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AGO3 Slicer activity regulates mitochondria–nuage localization of Armitage and piRNA amplification

In Drosophila melanogaster the reciprocal “Ping-Pong” cycle of PIWI-interacting RNA (piRNA)–directed RNA cleavage catalyzed by the endonuclease (or “Slicer”) activities of the PIWI proteins Aubergine (Aub) and Argonaute3 (AGO3) has been proposed to expand the secondary piRNA population. However, the...

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Autores principales: Huang, Haidong, Li, Yujing, Szulwach, Keith E., Zhang, Guoqiang, Jin, Peng, Chen, Dahua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Rockefeller University Press 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4107788/
https://www.ncbi.nlm.nih.gov/pubmed/25049272
http://dx.doi.org/10.1083/jcb.201401002
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author Huang, Haidong
Li, Yujing
Szulwach, Keith E.
Zhang, Guoqiang
Jin, Peng
Chen, Dahua
author_facet Huang, Haidong
Li, Yujing
Szulwach, Keith E.
Zhang, Guoqiang
Jin, Peng
Chen, Dahua
author_sort Huang, Haidong
collection PubMed
description In Drosophila melanogaster the reciprocal “Ping-Pong” cycle of PIWI-interacting RNA (piRNA)–directed RNA cleavage catalyzed by the endonuclease (or “Slicer”) activities of the PIWI proteins Aubergine (Aub) and Argonaute3 (AGO3) has been proposed to expand the secondary piRNA population. However, the role of AGO3/Aub Slicer activity in piRNA amplification remains to be explored. We show that AGO3 Slicer activity is essential for piRNA amplification and that AGO3 inhibits the homotypic Aub:Aub Ping-Pong process in a Slicer-independent manner. We also find that expression of an AGO3 Slicer mutant causes ectopic accumulation of Armitage, a key component in the primary piRNA pathway, in the Drosophila melanogaster germline granules known as nuage. AGO3 also coexists and interacts with Armitage in the mitochondrial fraction. Furthermore, AGO3 acts in conjunction with the mitochondria-associated protein Zucchini to control the dynamic subcellular localization of Armitage between mitochondria and nuage in a Slicer-dependent fashion. Collectively, our findings uncover a new mechanism that couples mitochondria with nuage to regulate secondary piRNA amplification.
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spelling pubmed-41077882015-01-21 AGO3 Slicer activity regulates mitochondria–nuage localization of Armitage and piRNA amplification Huang, Haidong Li, Yujing Szulwach, Keith E. Zhang, Guoqiang Jin, Peng Chen, Dahua J Cell Biol Research Articles In Drosophila melanogaster the reciprocal “Ping-Pong” cycle of PIWI-interacting RNA (piRNA)–directed RNA cleavage catalyzed by the endonuclease (or “Slicer”) activities of the PIWI proteins Aubergine (Aub) and Argonaute3 (AGO3) has been proposed to expand the secondary piRNA population. However, the role of AGO3/Aub Slicer activity in piRNA amplification remains to be explored. We show that AGO3 Slicer activity is essential for piRNA amplification and that AGO3 inhibits the homotypic Aub:Aub Ping-Pong process in a Slicer-independent manner. We also find that expression of an AGO3 Slicer mutant causes ectopic accumulation of Armitage, a key component in the primary piRNA pathway, in the Drosophila melanogaster germline granules known as nuage. AGO3 also coexists and interacts with Armitage in the mitochondrial fraction. Furthermore, AGO3 acts in conjunction with the mitochondria-associated protein Zucchini to control the dynamic subcellular localization of Armitage between mitochondria and nuage in a Slicer-dependent fashion. Collectively, our findings uncover a new mechanism that couples mitochondria with nuage to regulate secondary piRNA amplification. The Rockefeller University Press 2014-07-21 /pmc/articles/PMC4107788/ /pubmed/25049272 http://dx.doi.org/10.1083/jcb.201401002 Text en © 2014 Huang et al. This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/).
spellingShingle Research Articles
Huang, Haidong
Li, Yujing
Szulwach, Keith E.
Zhang, Guoqiang
Jin, Peng
Chen, Dahua
AGO3 Slicer activity regulates mitochondria–nuage localization of Armitage and piRNA amplification
title AGO3 Slicer activity regulates mitochondria–nuage localization of Armitage and piRNA amplification
title_full AGO3 Slicer activity regulates mitochondria–nuage localization of Armitage and piRNA amplification
title_fullStr AGO3 Slicer activity regulates mitochondria–nuage localization of Armitage and piRNA amplification
title_full_unstemmed AGO3 Slicer activity regulates mitochondria–nuage localization of Armitage and piRNA amplification
title_short AGO3 Slicer activity regulates mitochondria–nuage localization of Armitage and piRNA amplification
title_sort ago3 slicer activity regulates mitochondria–nuage localization of armitage and pirna amplification
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4107788/
https://www.ncbi.nlm.nih.gov/pubmed/25049272
http://dx.doi.org/10.1083/jcb.201401002
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