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Ageing-associated small RNA cargo of extracellular vesicles
Previous work on murine models and humans demonstrated global as well as tissue-specific molecular ageing trajectories of RNAs. Extracellular vesicles (EVs) are membrane vesicles mediating the horizontal transfer of genetic information between different tissues. We sequenced small regulatory RNAs (s...
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Published in: | RNA biology 2023-12, Vol.20 (1), p.482-494 |
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creator | Kern, Fabian Kuhn, Thomas Ludwig, Nicole Simon, Martin Gröger, Laura Fabis, Natalie Aparicio-Puerta, Ernesto Salhab, Abdulrahman Fehlmann, Tobias Hahn, Oliver Engel, Annika Wagner, Viktoria Koch, Marcus Winek, Katarzyna Soreq, Hermona Nazarenko, Irina Fuhrmann, Gregor Wyss-Coray, Tony Meese, Eckart Keller, Verena Laschke, Matthias W. Keller, Andreas |
description | Previous work on murine models and humans demonstrated global as well as tissue-specific molecular ageing trajectories of RNAs. Extracellular vesicles (EVs) are membrane vesicles mediating the horizontal transfer of genetic information between different tissues. We sequenced small regulatory RNAs (sncRNAs) in two mouse plasma fractions at five time points across the lifespan from 2-18 months: (1) sncRNAs that are free-circulating (fc-RNA) and (2) sncRNAs bound outside or inside EVs (EV-RNA). Different sncRNA classes exhibit unique ageing patterns that vary between the fcRNA and EV-RNA fractions. While tRNAs showed the highest correlation with ageing in both fractions, rRNAs exhibited inverse correlation trajectories between the EV- and fc-fractions. For miRNAs, the EV-RNA fraction was exceptionally strongly associated with ageing, especially the miR-29 family in adipose tissues. Sequencing of sncRNAs and coding genes in fat tissue of an independent cohort of aged mice up to 27 months highlighted the pivotal role of miR-29a-3p and miR-29b-3p in ageing-related gene regulation that we validated in a third cohort by RT-qPCR. |
doi_str_mv | 10.1080/15476286.2023.2234713 |
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Extracellular vesicles (EVs) are membrane vesicles mediating the horizontal transfer of genetic information between different tissues. We sequenced small regulatory RNAs (sncRNAs) in two mouse plasma fractions at five time points across the lifespan from 2-18 months: (1) sncRNAs that are free-circulating (fc-RNA) and (2) sncRNAs bound outside or inside EVs (EV-RNA). Different sncRNA classes exhibit unique ageing patterns that vary between the fcRNA and EV-RNA fractions. While tRNAs showed the highest correlation with ageing in both fractions, rRNAs exhibited inverse correlation trajectories between the EV- and fc-fractions. For miRNAs, the EV-RNA fraction was exceptionally strongly associated with ageing, especially the miR-29 family in adipose tissues. Sequencing of sncRNAs and coding genes in fat tissue of an independent cohort of aged mice up to 27 months highlighted the pivotal role of miR-29a-3p and miR-29b-3p in ageing-related gene regulation that we validated in a third cohort by RT-qPCR.</description><identifier>ISSN: 1547-6286</identifier><identifier>ISSN: 1555-8584</identifier><identifier>EISSN: 1555-8584</identifier><identifier>DOI: 10.1080/15476286.2023.2234713</identifier><identifier>PMID: 37498213</identifier><language>eng</language><publisher>United States: Taylor & Francis</publisher><subject>Aging - genetics ; Animals ; Biological Sciences ; extracellular vesicles ; Extracellular Vesicles - metabolism ; genes ; Humans ; longevity ; Mice ; microRNA ; MicroRNAs - genetics ; MicroRNAs - metabolism ; miRNA ; Noncoding RNA ; plasma ; Research Paper ; RNA, Small Untranslated - genetics ; RNA, Small Untranslated - metabolism ; RNA, Transfer - metabolism ; tissue ageing</subject><ispartof>RNA biology, 2023-12, Vol.20 (1), p.482-494</ispartof><rights>2023 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. 2023</rights><rights>2023 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. 2023 The Author(s)</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c568t-757255f27eb9bba01d7fe8bb83dd4bee63a201434bf737b39d2a2250c60131b03</citedby><cites>FETCH-LOGICAL-c568t-757255f27eb9bba01d7fe8bb83dd4bee63a201434bf737b39d2a2250c60131b03</cites><orcidid>0000-0001-9440-1152 ; 0000-0001-5570-3115 ; 0000-0002-3470-1425 ; 0000-0002-5361-0895 ; 0000-0003-1967-2918 ; 0000-0003-1043-3910 ; 0000-0002-9649-6922 ; 0000-0002-2633-1161 ; 0000-0002-1693-6829 ; 0000-0002-0962-7788 ; 0000-0003-3085-9054 ; 0000-0002-0955-526X ; 0000-0001-5893-0831 ; 0000-0002-7847-8456 ; 0000-0002-8223-3750 ; 0000-0003-2444-3204</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/PMC10376918/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10376918/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27479,27901,27902,53766,53768,59116,59117</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37498213$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kern, Fabian</creatorcontrib><creatorcontrib>Kuhn, Thomas</creatorcontrib><creatorcontrib>Ludwig, Nicole</creatorcontrib><creatorcontrib>Simon, Martin</creatorcontrib><creatorcontrib>Gröger, Laura</creatorcontrib><creatorcontrib>Fabis, Natalie</creatorcontrib><creatorcontrib>Aparicio-Puerta, Ernesto</creatorcontrib><creatorcontrib>Salhab, Abdulrahman</creatorcontrib><creatorcontrib>Fehlmann, Tobias</creatorcontrib><creatorcontrib>Hahn, Oliver</creatorcontrib><creatorcontrib>Engel, Annika</creatorcontrib><creatorcontrib>Wagner, Viktoria</creatorcontrib><creatorcontrib>Koch, Marcus</creatorcontrib><creatorcontrib>Winek, Katarzyna</creatorcontrib><creatorcontrib>Soreq, Hermona</creatorcontrib><creatorcontrib>Nazarenko, Irina</creatorcontrib><creatorcontrib>Fuhrmann, Gregor</creatorcontrib><creatorcontrib>Wyss-Coray, Tony</creatorcontrib><creatorcontrib>Meese, Eckart</creatorcontrib><creatorcontrib>Keller, Verena</creatorcontrib><creatorcontrib>Laschke, Matthias W.</creatorcontrib><creatorcontrib>Keller, Andreas</creatorcontrib><title>Ageing-associated small RNA cargo of extracellular vesicles</title><title>RNA biology</title><addtitle>RNA Biol</addtitle><description>Previous work on murine models and humans demonstrated global as well as tissue-specific molecular ageing trajectories of RNAs. 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Sequencing of sncRNAs and coding genes in fat tissue of an independent cohort of aged mice up to 27 months highlighted the pivotal role of miR-29a-3p and miR-29b-3p in ageing-related gene regulation that we validated in a third cohort by RT-qPCR.</description><subject>Aging - genetics</subject><subject>Animals</subject><subject>Biological Sciences</subject><subject>extracellular vesicles</subject><subject>Extracellular Vesicles - metabolism</subject><subject>genes</subject><subject>Humans</subject><subject>longevity</subject><subject>Mice</subject><subject>microRNA</subject><subject>MicroRNAs - genetics</subject><subject>MicroRNAs - metabolism</subject><subject>miRNA</subject><subject>Noncoding RNA</subject><subject>plasma</subject><subject>Research Paper</subject><subject>RNA, Small Untranslated - genetics</subject><subject>RNA, Small Untranslated - metabolism</subject><subject>RNA, Transfer - metabolism</subject><subject>tissue ageing</subject><issn>1547-6286</issn><issn>1555-8584</issn><issn>1555-8584</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>0YH</sourceid><sourceid>DOA</sourceid><recordid>eNqFkU9v1DAQxS0EoqXwEUA5cslie-zYFgdYVdBWqkBCcLb8N6Ry4mJnC_32JOy2ohc42bJ_8-bNPIReErwhWOI3hDPRUdltKKawoRSYIPAIHRPOeSu5ZI_XOxPtCh2hZ7VeYQydVPwpOgLBlKQEjtHbbR-GqW9NrdkNZg6-qaNJqfnyads4U_rc5NiEX3MxLqS0S6Y0N6EOLoX6HD2JJtXw4nCeoG8fP3w9PW8vP59dnG4vW8c7ObeCC8p5pCJYZa3BxIsYpLUSvGc2hA4MxYQBs1GAsKA8NZRy7DpMgFgMJ-hir-uzudLXZRhNudXZDPrPQy69NmVeLWnHopLKgXPgmZBURiyVEo4pGilWdNF6t9e63tkxeBemZbL0QPThzzR8132-0QSD6BSRi8Lrg0LJP3ahznoc6robM4W8qxowW_YsBCH_RalkgIET0S0o36Ou5FpLiPeWCNZr4PoucL0Grg-BL3Wv_p7nvuou4QV4vweGKeYymp-5JK9nc5tyicVMblgs_7vHb588uNw</recordid><startdate>20231231</startdate><enddate>20231231</enddate><creator>Kern, Fabian</creator><creator>Kuhn, Thomas</creator><creator>Ludwig, Nicole</creator><creator>Simon, Martin</creator><creator>Gröger, Laura</creator><creator>Fabis, Natalie</creator><creator>Aparicio-Puerta, Ernesto</creator><creator>Salhab, Abdulrahman</creator><creator>Fehlmann, Tobias</creator><creator>Hahn, Oliver</creator><creator>Engel, Annika</creator><creator>Wagner, Viktoria</creator><creator>Koch, Marcus</creator><creator>Winek, Katarzyna</creator><creator>Soreq, Hermona</creator><creator>Nazarenko, Irina</creator><creator>Fuhrmann, Gregor</creator><creator>Wyss-Coray, Tony</creator><creator>Meese, Eckart</creator><creator>Keller, Verena</creator><creator>Laschke, Matthias W.</creator><creator>Keller, Andreas</creator><general>Taylor & Francis</general><general>Taylor & Francis Group</general><scope>0YH</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>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-9440-1152</orcidid><orcidid>https://orcid.org/0000-0001-5570-3115</orcidid><orcidid>https://orcid.org/0000-0002-3470-1425</orcidid><orcidid>https://orcid.org/0000-0002-5361-0895</orcidid><orcidid>https://orcid.org/0000-0003-1967-2918</orcidid><orcidid>https://orcid.org/0000-0003-1043-3910</orcidid><orcidid>https://orcid.org/0000-0002-9649-6922</orcidid><orcidid>https://orcid.org/0000-0002-2633-1161</orcidid><orcidid>https://orcid.org/0000-0002-1693-6829</orcidid><orcidid>https://orcid.org/0000-0002-0962-7788</orcidid><orcidid>https://orcid.org/0000-0003-3085-9054</orcidid><orcidid>https://orcid.org/0000-0002-0955-526X</orcidid><orcidid>https://orcid.org/0000-0001-5893-0831</orcidid><orcidid>https://orcid.org/0000-0002-7847-8456</orcidid><orcidid>https://orcid.org/0000-0002-8223-3750</orcidid><orcidid>https://orcid.org/0000-0003-2444-3204</orcidid></search><sort><creationdate>20231231</creationdate><title>Ageing-associated small RNA cargo of extracellular vesicles</title><author>Kern, Fabian ; 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subjects | Aging - genetics Animals Biological Sciences extracellular vesicles Extracellular Vesicles - metabolism genes Humans longevity Mice microRNA MicroRNAs - genetics MicroRNAs - metabolism miRNA Noncoding RNA plasma Research Paper RNA, Small Untranslated - genetics RNA, Small Untranslated - metabolism RNA, Transfer - metabolism tissue ageing |
title | Ageing-associated small RNA cargo of extracellular vesicles |
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