An epigenetic feedback regulatory loop involving microRNA-195 and MBD1 governs neural stem cell differentiation
Epigenetic mechanisms, including DNA methylation, histone modification, and microRNAs, play pivotal roles in stem cell biology. Methyl-CpG binding protein 1 (MBD1), an important epigenetic regulator of adult neurogenesis, controls the proliferation and differentiation of adult neural stem/progenitor...
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| Veröffentlicht in: | PloS one 2013-01, Vol.8 (1), p.e51436-e51436 |
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| creator | Liu, Changmei Teng, Zhao-Qian McQuate, Andrea L Jobe, Emily M Christ, Christa C von Hoyningen-Huene, Sergei J Reyes, Marie D Polich, Eric D Xing, Yina Li, Yue Guo, Weixiang Zhao, Xinyu |
| description | Epigenetic mechanisms, including DNA methylation, histone modification, and microRNAs, play pivotal roles in stem cell biology. Methyl-CpG binding protein 1 (MBD1), an important epigenetic regulator of adult neurogenesis, controls the proliferation and differentiation of adult neural stem/progenitor cells (aNSCs). We recently demonstrated that MBD1 deficiency in aNSCs leads to altered expression of several noncoding microRNAs (miRNAs).
Here we show that one of these miRNAs, miR-195, and MBD1 form a negative feedback loop. While MBD1 directly represses the expression of miR-195 in aNSCs, high levels of miR-195 in turn repress the expression of MBD1. Both gain-of-function and loss-of-function investigations show that alterations of the MBD1-miR-195 feedback loop tip the balance between aNSC proliferation and differentiation.
Therefore the regulatory loop formed by MBD1 and miR-195 is an important component of the epigenetic network that controls aNSC fate. |
| doi_str_mv | 10.1371/journal.pone.0051436 |
| format | Article |
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Here we show that one of these miRNAs, miR-195, and MBD1 form a negative feedback loop. While MBD1 directly represses the expression of miR-195 in aNSCs, high levels of miR-195 in turn repress the expression of MBD1. Both gain-of-function and loss-of-function investigations show that alterations of the MBD1-miR-195 feedback loop tip the balance between aNSC proliferation and differentiation.
Therefore the regulatory loop formed by MBD1 and miR-195 is an important component of the epigenetic network that controls aNSC fate.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0051436</identifier><identifier>PMID: 23349673</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>3' Untranslated Regions - genetics ; Animals ; Biology ; Brain ; Cell cycle ; Cell differentiation ; Cell Differentiation - genetics ; Cell division ; Cell growth ; Cell Proliferation ; Cells (biology) ; Control theory ; CpG islands ; Dentate Gyrus - cytology ; Deoxyribonucleic acid ; Differentiation (biology) ; DNA ; DNA methylation ; DNA-Binding Proteins - deficiency ; DNA-Binding Proteins - genetics ; Epigenesis, Genetic ; Epigenetic inheritance ; Epigenetics ; Feedback ; Feedback loops ; Feedback, Physiological ; Gene expression ; Gene Expression Regulation - genetics ; Gene Knockout Techniques ; Male ; Medicine ; Methyl-CpG binding protein ; Methylation ; Mice ; MicroRNA ; MicroRNAs ; MicroRNAs - genetics ; miRNA ; Molecular biology ; Negative feedback ; Neural stem cells ; Neural Stem Cells - cytology ; Neural Stem Cells - metabolism ; Neurogenesis ; Neurosciences ; Phenotype ; Protein binding ; Ribonucleic acid ; RNA ; Stem cell research ; Stem cells</subject><ispartof>PloS one, 2013-01, Vol.8 (1), p.e51436-e51436</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Liu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://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>2013 Liu et al 2013 Liu et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-c4a4ae72c8e893b0277e33a6e4b57c2496abb57edc52e3eee69ee83626e4fd2d3</citedby><cites>FETCH-LOGICAL-c692t-c4a4ae72c8e893b0277e33a6e4b57c2496abb57edc52e3eee69ee83626e4fd2d3</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/PMC3547917/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3547917/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23349673$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Van Wijnen, Andre</contributor><creatorcontrib>Liu, Changmei</creatorcontrib><creatorcontrib>Teng, Zhao-Qian</creatorcontrib><creatorcontrib>McQuate, Andrea L</creatorcontrib><creatorcontrib>Jobe, Emily M</creatorcontrib><creatorcontrib>Christ, Christa C</creatorcontrib><creatorcontrib>von Hoyningen-Huene, Sergei J</creatorcontrib><creatorcontrib>Reyes, Marie D</creatorcontrib><creatorcontrib>Polich, Eric D</creatorcontrib><creatorcontrib>Xing, Yina</creatorcontrib><creatorcontrib>Li, Yue</creatorcontrib><creatorcontrib>Guo, Weixiang</creatorcontrib><creatorcontrib>Zhao, Xinyu</creatorcontrib><title>An epigenetic feedback regulatory loop involving microRNA-195 and MBD1 governs neural stem cell differentiation</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Epigenetic mechanisms, including DNA methylation, histone modification, and microRNAs, play pivotal roles in stem cell biology. Methyl-CpG binding protein 1 (MBD1), an important epigenetic regulator of adult neurogenesis, controls the proliferation and differentiation of adult neural stem/progenitor cells (aNSCs). We recently demonstrated that MBD1 deficiency in aNSCs leads to altered expression of several noncoding microRNAs (miRNAs).
Here we show that one of these miRNAs, miR-195, and MBD1 form a negative feedback loop. While MBD1 directly represses the expression of miR-195 in aNSCs, high levels of miR-195 in turn repress the expression of MBD1. Both gain-of-function and loss-of-function investigations show that alterations of the MBD1-miR-195 feedback loop tip the balance between aNSC proliferation and differentiation.
Therefore the regulatory loop formed by MBD1 and miR-195 is an important component of the epigenetic network that controls aNSC fate.</description><subject>3' Untranslated Regions - genetics</subject><subject>Animals</subject><subject>Biology</subject><subject>Brain</subject><subject>Cell cycle</subject><subject>Cell differentiation</subject><subject>Cell Differentiation - genetics</subject><subject>Cell division</subject><subject>Cell growth</subject><subject>Cell Proliferation</subject><subject>Cells (biology)</subject><subject>Control theory</subject><subject>CpG islands</subject><subject>Dentate Gyrus - cytology</subject><subject>Deoxyribonucleic acid</subject><subject>Differentiation (biology)</subject><subject>DNA</subject><subject>DNA methylation</subject><subject>DNA-Binding Proteins - deficiency</subject><subject>DNA-Binding Proteins - genetics</subject><subject>Epigenesis, Genetic</subject><subject>Epigenetic inheritance</subject><subject>Epigenetics</subject><subject>Feedback</subject><subject>Feedback loops</subject><subject>Feedback, Physiological</subject><subject>Gene expression</subject><subject>Gene Expression Regulation - genetics</subject><subject>Gene Knockout Techniques</subject><subject>Male</subject><subject>Medicine</subject><subject>Methyl-CpG binding protein</subject><subject>Methylation</subject><subject>Mice</subject><subject>MicroRNA</subject><subject>MicroRNAs</subject><subject>MicroRNAs - genetics</subject><subject>miRNA</subject><subject>Molecular biology</subject><subject>Negative feedback</subject><subject>Neural stem cells</subject><subject>Neural Stem Cells - cytology</subject><subject>Neural Stem Cells - metabolism</subject><subject>Neurogenesis</subject><subject>Neurosciences</subject><subject>Phenotype</subject><subject>Protein binding</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Stem cell research</subject><subject>Stem cells</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</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>eNqNk9tu1DAQhiMEoqXwBggsISG42MWHxE5uKi3ltFKhUjncWo4zyXrx2oudrOjb47Bp1UW9QLmIZX_ze-b3TJY9JXhOmCBv1n4ITtn51juYY1yQnPF72TGpGJ1xitn9W-uj7FGM6wSxkvOH2RFlLK-4YMeZXzgEW9OBg95o1AI0tdI_UYBusKr34QpZ77fIuJ23O-M6tDE6-MsvixmpCqRcgz6_fUdQ53cQXEQOhqAsij1skAZrUWPaFgK43qjeePc4e9AqG-HJ9D_Jvn94_-3s0-z84uPybHE-07yi_UznKlcgqC6hrFiNqRDAmOKQ14XQNCWv6rSCRhcUGADwCqBknCaibWjDTrLne92t9VFOXkVJGBW0KnCBE7HcE41Xa7kNZqPClfTKyL8bPnRSheSJBalr0ehyzIwWuWJljTHlQnHMaFtUmCSt0-m2od6kpFK5yYUD0cMTZ1YyWSZZkYuKiCTwahII_tcAsZcbE0f_lAM_pLxpSXFOSl4l9MU_6N3VTVSnUgHGtT7dq0dRuchFSXNa0THv-R1U-hpIz5waqzVp_yDg9UFAYnr43XdqiFEuv17-P3vx45B9eYtdgbL9Kno7jC0TD8F8D6YmjDFAe2MywXKci2s35DgXcpqLFPbs9gPdBF0PAvsDB50H2A</recordid><startdate>20130117</startdate><enddate>20130117</enddate><creator>Liu, Changmei</creator><creator>Teng, Zhao-Qian</creator><creator>McQuate, Andrea L</creator><creator>Jobe, Emily M</creator><creator>Christ, Christa C</creator><creator>von Hoyningen-Huene, Sergei J</creator><creator>Reyes, Marie D</creator><creator>Polich, Eric D</creator><creator>Xing, Yina</creator><creator>Li, Yue</creator><creator>Guo, Weixiang</creator><creator>Zhao, Xinyu</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>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>20130117</creationdate><title>An epigenetic feedback regulatory loop involving microRNA-195 and MBD1 governs neural stem cell differentiation</title><author>Liu, Changmei ; Teng, Zhao-Qian ; McQuate, Andrea L ; Jobe, Emily M ; Christ, Christa C ; von Hoyningen-Huene, Sergei J ; Reyes, Marie D ; Polich, Eric D ; Xing, Yina ; Li, Yue ; Guo, Weixiang ; Zhao, Xinyu</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-c4a4ae72c8e893b0277e33a6e4b57c2496abb57edc52e3eee69ee83626e4fd2d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>3' Untranslated Regions - 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genetics</topic><topic>miRNA</topic><topic>Molecular biology</topic><topic>Negative feedback</topic><topic>Neural stem cells</topic><topic>Neural Stem Cells - cytology</topic><topic>Neural Stem Cells - metabolism</topic><topic>Neurogenesis</topic><topic>Neurosciences</topic><topic>Phenotype</topic><topic>Protein binding</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>Stem cell research</topic><topic>Stem cells</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Changmei</creatorcontrib><creatorcontrib>Teng, Zhao-Qian</creatorcontrib><creatorcontrib>McQuate, Andrea L</creatorcontrib><creatorcontrib>Jobe, Emily M</creatorcontrib><creatorcontrib>Christ, Christa C</creatorcontrib><creatorcontrib>von Hoyningen-Huene, Sergei J</creatorcontrib><creatorcontrib>Reyes, Marie D</creatorcontrib><creatorcontrib>Polich, Eric D</creatorcontrib><creatorcontrib>Xing, Yina</creatorcontrib><creatorcontrib>Li, Yue</creatorcontrib><creatorcontrib>Guo, Weixiang</creatorcontrib><creatorcontrib>Zhao, Xinyu</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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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>Liu, Changmei</au><au>Teng, Zhao-Qian</au><au>McQuate, Andrea L</au><au>Jobe, Emily M</au><au>Christ, Christa C</au><au>von Hoyningen-Huene, Sergei J</au><au>Reyes, Marie D</au><au>Polich, Eric D</au><au>Xing, Yina</au><au>Li, Yue</au><au>Guo, Weixiang</au><au>Zhao, Xinyu</au><au>Van Wijnen, Andre</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>An epigenetic feedback regulatory loop involving microRNA-195 and MBD1 governs neural stem cell differentiation</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-01-17</date><risdate>2013</risdate><volume>8</volume><issue>1</issue><spage>e51436</spage><epage>e51436</epage><pages>e51436-e51436</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Epigenetic mechanisms, including DNA methylation, histone modification, and microRNAs, play pivotal roles in stem cell biology. Methyl-CpG binding protein 1 (MBD1), an important epigenetic regulator of adult neurogenesis, controls the proliferation and differentiation of adult neural stem/progenitor cells (aNSCs). We recently demonstrated that MBD1 deficiency in aNSCs leads to altered expression of several noncoding microRNAs (miRNAs).
Here we show that one of these miRNAs, miR-195, and MBD1 form a negative feedback loop. While MBD1 directly represses the expression of miR-195 in aNSCs, high levels of miR-195 in turn repress the expression of MBD1. Both gain-of-function and loss-of-function investigations show that alterations of the MBD1-miR-195 feedback loop tip the balance between aNSC proliferation and differentiation.
Therefore the regulatory loop formed by MBD1 and miR-195 is an important component of the epigenetic network that controls aNSC fate.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23349673</pmid><doi>10.1371/journal.pone.0051436</doi><tpages>e51436</tpages><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2013-01, Vol.8 (1), p.e51436-e51436 |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | 3' Untranslated Regions - genetics Animals Biology Brain Cell cycle Cell differentiation Cell Differentiation - genetics Cell division Cell growth Cell Proliferation Cells (biology) Control theory CpG islands Dentate Gyrus - cytology Deoxyribonucleic acid Differentiation (biology) DNA DNA methylation DNA-Binding Proteins - deficiency DNA-Binding Proteins - genetics Epigenesis, Genetic Epigenetic inheritance Epigenetics Feedback Feedback loops Feedback, Physiological Gene expression Gene Expression Regulation - genetics Gene Knockout Techniques Male Medicine Methyl-CpG binding protein Methylation Mice MicroRNA MicroRNAs MicroRNAs - genetics miRNA Molecular biology Negative feedback Neural stem cells Neural Stem Cells - cytology Neural Stem Cells - metabolism Neurogenesis Neurosciences Phenotype Protein binding Ribonucleic acid RNA Stem cell research Stem cells |
| title | An epigenetic feedback regulatory loop involving microRNA-195 and MBD1 governs neural stem cell differentiation |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-29T09%3A17%3A05IST&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=An%20epigenetic%20feedback%20regulatory%20loop%20involving%20microRNA-195%20and%20MBD1%20governs%20neural%20stem%20cell%20differentiation&rft.jtitle=PloS%20one&rft.au=Liu,%20Changmei&rft.date=2013-01-17&rft.volume=8&rft.issue=1&rft.spage=e51436&rft.epage=e51436&rft.pages=e51436-e51436&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0051436&rft_dat=%3Cgale_plos_%3EA478242921%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=1327295050&rft_id=info:pmid/23349673&rft_galeid=A478242921&rft_doaj_id=oai_doaj_org_article_cb7dc8c692254a38b00267a6032f5901&rfr_iscdi=true |