Partial Hepatectomy Induced Long Noncoding RNA Inhibits Hepatocyte Proliferation during Liver Regeneration
Liver regeneration after partial hepatectomy (PHx) is a complex and well-orchestrated biological process in which synchronized cell proliferation is induced in response to the loss of liver mass. To define long noncoding RNAs (lncRNAs) that participate in the regulation of liver regeneration, we per...
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| creator | Huang, Lulu Damle, Sagar S Booten, Sheri Singh, Priyam Sabripour, Mahyar Hsu, Jeff Jo, Minji Katz, Melanie Watt, Andy Hart, Christopher E Freier, Susan M Monia, Brett P Guo, Shuling |
| description | Liver regeneration after partial hepatectomy (PHx) is a complex and well-orchestrated biological process in which synchronized cell proliferation is induced in response to the loss of liver mass. To define long noncoding RNAs (lncRNAs) that participate in the regulation of liver regeneration, we performed microarray analysis and identified more than 400 lncRNAs exhibiting significantly altered expression. Of these, one lncRNA, LncPHx2 (Long noncoding RNA induced by PHx 2), was highly upregulated during liver regeneration. Depletion of LncPHx2 during liver regeneration using antisense oligonucleotides led to a transient increase in hepatocyte proliferation and more rapid liver regeneration. Gene expression analysis showed that LncPHx2 depletion resulted in upregulation of mRNAs encoding proteins known to promote cell proliferation, including MCM components, DNA polymerases, histone proteins, and transcription factors. LncPHx2 interacts with the mRNAs of MCM components, making it a candidate to regulate the expression of MCMs and other genes post-transcriptionally. Collectively, our data demonstrate that LncPHx2 is a key lncRNA that participates in a negative feedback loop modulating hepatocyte proliferation through RNA-RNA interactions. |
| doi_str_mv | 10.1371/journal.pone.0132798 |
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To define long noncoding RNAs (lncRNAs) that participate in the regulation of liver regeneration, we performed microarray analysis and identified more than 400 lncRNAs exhibiting significantly altered expression. Of these, one lncRNA, LncPHx2 (Long noncoding RNA induced by PHx 2), was highly upregulated during liver regeneration. Depletion of LncPHx2 during liver regeneration using antisense oligonucleotides led to a transient increase in hepatocyte proliferation and more rapid liver regeneration. Gene expression analysis showed that LncPHx2 depletion resulted in upregulation of mRNAs encoding proteins known to promote cell proliferation, including MCM components, DNA polymerases, histone proteins, and transcription factors. LncPHx2 interacts with the mRNAs of MCM components, making it a candidate to regulate the expression of MCMs and other genes post-transcriptionally. Collectively, our data demonstrate that LncPHx2 is a key lncRNA that participates in a negative feedback loop modulating hepatocyte proliferation through RNA-RNA interactions.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0132798</identifier><identifier>PMID: 26207833</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Antisense oligonucleotides ; Bioinformatics ; Biological activity ; Cell adhesion & migration ; Cell cycle ; Cell growth ; Cell proliferation ; Cell Proliferation - genetics ; Cells, Cultured ; Deoxyribonucleic acid ; Depletion ; DNA ; DNA microarrays ; DNA-directed DNA polymerase ; Feedback loops ; Gene expression ; Gene Expression Profiling ; Genomes ; Genomics ; Hepatectomy ; Hepatocytes - physiology ; Liver ; Liver Regeneration - genetics ; Male ; Mice ; Mice, Inbred C57BL ; Microarray Analysis ; Negative feedback ; Oligonucleotides ; Pharmaceuticals ; Post-transcription ; Proteins ; R&D ; Regeneration ; Research & development ; Ribonucleic acid ; RNA ; RNA, Long Noncoding - genetics ; RNA, Long Noncoding - physiology ; Stem cells ; Transcription factors ; Up-Regulation - genetics</subject><ispartof>PloS one, 2015-07, Vol.10 (7), p.e0132798-e0132798</ispartof><rights>2015 Huang 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 Huang et al 2015 Huang et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-184eddf2e4d2ce6a200cbffb2f9a1f19a253be6bdc4d443af8411ee5974507373</citedby><cites>FETCH-LOGICAL-c526t-184eddf2e4d2ce6a200cbffb2f9a1f19a253be6bdc4d443af8411ee5974507373</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/PMC4514479/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4514479/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26207833$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Zuo, Zhuang</contributor><creatorcontrib>Huang, Lulu</creatorcontrib><creatorcontrib>Damle, Sagar S</creatorcontrib><creatorcontrib>Booten, Sheri</creatorcontrib><creatorcontrib>Singh, Priyam</creatorcontrib><creatorcontrib>Sabripour, Mahyar</creatorcontrib><creatorcontrib>Hsu, Jeff</creatorcontrib><creatorcontrib>Jo, Minji</creatorcontrib><creatorcontrib>Katz, Melanie</creatorcontrib><creatorcontrib>Watt, Andy</creatorcontrib><creatorcontrib>Hart, Christopher E</creatorcontrib><creatorcontrib>Freier, Susan M</creatorcontrib><creatorcontrib>Monia, Brett P</creatorcontrib><creatorcontrib>Guo, Shuling</creatorcontrib><title>Partial Hepatectomy Induced Long Noncoding RNA Inhibits Hepatocyte Proliferation during Liver Regeneration</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Liver regeneration after partial hepatectomy (PHx) is a complex and well-orchestrated biological process in which synchronized cell proliferation is induced in response to the loss of liver mass. To define long noncoding RNAs (lncRNAs) that participate in the regulation of liver regeneration, we performed microarray analysis and identified more than 400 lncRNAs exhibiting significantly altered expression. Of these, one lncRNA, LncPHx2 (Long noncoding RNA induced by PHx 2), was highly upregulated during liver regeneration. Depletion of LncPHx2 during liver regeneration using antisense oligonucleotides led to a transient increase in hepatocyte proliferation and more rapid liver regeneration. Gene expression analysis showed that LncPHx2 depletion resulted in upregulation of mRNAs encoding proteins known to promote cell proliferation, including MCM components, DNA polymerases, histone proteins, and transcription factors. LncPHx2 interacts with the mRNAs of MCM components, making it a candidate to regulate the expression of MCMs and other genes post-transcriptionally. Collectively, our data demonstrate that LncPHx2 is a key lncRNA that participates in a negative feedback loop modulating hepatocyte proliferation through RNA-RNA interactions.</description><subject>Animals</subject><subject>Antisense oligonucleotides</subject><subject>Bioinformatics</subject><subject>Biological activity</subject><subject>Cell adhesion & migration</subject><subject>Cell cycle</subject><subject>Cell growth</subject><subject>Cell proliferation</subject><subject>Cell Proliferation - genetics</subject><subject>Cells, Cultured</subject><subject>Deoxyribonucleic acid</subject><subject>Depletion</subject><subject>DNA</subject><subject>DNA microarrays</subject><subject>DNA-directed DNA polymerase</subject><subject>Feedback loops</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Hepatectomy</subject><subject>Hepatocytes - physiology</subject><subject>Liver</subject><subject>Liver Regeneration - genetics</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Microarray Analysis</subject><subject>Negative feedback</subject><subject>Oligonucleotides</subject><subject>Pharmaceuticals</subject><subject>Post-transcription</subject><subject>Proteins</subject><subject>R&D</subject><subject>Regeneration</subject><subject>Research & development</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA, Long Noncoding - genetics</subject><subject>RNA, Long Noncoding - physiology</subject><subject>Stem cells</subject><subject>Transcription factors</subject><subject>Up-Regulation - genetics</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>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNptUl1rFDEUDaLYWv0HogO--LJrviaZvAilqF1Yain6HDLJzTbLbLImM4X99850p6UVn-7lnnPP_eAg9J7gJWGSfNmmIUfTLfcpwhITRqVqXqBTohhdCIrZyyf5CXpTyhbjmjVCvEYndCzKhrFTtL02uQ-mqy5hb3qwfdodqlV0gwVXrVPcVFcp2uTCmN1cnY_QbWhDX478ZA89VNc5dcFDNn1IsXJDnsjrcAe5uoENxBl5i1550xV4N8cz9Pv7t18Xl4v1zx-ri_P1wtZU9AvScHDOU-COWhCGYmxb71vqlSGeKENr1oJoneWOc2Z8wwkBqJXkNZZMsjP08ai771LR85uKJkI1ghAhychYHRkuma3e57Az-aCTCfq-kPJGT1-xHWhhW45xo7y0NWeCt0ZhybEnLSd1Y_Co9XWeNrQ7cBZin033TPQ5EsOt3qQ7zWvCuVSjwOdZIKc_A5Re70Kx0HUmQhru91ZcEaqmWZ_-of7_On5k2ZxKyeAflyFYT9Z56NKTdfRsnbHtw9NDHpsevML-Ak4Lw1Y</recordid><startdate>20150724</startdate><enddate>20150724</enddate><creator>Huang, Lulu</creator><creator>Damle, Sagar S</creator><creator>Booten, Sheri</creator><creator>Singh, Priyam</creator><creator>Sabripour, Mahyar</creator><creator>Hsu, Jeff</creator><creator>Jo, Minji</creator><creator>Katz, Melanie</creator><creator>Watt, Andy</creator><creator>Hart, Christopher E</creator><creator>Freier, Susan M</creator><creator>Monia, Brett P</creator><creator>Guo, Shuling</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>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>20150724</creationdate><title>Partial Hepatectomy Induced Long Noncoding RNA Inhibits Hepatocyte Proliferation during Liver Regeneration</title><author>Huang, Lulu ; Damle, Sagar S ; Booten, Sheri ; Singh, Priyam ; Sabripour, Mahyar ; Hsu, Jeff ; Jo, Minji ; Katz, Melanie ; Watt, Andy ; Hart, Christopher E ; Freier, Susan M ; Monia, Brett P ; Guo, Shuling</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c526t-184eddf2e4d2ce6a200cbffb2f9a1f19a253be6bdc4d443af8411ee5974507373</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Antisense oligonucleotides</topic><topic>Bioinformatics</topic><topic>Biological activity</topic><topic>Cell adhesion & migration</topic><topic>Cell cycle</topic><topic>Cell growth</topic><topic>Cell proliferation</topic><topic>Cell Proliferation - genetics</topic><topic>Cells, Cultured</topic><topic>Deoxyribonucleic acid</topic><topic>Depletion</topic><topic>DNA</topic><topic>DNA microarrays</topic><topic>DNA-directed DNA polymerase</topic><topic>Feedback loops</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Hepatectomy</topic><topic>Hepatocytes - physiology</topic><topic>Liver</topic><topic>Liver Regeneration - genetics</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Microarray Analysis</topic><topic>Negative feedback</topic><topic>Oligonucleotides</topic><topic>Pharmaceuticals</topic><topic>Post-transcription</topic><topic>Proteins</topic><topic>R&D</topic><topic>Regeneration</topic><topic>Research & development</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA, Long Noncoding - genetics</topic><topic>RNA, Long Noncoding - physiology</topic><topic>Stem cells</topic><topic>Transcription factors</topic><topic>Up-Regulation - 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To define long noncoding RNAs (lncRNAs) that participate in the regulation of liver regeneration, we performed microarray analysis and identified more than 400 lncRNAs exhibiting significantly altered expression. Of these, one lncRNA, LncPHx2 (Long noncoding RNA induced by PHx 2), was highly upregulated during liver regeneration. Depletion of LncPHx2 during liver regeneration using antisense oligonucleotides led to a transient increase in hepatocyte proliferation and more rapid liver regeneration. Gene expression analysis showed that LncPHx2 depletion resulted in upregulation of mRNAs encoding proteins known to promote cell proliferation, including MCM components, DNA polymerases, histone proteins, and transcription factors. LncPHx2 interacts with the mRNAs of MCM components, making it a candidate to regulate the expression of MCMs and other genes post-transcriptionally. Collectively, our data demonstrate that LncPHx2 is a key lncRNA that participates in a negative feedback loop modulating hepatocyte proliferation through RNA-RNA interactions.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26207833</pmid><doi>10.1371/journal.pone.0132798</doi><oa>free_for_read</oa></addata></record> |
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| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Animals Antisense oligonucleotides Bioinformatics Biological activity Cell adhesion & migration Cell cycle Cell growth Cell proliferation Cell Proliferation - genetics Cells, Cultured Deoxyribonucleic acid Depletion DNA DNA microarrays DNA-directed DNA polymerase Feedback loops Gene expression Gene Expression Profiling Genomes Genomics Hepatectomy Hepatocytes - physiology Liver Liver Regeneration - genetics Male Mice Mice, Inbred C57BL Microarray Analysis Negative feedback Oligonucleotides Pharmaceuticals Post-transcription Proteins R&D Regeneration Research & development Ribonucleic acid RNA RNA, Long Noncoding - genetics RNA, Long Noncoding - physiology Stem cells Transcription factors Up-Regulation - genetics |
| title | Partial Hepatectomy Induced Long Noncoding RNA Inhibits Hepatocyte Proliferation during Liver Regeneration |
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