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Small RNA profiling and characterization of piRNA clusters in the adult testes of the common marmoset, a model primate
Small RNAs mediate gene silencing by binding Argonaute/Piwi proteins to regulate target RNAs. Here, we describe small RNA profiling of the adult testes of Callithrix jacchus, the common marmoset. The most abundant class of small RNAs in the adult testis was piRNAs, although 353 novel miRNAs but few...
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Published in: | RNA (Cambridge) 2014-08, Vol.20 (8), p.1223-1237 |
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creator | Hirano, Takamasa Iwasaki, Yuka W Lin, Zachary Yu-Ching Imamura, Masanori Seki, Naomi M Sasaki, Erika Saito, Kuniaki Okano, Hideyuki Siomi, Mikiko C Siomi, Haruhiko |
description | Small RNAs mediate gene silencing by binding Argonaute/Piwi proteins to regulate target RNAs. Here, we describe small RNA profiling of the adult testes of Callithrix jacchus, the common marmoset. The most abundant class of small RNAs in the adult testis was piRNAs, although 353 novel miRNAs but few endo-siRNAs were also identified. MARWI, a marmoset homolog of mouse MIWI and a very abundant PIWI in adult testes, associates with piRNAs that show characteristics of mouse pachytene piRNAs. As in other mammals, most marmoset piRNAs are derived from conserved clustered regions in the genome, which are annotated as intergenic regions. However, unlike in mice, marmoset piRNA clusters are also found on the X chromosome, suggesting escape from meiotic sex chromosome inactivation by the X-linked clusters. Some of the piRNA clusters identified contain antisense-orientated pseudogenes, suggesting the possibility that pseudogene-derived piRNAs may regulate parental functional protein-coding genes. More piRNAs map to transposable element (TE) subfamilies when they have copies in piRNA clusters. In addition, the strand bias observed for piRNAs mapped to each TE subfamily correlates with the polarity of copies inserted in clusters. These findings suggest that pachytene piRNA clusters determine the abundance and strand-bias of TE-derived piRNAs, may regulate protein-coding genes via pseudogene-derived piRNAs, and may even play roles in meiosis in the adult marmoset testis. |
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Here, we describe small RNA profiling of the adult testes of Callithrix jacchus, the common marmoset. The most abundant class of small RNAs in the adult testis was piRNAs, although 353 novel miRNAs but few endo-siRNAs were also identified. MARWI, a marmoset homolog of mouse MIWI and a very abundant PIWI in adult testes, associates with piRNAs that show characteristics of mouse pachytene piRNAs. As in other mammals, most marmoset piRNAs are derived from conserved clustered regions in the genome, which are annotated as intergenic regions. However, unlike in mice, marmoset piRNA clusters are also found on the X chromosome, suggesting escape from meiotic sex chromosome inactivation by the X-linked clusters. Some of the piRNA clusters identified contain antisense-orientated pseudogenes, suggesting the possibility that pseudogene-derived piRNAs may regulate parental functional protein-coding genes. More piRNAs map to transposable element (TE) subfamilies when they have copies in piRNA clusters. In addition, the strand bias observed for piRNAs mapped to each TE subfamily correlates with the polarity of copies inserted in clusters. These findings suggest that pachytene piRNA clusters determine the abundance and strand-bias of TE-derived piRNAs, may regulate protein-coding genes via pseudogene-derived piRNAs, and may even play roles in meiosis in the adult marmoset testis.</description><identifier>ISSN: 1355-8382</identifier><identifier>EISSN: 1469-9001</identifier><identifier>DOI: 10.1261/rna.045310.114</identifier><identifier>PMID: 24914035</identifier><language>eng</language><publisher>United States: Cold Spring Harbor Laboratory Press</publisher><subject>Animals ; Argonaute Proteins - genetics ; Argonaute Proteins - metabolism ; Base Sequence ; Callithrix - genetics ; DNA Transposable Elements ; Gene Expression ; Gene Expression Profiling ; Genome ; Male ; Mice ; Molecular Sequence Data ; Multigene Family ; Nucleic Acid Conformation ; Physical Chromosome Mapping ; Protein Binding ; Pseudogenes ; RNA, Small Interfering - chemistry ; RNA, Small Interfering - genetics ; RNA, Small Interfering - metabolism ; RNA, Transfer - chemistry ; RNA, Transfer - metabolism ; Sequence Alignment ; Testis - metabolism</subject><ispartof>RNA (Cambridge), 2014-08, Vol.20 (8), p.1223-1237</ispartof><rights>2014 Hirano et al.; Published by Cold Spring Harbor Laboratory Press for the RNA Society.</rights><rights>2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c456t-f9df3d74151f71e06bae85b3785578507e3fbcca4d45fb8c0c17281779d8f08b3</citedby><cites>FETCH-LOGICAL-c456t-f9df3d74151f71e06bae85b3785578507e3fbcca4d45fb8c0c17281779d8f08b3</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/PMC4105748/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4105748/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24914035$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hirano, Takamasa</creatorcontrib><creatorcontrib>Iwasaki, Yuka W</creatorcontrib><creatorcontrib>Lin, Zachary Yu-Ching</creatorcontrib><creatorcontrib>Imamura, Masanori</creatorcontrib><creatorcontrib>Seki, Naomi M</creatorcontrib><creatorcontrib>Sasaki, Erika</creatorcontrib><creatorcontrib>Saito, Kuniaki</creatorcontrib><creatorcontrib>Okano, Hideyuki</creatorcontrib><creatorcontrib>Siomi, Mikiko C</creatorcontrib><creatorcontrib>Siomi, Haruhiko</creatorcontrib><title>Small RNA profiling and characterization of piRNA clusters in the adult testes of the common marmoset, a model primate</title><title>RNA (Cambridge)</title><addtitle>RNA</addtitle><description>Small RNAs mediate gene silencing by binding Argonaute/Piwi proteins to regulate target RNAs. Here, we describe small RNA profiling of the adult testes of Callithrix jacchus, the common marmoset. The most abundant class of small RNAs in the adult testis was piRNAs, although 353 novel miRNAs but few endo-siRNAs were also identified. MARWI, a marmoset homolog of mouse MIWI and a very abundant PIWI in adult testes, associates with piRNAs that show characteristics of mouse pachytene piRNAs. As in other mammals, most marmoset piRNAs are derived from conserved clustered regions in the genome, which are annotated as intergenic regions. However, unlike in mice, marmoset piRNA clusters are also found on the X chromosome, suggesting escape from meiotic sex chromosome inactivation by the X-linked clusters. Some of the piRNA clusters identified contain antisense-orientated pseudogenes, suggesting the possibility that pseudogene-derived piRNAs may regulate parental functional protein-coding genes. More piRNAs map to transposable element (TE) subfamilies when they have copies in piRNA clusters. In addition, the strand bias observed for piRNAs mapped to each TE subfamily correlates with the polarity of copies inserted in clusters. These findings suggest that pachytene piRNA clusters determine the abundance and strand-bias of TE-derived piRNAs, may regulate protein-coding genes via pseudogene-derived piRNAs, and may even play roles in meiosis in the adult marmoset testis.</description><subject>Animals</subject><subject>Argonaute Proteins - genetics</subject><subject>Argonaute Proteins - metabolism</subject><subject>Base Sequence</subject><subject>Callithrix - genetics</subject><subject>DNA Transposable Elements</subject><subject>Gene Expression</subject><subject>Gene Expression Profiling</subject><subject>Genome</subject><subject>Male</subject><subject>Mice</subject><subject>Molecular Sequence Data</subject><subject>Multigene Family</subject><subject>Nucleic Acid Conformation</subject><subject>Physical Chromosome Mapping</subject><subject>Protein Binding</subject><subject>Pseudogenes</subject><subject>RNA, Small Interfering - chemistry</subject><subject>RNA, Small Interfering - genetics</subject><subject>RNA, Small Interfering - metabolism</subject><subject>RNA, Transfer - chemistry</subject><subject>RNA, Transfer - metabolism</subject><subject>Sequence Alignment</subject><subject>Testis - metabolism</subject><issn>1355-8382</issn><issn>1469-9001</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><recordid>eNpVUUFvFiEQJY2Nra3XHg1HD91PZoFd9mLSNK01aWyi9kxYFvphYPkEton-elm_ttEDGebNmzczeQidAdlA28GHNKsNYZyuObADdAysG5qBEHhV_5TzRlDRHqE3Of-oIK3l1-ioZQMwQvkxevwWlPf465cLvEvROu_mB6zmCeutSkoXk9xvVVyccbR451ae9kuueMZuxmVrsJoWX3AxFcwra8V0DKH2BJVCzKacY4VDnIyvQ1xQxZyiQ6t8Nm-f4gm6v776fnnT3N59-nx5cdtoxrvS2GGydOoZcLA9GNKNygg-0l5wXh_pDbWj1opNjNtRaKKhbwX0_TAJS8RIT9DHve5uGYOZtJlLUl7-3SL9klE5-X9ldlv5EB8lA8J7JqrA-yeBFH8u9UYZXNbGezWbuGQJnHUtDIOASt3sqTrFnJOxL2OAyNUsWc2Se7NkNas2vPt3uRf6szv0D8ffkkI</recordid><startdate>20140801</startdate><enddate>20140801</enddate><creator>Hirano, Takamasa</creator><creator>Iwasaki, Yuka W</creator><creator>Lin, Zachary Yu-Ching</creator><creator>Imamura, Masanori</creator><creator>Seki, Naomi M</creator><creator>Sasaki, Erika</creator><creator>Saito, Kuniaki</creator><creator>Okano, Hideyuki</creator><creator>Siomi, Mikiko C</creator><creator>Siomi, Haruhiko</creator><general>Cold Spring Harbor Laboratory Press</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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20140801</creationdate><title>Small RNA profiling and characterization of piRNA clusters in the adult testes of the common marmoset, a model primate</title><author>Hirano, Takamasa ; Iwasaki, Yuka W ; Lin, Zachary Yu-Ching ; Imamura, Masanori ; Seki, Naomi M ; Sasaki, Erika ; Saito, Kuniaki ; Okano, Hideyuki ; Siomi, Mikiko C ; Siomi, Haruhiko</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c456t-f9df3d74151f71e06bae85b3785578507e3fbcca4d45fb8c0c17281779d8f08b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animals</topic><topic>Argonaute Proteins - genetics</topic><topic>Argonaute Proteins - metabolism</topic><topic>Base Sequence</topic><topic>Callithrix - genetics</topic><topic>DNA Transposable Elements</topic><topic>Gene Expression</topic><topic>Gene Expression Profiling</topic><topic>Genome</topic><topic>Male</topic><topic>Mice</topic><topic>Molecular Sequence Data</topic><topic>Multigene Family</topic><topic>Nucleic Acid Conformation</topic><topic>Physical Chromosome Mapping</topic><topic>Protein Binding</topic><topic>Pseudogenes</topic><topic>RNA, Small Interfering - chemistry</topic><topic>RNA, Small Interfering - genetics</topic><topic>RNA, Small Interfering - metabolism</topic><topic>RNA, Transfer - chemistry</topic><topic>RNA, Transfer - metabolism</topic><topic>Sequence Alignment</topic><topic>Testis - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hirano, Takamasa</creatorcontrib><creatorcontrib>Iwasaki, Yuka W</creatorcontrib><creatorcontrib>Lin, Zachary Yu-Ching</creatorcontrib><creatorcontrib>Imamura, Masanori</creatorcontrib><creatorcontrib>Seki, Naomi M</creatorcontrib><creatorcontrib>Sasaki, Erika</creatorcontrib><creatorcontrib>Saito, Kuniaki</creatorcontrib><creatorcontrib>Okano, Hideyuki</creatorcontrib><creatorcontrib>Siomi, Mikiko C</creatorcontrib><creatorcontrib>Siomi, Haruhiko</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>RNA (Cambridge)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hirano, Takamasa</au><au>Iwasaki, Yuka W</au><au>Lin, Zachary Yu-Ching</au><au>Imamura, Masanori</au><au>Seki, Naomi M</au><au>Sasaki, Erika</au><au>Saito, Kuniaki</au><au>Okano, Hideyuki</au><au>Siomi, Mikiko C</au><au>Siomi, Haruhiko</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Small RNA profiling and characterization of piRNA clusters in the adult testes of the common marmoset, a model primate</atitle><jtitle>RNA (Cambridge)</jtitle><addtitle>RNA</addtitle><date>2014-08-01</date><risdate>2014</risdate><volume>20</volume><issue>8</issue><spage>1223</spage><epage>1237</epage><pages>1223-1237</pages><issn>1355-8382</issn><eissn>1469-9001</eissn><abstract>Small RNAs mediate gene silencing by binding Argonaute/Piwi proteins to regulate target RNAs. Here, we describe small RNA profiling of the adult testes of Callithrix jacchus, the common marmoset. The most abundant class of small RNAs in the adult testis was piRNAs, although 353 novel miRNAs but few endo-siRNAs were also identified. MARWI, a marmoset homolog of mouse MIWI and a very abundant PIWI in adult testes, associates with piRNAs that show characteristics of mouse pachytene piRNAs. As in other mammals, most marmoset piRNAs are derived from conserved clustered regions in the genome, which are annotated as intergenic regions. However, unlike in mice, marmoset piRNA clusters are also found on the X chromosome, suggesting escape from meiotic sex chromosome inactivation by the X-linked clusters. Some of the piRNA clusters identified contain antisense-orientated pseudogenes, suggesting the possibility that pseudogene-derived piRNAs may regulate parental functional protein-coding genes. More piRNAs map to transposable element (TE) subfamilies when they have copies in piRNA clusters. In addition, the strand bias observed for piRNAs mapped to each TE subfamily correlates with the polarity of copies inserted in clusters. These findings suggest that pachytene piRNA clusters determine the abundance and strand-bias of TE-derived piRNAs, may regulate protein-coding genes via pseudogene-derived piRNAs, and may even play roles in meiosis in the adult marmoset testis.</abstract><cop>United States</cop><pub>Cold Spring Harbor Laboratory Press</pub><pmid>24914035</pmid><doi>10.1261/rna.045310.114</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Argonaute Proteins - genetics Argonaute Proteins - metabolism Base Sequence Callithrix - genetics DNA Transposable Elements Gene Expression Gene Expression Profiling Genome Male Mice Molecular Sequence Data Multigene Family Nucleic Acid Conformation Physical Chromosome Mapping Protein Binding Pseudogenes RNA, Small Interfering - chemistry RNA, Small Interfering - genetics RNA, Small Interfering - metabolism RNA, Transfer - chemistry RNA, Transfer - metabolism Sequence Alignment Testis - metabolism |
title | Small RNA profiling and characterization of piRNA clusters in the adult testes of the common marmoset, a model primate |
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