Differential second messenger signaling via dopamine neurons bidirectionally regulates memory retention
Memory formation and forgetting unnecessary memory must be balanced for adaptive animal behavior. While cyclic AMP (cAMP) signaling via dopamine neurons induces memory formation, here we report that cyclic guanine monophosphate (cGMP) signaling via dopamine neurons launches forgetting of unconsolida...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2023-09, Vol.120 (36), p.e2304851120-e2304851120 |
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| creator | Takakura, Mai Lam, Yu Hong Nakagawa, Reiko Ng, Man Yung Hu, Xinyue Bhargava, Priyanshu Alia, Abdalla G. Gu, Yuzhe Wang, Zigao Ota, Takeshi Kimura, Yoko Morimoto, Nao Osakada, Fumitaka Lee, Ah Young Leung, Danny Miyashita, Tomoyuki Du, Juan Okuno, Hiroyuki Hirano, Yukinori |
| description | Memory formation and forgetting unnecessary memory must be balanced for adaptive animal behavior. While cyclic AMP (cAMP) signaling via dopamine neurons induces memory formation, here we report that cyclic guanine monophosphate (cGMP) signaling via dopamine neurons launches forgetting of unconsolidated memory in
Drosophila
. Genetic screening and proteomic analyses showed that neural activation induces the complex formation of a histone H3K9 demethylase, Kdm4B, and a GMP synthetase, Bur, which is necessary and sufficient for forgetting unconsolidated memory. Kdm4B/Bur is activated by phosphorylation through NO-dependent cGMP signaling via dopamine neurons, inducing gene expression, including
kek2
encoding a presynaptic protein. Accordingly, Kdm4B/Bur activation induced presynaptic changes. Our data demonstrate a link between cGMP signaling and synapses via gene expression in forgetting, suggesting that the opposing functions of memory are orchestrated by distinct signaling via dopamine neurons, which affects synaptic integrity and thus balances animal behavior. |
| doi_str_mv | 10.1073/pnas.2304851120 |
| format | Article |
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Drosophila
. Genetic screening and proteomic analyses showed that neural activation induces the complex formation of a histone H3K9 demethylase, Kdm4B, and a GMP synthetase, Bur, which is necessary and sufficient for forgetting unconsolidated memory. Kdm4B/Bur is activated by phosphorylation through NO-dependent cGMP signaling via dopamine neurons, inducing gene expression, including
kek2
encoding a presynaptic protein. Accordingly, Kdm4B/Bur activation induced presynaptic changes. Our data demonstrate a link between cGMP signaling and synapses via gene expression in forgetting, suggesting that the opposing functions of memory are orchestrated by distinct signaling via dopamine neurons, which affects synaptic integrity and thus balances animal behavior.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.2304851120</identifier><identifier>PMID: 37639608</identifier><language>eng</language><publisher>Washington: National Academy of Sciences</publisher><subject>Animal behavior ; Biological Sciences ; Complex formation ; Cyclic AMP ; Cyclic GMP ; Dopamine ; Gene expression ; Genetic analysis ; Genetic screening ; Histones ; Neurons ; Phosphorylation ; Proteomics ; Synapses</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2023-09, Vol.120 (36), p.e2304851120-e2304851120</ispartof><rights>Copyright National Academy of Sciences Sep 5, 2023</rights><rights>Copyright © 2023 the Author(s). Published by PNAS. 2023</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c399t-a00ee356b805b1543ebd47aa63abf12e310fdcba11684f395b5ffe19f508151d3</citedby><cites>FETCH-LOGICAL-c399t-a00ee356b805b1543ebd47aa63abf12e310fdcba11684f395b5ffe19f508151d3</cites><orcidid>0009-0001-1787-5538 ; 0000-0002-9078-1458 ; 0000-0002-1850-3613 ; 0000-0001-9165-842X ; 0000-0002-7109-0096 ; 0000-0002-6178-2945 ; 0000-0003-3598-4890 ; 0009-0007-0436-5073</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10483633/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10483633/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,886,27929,27930,53796,53798</link.rule.ids></links><search><creatorcontrib>Takakura, Mai</creatorcontrib><creatorcontrib>Lam, Yu Hong</creatorcontrib><creatorcontrib>Nakagawa, Reiko</creatorcontrib><creatorcontrib>Ng, Man Yung</creatorcontrib><creatorcontrib>Hu, Xinyue</creatorcontrib><creatorcontrib>Bhargava, Priyanshu</creatorcontrib><creatorcontrib>Alia, Abdalla G.</creatorcontrib><creatorcontrib>Gu, Yuzhe</creatorcontrib><creatorcontrib>Wang, Zigao</creatorcontrib><creatorcontrib>Ota, Takeshi</creatorcontrib><creatorcontrib>Kimura, Yoko</creatorcontrib><creatorcontrib>Morimoto, Nao</creatorcontrib><creatorcontrib>Osakada, Fumitaka</creatorcontrib><creatorcontrib>Lee, Ah Young</creatorcontrib><creatorcontrib>Leung, Danny</creatorcontrib><creatorcontrib>Miyashita, Tomoyuki</creatorcontrib><creatorcontrib>Du, Juan</creatorcontrib><creatorcontrib>Okuno, Hiroyuki</creatorcontrib><creatorcontrib>Hirano, Yukinori</creatorcontrib><title>Differential second messenger signaling via dopamine neurons bidirectionally regulates memory retention</title><title>Proceedings of the National Academy of Sciences - PNAS</title><description>Memory formation and forgetting unnecessary memory must be balanced for adaptive animal behavior. While cyclic AMP (cAMP) signaling via dopamine neurons induces memory formation, here we report that cyclic guanine monophosphate (cGMP) signaling via dopamine neurons launches forgetting of unconsolidated memory in
Drosophila
. Genetic screening and proteomic analyses showed that neural activation induces the complex formation of a histone H3K9 demethylase, Kdm4B, and a GMP synthetase, Bur, which is necessary and sufficient for forgetting unconsolidated memory. Kdm4B/Bur is activated by phosphorylation through NO-dependent cGMP signaling via dopamine neurons, inducing gene expression, including
kek2
encoding a presynaptic protein. Accordingly, Kdm4B/Bur activation induced presynaptic changes. Our data demonstrate a link between cGMP signaling and synapses via gene expression in forgetting, suggesting that the opposing functions of memory are orchestrated by distinct signaling via dopamine neurons, which affects synaptic integrity and thus balances animal behavior.</description><subject>Animal behavior</subject><subject>Biological Sciences</subject><subject>Complex formation</subject><subject>Cyclic AMP</subject><subject>Cyclic GMP</subject><subject>Dopamine</subject><subject>Gene expression</subject><subject>Genetic analysis</subject><subject>Genetic screening</subject><subject>Histones</subject><subject>Neurons</subject><subject>Phosphorylation</subject><subject>Proteomics</subject><subject>Synapses</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNpdkU1P3TAQRS3Uqjyga7aR2HQT3owd59mrCvHVSkjdwNpykkkwSuyHnSDx73EEKmpXlsZHZ0b3MnaKcI6wE9u9t-mcC6iURORwwDYIGsu60vCFbQD4rlQVrw7ZUUpPAKClgm_sUOxqoWtQGzZcub6nSH52diwStcF3xUQpkR8oFskN3o7OD8WLs0UX9nZyngpPSww-FY3rXKR2diFT42sRaVhGO1PKiinEdTCv6uBP2Nfejom-f7zH7OHm-v7yV3n35_b35cVd2Qqt59ICEAlZNwpkg7IS1HTVztpa2KZHTgKh79rGItaq6oWWjczno-4lKJTYiWP28927X5qJujZvj3Y0--gmG19NsM78--PdoxnCi8GcoaiFyIYfH4YYnhdKs5lcamkcraewJMOVVFpzgDqjZ_-hT2GJOYqVyglzRMUztX2n2hhSitT_vQbBrC2atUXz2aJ4A6Hnkkc</recordid><startdate>20230905</startdate><enddate>20230905</enddate><creator>Takakura, Mai</creator><creator>Lam, Yu Hong</creator><creator>Nakagawa, Reiko</creator><creator>Ng, Man Yung</creator><creator>Hu, Xinyue</creator><creator>Bhargava, Priyanshu</creator><creator>Alia, Abdalla G.</creator><creator>Gu, Yuzhe</creator><creator>Wang, Zigao</creator><creator>Ota, Takeshi</creator><creator>Kimura, Yoko</creator><creator>Morimoto, Nao</creator><creator>Osakada, Fumitaka</creator><creator>Lee, Ah Young</creator><creator>Leung, Danny</creator><creator>Miyashita, Tomoyuki</creator><creator>Du, Juan</creator><creator>Okuno, Hiroyuki</creator><creator>Hirano, Yukinori</creator><general>National Academy of Sciences</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</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/0009-0001-1787-5538</orcidid><orcidid>https://orcid.org/0000-0002-9078-1458</orcidid><orcidid>https://orcid.org/0000-0002-1850-3613</orcidid><orcidid>https://orcid.org/0000-0001-9165-842X</orcidid><orcidid>https://orcid.org/0000-0002-7109-0096</orcidid><orcidid>https://orcid.org/0000-0002-6178-2945</orcidid><orcidid>https://orcid.org/0000-0003-3598-4890</orcidid><orcidid>https://orcid.org/0009-0007-0436-5073</orcidid></search><sort><creationdate>20230905</creationdate><title>Differential second messenger signaling via dopamine neurons bidirectionally regulates memory retention</title><author>Takakura, Mai ; 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While cyclic AMP (cAMP) signaling via dopamine neurons induces memory formation, here we report that cyclic guanine monophosphate (cGMP) signaling via dopamine neurons launches forgetting of unconsolidated memory in
Drosophila
. Genetic screening and proteomic analyses showed that neural activation induces the complex formation of a histone H3K9 demethylase, Kdm4B, and a GMP synthetase, Bur, which is necessary and sufficient for forgetting unconsolidated memory. Kdm4B/Bur is activated by phosphorylation through NO-dependent cGMP signaling via dopamine neurons, inducing gene expression, including
kek2
encoding a presynaptic protein. Accordingly, Kdm4B/Bur activation induced presynaptic changes. Our data demonstrate a link between cGMP signaling and synapses via gene expression in forgetting, suggesting that the opposing functions of memory are orchestrated by distinct signaling via dopamine neurons, which affects synaptic integrity and thus balances animal behavior.</abstract><cop>Washington</cop><pub>National Academy of Sciences</pub><pmid>37639608</pmid><doi>10.1073/pnas.2304851120</doi><orcidid>https://orcid.org/0009-0001-1787-5538</orcidid><orcidid>https://orcid.org/0000-0002-9078-1458</orcidid><orcidid>https://orcid.org/0000-0002-1850-3613</orcidid><orcidid>https://orcid.org/0000-0001-9165-842X</orcidid><orcidid>https://orcid.org/0000-0002-7109-0096</orcidid><orcidid>https://orcid.org/0000-0002-6178-2945</orcidid><orcidid>https://orcid.org/0000-0003-3598-4890</orcidid><orcidid>https://orcid.org/0009-0007-0436-5073</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animal behavior Biological Sciences Complex formation Cyclic AMP Cyclic GMP Dopamine Gene expression Genetic analysis Genetic screening Histones Neurons Phosphorylation Proteomics Synapses |
| title | Differential second messenger signaling via dopamine neurons bidirectionally regulates memory retention |
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