Planarians recruit piRNAs for mRNA turnover in adult stem cells

PIWI proteins utilize small RNAs called piRNAs to silence transposable elements, thereby protecting germline integrity. In planarian flatworms, PIWI proteins are essential for regeneration, which requires adult stem cells termed neoblasts. Here, we characterize planarian piRNAs and examine the roles...

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Published inGenes & development Vol. 33; no. 21-22; pp. 1575 - 1590
Main Authors Kim, Iana V, Duncan, Elizabeth M, Ross, Eric J, Gorbovytska, Vladyslava, Nowotarski, Stephanie H, Elliott, Sarah A, Sánchez Alvarado, Alejandro, Kuhn, Claus-D
Format Journal Article
LanguageEnglish
Published United States Cold Spring Harbor Laboratory Press 01.11.2019
Subjects
Adult Stem Cells - metabolism
Animals
Base Pairing
DNA Transposable Elements
Helminth Proteins - metabolism
Immunoprecipitation
Planarians - cytology
Planarians - metabolism
Protein Binding
Research Paper
RNA Stability
RNA, Messenger - metabolism
RNA, Small Interfering - metabolism
stem cells
S. mediterranea
regeneration
mRNA turnover
RNA-binding proteins
planarians
mRNA surveillance
piRNAs
PIWI proteins
posttranscriptional gene silencing
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Summary:PIWI proteins utilize small RNAs called piRNAs to silence transposable elements, thereby protecting germline integrity. In planarian flatworms, PIWI proteins are essential for regeneration, which requires adult stem cells termed neoblasts. Here, we characterize planarian piRNAs and examine the roles of PIWI proteins in neoblast biology. We find that the planarian PIWI proteins SMEDWI-2 and SMEDWI-3 cooperate to degrade active transposons via the ping-pong cycle. Unexpectedly, we discover that SMEDWI-3 plays an additional role in planarian mRNA surveillance. While SMEDWI-3 degrades numerous neoblast mRNAs in a homotypic ping-pong cycle, it is also guided to another subset of neoblast mRNAs by antisense piRNAs and binds these without degrading them. Mechanistically, the distinct activities of SMEDWI-3 are primarily dictated by the degree of complementarity between target mRNAs and antisense piRNAs. Thus, PIWI proteins enable planarians to repurpose piRNAs for potentially critical roles in neoblast mRNA turnover.
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Present address: Department of Biology, University of Kentucky, Lexington, Kentucky 40506, USA
ISSN:0890-9369
1549-5477
DOI:10.1101/gad.322776.118