Translational profiling of retinal ganglion cell optic nerve regeneration in Xenopus laevis
Unlike adult mammals, adult frogs regrow their optic nerve following a crush injury, making Xenopus laevis a compelling model for studying the molecular mechanisms that underlie neuronal regeneration. Using Translational Ribosome Affinity Purification (TRAP), a method to isolate ribosome-associated...
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Veröffentlicht in: | Developmental biology 2017-06, Vol.426 (2), p.360-373 |
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creator | Whitworth, G.B. Misaghi, B.C. Rosenthal, D.M. Mills, E.A. Heinen, D.J. Watson, A.H. Ives, C.W. Ali, S.H. Bezold, K. Marsh-Armstrong, N. Watson, F.L. |
description | Unlike adult mammals, adult frogs regrow their optic nerve following a crush injury, making Xenopus laevis a compelling model for studying the molecular mechanisms that underlie neuronal regeneration. Using Translational Ribosome Affinity Purification (TRAP), a method to isolate ribosome-associated mRNAs from a target cell population, we have generated a transcriptional profile by RNA-Seq for retinal ganglion cells (RGC) during the period of recovery following an optic nerve injury. Based on bioinformatic analysis using the Xenopus laevis 9.1 genome assembly, our results reveal a profound shift in the composition of ribosome-associated mRNAs during the early stages of RGC regeneration. As factors involved in cell signaling are rapidly down-regulated, those involved in protein biosynthesis are up-regulated alongside key initiators of axon development. Using the new genome assembly, we were also able to analyze gene expression profiles of homeologous gene pairs arising from a whole-genome duplication in the Xenopus lineage. Here we see evidence of divergence in regulatory control among a significant proportion of pairs. Our data should provide a valuable resource for identifying genes involved in the regeneration process to target for future functional studies, in both naturally regenerative and non-regenerative vertebrates.
•Generated TRAP expression profiles for retinal ganglion cells in an adult injury model.•RNA-Seq reveals down-regulation in cell signaling and cell-type specific factors after injury.•Injury leads to up-regulation in protein biosynthesis genes and initiators of axon development.•Sequence alignment to new gene models shows evidence for divergent regulation of homeolog pairs.•RNA-Seq data are available through public repository and interactive web application. |
doi_str_mv | 10.1016/j.ydbio.2016.06.003 |
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•Generated TRAP expression profiles for retinal ganglion cells in an adult injury model.•RNA-Seq reveals down-regulation in cell signaling and cell-type specific factors after injury.•Injury leads to up-regulation in protein biosynthesis genes and initiators of axon development.•Sequence alignment to new gene models shows evidence for divergent regulation of homeolog pairs.•RNA-Seq data are available through public repository and interactive web application.</description><identifier>ISSN: 0012-1606</identifier><identifier>EISSN: 1095-564X</identifier><identifier>DOI: 10.1016/j.ydbio.2016.06.003</identifier><identifier>PMID: 27471010</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Amino Acid Sequence ; Animals ; Animals, Genetically Modified ; Expression profile ; Eye Proteins - biosynthesis ; Eye Proteins - genetics ; Gene Expression Regulation ; Gene Ontology ; Molecular Sequence Annotation ; Nerve Crush ; Nerve Regeneration - physiology ; Nerve Tissue Proteins - biosynthesis ; Nerve Tissue Proteins - genetics ; Optic nerve crush injury ; Optic Nerve Injuries - physiopathology ; Retinal Ganglion Cells - metabolism ; Ribosomes - metabolism ; RNA, Messenger - genetics ; RNA, Messenger - isolation & purification ; Sequence Alignment ; Sequence Analysis, RNA ; Sequence Homology, Amino Acid ; Signal Transduction ; TRAP ; Xenopus laevis - genetics ; Xenopus laevis - physiology ; Xenopus Proteins - biosynthesis ; Xenopus Proteins - genetics</subject><ispartof>Developmental biology, 2017-06, Vol.426 (2), p.360-373</ispartof><rights>2016 Elsevier Inc.</rights><rights>Copyright © 2016 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c459t-5916aace4f34bc564657d91c1be3af189e7a1070367143ec00fe4d53e13c2ebc3</citedby><cites>FETCH-LOGICAL-c459t-5916aace4f34bc564657d91c1be3af189e7a1070367143ec00fe4d53e13c2ebc3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.ydbio.2016.06.003$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27471010$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Whitworth, G.B.</creatorcontrib><creatorcontrib>Misaghi, B.C.</creatorcontrib><creatorcontrib>Rosenthal, D.M.</creatorcontrib><creatorcontrib>Mills, E.A.</creatorcontrib><creatorcontrib>Heinen, D.J.</creatorcontrib><creatorcontrib>Watson, A.H.</creatorcontrib><creatorcontrib>Ives, C.W.</creatorcontrib><creatorcontrib>Ali, S.H.</creatorcontrib><creatorcontrib>Bezold, K.</creatorcontrib><creatorcontrib>Marsh-Armstrong, N.</creatorcontrib><creatorcontrib>Watson, F.L.</creatorcontrib><title>Translational profiling of retinal ganglion cell optic nerve regeneration in Xenopus laevis</title><title>Developmental biology</title><addtitle>Dev Biol</addtitle><description>Unlike adult mammals, adult frogs regrow their optic nerve following a crush injury, making Xenopus laevis a compelling model for studying the molecular mechanisms that underlie neuronal regeneration. Using Translational Ribosome Affinity Purification (TRAP), a method to isolate ribosome-associated mRNAs from a target cell population, we have generated a transcriptional profile by RNA-Seq for retinal ganglion cells (RGC) during the period of recovery following an optic nerve injury. Based on bioinformatic analysis using the Xenopus laevis 9.1 genome assembly, our results reveal a profound shift in the composition of ribosome-associated mRNAs during the early stages of RGC regeneration. As factors involved in cell signaling are rapidly down-regulated, those involved in protein biosynthesis are up-regulated alongside key initiators of axon development. Using the new genome assembly, we were also able to analyze gene expression profiles of homeologous gene pairs arising from a whole-genome duplication in the Xenopus lineage. Here we see evidence of divergence in regulatory control among a significant proportion of pairs. Our data should provide a valuable resource for identifying genes involved in the regeneration process to target for future functional studies, in both naturally regenerative and non-regenerative vertebrates.
•Generated TRAP expression profiles for retinal ganglion cells in an adult injury model.•RNA-Seq reveals down-regulation in cell signaling and cell-type specific factors after injury.•Injury leads to up-regulation in protein biosynthesis genes and initiators of axon development.•Sequence alignment to new gene models shows evidence for divergent regulation of homeolog pairs.•RNA-Seq data are available through public repository and interactive web application.</description><subject>Amino Acid Sequence</subject><subject>Animals</subject><subject>Animals, Genetically Modified</subject><subject>Expression profile</subject><subject>Eye Proteins - biosynthesis</subject><subject>Eye Proteins - genetics</subject><subject>Gene Expression Regulation</subject><subject>Gene Ontology</subject><subject>Molecular Sequence Annotation</subject><subject>Nerve Crush</subject><subject>Nerve Regeneration - physiology</subject><subject>Nerve Tissue Proteins - biosynthesis</subject><subject>Nerve Tissue Proteins - genetics</subject><subject>Optic nerve crush injury</subject><subject>Optic Nerve Injuries - physiopathology</subject><subject>Retinal Ganglion Cells - metabolism</subject><subject>Ribosomes - metabolism</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - isolation & purification</subject><subject>Sequence Alignment</subject><subject>Sequence Analysis, RNA</subject><subject>Sequence Homology, Amino Acid</subject><subject>Signal Transduction</subject><subject>TRAP</subject><subject>Xenopus laevis - genetics</subject><subject>Xenopus laevis - physiology</subject><subject>Xenopus Proteins - biosynthesis</subject><subject>Xenopus Proteins - genetics</subject><issn>0012-1606</issn><issn>1095-564X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kd9LHDEQx0Op1NP2LyhIHvuy52ST3ew-WCjSqiD4oiD0IWSzs9scuWRN9g787815VvRFGMiP-cx3JvkS8p3BkgGrT1fLx76zYVnmwxJyAP9EFgzaqqhqcf-ZLABYWbAa6kNylNIKMtE0_As5LKWQWQMW5O9t1D45PdvgtaNTDIN11o80DDTibHeXo_ajy3lq0Dkaptka6jFuMRMj5t1zNbWe3qMP0yZRp3Fr01dyMGiX8NvLekzu_vy-Pb8srm8urs5_XRdGVO1cVC2rtTYoBi46k0evK9m3zLAOuR5Y06LUDCTwWjLB0QAMKPqKI-OmxM7wY_JzrzttujX2Bv0ctVNTtGsdH1XQVr3PePtPjWGrqqaVICAL_HgRiOFhg2lWa5t2j9UewyYp1pS15BJKkVG-R00MKUUcXtswUDtb1Eo926J2tijIATxXnbyd8LXmvw8ZONsDmP9pazGqZCx6g72NaGbVB_thgyfZl6JC</recordid><startdate>20170615</startdate><enddate>20170615</enddate><creator>Whitworth, G.B.</creator><creator>Misaghi, B.C.</creator><creator>Rosenthal, D.M.</creator><creator>Mills, E.A.</creator><creator>Heinen, D.J.</creator><creator>Watson, A.H.</creator><creator>Ives, C.W.</creator><creator>Ali, S.H.</creator><creator>Bezold, K.</creator><creator>Marsh-Armstrong, N.</creator><creator>Watson, F.L.</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20170615</creationdate><title>Translational profiling of retinal ganglion cell optic nerve regeneration in Xenopus laevis</title><author>Whitworth, G.B. ; Misaghi, B.C. ; Rosenthal, D.M. ; Mills, E.A. ; Heinen, D.J. ; Watson, A.H. ; Ives, C.W. ; Ali, S.H. ; Bezold, K. ; Marsh-Armstrong, N. ; Watson, F.L.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c459t-5916aace4f34bc564657d91c1be3af189e7a1070367143ec00fe4d53e13c2ebc3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Amino Acid Sequence</topic><topic>Animals</topic><topic>Animals, Genetically Modified</topic><topic>Expression profile</topic><topic>Eye Proteins - biosynthesis</topic><topic>Eye Proteins - genetics</topic><topic>Gene Expression Regulation</topic><topic>Gene Ontology</topic><topic>Molecular Sequence Annotation</topic><topic>Nerve Crush</topic><topic>Nerve Regeneration - physiology</topic><topic>Nerve Tissue Proteins - biosynthesis</topic><topic>Nerve Tissue Proteins - genetics</topic><topic>Optic nerve crush injury</topic><topic>Optic Nerve Injuries - physiopathology</topic><topic>Retinal Ganglion Cells - metabolism</topic><topic>Ribosomes - metabolism</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - isolation & purification</topic><topic>Sequence Alignment</topic><topic>Sequence Analysis, RNA</topic><topic>Sequence Homology, Amino Acid</topic><topic>Signal Transduction</topic><topic>TRAP</topic><topic>Xenopus laevis - genetics</topic><topic>Xenopus laevis - physiology</topic><topic>Xenopus Proteins - biosynthesis</topic><topic>Xenopus Proteins - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Whitworth, G.B.</creatorcontrib><creatorcontrib>Misaghi, B.C.</creatorcontrib><creatorcontrib>Rosenthal, D.M.</creatorcontrib><creatorcontrib>Mills, E.A.</creatorcontrib><creatorcontrib>Heinen, D.J.</creatorcontrib><creatorcontrib>Watson, A.H.</creatorcontrib><creatorcontrib>Ives, C.W.</creatorcontrib><creatorcontrib>Ali, S.H.</creatorcontrib><creatorcontrib>Bezold, K.</creatorcontrib><creatorcontrib>Marsh-Armstrong, N.</creatorcontrib><creatorcontrib>Watson, F.L.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Developmental biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Whitworth, G.B.</au><au>Misaghi, B.C.</au><au>Rosenthal, D.M.</au><au>Mills, E.A.</au><au>Heinen, D.J.</au><au>Watson, A.H.</au><au>Ives, C.W.</au><au>Ali, S.H.</au><au>Bezold, K.</au><au>Marsh-Armstrong, N.</au><au>Watson, F.L.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Translational profiling of retinal ganglion cell optic nerve regeneration in Xenopus laevis</atitle><jtitle>Developmental biology</jtitle><addtitle>Dev Biol</addtitle><date>2017-06-15</date><risdate>2017</risdate><volume>426</volume><issue>2</issue><spage>360</spage><epage>373</epage><pages>360-373</pages><issn>0012-1606</issn><eissn>1095-564X</eissn><abstract>Unlike adult mammals, adult frogs regrow their optic nerve following a crush injury, making Xenopus laevis a compelling model for studying the molecular mechanisms that underlie neuronal regeneration. Using Translational Ribosome Affinity Purification (TRAP), a method to isolate ribosome-associated mRNAs from a target cell population, we have generated a transcriptional profile by RNA-Seq for retinal ganglion cells (RGC) during the period of recovery following an optic nerve injury. Based on bioinformatic analysis using the Xenopus laevis 9.1 genome assembly, our results reveal a profound shift in the composition of ribosome-associated mRNAs during the early stages of RGC regeneration. As factors involved in cell signaling are rapidly down-regulated, those involved in protein biosynthesis are up-regulated alongside key initiators of axon development. Using the new genome assembly, we were also able to analyze gene expression profiles of homeologous gene pairs arising from a whole-genome duplication in the Xenopus lineage. Here we see evidence of divergence in regulatory control among a significant proportion of pairs. Our data should provide a valuable resource for identifying genes involved in the regeneration process to target for future functional studies, in both naturally regenerative and non-regenerative vertebrates.
•Generated TRAP expression profiles for retinal ganglion cells in an adult injury model.•RNA-Seq reveals down-regulation in cell signaling and cell-type specific factors after injury.•Injury leads to up-regulation in protein biosynthesis genes and initiators of axon development.•Sequence alignment to new gene models shows evidence for divergent regulation of homeolog pairs.•RNA-Seq data are available through public repository and interactive web application.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>27471010</pmid><doi>10.1016/j.ydbio.2016.06.003</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Amino Acid Sequence Animals Animals, Genetically Modified Expression profile Eye Proteins - biosynthesis Eye Proteins - genetics Gene Expression Regulation Gene Ontology Molecular Sequence Annotation Nerve Crush Nerve Regeneration - physiology Nerve Tissue Proteins - biosynthesis Nerve Tissue Proteins - genetics Optic nerve crush injury Optic Nerve Injuries - physiopathology Retinal Ganglion Cells - metabolism Ribosomes - metabolism RNA, Messenger - genetics RNA, Messenger - isolation & purification Sequence Alignment Sequence Analysis, RNA Sequence Homology, Amino Acid Signal Transduction TRAP Xenopus laevis - genetics Xenopus laevis - physiology Xenopus Proteins - biosynthesis Xenopus Proteins - genetics |
title | Translational profiling of retinal ganglion cell optic nerve regeneration in Xenopus laevis |
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