Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo Journal Article
| Authors: | Rouget, C.; Papin, C.; Boureux, A.; Meunier, A. C.; Franco, B.; Robine, N.; Lai, E. C.; Pelisson, A.; Simonelig, M. |
| Article Title: | Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo |
| Abstract: | Piwi-associated RNAs (piRNAs), a specific class of 24- to 30-nucleotide-long RNAs produced by the Piwi-type of Argonaute proteins, have a specific germline function in repressing transposable elements. This repression is thought to involve heterochromatin formation and transcriptional and post-transcriptional silencing. The piRNA pathway has other essential functions in germline stem cell maintenance and in maintaining germline DNA integrity. Here we uncover an unexpected function of the piRNA pathway in the decay of maternal messenger RNAs and in translational repression in the early embryo. A subset of maternal mRNAs is degraded in the embryo at the maternal-to-zygotic transition. In Drosophila, maternal mRNA degradation depends on the RNA-binding protein Smaug and the deadenylase CCR4, as well as the zygotic expression of a microRNA cluster. Using mRNA encoding the embryonic posterior morphogen Nanos (Nos) as a paradigm to study maternal mRNA decay, we found that CCR4-mediated deadenylation of nos depends on components of the piRNA pathway including piRNAs complementary to a specific region in the nos 3-2 untranslated region. Reduced deadenylation when piRNA-induced regulation is impaired correlates with nos mRNA stabilization and translational derepression in the embryo, resulting in head development defects. Aubergine, one of the Argonaute proteins in the piRNA pathway, is present in a complex with Smaug, CCR4, nos mRNA and piRNAs that target the nos 3-2′ untranslated region, in the bulk of the embryo. We propose that piRNAs and their associated proteins act together with Smaug to recruit the CCR4 deadenylation complex to specific mRNAs, thus promoting their decay. Because the piRNAs involved in this regulation are produced from transposable elements, this identifies a direct developmental function for transposable elements in the regulation of gene expression. © 2010 Macmillan Publishers Limited. All rights reserved. |
| Keywords: | signal transduction; controlled study; unclassified drug; gene deletion; nonhuman; genetic analysis; animals; microrna; cluster analysis; gene expression; embryo; protein; rna, small interfering; morphogen; drosophila; rna binding protein; gene expression regulation; embryo, nonmammalian; gene expression regulation, developmental; rna-binding proteins; messenger rna; rna, messenger; gene repression; rna translation; cytoplasm; fly; 3' untranslated region; drosophila melanogaster; rna stability; developmental disorder; repressor proteins; argonaute protein; drosophila proteins; mothers; cell organelle; ribonucleases; piwi interacting rna; transposon; 3' untranslated regions; chemical modification; rna degradation; aubergine protein; ccr4 protein; nanos protein; not protein; smaug protein; biodegradation; stabilization; deadenylation; zygote; dna transposable elements; peptide initiation factors; polyadenylation; solanum melongena |
| Journal Title: | Nature |
| Volume: | 467 |
| Issue: | 7319 |
| ISSN: | 0028-0836 |
| Publisher: | Nature Publishing Group |
| Date Published: | 2010-10-28 |
| Start Page: | 1128 |
| End Page: | 1132 |
| Language: | English |
| DOI: | 10.1038/nature09465 |
| PUBMED: | 20953170 |
| PROVIDER: | scopus |
| PMCID: | PMC4505748 |
| DOI/URL: | |
| Notes: | --- - "Cited By (since 1996): 7" - "Export Date: 20 April 2011" - "CODEN: NATUA" - "Source: Scopus" |
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