLXAQ7AVZUSmgVlTAS7ICYLTuJJNn5E3OOwAQreCvyRlTXcso0BWJdzGXfJjMXLyrTD9g9nGqru_W91UwJcV58MFPNatG7L0pmKti0hZLldDF7eTLEfdThVOJafCTCfXg5zk6M84mVH_UGSuTM442HN6SVxsTMr57mufkx9XXh_VNffv9-tv6y23tBJWl7hvZmo2QvXSN5Kgaa5VtVC-l64zhrUAECrYXTFm0gIoyxylvZA-uQUR-Tj4_eue9XZK7JV4yQc_JjyYddDRe_7uZ_KC38ZeWTStURxfBxZMgxZ97zEWPPjsMwUwY91nTTjSCc5ByQT_-h-7iPi2fOFIKWtqw9iisHymXYs4JN6cwFPSxSr1UqU9VLvyH5xec6L_d8d-COpzq</recordid><startdate>20171106</startdate><enddate>20171106</enddate><creator>Anderson, Garret R</creator><creator>Maxeiner, Stephan</creator><creator>Sando, Richard</creator><creator>Tsetsenis, Theodoros</creator><creator>Malenka, Robert C</creator><creator>Südhof, Thomas C</creator><general>Rockefeller University Press</general><general>The Rockefeller University Press</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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4472-695X</orcidid><orcidid>https://orcid.org/0000-0003-4866-4255</orcidid></search><sort><creationdate>20171106</creationdate><title>Postsynaptic adhesion GPCR latrophilin-2 mediates target recognition in entorhinal-hippocampal synapse assembly</title><author>Anderson, Garret R ; Maxeiner, Stephan ; Sando, Richard ; Tsetsenis, Theodoros ; Malenka, Robert C ; Südhof, Thomas C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c415t-d657af45d5c653e86bb8b68d55c9aa374ee010bd428beb0e812c31365d0c6eee3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Adhesion</topic><topic>Animals</topic><topic>Assembly</topic><topic>Behavior, Animal</topic><topic>CA1 Region, Hippocampal - metabolism</topic><topic>CA1 Region, Hippocampal - pathology</topic><topic>CA1 Region, Hippocampal - physiopathology</topic><topic>Cell adhesion & migration</topic><topic>Cells, Cultured</topic><topic>Clonal deletion</topic><topic>Cortex (entorhinal)</topic><topic>Dendritic spines</topic><topic>Dendritic Spines - metabolism</topic><topic>Dendritic Spines - pathology</topic><topic>Entorhinal Cortex - metabolism</topic><topic>Entorhinal Cortex - pathology</topic><topic>Entorhinal Cortex - physiopathology</topic><topic>Fear</topic><topic>G protein-coupled receptors</topic><topic>Genotype</topic><topic>Hippocampus</topic><topic>Latrotoxin</topic><topic>Maze Learning</topic><topic>Memory</topic><topic>Memory tasks</topic><topic>Mental task performance</topic><topic>Mice, Mutant Strains</topic><topic>Motor Activity</topic><topic>Neurons</topic><topic>Neurons - metabolism</topic><topic>Neurons - pathology</topic><topic>Neurosciences</topic><topic>Phenotype</topic><topic>Presynaptic Terminals - metabolism</topic><topic>Presynaptic Terminals - pathology</topic><topic>Receptors, G-Protein-Coupled - genetics</topic><topic>Receptors, G-Protein-Coupled - metabolism</topic><topic>Receptors, Peptide - genetics</topic><topic>Receptors, Peptide - metabolism</topic><topic>Rotarod Performance Test</topic><topic>Smell</topic><topic>Spatial analysis</topic><topic>Spatial discrimination learning</topic><topic>Spatial memory</topic><topic>Spine</topic><topic>Synapses</topic><topic>Synaptic Membranes - metabolism</topic><topic>Synaptic Membranes - pathology</topic><topic>Synaptic Potentials</topic><topic>Synaptogenesis</topic><topic>Target recognition</topic><topic>Time Factors</topic><topic>Transfection</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Anderson, Garret R</creatorcontrib><creatorcontrib>Maxeiner, Stephan</creatorcontrib><creatorcontrib>Sando, Richard</creatorcontrib><creatorcontrib>Tsetsenis, Theodoros</creatorcontrib><creatorcontrib>Malenka, Robert C</creatorcontrib><creatorcontrib>Südhof, Thomas C</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of cell biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Anderson, Garret R</au><au>Maxeiner, Stephan</au><au>Sando, Richard</au><au>Tsetsenis, Theodoros</au><au>Malenka, Robert C</au><au>Südhof, Thomas C</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Postsynaptic adhesion GPCR latrophilin-2 mediates target recognition in entorhinal-hippocampal synapse assembly</atitle><jtitle>The Journal of cell biology</jtitle><addtitle>J Cell Biol</addtitle><date>2017-11-06</date><risdate>2017</risdate><volume>216</volume><issue>11</issue><spage>3831</spage><epage>3846</epage><pages>3831-3846</pages><issn>0021-9525</issn><eissn>1540-8140</eissn><abstract>Synapse assembly likely requires postsynaptic target recognition by incoming presynaptic afferents. Using newly generated conditional knock-in and knockout mice, we show in this study that latrophilin-2 (Lphn2), a cell-adhesion G protein-coupled receptor and presumptive α-latrotoxin receptor, controls the numbers of a specific subset of synapses in CA1-region hippocampal neurons, suggesting that Lphn2 acts as a synaptic target-recognition molecule. In cultured hippocampal neurons, Lphn2 maintained synapse numbers via a postsynaptic instead of a presynaptic mechanism, which was surprising given its presumptive role as an α-latrotoxin receptor. In CA1-region neurons in vivo, Lphn2 was specifically targeted to dendritic spines in the stratum lacunosum-moleculare, which form synapses with presynaptic entorhinal cortex afferents. In this study, postsynaptic deletion of Lphn2 selectively decreased spine numbers and impaired synaptic inputs from entorhinal but not Schaffer-collateral afferents. Behaviorally, loss of Lphn2 from the CA1 region increased spatial memory retention but decreased learning of sequential spatial memory tasks. Thus, Lphn2 appears to control synapse numbers in the entorhinal cortex/CA1 region circuit by acting as a domain-specific postsynaptic target-recognition molecule.</abstract><cop>United States</cop><pub>Rockefeller University Press</pub><pmid>28972101</pmid><doi>10.1083/jcb.201703042</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-4472-695X</orcidid><orcidid>https://orcid.org/0000-0003-4866-4255</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Adhesion Animals Assembly Behavior, Animal CA1 Region, Hippocampal - metabolism CA1 Region, Hippocampal - pathology CA1 Region, Hippocampal - physiopathology Cell adhesion & migration Cells, Cultured Clonal deletion Cortex (entorhinal) Dendritic spines Dendritic Spines - metabolism Dendritic Spines - pathology Entorhinal Cortex - metabolism Entorhinal Cortex - pathology Entorhinal Cortex - physiopathology Fear G protein-coupled receptors Genotype Hippocampus Latrotoxin Maze Learning Memory Memory tasks Mental task performance Mice, Mutant Strains Motor Activity Neurons Neurons - metabolism Neurons - pathology Neurosciences Phenotype Presynaptic Terminals - metabolism Presynaptic Terminals - pathology Receptors, G-Protein-Coupled - genetics Receptors, G-Protein-Coupled - metabolism Receptors, Peptide - genetics Receptors, Peptide - metabolism Rotarod Performance Test Smell Spatial analysis Spatial discrimination learning Spatial memory Spine Synapses Synaptic Membranes - metabolism Synaptic Membranes - pathology Synaptic Potentials Synaptogenesis Target recognition Time Factors Transfection |
| title | Postsynaptic adhesion GPCR latrophilin-2 mediates target recognition in entorhinal-hippocampal synapse assembly |
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