CREBA and CREBB in two identified neurons gate long-term memory formation in Drosophila
Episodic events are frequently consolidated into labile memory but are not necessarily transferred to persistent long-term memory (LTM). Regulatory mechanisms leading to LTM formation are poorly understood, however, especially at the resolution of identified neurons. Here, we demonstrate enhanced LT...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2021-09, Vol.118 (37), p.1-8 |
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| creator | Lin, Hsuan-Wen Chen, Chun-Chao de Belle, J. Steven Tully, Tim Chiang, Ann-Shyn |
| description | Episodic events are frequently consolidated into labile memory but are not necessarily transferred to persistent long-term memory (LTM). Regulatory mechanisms leading to LTM formation are poorly understood, however, especially at the resolution of identified neurons. Here, we demonstrate enhanced LTM following aversive olfactory conditioning in Drosophila when the transcription factor cyclic AMP response element binding protein A (CREBA) is induced in just two dorsal-anterior-lateral (DAL) neurons. Our experiments show that this process is regulated by protein–gene interactions in DAL neurons: (1) crebA transcription is induced by training and repressed by crebB overexpression, (2) CREBA bidirectionally modulates LTM formation, (3) crebA overexpression enhances training-induced gene transcription, and (4) increasing membrane excitability enhances LTM formation and gene expression. These findings suggest that activity-dependent gene expression in DAL neurons during LTM formation is regulated by CREB proteins. |
| doi_str_mv | 10.1073/pnas.2100624118 |
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Steven ; Tully, Tim ; Chiang, Ann-Shyn</creator><creatorcontrib>Lin, Hsuan-Wen ; Chen, Chun-Chao ; de Belle, J. Steven ; Tully, Tim ; Chiang, Ann-Shyn</creatorcontrib><description>Episodic events are frequently consolidated into labile memory but are not necessarily transferred to persistent long-term memory (LTM). Regulatory mechanisms leading to LTM formation are poorly understood, however, especially at the resolution of identified neurons. Here, we demonstrate enhanced LTM following aversive olfactory conditioning in Drosophila when the transcription factor cyclic AMP response element binding protein A (CREBA) is induced in just two dorsal-anterior-lateral (DAL) neurons. Our experiments show that this process is regulated by protein–gene interactions in DAL neurons: (1) crebA transcription is induced by training and repressed by crebB overexpression, (2) CREBA bidirectionally modulates LTM formation, (3) crebA overexpression enhances training-induced gene transcription, and (4) increasing membrane excitability enhances LTM formation and gene expression. These findings suggest that activity-dependent gene expression in DAL neurons during LTM formation is regulated by CREB proteins.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.2100624118</identifier><identifier>PMID: 34507985</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animals ; Biological Sciences ; Conditioning, Classical - physiology ; Conditioning, Psychological ; Cyclic AMP ; Cyclic AMP response element-binding protein ; Cyclic AMP Response Element-Binding Protein - genetics ; Cyclic AMP Response Element-Binding Protein - metabolism ; Cyclic AMP Response Element-Binding Protein - physiology ; Cyclic AMP Response Element-Binding Protein A - genetics ; Cyclic AMP Response Element-Binding Protein A - metabolism ; Cyclic AMP Response Element-Binding Protein A - physiology ; Drosophila ; Drosophila melanogaster ; Drosophila Proteins - metabolism ; Drosophila Proteins - physiology ; Excitability ; Female ; Fruit flies ; Gene expression ; Gene Expression - genetics ; Gene Expression Regulation - genetics ; Insects ; Long term memory ; Male ; Memory, Long-Term - physiology ; Neurons ; Neurons - metabolism ; Neurons - physiology ; Olfactory discrimination learning ; Olfactory Perception - physiology ; Protein A ; Proteins ; Regulatory mechanisms (biology) ; Smell - physiology ; Training ; Trans-Activators - metabolism ; Trans-Activators - physiology</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2021-09, Vol.118 (37), p.1-8</ispartof><rights>Copyright © 2021 the Author(s). Published by PNAS.</rights><rights>Copyright National Academy of Sciences Sep 14, 2021</rights><rights>Copyright © 2021 the Author(s). Published by PNAS. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c443t-8214b270a6bd783fb6f05ea8cc4bb0cc4312596758ae40dcbdeedfa8fcbdbcbc3</citedby><cites>FETCH-LOGICAL-c443t-8214b270a6bd783fb6f05ea8cc4bb0cc4312596758ae40dcbdeedfa8fcbdbcbc3</cites><orcidid>0000-0001-9668-7115 ; 0000-0001-6378-3944</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/27075772$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/27075772$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34507985$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lin, Hsuan-Wen</creatorcontrib><creatorcontrib>Chen, Chun-Chao</creatorcontrib><creatorcontrib>de Belle, J. Steven</creatorcontrib><creatorcontrib>Tully, Tim</creatorcontrib><creatorcontrib>Chiang, Ann-Shyn</creatorcontrib><title>CREBA and CREBB in two identified neurons gate long-term memory formation in Drosophila</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Episodic events are frequently consolidated into labile memory but are not necessarily transferred to persistent long-term memory (LTM). Regulatory mechanisms leading to LTM formation are poorly understood, however, especially at the resolution of identified neurons. Here, we demonstrate enhanced LTM following aversive olfactory conditioning in Drosophila when the transcription factor cyclic AMP response element binding protein A (CREBA) is induced in just two dorsal-anterior-lateral (DAL) neurons. Our experiments show that this process is regulated by protein–gene interactions in DAL neurons: (1) crebA transcription is induced by training and repressed by crebB overexpression, (2) CREBA bidirectionally modulates LTM formation, (3) crebA overexpression enhances training-induced gene transcription, and (4) increasing membrane excitability enhances LTM formation and gene expression. These findings suggest that activity-dependent gene expression in DAL neurons during LTM formation is regulated by CREB proteins.</description><subject>Animals</subject><subject>Biological Sciences</subject><subject>Conditioning, Classical - physiology</subject><subject>Conditioning, Psychological</subject><subject>Cyclic AMP</subject><subject>Cyclic AMP response element-binding protein</subject><subject>Cyclic AMP Response Element-Binding Protein - genetics</subject><subject>Cyclic AMP Response Element-Binding Protein - metabolism</subject><subject>Cyclic AMP Response Element-Binding Protein - physiology</subject><subject>Cyclic AMP Response Element-Binding Protein A - genetics</subject><subject>Cyclic AMP Response Element-Binding Protein A - metabolism</subject><subject>Cyclic AMP Response Element-Binding Protein A - physiology</subject><subject>Drosophila</subject><subject>Drosophila melanogaster</subject><subject>Drosophila Proteins - metabolism</subject><subject>Drosophila Proteins - physiology</subject><subject>Excitability</subject><subject>Female</subject><subject>Fruit flies</subject><subject>Gene expression</subject><subject>Gene Expression - genetics</subject><subject>Gene Expression Regulation - genetics</subject><subject>Insects</subject><subject>Long term memory</subject><subject>Male</subject><subject>Memory, Long-Term - physiology</subject><subject>Neurons</subject><subject>Neurons - metabolism</subject><subject>Neurons - physiology</subject><subject>Olfactory discrimination learning</subject><subject>Olfactory Perception - physiology</subject><subject>Protein A</subject><subject>Proteins</subject><subject>Regulatory mechanisms (biology)</subject><subject>Smell - physiology</subject><subject>Training</subject><subject>Trans-Activators - metabolism</subject><subject>Trans-Activators - physiology</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkc1rGzEQxUVoiJ0055xaBD1vMvpaaS-FxM0XBAKhpUch7WptGa_kSuuW_PeRceImF2lgfvP0NA-hMwLnBCS7WAeTzykBqCknRB2gKYGGVDVv4BOaAlBZKU75BB3nvASARig4QhPGBchGiSn6PXu6vrrEJnR4W11hH_D4L2LfuTD63rsOB7dJMWQ8N6PDqxjm1ejSgAc3xPSM-5gGM_oYtpM_UsxxvfAr8xkd9maV3enrfYJ-3Vz_nN1VD4-397PLh6rlnI2VooRbKsHUtpOK9bbuQTij2pZbC-VkhIqmlkIZx6Frbedc1xvVl8q2tmUn6PtOd72xg-va4jqZlV4nP5j0rKPx-mMn-IWex79acd4U8SLw7VUgxT8bl0e9jJsUimdNhWSqAaFYoS52VFt-mJPr9y8Q0Nsk9DYJ_T-JMvH1vbE9_7b6AnzZAcs8xrTvl2VIISVlL8l8kFo</recordid><startdate>20210914</startdate><enddate>20210914</enddate><creator>Lin, Hsuan-Wen</creator><creator>Chen, Chun-Chao</creator><creator>de Belle, J. Steven</creator><creator>Tully, Tim</creator><creator>Chiang, Ann-Shyn</creator><general>National Academy of Sciences</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>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>5PM</scope><orcidid>https://orcid.org/0000-0001-9668-7115</orcidid><orcidid>https://orcid.org/0000-0001-6378-3944</orcidid></search><sort><creationdate>20210914</creationdate><title>CREBA and CREBB in two identified neurons gate long-term memory formation in Drosophila</title><author>Lin, Hsuan-Wen ; Chen, Chun-Chao ; de Belle, J. Steven ; Tully, Tim ; Chiang, Ann-Shyn</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c443t-8214b270a6bd783fb6f05ea8cc4bb0cc4312596758ae40dcbdeedfa8fcbdbcbc3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>Biological Sciences</topic><topic>Conditioning, Classical - physiology</topic><topic>Conditioning, Psychological</topic><topic>Cyclic AMP</topic><topic>Cyclic AMP response element-binding protein</topic><topic>Cyclic AMP Response Element-Binding Protein - genetics</topic><topic>Cyclic AMP Response Element-Binding Protein - metabolism</topic><topic>Cyclic AMP Response Element-Binding Protein - physiology</topic><topic>Cyclic AMP Response Element-Binding Protein A - genetics</topic><topic>Cyclic AMP Response Element-Binding Protein A - metabolism</topic><topic>Cyclic AMP Response Element-Binding Protein A - physiology</topic><topic>Drosophila</topic><topic>Drosophila melanogaster</topic><topic>Drosophila Proteins - metabolism</topic><topic>Drosophila Proteins - physiology</topic><topic>Excitability</topic><topic>Female</topic><topic>Fruit flies</topic><topic>Gene expression</topic><topic>Gene Expression - genetics</topic><topic>Gene Expression Regulation - genetics</topic><topic>Insects</topic><topic>Long term memory</topic><topic>Male</topic><topic>Memory, Long-Term - physiology</topic><topic>Neurons</topic><topic>Neurons - metabolism</topic><topic>Neurons - physiology</topic><topic>Olfactory discrimination learning</topic><topic>Olfactory Perception - physiology</topic><topic>Protein A</topic><topic>Proteins</topic><topic>Regulatory mechanisms (biology)</topic><topic>Smell - physiology</topic><topic>Training</topic><topic>Trans-Activators - metabolism</topic><topic>Trans-Activators - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lin, Hsuan-Wen</creatorcontrib><creatorcontrib>Chen, Chun-Chao</creatorcontrib><creatorcontrib>de Belle, J. 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Steven</au><au>Tully, Tim</au><au>Chiang, Ann-Shyn</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>CREBA and CREBB in two identified neurons gate long-term memory formation in Drosophila</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2021-09-14</date><risdate>2021</risdate><volume>118</volume><issue>37</issue><spage>1</spage><epage>8</epage><pages>1-8</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Episodic events are frequently consolidated into labile memory but are not necessarily transferred to persistent long-term memory (LTM). Regulatory mechanisms leading to LTM formation are poorly understood, however, especially at the resolution of identified neurons. Here, we demonstrate enhanced LTM following aversive olfactory conditioning in Drosophila when the transcription factor cyclic AMP response element binding protein A (CREBA) is induced in just two dorsal-anterior-lateral (DAL) neurons. Our experiments show that this process is regulated by protein–gene interactions in DAL neurons: (1) crebA transcription is induced by training and repressed by crebB overexpression, (2) CREBA bidirectionally modulates LTM formation, (3) crebA overexpression enhances training-induced gene transcription, and (4) increasing membrane excitability enhances LTM formation and gene expression. These findings suggest that activity-dependent gene expression in DAL neurons during LTM formation is regulated by CREB proteins.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>34507985</pmid><doi>10.1073/pnas.2100624118</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0001-9668-7115</orcidid><orcidid>https://orcid.org/0000-0001-6378-3944</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Biological Sciences Conditioning, Classical - physiology Conditioning, Psychological Cyclic AMP Cyclic AMP response element-binding protein Cyclic AMP Response Element-Binding Protein - genetics Cyclic AMP Response Element-Binding Protein - metabolism Cyclic AMP Response Element-Binding Protein - physiology Cyclic AMP Response Element-Binding Protein A - genetics Cyclic AMP Response Element-Binding Protein A - metabolism Cyclic AMP Response Element-Binding Protein A - physiology Drosophila Drosophila melanogaster Drosophila Proteins - metabolism Drosophila Proteins - physiology Excitability Female Fruit flies Gene expression Gene Expression - genetics Gene Expression Regulation - genetics Insects Long term memory Male Memory, Long-Term - physiology Neurons Neurons - metabolism Neurons - physiology Olfactory discrimination learning Olfactory Perception - physiology Protein A Proteins Regulatory mechanisms (biology) Smell - physiology Training Trans-Activators - metabolism Trans-Activators - physiology |
| title | CREBA and CREBB in two identified neurons gate long-term memory formation in Drosophila |
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