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microRNAs That Promote or Inhibit Memory Formation in Drosophila melanogaster
microRNAs (miRNAs) are small noncoding RNAs that regulate gene expression post-transcriptionally. Prior studies have shown that they regulate numerous physiological processes critical for normal development, cellular growth control, and organismal behavior. Here, we systematically surveyed 134 diffe...
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Published in: | Genetics (Austin) 2015-06, Vol.200 (2), p.569-580 |
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description | microRNAs (miRNAs) are small noncoding RNAs that regulate gene expression post-transcriptionally. Prior studies have shown that they regulate numerous physiological processes critical for normal development, cellular growth control, and organismal behavior. Here, we systematically surveyed 134 different miRNAs for roles in olfactory learning and memory formation using "sponge" technology to titrate their activity broadly in the Drosophila melanogaster central nervous system. We identified at least five different miRNAs involved in memory formation or retention from this large screen, including miR-9c, miR-31a, miR-305, miR-974, and miR-980. Surprisingly, the titration of some miRNAs increased memory, while the titration of others decreased memory. We performed more detailed experiments on two miRNAs, miR-974 and miR-31a, by mapping their roles to subpopulations of brain neurons and testing the functional involvement in memory of potential mRNA targets through bioinformatics and a RNA interference knockdown approach. This screen offers an important first step toward the comprehensive identification of all miRNAs and their potential targets that serve in gene regulatory networks important for normal learning and memory. |
doi_str_mv | 10.1534/genetics.114.169623 |
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Prior studies have shown that they regulate numerous physiological processes critical for normal development, cellular growth control, and organismal behavior. Here, we systematically surveyed 134 different miRNAs for roles in olfactory learning and memory formation using "sponge" technology to titrate their activity broadly in the Drosophila melanogaster central nervous system. We identified at least five different miRNAs involved in memory formation or retention from this large screen, including miR-9c, miR-31a, miR-305, miR-974, and miR-980. Surprisingly, the titration of some miRNAs increased memory, while the titration of others decreased memory. We performed more detailed experiments on two miRNAs, miR-974 and miR-31a, by mapping their roles to subpopulations of brain neurons and testing the functional involvement in memory of potential mRNA targets through bioinformatics and a RNA interference knockdown approach. This screen offers an important first step toward the comprehensive identification of all miRNAs and their potential targets that serve in gene regulatory networks important for normal learning and memory.</description><identifier>ISSN: 1943-2631</identifier><identifier>ISSN: 0016-6731</identifier><identifier>EISSN: 1943-2631</identifier><identifier>DOI: 10.1534/genetics.114.169623</identifier><identifier>PMID: 26088433</identifier><identifier>CODEN: GENTAE</identifier><language>eng</language><publisher>United States: Genetics Society of America</publisher><subject>Animal memory ; Animals ; Behavior, Animal ; Cholinergic Neurons - metabolism ; Drosophila melanogaster ; Drosophila melanogaster - genetics ; Gene Expression ; Insects ; Investigations ; Learning ; Memory ; MicroRNAs ; MicroRNAs - genetics ; Olfactory Receptor Neurons - metabolism ; Time Factors</subject><ispartof>Genetics (Austin), 2015-06, Vol.200 (2), p.569-580</ispartof><rights>Copyright © 2015 by the Genetics Society of America.</rights><rights>Copyright Genetics Society of America Jun 2015</rights><rights>Copyright © 2015 by the Genetics Society of America 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c466t-3df6664f5eb6f6cdbd3e63d521710d09ad16557646a84384426e79229d14c8ae3</citedby><cites>FETCH-LOGICAL-c466t-3df6664f5eb6f6cdbd3e63d521710d09ad16557646a84384426e79229d14c8ae3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26088433$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Busto, Germain U</creatorcontrib><creatorcontrib>Guven-Ozkan, Tugba</creatorcontrib><creatorcontrib>Fulga, Tudor A</creatorcontrib><creatorcontrib>Van Vactor, David</creatorcontrib><creatorcontrib>Davis, Ronald L</creatorcontrib><title>microRNAs That Promote or Inhibit Memory Formation in Drosophila melanogaster</title><title>Genetics (Austin)</title><addtitle>Genetics</addtitle><description>microRNAs (miRNAs) are small noncoding RNAs that regulate gene expression post-transcriptionally. Prior studies have shown that they regulate numerous physiological processes critical for normal development, cellular growth control, and organismal behavior. Here, we systematically surveyed 134 different miRNAs for roles in olfactory learning and memory formation using "sponge" technology to titrate their activity broadly in the Drosophila melanogaster central nervous system. We identified at least five different miRNAs involved in memory formation or retention from this large screen, including miR-9c, miR-31a, miR-305, miR-974, and miR-980. Surprisingly, the titration of some miRNAs increased memory, while the titration of others decreased memory. We performed more detailed experiments on two miRNAs, miR-974 and miR-31a, by mapping their roles to subpopulations of brain neurons and testing the functional involvement in memory of potential mRNA targets through bioinformatics and a RNA interference knockdown approach. This screen offers an important first step toward the comprehensive identification of all miRNAs and their potential targets that serve in gene regulatory networks important for normal learning and memory.</description><subject>Animal memory</subject><subject>Animals</subject><subject>Behavior, Animal</subject><subject>Cholinergic Neurons - metabolism</subject><subject>Drosophila melanogaster</subject><subject>Drosophila melanogaster - genetics</subject><subject>Gene Expression</subject><subject>Insects</subject><subject>Investigations</subject><subject>Learning</subject><subject>Memory</subject><subject>MicroRNAs</subject><subject>MicroRNAs - genetics</subject><subject>Olfactory Receptor Neurons - metabolism</subject><subject>Time Factors</subject><issn>1943-2631</issn><issn>0016-6731</issn><issn>1943-2631</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><recordid>eNqFkU1rGzEQhkVpqR23vyAQBL30YldfO7u6BEKaD4PdlpKehbw7ayvsrhxJDuTfR8FxSHLpSQN65mVmHkKOOZvxQqofaxwwuTrOOFczDhqE_EDGXCs5FSD5x1f1iBzFeMsYA11Un8lIAKsqJeWYLHtXB__311mkNxub6J_ge5-Q-kDnw8atXKJL7H14oJc-9DY5P1A30J_BR7_duM7SHjs7-LWNCcMX8qm1XcSvz--E_Lu8uDm_ni5-X83PzxbTWgGkqWxaAFBtgStooW5WjUSQTSF4yVnDtG04FEUJCmyeslJKAJZaCN1wVVcW5YSc7nO3u1WPTY1DCrYz2-B6Gx6Mt868_Rncxqz9vVFKC1mxHPD9OSD4ux3GZHoXa-zyKuh30fCSaa65VOX_UdBMsEpkJxPy7R1663dhyJd4okSpmGQyU3JP5cPHGLB9mZsz82TWHMyabNbszeauk9crv_QcVMpHYROg2w</recordid><startdate>20150601</startdate><enddate>20150601</enddate><creator>Busto, Germain U</creator><creator>Guven-Ozkan, Tugba</creator><creator>Fulga, Tudor A</creator><creator>Van Vactor, David</creator><creator>Davis, Ronald L</creator><general>Genetics Society of America</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>3V.</scope><scope>4T-</scope><scope>4U-</scope><scope>7QP</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>K9-</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0R</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20150601</creationdate><title>microRNAs That Promote or Inhibit Memory Formation in Drosophila melanogaster</title><author>Busto, Germain U ; Guven-Ozkan, Tugba ; Fulga, Tudor A ; Van Vactor, David ; Davis, Ronald L</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c466t-3df6664f5eb6f6cdbd3e63d521710d09ad16557646a84384426e79229d14c8ae3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animal memory</topic><topic>Animals</topic><topic>Behavior, Animal</topic><topic>Cholinergic Neurons - metabolism</topic><topic>Drosophila melanogaster</topic><topic>Drosophila melanogaster - genetics</topic><topic>Gene Expression</topic><topic>Insects</topic><topic>Investigations</topic><topic>Learning</topic><topic>Memory</topic><topic>MicroRNAs</topic><topic>MicroRNAs - genetics</topic><topic>Olfactory Receptor Neurons - metabolism</topic><topic>Time Factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Busto, Germain U</creatorcontrib><creatorcontrib>Guven-Ozkan, Tugba</creatorcontrib><creatorcontrib>Fulga, Tudor A</creatorcontrib><creatorcontrib>Van Vactor, David</creatorcontrib><creatorcontrib>Davis, Ronald L</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Docstoc</collection><collection>University Readers</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Agricultural Science Collection</collection><collection>ProQuest Health and Medical</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</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>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>ProQuest Natural Science Collection</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>Research Library Prep</collection><collection>SciTech Premium Collection</collection><collection>Consumer Health Database (Alumni Edition)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Agriculture Science Database</collection><collection>Consumer Database (Proquest)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>ProQuest research library</collection><collection>ProQuest Science Journals</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>ProQuest Biological Science Journals</collection><collection>Research Library (Corporate)</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 Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genetics (Austin)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Busto, Germain U</au><au>Guven-Ozkan, Tugba</au><au>Fulga, Tudor A</au><au>Van Vactor, David</au><au>Davis, Ronald L</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>microRNAs That Promote or Inhibit Memory Formation in Drosophila melanogaster</atitle><jtitle>Genetics (Austin)</jtitle><addtitle>Genetics</addtitle><date>2015-06-01</date><risdate>2015</risdate><volume>200</volume><issue>2</issue><spage>569</spage><epage>580</epage><pages>569-580</pages><issn>1943-2631</issn><issn>0016-6731</issn><eissn>1943-2631</eissn><coden>GENTAE</coden><abstract>microRNAs (miRNAs) are small noncoding RNAs that regulate gene expression post-transcriptionally. Prior studies have shown that they regulate numerous physiological processes critical for normal development, cellular growth control, and organismal behavior. Here, we systematically surveyed 134 different miRNAs for roles in olfactory learning and memory formation using "sponge" technology to titrate their activity broadly in the Drosophila melanogaster central nervous system. We identified at least five different miRNAs involved in memory formation or retention from this large screen, including miR-9c, miR-31a, miR-305, miR-974, and miR-980. Surprisingly, the titration of some miRNAs increased memory, while the titration of others decreased memory. We performed more detailed experiments on two miRNAs, miR-974 and miR-31a, by mapping their roles to subpopulations of brain neurons and testing the functional involvement in memory of potential mRNA targets through bioinformatics and a RNA interference knockdown approach. This screen offers an important first step toward the comprehensive identification of all miRNAs and their potential targets that serve in gene regulatory networks important for normal learning and memory.</abstract><cop>United States</cop><pub>Genetics Society of America</pub><pmid>26088433</pmid><doi>10.1534/genetics.114.169623</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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source | Freely Accessible Science Journals - check A-Z of ejournals; Oxford Journals Online; Alma/SFX Local Collection |
subjects | Animal memory Animals Behavior, Animal Cholinergic Neurons - metabolism Drosophila melanogaster Drosophila melanogaster - genetics Gene Expression Insects Investigations Learning Memory MicroRNAs MicroRNAs - genetics Olfactory Receptor Neurons - metabolism Time Factors |
title | microRNAs That Promote or Inhibit Memory Formation in Drosophila melanogaster |
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