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Optic nerve crush induces spatial and temporal gene expression patterns in retina and optic nerve of BALB/cJ mice
Central nervous system (CNS) trauma and neurodegenerative disorders trigger a cascade of cellular and molecular events resulting in neuronal apoptosis and regenerative failure. The pathogenic mechanisms and gene expression changes associated with these detrimental events can be effectively studied u...
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| Published in: | Molecular neurodegeneration 2014-04, Vol.9 (1), p.14-14, Article 14 |
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| creator | Sharma, Tasneem P McDowell, Colleen M Liu, Yang Wagner, Alex H Thole, David Faga, Benjamin P Wordinger, Robert J Braun, Terry A Clark, Abbot F |
| description | Central nervous system (CNS) trauma and neurodegenerative disorders trigger a cascade of cellular and molecular events resulting in neuronal apoptosis and regenerative failure. The pathogenic mechanisms and gene expression changes associated with these detrimental events can be effectively studied using a rodent optic nerve crush (ONC) model. The purpose of this study was to use a mouse ONC model to: (a) evaluate changes in retina and optic nerve (ON) gene expression, (b) identify neurodegenerative pathogenic pathways and (c) discover potential new therapeutic targets.
Only 54% of total neurons survived in the ganglion cell layer (GCL) 28 days post crush. Using Bayesian Estimation of Temporal Regulation (BETR) gene expression analysis, we identified significantly altered expression of 1,723 and 2,110 genes in the retina and ON, respectively. Meta-analysis of altered gene expression (≥1.5, ≤-1.5, p |
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Only 54% of total neurons survived in the ganglion cell layer (GCL) 28 days post crush. Using Bayesian Estimation of Temporal Regulation (BETR) gene expression analysis, we identified significantly altered expression of 1,723 and 2,110 genes in the retina and ON, respectively. Meta-analysis of altered gene expression (≥1.5, ≤-1.5, p < 0.05) using Partek and DAVID demonstrated 28 up and 20 down-regulated retinal gene clusters and 57 up and 41 down-regulated optic nerve clusters. Regulated gene clusters included regenerative change, synaptic plasticity, axonogenesis, neuron projection, and neuron differentiation. Expression of selected genes (Vsnl1, Syt1, Synpr and Nrn1) from retinal and ON neuronal clusters were quantitatively and qualitatively examined for their relation to axonal neurodegeneration by immunohistochemistry and qRT-PCR.
A number of detrimental gene expression changes occur that contribute to trauma-induced neurodegeneration after injury to ON axons. Nrn1 (synaptic plasticity gene), Synpr and Syt1 (synaptic vesicle fusion genes), and Vsnl1 (neuron differentiation associated gene) were a few of the potentially unique genes identified that were down-regulated spatially and temporally in our rodent ONC model. Bioinformatic meta-analysis identified significant tissue-specific and time-dependent gene clusters associated with regenerative changes, synaptic plasticity, axonogenesis, neuron projection, and neuron differentiation. These ONC induced neuronal loss and regenerative failure associated clusters can be extrapolated to changes occurring in other forms of CNS trauma or in clinical neurodegenerative pathological settings. In conclusion, this study identified potential therapeutic targets to address two key mechanisms of CNS trauma and neurodegeneration: neuronal loss and regenerative failure.</description><identifier>ISSN: 1750-1326</identifier><identifier>EISSN: 1750-1326</identifier><identifier>DOI: 10.1186/1750-1326-9-14</identifier><identifier>PMID: 24767545</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Analysis ; Animals ; Apoptosis ; Apoptosis - genetics ; Bioinformatics ; Biotechnology industry ; Computer software industry ; Disease Models, Animal ; Gene expression ; Gene Expression Regulation - genetics ; Genetic aspects ; Health aspects ; Immunohistochemistry ; Injuries ; Mice ; Mice, Inbred BALB C ; Nerve Crush ; Nerve Degeneration - genetics ; Nerve Regeneration - genetics ; Nervous system ; Neurodegeneration ; Neurodegenerative Diseases - genetics ; Neurodegenerative Diseases - metabolism ; Neurodegenerative Diseases - pathology ; Neurons ; Oligonucleotide Array Sequence Analysis ; Optic nerve ; Optic Nerve - metabolism ; Optic Nerve - pathology ; Optics ; Proteins ; Real-Time Polymerase Chain Reaction ; Retina - metabolism ; Retina - pathology ; Reverse Transcriptase Polymerase Chain Reaction ; Studies ; Survival analysis ; Transcriptome ; Variance analysis</subject><ispartof>Molecular neurodegeneration, 2014-04, Vol.9 (1), p.14-14, Article 14</ispartof><rights>COPYRIGHT 2014 BioMed Central Ltd.</rights><rights>2014 Sharma et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.</rights><rights>Copyright © 2014 Sharma et al.; licensee BioMed Central Ltd. 2014 Sharma et al.; licensee BioMed Central Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c584t-7b4be631f861d3cf29c167ef67076accff9ab4f0dc31c1f47ce35a98edf35f393</citedby><cites>FETCH-LOGICAL-c584t-7b4be631f861d3cf29c167ef67076accff9ab4f0dc31c1f47ce35a98edf35f393</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/PMC4113182/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1524005467?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25751,27922,27923,37010,37011,44588,53789,53791</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24767545$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sharma, Tasneem P</creatorcontrib><creatorcontrib>McDowell, Colleen M</creatorcontrib><creatorcontrib>Liu, Yang</creatorcontrib><creatorcontrib>Wagner, Alex H</creatorcontrib><creatorcontrib>Thole, David</creatorcontrib><creatorcontrib>Faga, Benjamin P</creatorcontrib><creatorcontrib>Wordinger, Robert J</creatorcontrib><creatorcontrib>Braun, Terry A</creatorcontrib><creatorcontrib>Clark, Abbot F</creatorcontrib><title>Optic nerve crush induces spatial and temporal gene expression patterns in retina and optic nerve of BALB/cJ mice</title><title>Molecular neurodegeneration</title><addtitle>Mol Neurodegener</addtitle><description>Central nervous system (CNS) trauma and neurodegenerative disorders trigger a cascade of cellular and molecular events resulting in neuronal apoptosis and regenerative failure. The pathogenic mechanisms and gene expression changes associated with these detrimental events can be effectively studied using a rodent optic nerve crush (ONC) model. The purpose of this study was to use a mouse ONC model to: (a) evaluate changes in retina and optic nerve (ON) gene expression, (b) identify neurodegenerative pathogenic pathways and (c) discover potential new therapeutic targets.
Only 54% of total neurons survived in the ganglion cell layer (GCL) 28 days post crush. Using Bayesian Estimation of Temporal Regulation (BETR) gene expression analysis, we identified significantly altered expression of 1,723 and 2,110 genes in the retina and ON, respectively. Meta-analysis of altered gene expression (≥1.5, ≤-1.5, p < 0.05) using Partek and DAVID demonstrated 28 up and 20 down-regulated retinal gene clusters and 57 up and 41 down-regulated optic nerve clusters. Regulated gene clusters included regenerative change, synaptic plasticity, axonogenesis, neuron projection, and neuron differentiation. Expression of selected genes (Vsnl1, Syt1, Synpr and Nrn1) from retinal and ON neuronal clusters were quantitatively and qualitatively examined for their relation to axonal neurodegeneration by immunohistochemistry and qRT-PCR.
A number of detrimental gene expression changes occur that contribute to trauma-induced neurodegeneration after injury to ON axons. Nrn1 (synaptic plasticity gene), Synpr and Syt1 (synaptic vesicle fusion genes), and Vsnl1 (neuron differentiation associated gene) were a few of the potentially unique genes identified that were down-regulated spatially and temporally in our rodent ONC model. Bioinformatic meta-analysis identified significant tissue-specific and time-dependent gene clusters associated with regenerative changes, synaptic plasticity, axonogenesis, neuron projection, and neuron differentiation. These ONC induced neuronal loss and regenerative failure associated clusters can be extrapolated to changes occurring in other forms of CNS trauma or in clinical neurodegenerative pathological settings. In conclusion, this study identified potential therapeutic targets to address two key mechanisms of CNS trauma and neurodegeneration: neuronal loss and regenerative failure.</description><subject>Analysis</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Apoptosis - genetics</subject><subject>Bioinformatics</subject><subject>Biotechnology industry</subject><subject>Computer software industry</subject><subject>Disease Models, Animal</subject><subject>Gene expression</subject><subject>Gene Expression Regulation - genetics</subject><subject>Genetic aspects</subject><subject>Health aspects</subject><subject>Immunohistochemistry</subject><subject>Injuries</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Nerve Crush</subject><subject>Nerve Degeneration - genetics</subject><subject>Nerve Regeneration - genetics</subject><subject>Nervous system</subject><subject>Neurodegeneration</subject><subject>Neurodegenerative Diseases - genetics</subject><subject>Neurodegenerative Diseases - metabolism</subject><subject>Neurodegenerative Diseases - pathology</subject><subject>Neurons</subject><subject>Oligonucleotide Array Sequence Analysis</subject><subject>Optic nerve</subject><subject>Optic Nerve - metabolism</subject><subject>Optic Nerve - pathology</subject><subject>Optics</subject><subject>Proteins</subject><subject>Real-Time Polymerase Chain Reaction</subject><subject>Retina - metabolism</subject><subject>Retina - pathology</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Studies</subject><subject>Survival analysis</subject><subject>Transcriptome</subject><subject>Variance analysis</subject><issn>1750-1326</issn><issn>1750-1326</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><recordid>eNqNks1vFSEUxSdGY2t169KQuHEzLQxfw8bktana5iXd6JrwmMsrzQxMYabR_16m1udr04VhAVx-9wQOp6reE3xMSCtOiOS4JrQRtaoJe1Ed7gov99YH1ZucbzBmEmP-ujpomBSSM35Y3V6Nk7coQLoDZNOcr5EP3WwhozyayZsemdChCYYxprLZQgAEP8cEOfsYUGEmSCGXLpRg8sHc83FPNTp0ulqfnthLNHgLb6tXzvQZ3j3MR9WPL-ffz77V66uvF2erdW15y6ZabtgGBCWuFaSj1jXKEiHBCYmlMNY6p8yGOdxZSixxTFqg3KgWOke5o4oeVZ__6I7zZoDOQpjKA_SY_GDSLx2N149Pgr_W23inGSGUtE0R-PQgkOLtDHnSg88W-t4EiHPWhNPio2oa9h9ooxRlQomCfnyC3sQ5heLEQrHyP0zIf9TW9KB9cLFc0S6iesUZFhxLhgt1_AxVRgfF6RjA-VJ_rsGmmHMCt7ODYL3kSS-R0UtktNJkediHfRN3-N8A0d98KcT0</recordid><startdate>20140427</startdate><enddate>20140427</enddate><creator>Sharma, Tasneem P</creator><creator>McDowell, Colleen M</creator><creator>Liu, Yang</creator><creator>Wagner, Alex H</creator><creator>Thole, David</creator><creator>Faga, Benjamin P</creator><creator>Wordinger, Robert J</creator><creator>Braun, Terry A</creator><creator>Clark, Abbot F</creator><general>BioMed Central Ltd</general><general>BioMed Central</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>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20140427</creationdate><title>Optic nerve crush induces spatial and temporal gene expression patterns in retina and optic nerve of BALB/cJ mice</title><author>Sharma, Tasneem P ; McDowell, Colleen M ; Liu, Yang ; Wagner, Alex H ; Thole, David ; Faga, Benjamin P ; Wordinger, Robert J ; Braun, Terry A ; Clark, Abbot F</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c584t-7b4be631f861d3cf29c167ef67076accff9ab4f0dc31c1f47ce35a98edf35f393</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Analysis</topic><topic>Animals</topic><topic>Apoptosis</topic><topic>Apoptosis - genetics</topic><topic>Bioinformatics</topic><topic>Biotechnology industry</topic><topic>Computer software industry</topic><topic>Disease Models, Animal</topic><topic>Gene expression</topic><topic>Gene Expression Regulation - genetics</topic><topic>Genetic aspects</topic><topic>Health aspects</topic><topic>Immunohistochemistry</topic><topic>Injuries</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Nerve Crush</topic><topic>Nerve Degeneration - genetics</topic><topic>Nerve Regeneration - genetics</topic><topic>Nervous system</topic><topic>Neurodegeneration</topic><topic>Neurodegenerative Diseases - genetics</topic><topic>Neurodegenerative Diseases - metabolism</topic><topic>Neurodegenerative Diseases - pathology</topic><topic>Neurons</topic><topic>Oligonucleotide Array Sequence Analysis</topic><topic>Optic nerve</topic><topic>Optic Nerve - metabolism</topic><topic>Optic Nerve - pathology</topic><topic>Optics</topic><topic>Proteins</topic><topic>Real-Time Polymerase Chain Reaction</topic><topic>Retina - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular neurodegeneration</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sharma, Tasneem P</au><au>McDowell, Colleen M</au><au>Liu, Yang</au><au>Wagner, Alex H</au><au>Thole, David</au><au>Faga, Benjamin P</au><au>Wordinger, Robert J</au><au>Braun, Terry A</au><au>Clark, Abbot F</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Optic nerve crush induces spatial and temporal gene expression patterns in retina and optic nerve of BALB/cJ mice</atitle><jtitle>Molecular neurodegeneration</jtitle><addtitle>Mol Neurodegener</addtitle><date>2014-04-27</date><risdate>2014</risdate><volume>9</volume><issue>1</issue><spage>14</spage><epage>14</epage><pages>14-14</pages><artnum>14</artnum><issn>1750-1326</issn><eissn>1750-1326</eissn><abstract>Central nervous system (CNS) trauma and neurodegenerative disorders trigger a cascade of cellular and molecular events resulting in neuronal apoptosis and regenerative failure. The pathogenic mechanisms and gene expression changes associated with these detrimental events can be effectively studied using a rodent optic nerve crush (ONC) model. The purpose of this study was to use a mouse ONC model to: (a) evaluate changes in retina and optic nerve (ON) gene expression, (b) identify neurodegenerative pathogenic pathways and (c) discover potential new therapeutic targets.
Only 54% of total neurons survived in the ganglion cell layer (GCL) 28 days post crush. Using Bayesian Estimation of Temporal Regulation (BETR) gene expression analysis, we identified significantly altered expression of 1,723 and 2,110 genes in the retina and ON, respectively. Meta-analysis of altered gene expression (≥1.5, ≤-1.5, p < 0.05) using Partek and DAVID demonstrated 28 up and 20 down-regulated retinal gene clusters and 57 up and 41 down-regulated optic nerve clusters. Regulated gene clusters included regenerative change, synaptic plasticity, axonogenesis, neuron projection, and neuron differentiation. Expression of selected genes (Vsnl1, Syt1, Synpr and Nrn1) from retinal and ON neuronal clusters were quantitatively and qualitatively examined for their relation to axonal neurodegeneration by immunohistochemistry and qRT-PCR.
A number of detrimental gene expression changes occur that contribute to trauma-induced neurodegeneration after injury to ON axons. Nrn1 (synaptic plasticity gene), Synpr and Syt1 (synaptic vesicle fusion genes), and Vsnl1 (neuron differentiation associated gene) were a few of the potentially unique genes identified that were down-regulated spatially and temporally in our rodent ONC model. Bioinformatic meta-analysis identified significant tissue-specific and time-dependent gene clusters associated with regenerative changes, synaptic plasticity, axonogenesis, neuron projection, and neuron differentiation. These ONC induced neuronal loss and regenerative failure associated clusters can be extrapolated to changes occurring in other forms of CNS trauma or in clinical neurodegenerative pathological settings. In conclusion, this study identified potential therapeutic targets to address two key mechanisms of CNS trauma and neurodegeneration: neuronal loss and regenerative failure.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>24767545</pmid><doi>10.1186/1750-1326-9-14</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Molecular neurodegeneration, 2014-04, Vol.9 (1), p.14-14, Article 14 |
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| subjects | Analysis Animals Apoptosis Apoptosis - genetics Bioinformatics Biotechnology industry Computer software industry Disease Models, Animal Gene expression Gene Expression Regulation - genetics Genetic aspects Health aspects Immunohistochemistry Injuries Mice Mice, Inbred BALB C Nerve Crush Nerve Degeneration - genetics Nerve Regeneration - genetics Nervous system Neurodegeneration Neurodegenerative Diseases - genetics Neurodegenerative Diseases - metabolism Neurodegenerative Diseases - pathology Neurons Oligonucleotide Array Sequence Analysis Optic nerve Optic Nerve - metabolism Optic Nerve - pathology Optics Proteins Real-Time Polymerase Chain Reaction Retina - metabolism Retina - pathology Reverse Transcriptase Polymerase Chain Reaction Studies Survival analysis Transcriptome Variance analysis |
| title | Optic nerve crush induces spatial and temporal gene expression patterns in retina and optic nerve of BALB/cJ mice |
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