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Daedalus and Gasz recruit Armitage to mitochondria, bringing piRNA precursors to the biogenesis machinery

The Piwi-interacting RNA (piRNA) pathway is a small RNA-based immune system that silences mobile genetic elements in animal germlines. piRNA biogenesis requires a specialized machinery that converts long single-stranded precursors into small RNAs of ∼25-nucleotides in length. This process involves f...

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Autores principales: Munafò, Marzia, Manelli, Vera, Falconio, Federica A., Sawle, Ashley, Kneuss, Emma, Eastwood, Evelyn L., Seah, Jun Wen Eugene, Czech, Benjamin, Hannon, Gregory J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6601507/
https://www.ncbi.nlm.nih.gov/pubmed/31123065
http://dx.doi.org/10.1101/gad.325662.119
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author Munafò, Marzia
Manelli, Vera
Falconio, Federica A.
Sawle, Ashley
Kneuss, Emma
Eastwood, Evelyn L.
Seah, Jun Wen Eugene
Czech, Benjamin
Hannon, Gregory J.
author_facet Munafò, Marzia
Manelli, Vera
Falconio, Federica A.
Sawle, Ashley
Kneuss, Emma
Eastwood, Evelyn L.
Seah, Jun Wen Eugene
Czech, Benjamin
Hannon, Gregory J.
author_sort Munafò, Marzia
collection PubMed
description The Piwi-interacting RNA (piRNA) pathway is a small RNA-based immune system that silences mobile genetic elements in animal germlines. piRNA biogenesis requires a specialized machinery that converts long single-stranded precursors into small RNAs of ∼25-nucleotides in length. This process involves factors that operate in two different subcellular compartments: the nuage/Yb body and mitochondria. How these two sites communicate to achieve accurate substrate selection and efficient processing remains unclear. Here, we investigate a previously uncharacterized piRNA biogenesis factor, Daedalus (Daed), that is located on the outer mitochondrial membrane. Daed is essential for Zucchini-mediated piRNA production and the correct localization of the indispensable piRNA biogenesis factor Armitage (Armi). We found that Gasz and Daed interact with each other and likely provide a mitochondrial “anchoring platform” to ensure that Armi is held in place, proximal to Zucchini, during piRNA processing. Our data suggest that Armi initially identifies piRNA precursors in nuage/Yb bodies in a manner that depends on Piwi and then moves to mitochondria to present precursors to the mitochondrial biogenesis machinery. These results represent a significant step in understanding a critical aspect of transposon silencing; namely, how RNAs are chosen to instruct the piRNA machinery in the nature of its silencing targets.
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spelling pubmed-66015072019-07-18 Daedalus and Gasz recruit Armitage to mitochondria, bringing piRNA precursors to the biogenesis machinery Munafò, Marzia Manelli, Vera Falconio, Federica A. Sawle, Ashley Kneuss, Emma Eastwood, Evelyn L. Seah, Jun Wen Eugene Czech, Benjamin Hannon, Gregory J. Genes Dev Research Paper The Piwi-interacting RNA (piRNA) pathway is a small RNA-based immune system that silences mobile genetic elements in animal germlines. piRNA biogenesis requires a specialized machinery that converts long single-stranded precursors into small RNAs of ∼25-nucleotides in length. This process involves factors that operate in two different subcellular compartments: the nuage/Yb body and mitochondria. How these two sites communicate to achieve accurate substrate selection and efficient processing remains unclear. Here, we investigate a previously uncharacterized piRNA biogenesis factor, Daedalus (Daed), that is located on the outer mitochondrial membrane. Daed is essential for Zucchini-mediated piRNA production and the correct localization of the indispensable piRNA biogenesis factor Armitage (Armi). We found that Gasz and Daed interact with each other and likely provide a mitochondrial “anchoring platform” to ensure that Armi is held in place, proximal to Zucchini, during piRNA processing. Our data suggest that Armi initially identifies piRNA precursors in nuage/Yb bodies in a manner that depends on Piwi and then moves to mitochondria to present precursors to the mitochondrial biogenesis machinery. These results represent a significant step in understanding a critical aspect of transposon silencing; namely, how RNAs are chosen to instruct the piRNA machinery in the nature of its silencing targets. Cold Spring Harbor Laboratory Press 2019-07-01 /pmc/articles/PMC6601507/ /pubmed/31123065 http://dx.doi.org/10.1101/gad.325662.119 Text en © 2019 Munafò et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/4.0/ This article, published in Genes & Development, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
spellingShingle Research Paper
Munafò, Marzia
Manelli, Vera
Falconio, Federica A.
Sawle, Ashley
Kneuss, Emma
Eastwood, Evelyn L.
Seah, Jun Wen Eugene
Czech, Benjamin
Hannon, Gregory J.
Daedalus and Gasz recruit Armitage to mitochondria, bringing piRNA precursors to the biogenesis machinery
title Daedalus and Gasz recruit Armitage to mitochondria, bringing piRNA precursors to the biogenesis machinery
title_full Daedalus and Gasz recruit Armitage to mitochondria, bringing piRNA precursors to the biogenesis machinery
title_fullStr Daedalus and Gasz recruit Armitage to mitochondria, bringing piRNA precursors to the biogenesis machinery
title_full_unstemmed Daedalus and Gasz recruit Armitage to mitochondria, bringing piRNA precursors to the biogenesis machinery
title_short Daedalus and Gasz recruit Armitage to mitochondria, bringing piRNA precursors to the biogenesis machinery
title_sort daedalus and gasz recruit armitage to mitochondria, bringing pirna precursors to the biogenesis machinery
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6601507/
https://www.ncbi.nlm.nih.gov/pubmed/31123065
http://dx.doi.org/10.1101/gad.325662.119
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