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Terminal Modification, Sequence, and Length Determine Small RNA Stability in Animals

Ildar Gainetdinov, Cansu Colpan, Katharine Cecchini, Paul Albosta, Karina Jouravleva, Joel Vega-Badillo, Yongjin Lee, Deniz M. Özata, View ORCID ProfilePhillip D. Zamore
doi: https://doi.org/10.1101/2020.09.08.287979
Ildar Gainetdinov
1RNA Therapeutics Institute and Howard Hughes Medical Institute University of Massachusetts Medical School, 368 Plantation Street, Worcester, MA 01605, USA
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  • For correspondence: Ildar.Gainetdinov@umassmed.edu Phillip.Zamore@umassmed.edu
Cansu Colpan
1RNA Therapeutics Institute and Howard Hughes Medical Institute University of Massachusetts Medical School, 368 Plantation Street, Worcester, MA 01605, USA
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Katharine Cecchini
1RNA Therapeutics Institute and Howard Hughes Medical Institute University of Massachusetts Medical School, 368 Plantation Street, Worcester, MA 01605, USA
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Paul Albosta
1RNA Therapeutics Institute and Howard Hughes Medical Institute University of Massachusetts Medical School, 368 Plantation Street, Worcester, MA 01605, USA
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Karina Jouravleva
1RNA Therapeutics Institute and Howard Hughes Medical Institute University of Massachusetts Medical School, 368 Plantation Street, Worcester, MA 01605, USA
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Joel Vega-Badillo
1RNA Therapeutics Institute and Howard Hughes Medical Institute University of Massachusetts Medical School, 368 Plantation Street, Worcester, MA 01605, USA
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Yongjin Lee
1RNA Therapeutics Institute and Howard Hughes Medical Institute University of Massachusetts Medical School, 368 Plantation Street, Worcester, MA 01605, USA
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Deniz M. Özata
1RNA Therapeutics Institute and Howard Hughes Medical Institute University of Massachusetts Medical School, 368 Plantation Street, Worcester, MA 01605, USA
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Phillip D. Zamore
1RNA Therapeutics Institute and Howard Hughes Medical Institute University of Massachusetts Medical School, 368 Plantation Street, Worcester, MA 01605, USA
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  • ORCID record for Phillip D. Zamore
  • For correspondence: Ildar.Gainetdinov@umassmed.edu Phillip.Zamore@umassmed.edu
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ABSTRACT

In animals, piRNAs, siRNAs, and miRNAs silence transposons, fight viral infections, and regulate gene expression. piRNA biogenesis concludes with 3′ terminal trimming and 2′-O-methylation. Both trimming and methylation influence piRNA stability. Here, we report that trimming and methylation protect mouse piRNAs from different decay mechanisms. In the absence of 2′-O-methylation, mouse piRNAs with extensive complementarity to long RNAs become unstable. In flies, 2′-O-methylation similarly protects both piRNAs and siRNAs from complementarity-dependent destabilization. Animal miRNAs are unmethylated, and complementarity-dependent destabilization helps explain differences in miRNA decay rates in both mice and flies. In contrast, trimming protects mouse piRNAs from a separate degradation pathway unaffected by target complementarity but sensitive to the 3′ terminal, untrimmed sequence. Because distinct sets of mouse piRNAs are protected by each of these mechanisms, loss of both trimming and 2′-O-methylation causes the piRNA pathway to collapse, demonstrating that these two small RNA modifications collaborate to stabilize piRNAs.

Highlights

  • 2′-O-methylation protects mouse and fly piRNAs from complementarity-dependent decay

  • 2′-O-methylation protects fly siRNAs with extensive complementarity to long RNAs

  • Complementarity to long RNAs predicts the half-life of fly and mouse miRNAs

  • Mouse pre-piRNA decay reflects both pre-piRNA sequence and PIWI protein identity

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵3 Lead Contact

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Terminal Modification, Sequence, and Length Determine Small RNA Stability in Animals
Ildar Gainetdinov, Cansu Colpan, Katharine Cecchini, Paul Albosta, Karina Jouravleva, Joel Vega-Badillo, Yongjin Lee, Deniz M. Özata, Phillip D. Zamore
bioRxiv 2020.09.08.287979; doi: https://doi.org/10.1101/2020.09.08.287979
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Terminal Modification, Sequence, and Length Determine Small RNA Stability in Animals
Ildar Gainetdinov, Cansu Colpan, Katharine Cecchini, Paul Albosta, Karina Jouravleva, Joel Vega-Badillo, Yongjin Lee, Deniz M. Özata, Phillip D. Zamore
bioRxiv 2020.09.08.287979; doi: https://doi.org/10.1101/2020.09.08.287979

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