Publication Date:
2016-03-08
Description:
The conserved Piwi family of proteins and piwi-interacting RNAs (piRNAs) have a central role in genomic stability, which is inextricably linked to germ-cell formation, by forming Piwi ribonucleoproteins (piRNPs) that silence transposable elements. In Drosophila melanogaster and other animals, primordial germ-cell specification in the developing embryo is driven by maternal messenger RNAs and proteins that assemble into specialized messenger ribonucleoproteins (mRNPs) localized in the germ (pole) plasm at the posterior of the oocyte. Maternal piRNPs, especially those loaded on the Piwi protein Aubergine (Aub), are transmitted to the germ plasm to initiate transposon silencing in the offspring germ line. The transport of mRNAs to the oocyte by midoogenesis is an active, microtubule-dependent process; mRNAs necessary for primordial germ-cell formation are enriched in the germ plasm at late oogenesis via a diffusion and entrapment mechanism, the molecular identity of which remains unknown. Aub is a central component of germ granule RNPs, which house mRNAs in the germ plasm, and interactions between Aub and Tudor are essential for the formation of germ granules. Here we show that Aub-loaded piRNAs use partial base-pairing characteristics of Argonaute RNPs to bind mRNAs randomly in Drosophila, acting as an adhesive trap that captures mRNAs in the germ plasm, in a Tudor-dependent manner. Notably, germ plasm mRNAs in drosophilids are generally longer and more abundant than other mRNAs, suggesting that they provide more target sites for piRNAs to promote their preferential tethering in germ granules. Thus, complexes containing Tudor, Aub piRNPs and mRNAs couple piRNA inheritance with germline specification. Our findings reveal an unexpected function for piRNP complexes in mRNA trapping that may be generally relevant to the function of animal germ granules.〈br /〉〈br /〉〈a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4795963/" target="_blank"〉〈img src="https://static.pubmed.gov/portal/portal3rc.fcgi/4089621/img/3977009" border="0"〉〈/a〉 〈a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4795963/" target="_blank"〉This paper as free author manuscript - peer-reviewed and accepted for publication〈/a〉〈br /〉〈br /〉〈span class="detail_caption"〉Notes: 〈/span〉Vourekas, Anastassios -- Alexiou, Panagiotis -- Vrettos, Nicholas -- Maragkakis, Manolis -- Mourelatos, Zissimos -- GM072777/GM/NIGMS NIH HHS/ -- R01 GM072777/GM/NIGMS NIH HHS/ -- England -- Nature. 2016 Mar 17;531(7594):390-4. doi: 10.1038/nature17150. Epub 2016 Mar 7.〈br /〉〈span class="detail_caption"〉Author address: 〈/span〉Department of Pathology and Laboratory Medicine, Division of Neuropathology, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine; PENN Genome Frontiers Institute, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.〈br /〉〈span class="detail_caption"〉Record origin:〈/span〉 〈a href="http://www.ncbi.nlm.nih.gov/pubmed/26950602" target="_blank"〉PubMed〈/a〉
Keywords:
Animals
;
Argonaute Proteins/metabolism
;
Base Pairing
;
Binding Sites
;
Cytoplasm/*genetics/*metabolism
;
DNA Transposable Elements/genetics
;
Diffusion
;
Drosophila Proteins/metabolism
;
Drosophila melanogaster/cytology/*genetics/metabolism
;
Female
;
Male
;
Membrane Transport Proteins/metabolism
;
Oocytes/*cytology/metabolism
;
Oogenesis
;
Peptide Initiation Factors/metabolism
;
RNA Interference
;
*RNA Transport
;
RNA, Messenger/chemistry/*genetics/metabolism
;
RNA, Small Interfering/chemistry/*genetics/metabolism
;
Ribonucleoproteins/metabolism
;
Transcriptome/genetics
Print ISSN:
0028-0836
Electronic ISSN:
1476-4687
Topics:
Biology
,
Chemistry and Pharmacology
,
Medicine
,
Natural Sciences in General
,
Physics
