A non-canonical role for the EDC4 decapping factor in regulating MARF1-mediated mRNA decay

EDC4 is a core component of processing (P)-bodies that binds the DCP2 decapping enzyme and stimulates mRNA decay. EDC4 also interacts with mammalian MARF1, a recently identified endoribonuclease that promotes oogenesis and contains a number of RNA binding domains, including two RRMs and multiple LOT...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:eLife 2020-06, Vol.9, Article 54995
Hauptverfasser: Brothers, William R., Hebert, Steven, Kleinman, Claudia L., Fabian, Marc R.
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page
container_issue
container_start_page
container_title eLife
container_volume 9
creator Brothers, William R.
Hebert, Steven
Kleinman, Claudia L.
Fabian, Marc R.
description EDC4 is a core component of processing (P)-bodies that binds the DCP2 decapping enzyme and stimulates mRNA decay. EDC4 also interacts with mammalian MARF1, a recently identified endoribonuclease that promotes oogenesis and contains a number of RNA binding domains, including two RRMs and multiple LOTUS domains. How EDC4 regulates MARF1 action and the identity of MARF1 target mRNAs is not known. Our transcriptome-wide analysis identifies bona fide MARF1 target mRNAs and indicates that MARF1 predominantly binds their 3' UTRs via its LOTUS domains to promote their decay. We also show that a MARF1 RRM plays an essential role in enhancing its endonuclease activity. Importantly, we establish that EDC4 impairs MARF1 activity by preventing its LOTUS domains from binding target mRNAs. Thus, EDC4 not only serves as an enhancer of mRNA turnover that binds DCP2, but also as a repressor that binds MARF1 to prevent the decay of MARF1 target mRNAs.
doi_str_mv 10.7554/eLife.54995
format Article
fullrecord <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_journals_2418973049</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><doaj_id>oai_doaj_org_article_2a9d8c4dbd154405bd634fc367851e06</doaj_id><sourcerecordid>2410707786</sourcerecordid><originalsourceid>FETCH-LOGICAL-c475t-4f5c075156f1d4c1cbf46a9ec0a84f8cf0a08fb1a8e1f2c2eb6b04e08806ccc33</originalsourceid><addsrcrecordid>eNqNks-L1DAUx4so7rLuybsUvAjSNWmTJr0IQ91fMCosCuIlpK8vsxk6yZimyv73pjPruOvJHJLw3ud985J8s-wlJWeCc_YOl9bgGWdNw59kxyXhpCCSfXv6YH-UnY7jmqQhmJS0eZ4dVSWnpCqr4-z7InfeFaDTbEEPefAD5saHPN5ifv6hZXmPoLdb61a50RBTxro84GoadJyDHxc3F7TYYG91xD7f3Hxa7EruXmTPjB5GPL1fT7KvF-df2qti-fnyul0sC2CCx4IZDkRwymtDewYUOsNq3SAQLZmRYIgm0nRUS6SmhBK7uiMMiZSkBoCqOsmu97q912u1DXajw53y2qpdwIeV0iFaGFCVuuklsL7rKWeM8K6vK2agqoXkFEmdtN7vtbZTl64E6GLQwyPRxxlnb9XK_1SiFI2UIgm8uRcI_seEY1QbOwIOg3bop1GVjBJBhJDzWa__Qdd-Ci491UzJRlSENYl6u6cg-HEMaA7NUKJmC6idBdTOAol-9bD_A_vnwxMg98Av7LwZwaIDPGDJI5xRRutmtgttbUx_7F3rJxf_dvI_pdVvM_zMNw</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2418973049</pqid></control><display><type>article</type><title>A non-canonical role for the EDC4 decapping factor in regulating MARF1-mediated mRNA decay</title><source>MEDLINE</source><source>DOAJ Directory of Open Access Journals</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>PubMed Central Open Access</source><source>Web of Science - Science Citation Index Expanded - 2020&lt;img src="https://exlibris-pub.s3.amazonaws.com/fromwos-v2.jpg" /&gt;</source><source>PubMed Central</source><creator>Brothers, William R. ; Hebert, Steven ; Kleinman, Claudia L. ; Fabian, Marc R.</creator><creatorcontrib>Brothers, William R. ; Hebert, Steven ; Kleinman, Claudia L. ; Fabian, Marc R.</creatorcontrib><description>EDC4 is a core component of processing (P)-bodies that binds the DCP2 decapping enzyme and stimulates mRNA decay. EDC4 also interacts with mammalian MARF1, a recently identified endoribonuclease that promotes oogenesis and contains a number of RNA binding domains, including two RRMs and multiple LOTUS domains. How EDC4 regulates MARF1 action and the identity of MARF1 target mRNAs is not known. Our transcriptome-wide analysis identifies bona fide MARF1 target mRNAs and indicates that MARF1 predominantly binds their 3' UTRs via its LOTUS domains to promote their decay. We also show that a MARF1 RRM plays an essential role in enhancing its endonuclease activity. Importantly, we establish that EDC4 impairs MARF1 activity by preventing its LOTUS domains from binding target mRNAs. Thus, EDC4 not only serves as an enhancer of mRNA turnover that binds DCP2, but also as a repressor that binds MARF1 to prevent the decay of MARF1 target mRNAs.</description><identifier>ISSN: 2050-084X</identifier><identifier>EISSN: 2050-084X</identifier><identifier>DOI: 10.7554/eLife.54995</identifier><identifier>PMID: 32510323</identifier><language>eng</language><publisher>CAMBRIDGE: Elife Sciences Publications Ltd</publisher><subject>Animals ; Biology ; Cell Cycle Proteins - chemistry ; Cell Cycle Proteins - genetics ; Cell Cycle Proteins - metabolism ; Chromosomes and Gene Expression ; Endonuclease ; Endoribonucleases - chemistry ; Endoribonucleases - genetics ; Endoribonucleases - metabolism ; Experiments ; Gene expression ; HEK293 Cells ; Humans ; Life Sciences &amp; Biomedicine ; Life Sciences &amp; Biomedicine - Other Topics ; mRNA decapping ; mRNA decay ; mRNA turnover ; Oogenesis ; Proteins ; Proteins - chemistry ; Proteins - genetics ; Proteins - metabolism ; RNA binding protein ; RNA Caps - metabolism ; RNA Stability - genetics ; RNA, Messenger - chemistry ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Science &amp; Technology ; Transcriptome - genetics</subject><ispartof>eLife, 2020-06, Vol.9, Article 54995</ispartof><rights>2020, Brothers et al.</rights><rights>2020, Brothers et al. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2020, Brothers et al 2020 Brothers et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>12</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000541416900001</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c475t-4f5c075156f1d4c1cbf46a9ec0a84f8cf0a08fb1a8e1f2c2eb6b04e08806ccc33</citedby><cites>FETCH-LOGICAL-c475t-4f5c075156f1d4c1cbf46a9ec0a84f8cf0a08fb1a8e1f2c2eb6b04e08806ccc33</cites><orcidid>0000-0003-3700-7604 ; 0000-0001-8962-7974</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7279887/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7279887/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,2103,2115,27929,27930,28253,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32510323$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Brothers, William R.</creatorcontrib><creatorcontrib>Hebert, Steven</creatorcontrib><creatorcontrib>Kleinman, Claudia L.</creatorcontrib><creatorcontrib>Fabian, Marc R.</creatorcontrib><title>A non-canonical role for the EDC4 decapping factor in regulating MARF1-mediated mRNA decay</title><title>eLife</title><addtitle>ELIFE</addtitle><addtitle>Elife</addtitle><description>EDC4 is a core component of processing (P)-bodies that binds the DCP2 decapping enzyme and stimulates mRNA decay. EDC4 also interacts with mammalian MARF1, a recently identified endoribonuclease that promotes oogenesis and contains a number of RNA binding domains, including two RRMs and multiple LOTUS domains. How EDC4 regulates MARF1 action and the identity of MARF1 target mRNAs is not known. Our transcriptome-wide analysis identifies bona fide MARF1 target mRNAs and indicates that MARF1 predominantly binds their 3' UTRs via its LOTUS domains to promote their decay. We also show that a MARF1 RRM plays an essential role in enhancing its endonuclease activity. Importantly, we establish that EDC4 impairs MARF1 activity by preventing its LOTUS domains from binding target mRNAs. Thus, EDC4 not only serves as an enhancer of mRNA turnover that binds DCP2, but also as a repressor that binds MARF1 to prevent the decay of MARF1 target mRNAs.</description><subject>Animals</subject><subject>Biology</subject><subject>Cell Cycle Proteins - chemistry</subject><subject>Cell Cycle Proteins - genetics</subject><subject>Cell Cycle Proteins - metabolism</subject><subject>Chromosomes and Gene Expression</subject><subject>Endonuclease</subject><subject>Endoribonucleases - chemistry</subject><subject>Endoribonucleases - genetics</subject><subject>Endoribonucleases - metabolism</subject><subject>Experiments</subject><subject>Gene expression</subject><subject>HEK293 Cells</subject><subject>Humans</subject><subject>Life Sciences &amp; Biomedicine</subject><subject>Life Sciences &amp; Biomedicine - Other Topics</subject><subject>mRNA decapping</subject><subject>mRNA decay</subject><subject>mRNA turnover</subject><subject>Oogenesis</subject><subject>Proteins</subject><subject>Proteins - chemistry</subject><subject>Proteins - genetics</subject><subject>Proteins - metabolism</subject><subject>RNA binding protein</subject><subject>RNA Caps - metabolism</subject><subject>RNA Stability - genetics</subject><subject>RNA, Messenger - chemistry</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Science &amp; Technology</subject><subject>Transcriptome - genetics</subject><issn>2050-084X</issn><issn>2050-084X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>AOWDO</sourceid><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>eNqNks-L1DAUx4so7rLuybsUvAjSNWmTJr0IQ91fMCosCuIlpK8vsxk6yZimyv73pjPruOvJHJLw3ud985J8s-wlJWeCc_YOl9bgGWdNw59kxyXhpCCSfXv6YH-UnY7jmqQhmJS0eZ4dVSWnpCqr4-z7InfeFaDTbEEPefAD5saHPN5ifv6hZXmPoLdb61a50RBTxro84GoadJyDHxc3F7TYYG91xD7f3Hxa7EruXmTPjB5GPL1fT7KvF-df2qti-fnyul0sC2CCx4IZDkRwymtDewYUOsNq3SAQLZmRYIgm0nRUS6SmhBK7uiMMiZSkBoCqOsmu97q912u1DXajw53y2qpdwIeV0iFaGFCVuuklsL7rKWeM8K6vK2agqoXkFEmdtN7vtbZTl64E6GLQwyPRxxlnb9XK_1SiFI2UIgm8uRcI_seEY1QbOwIOg3bop1GVjBJBhJDzWa__Qdd-Ci491UzJRlSENYl6u6cg-HEMaA7NUKJmC6idBdTOAol-9bD_A_vnwxMg98Av7LwZwaIDPGDJI5xRRutmtgttbUx_7F3rJxf_dvI_pdVvM_zMNw</recordid><startdate>20200608</startdate><enddate>20200608</enddate><creator>Brothers, William R.</creator><creator>Hebert, Steven</creator><creator>Kleinman, Claudia L.</creator><creator>Fabian, Marc R.</creator><general>Elife Sciences Publications Ltd</general><general>eLife Sciences Publications Ltd</general><general>eLife Sciences Publications, Ltd</general><scope>AOWDO</scope><scope>BLEPL</scope><scope>DTL</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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0003-3700-7604</orcidid><orcidid>https://orcid.org/0000-0001-8962-7974</orcidid></search><sort><creationdate>20200608</creationdate><title>A non-canonical role for the EDC4 decapping factor in regulating MARF1-mediated mRNA decay</title><author>Brothers, William R. ; Hebert, Steven ; Kleinman, Claudia L. ; Fabian, Marc R.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c475t-4f5c075156f1d4c1cbf46a9ec0a84f8cf0a08fb1a8e1f2c2eb6b04e08806ccc33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>Biology</topic><topic>Cell Cycle Proteins - chemistry</topic><topic>Cell Cycle Proteins - genetics</topic><topic>Cell Cycle Proteins - metabolism</topic><topic>Chromosomes and Gene Expression</topic><topic>Endonuclease</topic><topic>Endoribonucleases - chemistry</topic><topic>Endoribonucleases - genetics</topic><topic>Endoribonucleases - metabolism</topic><topic>Experiments</topic><topic>Gene expression</topic><topic>HEK293 Cells</topic><topic>Humans</topic><topic>Life Sciences &amp; Biomedicine</topic><topic>Life Sciences &amp; Biomedicine - Other Topics</topic><topic>mRNA decapping</topic><topic>mRNA decay</topic><topic>mRNA turnover</topic><topic>Oogenesis</topic><topic>Proteins</topic><topic>Proteins - chemistry</topic><topic>Proteins - genetics</topic><topic>Proteins - metabolism</topic><topic>RNA binding protein</topic><topic>RNA Caps - metabolism</topic><topic>RNA Stability - genetics</topic><topic>RNA, Messenger - chemistry</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>Science &amp; Technology</topic><topic>Transcriptome - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Brothers, William R.</creatorcontrib><creatorcontrib>Hebert, Steven</creatorcontrib><creatorcontrib>Kleinman, Claudia L.</creatorcontrib><creatorcontrib>Fabian, Marc R.</creatorcontrib><collection>Web of Science - Science Citation Index Expanded - 2020</collection><collection>Web of Science Core Collection</collection><collection>Science Citation Index Expanded</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest SciTech 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>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>Proquest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>Biological Science Database</collection><collection>Access via ProQuest (Open Access)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>eLife</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Brothers, William R.</au><au>Hebert, Steven</au><au>Kleinman, Claudia L.</au><au>Fabian, Marc R.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A non-canonical role for the EDC4 decapping factor in regulating MARF1-mediated mRNA decay</atitle><jtitle>eLife</jtitle><stitle>ELIFE</stitle><addtitle>Elife</addtitle><date>2020-06-08</date><risdate>2020</risdate><volume>9</volume><artnum>54995</artnum><issn>2050-084X</issn><eissn>2050-084X</eissn><abstract>EDC4 is a core component of processing (P)-bodies that binds the DCP2 decapping enzyme and stimulates mRNA decay. EDC4 also interacts with mammalian MARF1, a recently identified endoribonuclease that promotes oogenesis and contains a number of RNA binding domains, including two RRMs and multiple LOTUS domains. How EDC4 regulates MARF1 action and the identity of MARF1 target mRNAs is not known. Our transcriptome-wide analysis identifies bona fide MARF1 target mRNAs and indicates that MARF1 predominantly binds their 3' UTRs via its LOTUS domains to promote their decay. We also show that a MARF1 RRM plays an essential role in enhancing its endonuclease activity. Importantly, we establish that EDC4 impairs MARF1 activity by preventing its LOTUS domains from binding target mRNAs. Thus, EDC4 not only serves as an enhancer of mRNA turnover that binds DCP2, but also as a repressor that binds MARF1 to prevent the decay of MARF1 target mRNAs.</abstract><cop>CAMBRIDGE</cop><pub>Elife Sciences Publications Ltd</pub><pmid>32510323</pmid><doi>10.7554/eLife.54995</doi><tpages>23</tpages><orcidid>https://orcid.org/0000-0003-3700-7604</orcidid><orcidid>https://orcid.org/0000-0001-8962-7974</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 2050-084X
ispartof eLife, 2020-06, Vol.9, Article 54995
issn 2050-084X
2050-084X
language eng
recordid cdi_proquest_journals_2418973049
source MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central Open Access; Web of Science - Science Citation Index Expanded - 2020<img src="https://exlibris-pub.s3.amazonaws.com/fromwos-v2.jpg" />; PubMed Central
subjects Animals
Biology
Cell Cycle Proteins - chemistry
Cell Cycle Proteins - genetics
Cell Cycle Proteins - metabolism
Chromosomes and Gene Expression
Endonuclease
Endoribonucleases - chemistry
Endoribonucleases - genetics
Endoribonucleases - metabolism
Experiments
Gene expression
HEK293 Cells
Humans
Life Sciences & Biomedicine
Life Sciences & Biomedicine - Other Topics
mRNA decapping
mRNA decay
mRNA turnover
Oogenesis
Proteins
Proteins - chemistry
Proteins - genetics
Proteins - metabolism
RNA binding protein
RNA Caps - metabolism
RNA Stability - genetics
RNA, Messenger - chemistry
RNA, Messenger - genetics
RNA, Messenger - metabolism
Science & Technology
Transcriptome - genetics
title A non-canonical role for the EDC4 decapping factor in regulating MARF1-mediated mRNA decay
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-14T19%3A50%3A31IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=A%20non-canonical%20role%20for%20the%20EDC4%20decapping%20factor%20in%20regulating%20MARF1-mediated%20mRNA%20decay&rft.jtitle=eLife&rft.au=Brothers,%20William%20R.&rft.date=2020-06-08&rft.volume=9&rft.artnum=54995&rft.issn=2050-084X&rft.eissn=2050-084X&rft_id=info:doi/10.7554/eLife.54995&rft_dat=%3Cproquest_cross%3E2410707786%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2418973049&rft_id=info:pmid/32510323&rft_doaj_id=oai_doaj_org_article_2a9d8c4dbd154405bd634fc367851e06&rfr_iscdi=true