Ageing-associated small RNA cargo of extracellular vesicles

Fabian Kern; Thomas Kuhn; Nicole Ludwig; Martin Simon; Laura Gröger; Natalie Fabis; Ernesto Aparicio-Puerta; Abdulrahman Salhab; Tobias Fehlmann; Oliver Hahn; Annika Engel; Viktoria Wagner; Marcus Koch; Katarzyna Winek; Hermona Soreq; Irina Nazarenko; Gregor Fuhrmann; Tony Wyss-Coray; Eckart Meese; Verena Keller; Matthias W. Laschke; Andreas Keller

doi:10.1080/15476286.2023.2234713

Ageing-associated small RNA cargo of extracellular vesicles

Fabian Kern, Thomas Kuhn, Nicole Ludwig, Martin Simon, Laura Gröger, Natalie Fabis, Ernesto Aparicio-Puerta, Abdulrahman Salhab, Tobias Fehlmann, Oliver Hahn, Annika Engel, Viktoria Wagner, Marcus Koch, Katarzyna Winek, Hermona Soreq, Irina Nazarenko, Gregor Fuhrmann, Tony Wyss-Coray, Eckart Meese, Verena KellerMatthias W. Laschke, Andreas Keller^*

^*Corresponding author for this work

Alexander Silberman Institute of Life Sciences

Research output: Contribution to journal › Article › peer-review

8 Scopus citations

Abstract

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.

Original language	English
Pages (from-to)	482-494
Number of pages	13
Journal	RNA Biology
Volume	20
Issue number	1
DOIs	https://doi.org/10.1080/15476286.2023.2234713
State	Published - 2023

Bibliographical note

Publisher Copyright:
© 2023 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.

Keywords

Noncoding RNA
extracellular vesicles
miRNA
plasma
tissue ageing

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10.1080/15476286.2023.2234713

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Kern, F., Kuhn, T., Ludwig, N., Simon, M., Gröger, L., Fabis, N., Aparicio-Puerta, E., Salhab, A., Fehlmann, T., Hahn, O., Engel, A., Wagner, V., Koch, M., Winek, K., Soreq, H., Nazarenko, I., Fuhrmann, G., Wyss-Coray, T., Meese, E., ... Keller, A. (2023). Ageing-associated small RNA cargo of extracellular vesicles. RNA Biology, 20(1), 482-494. https://doi.org/10.1080/15476286.2023.2234713

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title = "Ageing-associated small RNA cargo of extracellular vesicles",

abstract = "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.",

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year = "2023",

doi = "10.1080/15476286.2023.2234713",

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Kern, F, Kuhn, T, Ludwig, N, Simon, M, Gröger, L, Fabis, N, Aparicio-Puerta, E, Salhab, A, Fehlmann, T, Hahn, O, Engel, A, Wagner, V, Koch, M, Winek, K, Soreq, H, Nazarenko, I, Fuhrmann, G, Wyss-Coray, T, Meese, E, Keller, V, Laschke, MW & Keller, A 2023, 'Ageing-associated small RNA cargo of extracellular vesicles', RNA Biology, vol. 20, no. 1, pp. 482-494. https://doi.org/10.1080/15476286.2023.2234713

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AU - Kern, Fabian

AU - Kuhn, Thomas

AU - Ludwig, Nicole

AU - Simon, Martin

AU - Gröger, Laura

AU - Fabis, Natalie

AU - Aparicio-Puerta, Ernesto

AU - Salhab, Abdulrahman

AU - Fehlmann, Tobias

AU - Hahn, Oliver

AU - Engel, Annika

AU - Wagner, Viktoria

AU - Koch, Marcus

AU - Winek, Katarzyna

AU - Soreq, Hermona

AU - Nazarenko, Irina

AU - Fuhrmann, Gregor

AU - Wyss-Coray, Tony

AU - Meese, Eckart

AU - Keller, Verena

AU - Laschke, Matthias W.

AU - Keller, Andreas

PY - 2023

Y1 - 2023

N2 - 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.

AB - 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.

KW - Noncoding RNA

KW - extracellular vesicles

KW - miRNA

KW - plasma

KW - tissue ageing

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VL - 20

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EP - 494

JO - RNA Biology

JF - RNA Biology

IS - 1

ER -

Ageing-associated small RNA cargo of extracellular vesicles

Abstract

Bibliographical note

Keywords

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