Sperm acrosome overgrowth and infertility in mice lacking chromosome 18 pachytene piRNA
piRNAs are small non-coding RNAs required to maintain genome integrity and preserve RNA homeostasis during male gametogenesis. In murine adult testes, the highest levels of piRNAs are present in the pachytene stage of meiosis, but their mode of action and function remain incompletely understood. We...
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| Veröffentlicht in: | PLoS genetics 2021-04, Vol.17 (4), p.e1009485-e1009485 |
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| description | piRNAs are small non-coding RNAs required to maintain genome integrity and preserve RNA homeostasis during male gametogenesis. In murine adult testes, the highest levels of piRNAs are present in the pachytene stage of meiosis, but their mode of action and function remain incompletely understood. We previously reported that BTBD18 binds to 50 pachytene piRNA-producing loci. Here we show that spermatozoa in gene-edited mice lacking a BTBD18 targeted pachytene piRNA cluster on Chr18 have severe sperm head dysmorphology, poor motility, impaired acrosome exocytosis, zona pellucida penetration and are sterile. The mutant phenotype arises from aberrant formation of proacrosomal vesicles, distortion of the trans-Golgi network, and up-regulation of GOLGA2 transcripts and protein associated with acrosome dysgenesis. Collectively, our findings reveal central role of pachytene piRNAs in controlling spermiogenesis and male fertility. |
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In murine adult testes, the highest levels of piRNAs are present in the pachytene stage of meiosis, but their mode of action and function remain incompletely understood. We previously reported that BTBD18 binds to 50 pachytene piRNA-producing loci. Here we show that spermatozoa in gene-edited mice lacking a BTBD18 targeted pachytene piRNA cluster on Chr18 have severe sperm head dysmorphology, poor motility, impaired acrosome exocytosis, zona pellucida penetration and are sterile. The mutant phenotype arises from aberrant formation of proacrosomal vesicles, distortion of the trans-Golgi network, and up-regulation of GOLGA2 transcripts and protein associated with acrosome dysgenesis. Collectively, our findings reveal central role of pachytene piRNAs in controlling spermiogenesis and male fertility.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1009485</identifier><identifier>PMID: 33831001</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acrosome - pathology ; Acrosomes ; Analysis ; Animals ; Biology and Life Sciences ; Biosynthesis ; Chromatin ; Chromosome 18 ; Chromosomes - genetics ; CRISPR ; Females ; Fertility ; Gametogenesis ; Gene deletion ; Genetic aspects ; Genomes ; Genomics ; Growth rate ; Histones ; Humans ; Identification and classification ; Infertility ; Infertility, Male - genetics ; Infertility, Male - pathology ; Male ; Medicine and Health Sciences ; Meiosis - genetics ; Mice ; MicroRNAs ; Molecular modelling ; Motility ; Pachytene ; Pachytene Stage - genetics ; Post-transcription ; Quality control ; RNA ; RNA polymerase ; RNA, Small Interfering - genetics ; Rodents ; Sperm ; Spermatids ; Spermatids - growth & development ; Spermatids - pathology ; Spermatogenesis ; Spermatogenesis - genetics ; Spermatozoa - pathology ; Spermiogenesis ; Testes ; Testis - growth & development ; Testis - pathology</subject><ispartof>PLoS genetics, 2021-04, Vol.17 (4), p.e1009485-e1009485</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication: https://creativecommons.org/publicdomain/zero/1.0/ (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-c792t-105243db4df7840f0688541aef89d2a1821c74cc316a3305c5f44e03f9b6a70e3</citedby><cites>FETCH-LOGICAL-c792t-105243db4df7840f0688541aef89d2a1821c74cc316a3305c5f44e03f9b6a70e3</cites><orcidid>0000-0002-7127-0871 ; 0000-0003-4945-5674 ; 0000-0001-5388-1516</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/PMC8057611/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8057611/$$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/33831001$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Cohen, Paula E.</contributor><creatorcontrib>Choi, Heejin</creatorcontrib><creatorcontrib>Wang, Zhengpin</creatorcontrib><creatorcontrib>Dean, Jurrien</creatorcontrib><title>Sperm acrosome overgrowth and infertility in mice lacking chromosome 18 pachytene piRNA</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>piRNAs are small non-coding RNAs required to maintain genome integrity and preserve RNA homeostasis during male gametogenesis. In murine adult testes, the highest levels of piRNAs are present in the pachytene stage of meiosis, but their mode of action and function remain incompletely understood. We previously reported that BTBD18 binds to 50 pachytene piRNA-producing loci. Here we show that spermatozoa in gene-edited mice lacking a BTBD18 targeted pachytene piRNA cluster on Chr18 have severe sperm head dysmorphology, poor motility, impaired acrosome exocytosis, zona pellucida penetration and are sterile. The mutant phenotype arises from aberrant formation of proacrosomal vesicles, distortion of the trans-Golgi network, and up-regulation of GOLGA2 transcripts and protein associated with acrosome dysgenesis. Collectively, our findings reveal central role of pachytene piRNAs in controlling spermiogenesis and male fertility.</description><subject>Acrosome - pathology</subject><subject>Acrosomes</subject><subject>Analysis</subject><subject>Animals</subject><subject>Biology and Life Sciences</subject><subject>Biosynthesis</subject><subject>Chromatin</subject><subject>Chromosome 18</subject><subject>Chromosomes - genetics</subject><subject>CRISPR</subject><subject>Females</subject><subject>Fertility</subject><subject>Gametogenesis</subject><subject>Gene deletion</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Growth rate</subject><subject>Histones</subject><subject>Humans</subject><subject>Identification and classification</subject><subject>Infertility</subject><subject>Infertility, Male - genetics</subject><subject>Infertility, Male - pathology</subject><subject>Male</subject><subject>Medicine and Health Sciences</subject><subject>Meiosis - 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pathology</topic><topic>Acrosomes</topic><topic>Analysis</topic><topic>Animals</topic><topic>Biology and Life Sciences</topic><topic>Biosynthesis</topic><topic>Chromatin</topic><topic>Chromosome 18</topic><topic>Chromosomes - genetics</topic><topic>CRISPR</topic><topic>Females</topic><topic>Fertility</topic><topic>Gametogenesis</topic><topic>Gene deletion</topic><topic>Genetic aspects</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Growth rate</topic><topic>Histones</topic><topic>Humans</topic><topic>Identification and classification</topic><topic>Infertility</topic><topic>Infertility, Male - genetics</topic><topic>Infertility, Male - pathology</topic><topic>Male</topic><topic>Medicine and Health Sciences</topic><topic>Meiosis - genetics</topic><topic>Mice</topic><topic>MicroRNAs</topic><topic>Molecular modelling</topic><topic>Motility</topic><topic>Pachytene</topic><topic>Pachytene Stage - genetics</topic><topic>Post-transcription</topic><topic>Quality control</topic><topic>RNA</topic><topic>RNA polymerase</topic><topic>RNA, Small Interfering - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Choi, Heejin</au><au>Wang, Zhengpin</au><au>Dean, Jurrien</au><au>Cohen, Paula E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Sperm acrosome overgrowth and infertility in mice lacking chromosome 18 pachytene piRNA</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2021-04-08</date><risdate>2021</risdate><volume>17</volume><issue>4</issue><spage>e1009485</spage><epage>e1009485</epage><pages>e1009485-e1009485</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>piRNAs are small non-coding RNAs required to maintain genome integrity and preserve RNA homeostasis during male gametogenesis. In murine adult testes, the highest levels of piRNAs are present in the pachytene stage of meiosis, but their mode of action and function remain incompletely understood. We previously reported that BTBD18 binds to 50 pachytene piRNA-producing loci. Here we show that spermatozoa in gene-edited mice lacking a BTBD18 targeted pachytene piRNA cluster on Chr18 have severe sperm head dysmorphology, poor motility, impaired acrosome exocytosis, zona pellucida penetration and are sterile. The mutant phenotype arises from aberrant formation of proacrosomal vesicles, distortion of the trans-Golgi network, and up-regulation of GOLGA2 transcripts and protein associated with acrosome dysgenesis. Collectively, our findings reveal central role of pachytene piRNAs in controlling spermiogenesis and male fertility.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>33831001</pmid><doi>10.1371/journal.pgen.1009485</doi><orcidid>https://orcid.org/0000-0002-7127-0871</orcidid><orcidid>https://orcid.org/0000-0003-4945-5674</orcidid><orcidid>https://orcid.org/0000-0001-5388-1516</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Acrosome - pathology Acrosomes Analysis Animals Biology and Life Sciences Biosynthesis Chromatin Chromosome 18 Chromosomes - genetics CRISPR Females Fertility Gametogenesis Gene deletion Genetic aspects Genomes Genomics Growth rate Histones Humans Identification and classification Infertility Infertility, Male - genetics Infertility, Male - pathology Male Medicine and Health Sciences Meiosis - genetics Mice MicroRNAs Molecular modelling Motility Pachytene Pachytene Stage - genetics Post-transcription Quality control RNA RNA polymerase RNA, Small Interfering - genetics Rodents Sperm Spermatids Spermatids - growth & development Spermatids - pathology Spermatogenesis Spermatogenesis - genetics Spermatozoa - pathology Spermiogenesis Testes Testis - growth & development Testis - pathology |
| title | Sperm acrosome overgrowth and infertility in mice lacking chromosome 18 pachytene piRNA |
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