PNLDC1 catalysis and postnatal germline function are required for piRNA trimming, LINE1 silencing, and spermatogenesis in mice
PIWI-interacting RNAs (piRNAs) play critical and conserved roles in transposon silencing and gene regulation in the animal germline. Three distinct piRNA populations are present during mouse spermatogenesis: fetal piRNAs in fetal/perinatal testes, pre-pachytene and pachytene piRNAs in postnatal test...
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| Veröffentlicht in: | PLoS genetics 2024-09, Vol.20 (9), p.e1011429 |
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| creator | Wei, Chao Yan, Xiaoyuan Mann, Jeffrey M Geng, Ruirong Wang, Qianyi Xie, Huirong Demireva, Elena Y Sun, Liangliang Ding, Deqiang Chen, Chen |
| description | PIWI-interacting RNAs (piRNAs) play critical and conserved roles in transposon silencing and gene regulation in the animal germline. Three distinct piRNA populations are present during mouse spermatogenesis: fetal piRNAs in fetal/perinatal testes, pre-pachytene and pachytene piRNAs in postnatal testes. PNLDC1 is required for piRNA 3' end maturation in multiple species. However, whether PNLDC1 is the bona fide piRNA trimmer and the physiological role of 3' trimming of different piRNA populations in spermatogenesis in mammals remain unclear. Here, by inactivating Pnldc1 exonuclease activity in vitro and in mice, we reveal that the PNLDC1 trimmer activity is essential for spermatogenesis and male fertility. PNLDC1 catalytic activity is required for both fetal and postnatal piRNA 3' end trimming. Despite this, postnatal piRNA trimming but not fetal piRNA trimming is critical for LINE1 transposon silencing. Furthermore, conditional inactivation of Pnldc1 in postnatal germ cells causes LINE1 transposon de-repression and spermatogenic arrest in mice, indicating that germline-specific postnatal piRNA trimming is essential for transposon silencing and germ cell development. Our findings highlight the germ cell-intrinsic role of PNLDC1 and piRNA trimming in mammals to safeguard the germline genome and promote fertility. |
| doi_str_mv | 10.1371/journal.pgen.1011429 |
| format | Article |
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Jeremy</contributor><creatorcontrib>Wei, Chao ; Yan, Xiaoyuan ; Mann, Jeffrey M ; Geng, Ruirong ; Wang, Qianyi ; Xie, Huirong ; Demireva, Elena Y ; Sun, Liangliang ; Ding, Deqiang ; Chen, Chen ; Wang, P. Jeremy</creatorcontrib><description>PIWI-interacting RNAs (piRNAs) play critical and conserved roles in transposon silencing and gene regulation in the animal germline. Three distinct piRNA populations are present during mouse spermatogenesis: fetal piRNAs in fetal/perinatal testes, pre-pachytene and pachytene piRNAs in postnatal testes. PNLDC1 is required for piRNA 3' end maturation in multiple species. However, whether PNLDC1 is the bona fide piRNA trimmer and the physiological role of 3' trimming of different piRNA populations in spermatogenesis in mammals remain unclear. Here, by inactivating Pnldc1 exonuclease activity in vitro and in mice, we reveal that the PNLDC1 trimmer activity is essential for spermatogenesis and male fertility. PNLDC1 catalytic activity is required for both fetal and postnatal piRNA 3' end trimming. Despite this, postnatal piRNA trimming but not fetal piRNA trimming is critical for LINE1 transposon silencing. Furthermore, conditional inactivation of Pnldc1 in postnatal germ cells causes LINE1 transposon de-repression and spermatogenic arrest in mice, indicating that germline-specific postnatal piRNA trimming is essential for transposon silencing and germ cell development. Our findings highlight the germ cell-intrinsic role of PNLDC1 and piRNA trimming in mammals to safeguard the germline genome and promote fertility.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1011429</identifier><identifier>PMID: 39312580</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animals ; Biology and Life Sciences ; Catalysis ; DNA Transposable Elements - genetics ; Exonucleases ; Fertility ; Fertility - genetics ; Gene Silencing ; Genes ; Genomics ; Germ Cells - growth & development ; Germ Cells - metabolism ; Identification and classification ; Long Interspersed Nucleotide Elements - genetics ; Male ; Medicine and Health Sciences ; Mice ; Physiological aspects ; Piwi-Interacting RNA ; Research and Analysis Methods ; RNA ; RNA, Small Interfering - genetics ; RNA, Small Interfering - metabolism ; Scientific equipment and supplies industry ; Spermatogenesis ; Spermatogenesis - genetics ; Testis - growth & development ; Testis - metabolism ; Transposons</subject><ispartof>PLoS genetics, 2024-09, Vol.20 (9), p.e1011429</ispartof><rights>Copyright: © 2024 Wei et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2024 Public Library of Science</rights><rights>2024 Wei et al 2024 Wei et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c488t-482727adb6296335c8c0718a65f2eb59a2bc13df112fc0813a7406ed082516403</cites><orcidid>0009-0002-4405-7888 ; 0000-0002-7959-5654 ; 0000-0001-9159-4489 ; 0000-0002-4708-5836</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/PMC11449332/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449332/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2915,27905,27906,53772,53774</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39312580$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Wang, P. Jeremy</contributor><creatorcontrib>Wei, Chao</creatorcontrib><creatorcontrib>Yan, Xiaoyuan</creatorcontrib><creatorcontrib>Mann, Jeffrey M</creatorcontrib><creatorcontrib>Geng, Ruirong</creatorcontrib><creatorcontrib>Wang, Qianyi</creatorcontrib><creatorcontrib>Xie, Huirong</creatorcontrib><creatorcontrib>Demireva, Elena Y</creatorcontrib><creatorcontrib>Sun, Liangliang</creatorcontrib><creatorcontrib>Ding, Deqiang</creatorcontrib><creatorcontrib>Chen, Chen</creatorcontrib><title>PNLDC1 catalysis and postnatal germline function are required for piRNA trimming, LINE1 silencing, and spermatogenesis in mice</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>PIWI-interacting RNAs (piRNAs) play critical and conserved roles in transposon silencing and gene regulation in the animal germline. Three distinct piRNA populations are present during mouse spermatogenesis: fetal piRNAs in fetal/perinatal testes, pre-pachytene and pachytene piRNAs in postnatal testes. PNLDC1 is required for piRNA 3' end maturation in multiple species. However, whether PNLDC1 is the bona fide piRNA trimmer and the physiological role of 3' trimming of different piRNA populations in spermatogenesis in mammals remain unclear. Here, by inactivating Pnldc1 exonuclease activity in vitro and in mice, we reveal that the PNLDC1 trimmer activity is essential for spermatogenesis and male fertility. PNLDC1 catalytic activity is required for both fetal and postnatal piRNA 3' end trimming. Despite this, postnatal piRNA trimming but not fetal piRNA trimming is critical for LINE1 transposon silencing. Furthermore, conditional inactivation of Pnldc1 in postnatal germ cells causes LINE1 transposon de-repression and spermatogenic arrest in mice, indicating that germline-specific postnatal piRNA trimming is essential for transposon silencing and germ cell development. Our findings highlight the germ cell-intrinsic role of PNLDC1 and piRNA trimming in mammals to safeguard the germline genome and promote fertility.</description><subject>Analysis</subject><subject>Animals</subject><subject>Biology and Life Sciences</subject><subject>Catalysis</subject><subject>DNA Transposable Elements - genetics</subject><subject>Exonucleases</subject><subject>Fertility</subject><subject>Fertility - genetics</subject><subject>Gene Silencing</subject><subject>Genes</subject><subject>Genomics</subject><subject>Germ Cells - growth & development</subject><subject>Germ Cells - metabolism</subject><subject>Identification and classification</subject><subject>Long Interspersed Nucleotide Elements - genetics</subject><subject>Male</subject><subject>Medicine and Health Sciences</subject><subject>Mice</subject><subject>Physiological aspects</subject><subject>Piwi-Interacting RNA</subject><subject>Research and Analysis Methods</subject><subject>RNA</subject><subject>RNA, Small Interfering - genetics</subject><subject>RNA, Small Interfering - metabolism</subject><subject>Scientific equipment and supplies industry</subject><subject>Spermatogenesis</subject><subject>Spermatogenesis - genetics</subject><subject>Testis - growth & development</subject><subject>Testis - metabolism</subject><subject>Transposons</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqVkl-LEzEUxQdR3HX1G4gEBHHB1mQy6WSepNRVC6Ur65_XkGbuTLNkktkkI-6Ln30zti4t-KDkISH53ZObk5NlzwmeElqSt9du8Faaad-CnRJMSJFXD7JTwhidlAUuHh6sT7InIVxjTBmvysfZCa0oyRnHp9mvz-vV-wVBSkZpboMOSNoa9S5EO-6gFnxntAXUDFZF7SySHpCHm0F7qFHjPOr11XqOotddp237Bq2W6wuCgjZg1e-NUTH0SUhGl5qF8RZtUacVPM0eNdIEeLafz7JvHy6-Lj5NVpcfl4v5aqIKzuOk4HmZl7LezPJqRilTXOGScDljTQ4bVsl8owitG0LyRmFOqEyvnkGNec7IrMD0LHu30-2HTQe1Ahu9NKJPTUt_K5zU4vjE6q1o3Q-RbC0qSvOk8Hqv4N3NACGKTgcFxkgLbgiCEszL1FtZJvTlDm2lAaFt45KkGnEx50mQEVaxRE3_QqVRQ3LGWWiSg8cF50cFiYnwM7ZyCEEsv1z9B7v-d_by-zH76oDdgjRxG5wZxmSEY7DYgcq7EDw0914TLMb8in1-xZhfsc9vKntx-E_3RX8CS-8AVT7rMg</recordid><startdate>20240923</startdate><enddate>20240923</enddate><creator>Wei, Chao</creator><creator>Yan, Xiaoyuan</creator><creator>Mann, Jeffrey M</creator><creator>Geng, Ruirong</creator><creator>Wang, Qianyi</creator><creator>Xie, Huirong</creator><creator>Demireva, Elena Y</creator><creator>Sun, Liangliang</creator><creator>Ding, Deqiang</creator><creator>Chen, Chen</creator><general>Public Library of Science</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>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0009-0002-4405-7888</orcidid><orcidid>https://orcid.org/0000-0002-7959-5654</orcidid><orcidid>https://orcid.org/0000-0001-9159-4489</orcidid><orcidid>https://orcid.org/0000-0002-4708-5836</orcidid></search><sort><creationdate>20240923</creationdate><title>PNLDC1 catalysis and postnatal germline function are required for piRNA trimming, LINE1 silencing, and spermatogenesis in mice</title><author>Wei, Chao ; Yan, Xiaoyuan ; Mann, Jeffrey M ; Geng, Ruirong ; Wang, Qianyi ; Xie, Huirong ; Demireva, Elena Y ; Sun, Liangliang ; Ding, Deqiang ; Chen, Chen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c488t-482727adb6296335c8c0718a65f2eb59a2bc13df112fc0813a7406ed082516403</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Analysis</topic><topic>Animals</topic><topic>Biology and Life Sciences</topic><topic>Catalysis</topic><topic>DNA Transposable Elements - genetics</topic><topic>Exonucleases</topic><topic>Fertility</topic><topic>Fertility - genetics</topic><topic>Gene Silencing</topic><topic>Genes</topic><topic>Genomics</topic><topic>Germ Cells - growth & development</topic><topic>Germ Cells - metabolism</topic><topic>Identification and classification</topic><topic>Long Interspersed Nucleotide Elements - genetics</topic><topic>Male</topic><topic>Medicine and Health Sciences</topic><topic>Mice</topic><topic>Physiological aspects</topic><topic>Piwi-Interacting RNA</topic><topic>Research and Analysis Methods</topic><topic>RNA</topic><topic>RNA, Small Interfering - genetics</topic><topic>RNA, Small Interfering - metabolism</topic><topic>Scientific equipment and supplies industry</topic><topic>Spermatogenesis</topic><topic>Spermatogenesis - genetics</topic><topic>Testis - growth & development</topic><topic>Testis - metabolism</topic><topic>Transposons</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wei, Chao</creatorcontrib><creatorcontrib>Yan, Xiaoyuan</creatorcontrib><creatorcontrib>Mann, Jeffrey M</creatorcontrib><creatorcontrib>Geng, Ruirong</creatorcontrib><creatorcontrib>Wang, Qianyi</creatorcontrib><creatorcontrib>Xie, Huirong</creatorcontrib><creatorcontrib>Demireva, Elena Y</creatorcontrib><creatorcontrib>Sun, Liangliang</creatorcontrib><creatorcontrib>Ding, Deqiang</creatorcontrib><creatorcontrib>Chen, Chen</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: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wei, Chao</au><au>Yan, Xiaoyuan</au><au>Mann, Jeffrey M</au><au>Geng, Ruirong</au><au>Wang, Qianyi</au><au>Xie, Huirong</au><au>Demireva, Elena Y</au><au>Sun, Liangliang</au><au>Ding, Deqiang</au><au>Chen, Chen</au><au>Wang, P. Jeremy</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>PNLDC1 catalysis and postnatal germline function are required for piRNA trimming, LINE1 silencing, and spermatogenesis in mice</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2024-09-23</date><risdate>2024</risdate><volume>20</volume><issue>9</issue><spage>e1011429</spage><pages>e1011429-</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>PIWI-interacting RNAs (piRNAs) play critical and conserved roles in transposon silencing and gene regulation in the animal germline. Three distinct piRNA populations are present during mouse spermatogenesis: fetal piRNAs in fetal/perinatal testes, pre-pachytene and pachytene piRNAs in postnatal testes. PNLDC1 is required for piRNA 3' end maturation in multiple species. However, whether PNLDC1 is the bona fide piRNA trimmer and the physiological role of 3' trimming of different piRNA populations in spermatogenesis in mammals remain unclear. Here, by inactivating Pnldc1 exonuclease activity in vitro and in mice, we reveal that the PNLDC1 trimmer activity is essential for spermatogenesis and male fertility. PNLDC1 catalytic activity is required for both fetal and postnatal piRNA 3' end trimming. Despite this, postnatal piRNA trimming but not fetal piRNA trimming is critical for LINE1 transposon silencing. Furthermore, conditional inactivation of Pnldc1 in postnatal germ cells causes LINE1 transposon de-repression and spermatogenic arrest in mice, indicating that germline-specific postnatal piRNA trimming is essential for transposon silencing and germ cell development. Our findings highlight the germ cell-intrinsic role of PNLDC1 and piRNA trimming in mammals to safeguard the germline genome and promote fertility.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>39312580</pmid><doi>10.1371/journal.pgen.1011429</doi><tpages>e1011429</tpages><orcidid>https://orcid.org/0009-0002-4405-7888</orcidid><orcidid>https://orcid.org/0000-0002-7959-5654</orcidid><orcidid>https://orcid.org/0000-0001-9159-4489</orcidid><orcidid>https://orcid.org/0000-0002-4708-5836</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Analysis Animals Biology and Life Sciences Catalysis DNA Transposable Elements - genetics Exonucleases Fertility Fertility - genetics Gene Silencing Genes Genomics Germ Cells - growth & development Germ Cells - metabolism Identification and classification Long Interspersed Nucleotide Elements - genetics Male Medicine and Health Sciences Mice Physiological aspects Piwi-Interacting RNA Research and Analysis Methods RNA RNA, Small Interfering - genetics RNA, Small Interfering - metabolism Scientific equipment and supplies industry Spermatogenesis Spermatogenesis - genetics Testis - growth & development Testis - metabolism Transposons |
| title | PNLDC1 catalysis and postnatal germline function are required for piRNA trimming, LINE1 silencing, and spermatogenesis in mice |
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