MicroRNAs, miR-23a-3p and miR-151-3p, Are Regulated in Dentate Gyrus Neuropil following Induction of Long-Term Potentiation In Vivo
Translation of synaptic mRNA contributes to alterations in the proteome necessary to consolidate long-term potentiation (LTP), a model of memory processes. Yet, how this process is controlled is not fully resolved. MicroRNAs are non-coding RNAs that negatively regulate gene expression by suppressing...
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| description | Translation of synaptic mRNA contributes to alterations in the proteome necessary to consolidate long-term potentiation (LTP), a model of memory processes. Yet, how this process is controlled is not fully resolved. MicroRNAs are non-coding RNAs that negatively regulate gene expression by suppressing translation or promoting mRNA degradation. As specific microRNAs are synaptically located, we hypothesized that they are ideally suited to couple synaptic activation, translational regulation, and LTP persistence. The aim of this study was to identify LTP-regulated microRNAs at or near synapses. Accordingly, LTP was induced unilaterally at perforant path-dentate gyrus synapses in awake adult Sprague-Dawley rats. Five hours later, dentate gyrus middle molecular layer neuropil, containing potentiated synapses, was laser-microdissected. MicroRNA expression profiling, using TaqMan Low Density MicroRNA Microarrays (n = 4), identified eight regulated microRNAs. Subsequent individual TaqMan assays confirmed upregulation of miR-23a-3p (1.30 ± 0.10; p = 0.015) and miR-151-3p (1.17 ± 0.19; p = 0.045) in a second cohort (n = 7). Interestingly, bioinformatic analysis indicated that miR-151-3p and miR-23a-3p regulate synaptic reorganisation and transcription, respectively. In summary, we have demonstrated for the first time that microRNAs are regulated in isolated neuropil following LTP induction in vivo, supporting the hypothesis that synaptic, LTP-responsive microRNAs contribute to LTP persistence via regulation of the synaptic proteome. |
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Yet, how this process is controlled is not fully resolved. MicroRNAs are non-coding RNAs that negatively regulate gene expression by suppressing translation or promoting mRNA degradation. As specific microRNAs are synaptically located, we hypothesized that they are ideally suited to couple synaptic activation, translational regulation, and LTP persistence. The aim of this study was to identify LTP-regulated microRNAs at or near synapses. Accordingly, LTP was induced unilaterally at perforant path-dentate gyrus synapses in awake adult Sprague-Dawley rats. Five hours later, dentate gyrus middle molecular layer neuropil, containing potentiated synapses, was laser-microdissected. MicroRNA expression profiling, using TaqMan Low Density MicroRNA Microarrays (n = 4), identified eight regulated microRNAs. Subsequent individual TaqMan assays confirmed upregulation of miR-23a-3p (1.30 ± 0.10; p = 0.015) and miR-151-3p (1.17 ± 0.19; p = 0.045) in a second cohort (n = 7). Interestingly, bioinformatic analysis indicated that miR-151-3p and miR-23a-3p regulate synaptic reorganisation and transcription, respectively. In summary, we have demonstrated for the first time that microRNAs are regulated in isolated neuropil following LTP induction in vivo, supporting the hypothesis that synaptic, LTP-responsive microRNAs contribute to LTP persistence via regulation of the synaptic proteome.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0170407</identifier><identifier>PMID: 28125614</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animal control ; Animals ; Biology and life sciences ; Brain research ; Coding ; Consolidation ; Dentate gyrus ; Dentate Gyrus - metabolism ; DNA microarrays ; Gene expression ; Gene Expression Regulation ; Genes ; Genetic aspects ; Information storage ; Lasers ; Localization ; Long-term potentiation ; Long-Term Potentiation - physiology ; Male ; Medical research ; Medicine and Health Sciences ; MicroRNA ; MicroRNAs ; MicroRNAs - genetics ; MicroRNAs - metabolism ; miRNA ; Neuropil ; Neuropil - metabolism ; Neurosciences ; Non-coding RNA ; Proteins ; Proteomes ; Psychological aspects ; Rats ; Rats, Sprague-Dawley ; Ribonucleic acid ; RNA ; Rodents ; Synapses ; Synapses - metabolism ; Synaptic transmission ; Transcription ; Translation</subject><ispartof>PloS one, 2017-01, Vol.12 (1), p.e0170407-e0170407</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Ryan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2017 Ryan et al 2017 Ryan et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c725t-cf5238703c9bd7956a184ec4a163f9918a75e1428c0076b6b9af04c37abb25563</citedby><cites>FETCH-LOGICAL-c725t-cf5238703c9bd7956a184ec4a163f9918a75e1428c0076b6b9af04c37abb25563</cites><orcidid>0000-0003-3936-2220</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/PMC5268419/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5268419/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2095,2914,23846,27903,27904,53770,53772,79347,79348</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28125614$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Ginsberg, Stephen D</contributor><creatorcontrib>Ryan, Brigid</creatorcontrib><creatorcontrib>Logan, Barbara J</creatorcontrib><creatorcontrib>Abraham, Wickliffe C</creatorcontrib><creatorcontrib>Williams, Joanna M</creatorcontrib><title>MicroRNAs, miR-23a-3p and miR-151-3p, Are Regulated in Dentate Gyrus Neuropil following Induction of Long-Term Potentiation In Vivo</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Translation of synaptic mRNA contributes to alterations in the proteome necessary to consolidate long-term potentiation (LTP), a model of memory processes. Yet, how this process is controlled is not fully resolved. MicroRNAs are non-coding RNAs that negatively regulate gene expression by suppressing translation or promoting mRNA degradation. As specific microRNAs are synaptically located, we hypothesized that they are ideally suited to couple synaptic activation, translational regulation, and LTP persistence. The aim of this study was to identify LTP-regulated microRNAs at or near synapses. Accordingly, LTP was induced unilaterally at perforant path-dentate gyrus synapses in awake adult Sprague-Dawley rats. Five hours later, dentate gyrus middle molecular layer neuropil, containing potentiated synapses, was laser-microdissected. MicroRNA expression profiling, using TaqMan Low Density MicroRNA Microarrays (n = 4), identified eight regulated microRNAs. Subsequent individual TaqMan assays confirmed upregulation of miR-23a-3p (1.30 ± 0.10; p = 0.015) and miR-151-3p (1.17 ± 0.19; p = 0.045) in a second cohort (n = 7). Interestingly, bioinformatic analysis indicated that miR-151-3p and miR-23a-3p regulate synaptic reorganisation and transcription, respectively. In summary, we have demonstrated for the first time that microRNAs are regulated in isolated neuropil following LTP induction in vivo, supporting the hypothesis that synaptic, LTP-responsive microRNAs contribute to LTP persistence via regulation of the synaptic proteome.</description><subject>Animal control</subject><subject>Animals</subject><subject>Biology and life sciences</subject><subject>Brain research</subject><subject>Coding</subject><subject>Consolidation</subject><subject>Dentate gyrus</subject><subject>Dentate Gyrus - metabolism</subject><subject>DNA microarrays</subject><subject>Gene expression</subject><subject>Gene Expression Regulation</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Information storage</subject><subject>Lasers</subject><subject>Localization</subject><subject>Long-term potentiation</subject><subject>Long-Term Potentiation - physiology</subject><subject>Male</subject><subject>Medical research</subject><subject>Medicine and Health Sciences</subject><subject>MicroRNA</subject><subject>MicroRNAs</subject><subject>MicroRNAs - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ryan, Brigid</au><au>Logan, Barbara J</au><au>Abraham, Wickliffe C</au><au>Williams, Joanna M</au><au>Ginsberg, Stephen D</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>MicroRNAs, miR-23a-3p and miR-151-3p, Are Regulated in Dentate Gyrus Neuropil following Induction of Long-Term Potentiation In Vivo</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2017-01-26</date><risdate>2017</risdate><volume>12</volume><issue>1</issue><spage>e0170407</spage><epage>e0170407</epage><pages>e0170407-e0170407</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Translation of synaptic mRNA contributes to alterations in the proteome necessary to consolidate long-term potentiation (LTP), a model of memory processes. Yet, how this process is controlled is not fully resolved. MicroRNAs are non-coding RNAs that negatively regulate gene expression by suppressing translation or promoting mRNA degradation. As specific microRNAs are synaptically located, we hypothesized that they are ideally suited to couple synaptic activation, translational regulation, and LTP persistence. The aim of this study was to identify LTP-regulated microRNAs at or near synapses. Accordingly, LTP was induced unilaterally at perforant path-dentate gyrus synapses in awake adult Sprague-Dawley rats. Five hours later, dentate gyrus middle molecular layer neuropil, containing potentiated synapses, was laser-microdissected. MicroRNA expression profiling, using TaqMan Low Density MicroRNA Microarrays (n = 4), identified eight regulated microRNAs. Subsequent individual TaqMan assays confirmed upregulation of miR-23a-3p (1.30 ± 0.10; p = 0.015) and miR-151-3p (1.17 ± 0.19; p = 0.045) in a second cohort (n = 7). Interestingly, bioinformatic analysis indicated that miR-151-3p and miR-23a-3p regulate synaptic reorganisation and transcription, respectively. In summary, we have demonstrated for the first time that microRNAs are regulated in isolated neuropil following LTP induction in vivo, supporting the hypothesis that synaptic, LTP-responsive microRNAs contribute to LTP persistence via regulation of the synaptic proteome.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28125614</pmid><doi>10.1371/journal.pone.0170407</doi><tpages>e0170407</tpages><orcidid>https://orcid.org/0000-0003-3936-2220</orcidid><oa>free_for_read</oa></addata></record> |
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| issn | 1932-6203 1932-6203 |
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| subjects | Animal control Animals Biology and life sciences Brain research Coding Consolidation Dentate gyrus Dentate Gyrus - metabolism DNA microarrays Gene expression Gene Expression Regulation Genes Genetic aspects Information storage Lasers Localization Long-term potentiation Long-Term Potentiation - physiology Male Medical research Medicine and Health Sciences MicroRNA MicroRNAs MicroRNAs - genetics MicroRNAs - metabolism miRNA Neuropil Neuropil - metabolism Neurosciences Non-coding RNA Proteins Proteomes Psychological aspects Rats Rats, Sprague-Dawley Ribonucleic acid RNA Rodents Synapses Synapses - metabolism Synaptic transmission Transcription Translation |
| title | MicroRNAs, miR-23a-3p and miR-151-3p, Are Regulated in Dentate Gyrus Neuropil following Induction of Long-Term Potentiation In Vivo |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-21T18%3A00%3A49IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=MicroRNAs,%20miR-23a-3p%20and%20miR-151-3p,%20Are%20Regulated%20in%20Dentate%20Gyrus%20Neuropil%20following%20Induction%20of%20Long-Term%20Potentiation%20In%20Vivo&rft.jtitle=PloS%20one&rft.au=Ryan,%20Brigid&rft.date=2017-01-26&rft.volume=12&rft.issue=1&rft.spage=e0170407&rft.epage=e0170407&rft.pages=e0170407-e0170407&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0170407&rft_dat=%3Cgale_plos_%3EA479045540%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1862133135&rft_id=info:pmid/28125614&rft_galeid=A479045540&rft_doaj_id=oai_doaj_org_article_e371dc051417451fab0cdd7cac7b483f&rfr_iscdi=true |