VIRMA mediates preferential m6A mRNA methylation in 3′UTR and near stop codon and associates with alternative polyadenylation
N 6 -methyladenosine (m 6 A) is enriched in 3′untranslated region (3′UTR) and near stop codon of mature polyadenylated mRNAs in mammalian systems and has regulatory roles in eukaryotic mRNA transcriptome switch. Significantly, the mechanism for this modification preference remains unknown, however....
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| Veröffentlicht in: | Cell discovery 2018-02, Vol.4 (1), p.1-17, Article 10 |
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| creator | Yue, Yanan Liu, Jun Cui, Xiaolong Cao, Jie Luo, Guanzheng Zhang, Zezhou Cheng, Tao Gao, Minsong Shu, Xiao Ma, Honghui Wang, Fengqin Wang, Xinxia Shen, Bin Wang, Yizhen Feng, Xinhua He, Chuan Liu, Jianzhao |
| description | N
6
-methyladenosine (m
6
A) is enriched in 3′untranslated region (3′UTR) and near stop codon of mature polyadenylated mRNAs in mammalian systems and has regulatory roles in eukaryotic mRNA transcriptome switch. Significantly, the mechanism for this modification preference remains unknown, however. Herein we report a characterization of the full m
6
A methyltransferase complex in HeLa cells identifying METTL3/METTL14/WTAP/VIRMA/HAKAI/ZC3H13 as the key components, and we show that VIRMA mediates preferential mRNA methylation in 3′UTR and near stop codon. Biochemical studies reveal that VIRMA recruits the catalytic core components METTL3/METTL14/WTAP to guide region-selective methylations. Around 60% of VIRMA mRNA immunoprecipitation targets manifest strong m
6
A enrichment in 3′UTR. Depletions of
VIRMA
and
METTL3
induce 3′UTR lengthening of several hundred mRNAs with over 50% targets in common. VIRMA associates with polyadenylation cleavage factors CPSF5 and CPSF6 in an RNA-dependent manner. Depletion of CPSF5 leads to significant shortening of 3′UTR of over 2800 mRNAs, 84% of which are modified with m
6
A and have increased m
6
A peak density in 3′UTR and near stop codon after CPSF5 knockdown. Together, our studies provide insights into m
6
A deposition specificity in 3′UTR and its correlation with alternative polyadenylation. |
| doi_str_mv | 10.1038/s41421-018-0019-0 |
| format | Article |
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6
-methyladenosine (m
6
A) is enriched in 3′untranslated region (3′UTR) and near stop codon of mature polyadenylated mRNAs in mammalian systems and has regulatory roles in eukaryotic mRNA transcriptome switch. Significantly, the mechanism for this modification preference remains unknown, however. Herein we report a characterization of the full m
6
A methyltransferase complex in HeLa cells identifying METTL3/METTL14/WTAP/VIRMA/HAKAI/ZC3H13 as the key components, and we show that VIRMA mediates preferential mRNA methylation in 3′UTR and near stop codon. Biochemical studies reveal that VIRMA recruits the catalytic core components METTL3/METTL14/WTAP to guide region-selective methylations. Around 60% of VIRMA mRNA immunoprecipitation targets manifest strong m
6
A enrichment in 3′UTR. Depletions of
VIRMA
and
METTL3
induce 3′UTR lengthening of several hundred mRNAs with over 50% targets in common. VIRMA associates with polyadenylation cleavage factors CPSF5 and CPSF6 in an RNA-dependent manner. Depletion of CPSF5 leads to significant shortening of 3′UTR of over 2800 mRNAs, 84% of which are modified with m
6
A and have increased m
6
A peak density in 3′UTR and near stop codon after CPSF5 knockdown. Together, our studies provide insights into m
6
A deposition specificity in 3′UTR and its correlation with alternative polyadenylation.</description><identifier>ISSN: 2056-5968</identifier><identifier>EISSN: 2056-5968</identifier><identifier>DOI: 10.1038/s41421-018-0019-0</identifier><identifier>PMID: 29507755</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>3' Untranslated regions ; 631/337/1645/2570 ; 631/80 ; Biomedical and Life Sciences ; Cell Biology ; Cell Culture ; Cell Cycle Analysis ; Cell Physiology ; Eukaryotes ; Gene expression ; Immunoprecipitation ; Life Sciences ; Methylation ; Methyltransferase ; N6-methyladenosine ; Polyadenylation ; Stem Cells ; Stop codon</subject><ispartof>Cell discovery, 2018-02, Vol.4 (1), p.1-17, Article 10</ispartof><rights>The Author(s) 2018</rights><rights>2018. 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><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c344t-c6ac82a5c5c4ab805371e30b41a2913b27e2269497360dcba492b7c03e1560433</citedby><cites>FETCH-LOGICAL-c344t-c6ac82a5c5c4ab805371e30b41a2913b27e2269497360dcba492b7c03e1560433</cites><orcidid>0000-0001-9465-6075 ; 0000-0002-6797-9319 ; 0000-0003-4319-7424</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/PMC5826926/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5826926/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,27922,27923,41118,42187,51574,53789,53791</link.rule.ids></links><search><creatorcontrib>Yue, Yanan</creatorcontrib><creatorcontrib>Liu, Jun</creatorcontrib><creatorcontrib>Cui, Xiaolong</creatorcontrib><creatorcontrib>Cao, Jie</creatorcontrib><creatorcontrib>Luo, Guanzheng</creatorcontrib><creatorcontrib>Zhang, Zezhou</creatorcontrib><creatorcontrib>Cheng, Tao</creatorcontrib><creatorcontrib>Gao, Minsong</creatorcontrib><creatorcontrib>Shu, Xiao</creatorcontrib><creatorcontrib>Ma, Honghui</creatorcontrib><creatorcontrib>Wang, Fengqin</creatorcontrib><creatorcontrib>Wang, Xinxia</creatorcontrib><creatorcontrib>Shen, Bin</creatorcontrib><creatorcontrib>Wang, Yizhen</creatorcontrib><creatorcontrib>Feng, Xinhua</creatorcontrib><creatorcontrib>He, Chuan</creatorcontrib><creatorcontrib>Liu, Jianzhao</creatorcontrib><title>VIRMA mediates preferential m6A mRNA methylation in 3′UTR and near stop codon and associates with alternative polyadenylation</title><title>Cell discovery</title><addtitle>Cell Discov</addtitle><description>N
6
-methyladenosine (m
6
A) is enriched in 3′untranslated region (3′UTR) and near stop codon of mature polyadenylated mRNAs in mammalian systems and has regulatory roles in eukaryotic mRNA transcriptome switch. Significantly, the mechanism for this modification preference remains unknown, however. Herein we report a characterization of the full m
6
A methyltransferase complex in HeLa cells identifying METTL3/METTL14/WTAP/VIRMA/HAKAI/ZC3H13 as the key components, and we show that VIRMA mediates preferential mRNA methylation in 3′UTR and near stop codon. Biochemical studies reveal that VIRMA recruits the catalytic core components METTL3/METTL14/WTAP to guide region-selective methylations. Around 60% of VIRMA mRNA immunoprecipitation targets manifest strong m
6
A enrichment in 3′UTR. Depletions of
VIRMA
and
METTL3
induce 3′UTR lengthening of several hundred mRNAs with over 50% targets in common. VIRMA associates with polyadenylation cleavage factors CPSF5 and CPSF6 in an RNA-dependent manner. Depletion of CPSF5 leads to significant shortening of 3′UTR of over 2800 mRNAs, 84% of which are modified with m
6
A and have increased m
6
A peak density in 3′UTR and near stop codon after CPSF5 knockdown. Together, our studies provide insights into m
6
A deposition specificity in 3′UTR and its correlation with alternative polyadenylation.</description><subject>3' Untranslated regions</subject><subject>631/337/1645/2570</subject><subject>631/80</subject><subject>Biomedical and Life Sciences</subject><subject>Cell Biology</subject><subject>Cell Culture</subject><subject>Cell Cycle Analysis</subject><subject>Cell Physiology</subject><subject>Eukaryotes</subject><subject>Gene expression</subject><subject>Immunoprecipitation</subject><subject>Life Sciences</subject><subject>Methylation</subject><subject>Methyltransferase</subject><subject>N6-methyladenosine</subject><subject>Polyadenylation</subject><subject>Stem Cells</subject><subject>Stop codon</subject><issn>2056-5968</issn><issn>2056-5968</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp1kc1u1DAUhS0EolXpA7CzxDpw_Rtng1RV_FQqrTRq2Vo3jttJlbGD7SmaFTwTj8ST4FFG_CxY2fI557u6PoS8ZPCagTBvsmSSswaYaQBY18ATcsxB6UZ12jz9635ETnN-gGpS3BijnpMj3iloW6WOybfPF6tPZ3TjhxGLz3RO_s4nH8qIE93oqqyu9nJZ7yYsYwx0DFT8_P7j9mZFMQw0eEw0lzhTF4cq798w5-gW3texrClOxadQ44-eznHa4eDDAfeCPLvDKfvTw3lCbt-_uzn_2Fxef7g4P7tsnJCyNE6jMxyVU05ib0CJlnkBvWTIOyZ63nrOdSe7VmgYXI-y433rQHimNEghTsjbhTtv-7qsqxsmnOycxg2mnY042n-VMK7tfXy0ylQu1xXw6gBI8cvW52If4rYuNWXLAYxQrNWsutjicinmXP_y9wQGdl-bXWqztTa7r81CzfAlk6s33Pv0h_z_0C938JrZ</recordid><startdate>20180227</startdate><enddate>20180227</enddate><creator>Yue, Yanan</creator><creator>Liu, Jun</creator><creator>Cui, Xiaolong</creator><creator>Cao, Jie</creator><creator>Luo, Guanzheng</creator><creator>Zhang, Zezhou</creator><creator>Cheng, Tao</creator><creator>Gao, Minsong</creator><creator>Shu, Xiao</creator><creator>Ma, Honghui</creator><creator>Wang, Fengqin</creator><creator>Wang, Xinxia</creator><creator>Shen, Bin</creator><creator>Wang, Yizhen</creator><creator>Feng, Xinhua</creator><creator>He, Chuan</creator><creator>Liu, Jianzhao</creator><general>Nature Publishing Group UK</general><general>Springer Nature B.V</general><scope>C6C</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</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>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9465-6075</orcidid><orcidid>https://orcid.org/0000-0002-6797-9319</orcidid><orcidid>https://orcid.org/0000-0003-4319-7424</orcidid></search><sort><creationdate>20180227</creationdate><title>VIRMA mediates preferential m6A mRNA methylation in 3′UTR and near stop codon and associates with alternative polyadenylation</title><author>Yue, Yanan ; Liu, Jun ; Cui, Xiaolong ; Cao, Jie ; Luo, Guanzheng ; Zhang, Zezhou ; Cheng, Tao ; Gao, Minsong ; Shu, Xiao ; Ma, Honghui ; Wang, Fengqin ; Wang, Xinxia ; Shen, Bin ; Wang, Yizhen ; Feng, Xinhua ; He, Chuan ; Liu, Jianzhao</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c344t-c6ac82a5c5c4ab805371e30b41a2913b27e2269497360dcba492b7c03e1560433</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>3' Untranslated regions</topic><topic>631/337/1645/2570</topic><topic>631/80</topic><topic>Biomedical and Life Sciences</topic><topic>Cell Biology</topic><topic>Cell Culture</topic><topic>Cell Cycle Analysis</topic><topic>Cell Physiology</topic><topic>Eukaryotes</topic><topic>Gene expression</topic><topic>Immunoprecipitation</topic><topic>Life Sciences</topic><topic>Methylation</topic><topic>Methyltransferase</topic><topic>N6-methyladenosine</topic><topic>Polyadenylation</topic><topic>Stem Cells</topic><topic>Stop codon</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yue, Yanan</creatorcontrib><creatorcontrib>Liu, Jun</creatorcontrib><creatorcontrib>Cui, Xiaolong</creatorcontrib><creatorcontrib>Cao, Jie</creatorcontrib><creatorcontrib>Luo, Guanzheng</creatorcontrib><creatorcontrib>Zhang, Zezhou</creatorcontrib><creatorcontrib>Cheng, Tao</creatorcontrib><creatorcontrib>Gao, Minsong</creatorcontrib><creatorcontrib>Shu, Xiao</creatorcontrib><creatorcontrib>Ma, Honghui</creatorcontrib><creatorcontrib>Wang, Fengqin</creatorcontrib><creatorcontrib>Wang, Xinxia</creatorcontrib><creatorcontrib>Shen, Bin</creatorcontrib><creatorcontrib>Wang, Yizhen</creatorcontrib><creatorcontrib>Feng, Xinhua</creatorcontrib><creatorcontrib>He, Chuan</creatorcontrib><creatorcontrib>Liu, Jianzhao</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</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 & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Biological Science Database</collection><collection>Publicly Available Content Database</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>PubMed Central (Full Participant titles)</collection><jtitle>Cell discovery</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yue, Yanan</au><au>Liu, Jun</au><au>Cui, Xiaolong</au><au>Cao, Jie</au><au>Luo, Guanzheng</au><au>Zhang, Zezhou</au><au>Cheng, Tao</au><au>Gao, Minsong</au><au>Shu, Xiao</au><au>Ma, Honghui</au><au>Wang, Fengqin</au><au>Wang, Xinxia</au><au>Shen, Bin</au><au>Wang, Yizhen</au><au>Feng, Xinhua</au><au>He, Chuan</au><au>Liu, Jianzhao</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>VIRMA mediates preferential m6A mRNA methylation in 3′UTR and near stop codon and associates with alternative polyadenylation</atitle><jtitle>Cell discovery</jtitle><stitle>Cell Discov</stitle><date>2018-02-27</date><risdate>2018</risdate><volume>4</volume><issue>1</issue><spage>1</spage><epage>17</epage><pages>1-17</pages><artnum>10</artnum><issn>2056-5968</issn><eissn>2056-5968</eissn><abstract>N
6
-methyladenosine (m
6
A) is enriched in 3′untranslated region (3′UTR) and near stop codon of mature polyadenylated mRNAs in mammalian systems and has regulatory roles in eukaryotic mRNA transcriptome switch. Significantly, the mechanism for this modification preference remains unknown, however. Herein we report a characterization of the full m
6
A methyltransferase complex in HeLa cells identifying METTL3/METTL14/WTAP/VIRMA/HAKAI/ZC3H13 as the key components, and we show that VIRMA mediates preferential mRNA methylation in 3′UTR and near stop codon. Biochemical studies reveal that VIRMA recruits the catalytic core components METTL3/METTL14/WTAP to guide region-selective methylations. Around 60% of VIRMA mRNA immunoprecipitation targets manifest strong m
6
A enrichment in 3′UTR. Depletions of
VIRMA
and
METTL3
induce 3′UTR lengthening of several hundred mRNAs with over 50% targets in common. VIRMA associates with polyadenylation cleavage factors CPSF5 and CPSF6 in an RNA-dependent manner. Depletion of CPSF5 leads to significant shortening of 3′UTR of over 2800 mRNAs, 84% of which are modified with m
6
A and have increased m
6
A peak density in 3′UTR and near stop codon after CPSF5 knockdown. Together, our studies provide insights into m
6
A deposition specificity in 3′UTR and its correlation with alternative polyadenylation.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>29507755</pmid><doi>10.1038/s41421-018-0019-0</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0001-9465-6075</orcidid><orcidid>https://orcid.org/0000-0002-6797-9319</orcidid><orcidid>https://orcid.org/0000-0003-4319-7424</orcidid><oa>free_for_read</oa></addata></record> |
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| language | eng |
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| source | DOAJ Directory of Open Access Journals; Springer Nature OA Free Journals; Nature Free; EZB-FREE-00999 freely available EZB journals; PubMed Central |
| subjects | 3' Untranslated regions 631/337/1645/2570 631/80 Biomedical and Life Sciences Cell Biology Cell Culture Cell Cycle Analysis Cell Physiology Eukaryotes Gene expression Immunoprecipitation Life Sciences Methylation Methyltransferase N6-methyladenosine Polyadenylation Stem Cells Stop codon |
| title | VIRMA mediates preferential m6A mRNA methylation in 3′UTR and near stop codon and associates with alternative polyadenylation |
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