Dynamic Change and Target Prediction of Axon-Specific MicroRNAs in Regenerating Sciatic Nerve
Injury to axons in the peripheral nervous system induces rapid and local regenerative responses to form a new growth cone, and to generate a retrogradely transporting injury signal. The evidence for essential roles of intra-axonal protein synthesis during regeneration is now compelling. MicroRNA (mi...
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| Veröffentlicht in: | PloS one 2015-09, Vol.10 (9), p.e0137461-e0137461 |
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| description | Injury to axons in the peripheral nervous system induces rapid and local regenerative responses to form a new growth cone, and to generate a retrogradely transporting injury signal. The evidence for essential roles of intra-axonal protein synthesis during regeneration is now compelling. MicroRNA (miRNA) has recently been recognized as a prominent player in post-transcriptional regulation of axonal protein synthesis. Here, we directly contrast temporal changes of miRNA levels in the sciatic nerve following injury, as compared to those in an uninjured nerve using deep sequencing. Small RNAs ( |
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The evidence for essential roles of intra-axonal protein synthesis during regeneration is now compelling. MicroRNA (miRNA) has recently been recognized as a prominent player in post-transcriptional regulation of axonal protein synthesis. Here, we directly contrast temporal changes of miRNA levels in the sciatic nerve following injury, as compared to those in an uninjured nerve using deep sequencing. Small RNAs (<200 nucleotides in length) were fractionated from the proximal nerve stumps to improve the representation of differential miRNA levels. Of 141 axoplasmic miRNAs annotated, 63 rat miRNAs showed significantly differential levels at five time points following injury, compared to an uninjured nerve. The differential changes in miRNA levels responding to injury were processed for hierarchical clustering analyses, and used to predict target mRNAs by Targetscan and miRanda. By overlapping these predicted targets with 2,924 axonally localizing transcripts previously reported, the overlapping set of 214 transcripts was further analyzed by the Gene Ontology enrichment and Ingenuity Pathway Analyses. These results suggest the possibility that the potential targets for these miRNAs play key roles in numerous neurological functions involved in ER stress response, cytoskeleton dynamics, vesicle formation, and neuro-degeneration and-regeneration. Finally, our results suggest that miRNAs could play a direct role in regenerative response and may be manipulated to promote regenerative ability of injured nerves.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0137461</identifier><identifier>PMID: 26331719</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Axon guidance ; Axons ; Biomedical research ; Cellular stress response ; Cluster analysis ; Clustering ; Comparative analysis ; Cytoskeleton ; Degeneration ; Gene regulation ; Genetic aspects ; Genomics ; Injuries ; Injury analysis ; Kinases ; Localization ; Male ; MicroRNA ; MicroRNAs ; MicroRNAs - physiology ; Miranda ; miRNA ; Nerve Regeneration - genetics ; Nerves ; Nervous system ; Nucleotides ; Pain ; Peripheral nervous system ; Physiological aspects ; Polymerase Chain Reaction ; Post-transcription ; Predictions ; Protein biosynthesis ; Protein synthesis ; Proteins ; Rats ; Rats, Sprague-Dawley ; Regeneration ; Ribonucleic acid ; RNA ; Sciatic nerve ; Sciatic Nerve - physiology ; Sequence Analysis, RNA ; Spinal cord injuries</subject><ispartof>PloS one, 2015-09, Vol.10 (9), p.e0137461-e0137461</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Phay 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>2015 Phay et al 2015 Phay et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-10e16a92aecff035c01b938405efafb76ea5487281d9716c73e40836a30e1fbf3</citedby><cites>FETCH-LOGICAL-c692t-10e16a92aecff035c01b938405efafb76ea5487281d9716c73e40836a30e1fbf3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4557935/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4557935/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2095,2914,23846,27903,27904,53769,53771,79346,79347</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26331719$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Di Giovanni, Simone</contributor><creatorcontrib>Phay, Monichan</creatorcontrib><creatorcontrib>Kim, Hak Hee</creatorcontrib><creatorcontrib>Yoo, Soonmoon</creatorcontrib><title>Dynamic Change and Target Prediction of Axon-Specific MicroRNAs in Regenerating Sciatic Nerve</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Injury to axons in the peripheral nervous system induces rapid and local regenerative responses to form a new growth cone, and to generate a retrogradely transporting injury signal. The evidence for essential roles of intra-axonal protein synthesis during regeneration is now compelling. MicroRNA (miRNA) has recently been recognized as a prominent player in post-transcriptional regulation of axonal protein synthesis. Here, we directly contrast temporal changes of miRNA levels in the sciatic nerve following injury, as compared to those in an uninjured nerve using deep sequencing. Small RNAs (<200 nucleotides in length) were fractionated from the proximal nerve stumps to improve the representation of differential miRNA levels. Of 141 axoplasmic miRNAs annotated, 63 rat miRNAs showed significantly differential levels at five time points following injury, compared to an uninjured nerve. The differential changes in miRNA levels responding to injury were processed for hierarchical clustering analyses, and used to predict target mRNAs by Targetscan and miRanda. By overlapping these predicted targets with 2,924 axonally localizing transcripts previously reported, the overlapping set of 214 transcripts was further analyzed by the Gene Ontology enrichment and Ingenuity Pathway Analyses. These results suggest the possibility that the potential targets for these miRNAs play key roles in numerous neurological functions involved in ER stress response, cytoskeleton dynamics, vesicle formation, and neuro-degeneration and-regeneration. Finally, our results suggest that miRNAs could play a direct role in regenerative response and may be manipulated to promote regenerative ability of injured nerves.</description><subject>Animals</subject><subject>Axon guidance</subject><subject>Axons</subject><subject>Biomedical research</subject><subject>Cellular stress response</subject><subject>Cluster analysis</subject><subject>Clustering</subject><subject>Comparative analysis</subject><subject>Cytoskeleton</subject><subject>Degeneration</subject><subject>Gene regulation</subject><subject>Genetic aspects</subject><subject>Genomics</subject><subject>Injuries</subject><subject>Injury analysis</subject><subject>Kinases</subject><subject>Localization</subject><subject>Male</subject><subject>MicroRNA</subject><subject>MicroRNAs</subject><subject>MicroRNAs - physiology</subject><subject>Miranda</subject><subject>miRNA</subject><subject>Nerve Regeneration - genetics</subject><subject>Nerves</subject><subject>Nervous system</subject><subject>Nucleotides</subject><subject>Pain</subject><subject>Peripheral nervous system</subject><subject>Physiological aspects</subject><subject>Polymerase Chain Reaction</subject><subject>Post-transcription</subject><subject>Predictions</subject><subject>Protein biosynthesis</subject><subject>Protein synthesis</subject><subject>Proteins</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Regeneration</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Sciatic nerve</subject><subject>Sciatic Nerve - physiology</subject><subject>Sequence Analysis, RNA</subject><subject>Spinal cord injuries</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk11v0zAUhiMEYmPwDxBEQkJw0WLHjhPfIFXlq9LYUDu4Q5brHKeeUrvYybT9e5w1mxq0C-SLWCfPec-Hz0mSlxhNMSnwh0vXeSub6c5ZmKJoogw_So4xJ9mEZYg8PrgfJc9CuEQoJyVjT5OjjBGCC8yPk9-fbqzcGpXON9LWkEpbpRfS19CmPzxURrXG2dTpdHbt7GS1A2V0pL8b5d3ybBZSY9Ml1GDBy9bYOl0pEy8qPQN_Bc-TJ1o2AV4M35Pk55fPF_Nvk9Pzr4v57HSiGM_aCUaAmeSZBKU1IrlCeM1JSVEOWup1wUDmtCyyEle8wEwVBCgqCZMkOuq1JifJ673urnFBDJ0JIpaICCIlLiOx2BOVk5di581W-hvhpBG3BudrIX3MuwGhS05LWkgguqI5plxXkrIKZUA5Z5hErY9DtG69hUqBbb1sRqLjP9ZsRO2uBM3zgpM8CrwbBLz700FoxdYEBU0jLbiuzxvx29SLiL75B324uoGqZSzAWO1iXNWLihnNihwXOe3DTh-g4qkgTkAcI22ifeTwfuQQmRau21p2IYjFavn_7PmvMfv2gN2AbNpNcE3Xz1oYg3QPxmkLwYO-bzJGot-Cu26IfgvEsAXR7dXhA9073Y09-QtV-wA2</recordid><startdate>20150902</startdate><enddate>20150902</enddate><creator>Phay, Monichan</creator><creator>Kim, Hak Hee</creator><creator>Yoo, Soonmoon</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20150902</creationdate><title>Dynamic Change and Target Prediction of Axon-Specific MicroRNAs in Regenerating Sciatic Nerve</title><author>Phay, Monichan ; Kim, Hak Hee ; Yoo, Soonmoon</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-10e16a92aecff035c01b938405efafb76ea5487281d9716c73e40836a30e1fbf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Axon guidance</topic><topic>Axons</topic><topic>Biomedical research</topic><topic>Cellular stress response</topic><topic>Cluster analysis</topic><topic>Clustering</topic><topic>Comparative analysis</topic><topic>Cytoskeleton</topic><topic>Degeneration</topic><topic>Gene regulation</topic><topic>Genetic aspects</topic><topic>Genomics</topic><topic>Injuries</topic><topic>Injury analysis</topic><topic>Kinases</topic><topic>Localization</topic><topic>Male</topic><topic>MicroRNA</topic><topic>MicroRNAs</topic><topic>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>Phay, Monichan</au><au>Kim, Hak Hee</au><au>Yoo, Soonmoon</au><au>Di Giovanni, Simone</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dynamic Change and Target Prediction of Axon-Specific MicroRNAs in Regenerating Sciatic Nerve</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-09-02</date><risdate>2015</risdate><volume>10</volume><issue>9</issue><spage>e0137461</spage><epage>e0137461</epage><pages>e0137461-e0137461</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Injury to axons in the peripheral nervous system induces rapid and local regenerative responses to form a new growth cone, and to generate a retrogradely transporting injury signal. The evidence for essential roles of intra-axonal protein synthesis during regeneration is now compelling. MicroRNA (miRNA) has recently been recognized as a prominent player in post-transcriptional regulation of axonal protein synthesis. Here, we directly contrast temporal changes of miRNA levels in the sciatic nerve following injury, as compared to those in an uninjured nerve using deep sequencing. Small RNAs (<200 nucleotides in length) were fractionated from the proximal nerve stumps to improve the representation of differential miRNA levels. Of 141 axoplasmic miRNAs annotated, 63 rat miRNAs showed significantly differential levels at five time points following injury, compared to an uninjured nerve. The differential changes in miRNA levels responding to injury were processed for hierarchical clustering analyses, and used to predict target mRNAs by Targetscan and miRanda. By overlapping these predicted targets with 2,924 axonally localizing transcripts previously reported, the overlapping set of 214 transcripts was further analyzed by the Gene Ontology enrichment and Ingenuity Pathway Analyses. These results suggest the possibility that the potential targets for these miRNAs play key roles in numerous neurological functions involved in ER stress response, cytoskeleton dynamics, vesicle formation, and neuro-degeneration and-regeneration. Finally, our results suggest that miRNAs could play a direct role in regenerative response and may be manipulated to promote regenerative ability of injured nerves.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26331719</pmid><doi>10.1371/journal.pone.0137461</doi><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Full-Text Journals in Chemistry (Open access); DOAJ Directory of Open Access Journals; Public Library of Science; EZB-FREE-00999 freely available EZB journals; PubMed Central |
| subjects | Animals Axon guidance Axons Biomedical research Cellular stress response Cluster analysis Clustering Comparative analysis Cytoskeleton Degeneration Gene regulation Genetic aspects Genomics Injuries Injury analysis Kinases Localization Male MicroRNA MicroRNAs MicroRNAs - physiology Miranda miRNA Nerve Regeneration - genetics Nerves Nervous system Nucleotides Pain Peripheral nervous system Physiological aspects Polymerase Chain Reaction Post-transcription Predictions Protein biosynthesis Protein synthesis Proteins Rats Rats, Sprague-Dawley Regeneration Ribonucleic acid RNA Sciatic nerve Sciatic Nerve - physiology Sequence Analysis, RNA Spinal cord injuries |
| title | Dynamic Change and Target Prediction of Axon-Specific MicroRNAs in Regenerating Sciatic Nerve |
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