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A novel organelle, the piNG-body, in the nuage of Drosophila male germ cells is associated with piRNA-mediated gene silencing.

ABSTRACT: Proteins of the PIWI subfamily Aub and AGO3 associated with the germline-specific perinuclear granules (nuage) are involved in the silencing of retrotransposons and other selfish repetitive elements in the Drosophila genome. PIWI proteins and their 25- to 30-nt PIWI-interacting RNA (piRNAs) are considered as key participants of the piRNA pathway. Using immunostaining, we found a large, nuage-associated organelle in the testes, the piNG-body (piRNA nuage giant body), which was significantly more massive than an ordinary nuage granule. This body contains known ovarian nuage proteins, including Vasa, Aub, AGO3, Tud, Spn-E, Bel, Squ, and Cuff, as well as AGO1, the key component of the microRNA pathway. piNG-bodies emerge at the primary spermatocyte stage of spermatogenesis during the period of active transcription. Aub, Vasa, and Tud are located at the periphery of the piNG-body, whereas AGO3 is found in its core. Mutational analysis revealed that Vasa, Aub, and AGO3 were crucial for both the maintenance of the piNG-body structure and the silencing of selfish Stellate repeats. The piNG-body destruction caused by csul mutations that abolish specific posttranslational symmetrical arginine methylation of PIWI proteins is accompanied by strong derepression of Stellate genes known to be silenced via the piRNA pathway.

SUBMITTER: Kibanov MV

PROVIDER: S-EPMC3172265 | biostudies-literature | 2011 Sep

REPOSITORIES: biostudies-literature

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A novel organelle, the piNG-body, in the nuage of Drosophila male germ cells is associated with piRNA-mediated gene silencing.

Kibanov Mikhail V MV Egorova Ksenia S KS Ryazansky Sergei S SS Sokolova Olesia A OA Kotov Alexei A AA Olenkina Oxana M OM Stolyarenko Anastasia D AD Gvozdev Vladimir A VA Olenina Ludmila V LV

Molecular biology of the cell 20110720 18

Proteins of the PIWI subfamily Aub and AGO3 associated with the germline-specific perinuclear granules (nuage) are involved in the silencing of retrotransposons and other selfish repetitive elements in the Drosophila genome. PIWI proteins and their 25- to 30-nt PIWI-interacting RNA (piRNAs) are considered as key participants of the piRNA pathway. Using immunostaining, we found a large, nuage-associated organelle in the testes, the piNG-body (piRNA nuage giant body), which was significantly more ...[more]

PMID: 21775629

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Project description:The piwi-interacting RNAs (piRNA) are small RNAs that target selfish transposable elements (TEs) in many animal genomes. Until now, piRNAs' role in TE population dynamics has only been discussed in the context of their suppression of TE transposition, which alone is not sufficient to account for the skewed frequency spectrum and stable containment of TEs. On the other hand, euchromatic TEs can be epigenetically silenced via piRNA-dependent heterochromatin formation and, similar to the widely known "Position-effect variegation", heterochromatin induced by TEs can "spread" into nearby genes. We hypothesized that the piRNA-mediated spread of heterochromatin from TEs into adjacent genes has deleterious functional effects and leads to selection against individual TEs. Unlike previously identified deleterious effects of TEs due to the physical disruption of DNA, the functional effect we investigated here is mediated through the epigenetic influences of TEs. We found that the repressive chromatin mark, H3K9me, is elevated in sequences adjacent to euchromatic TEs at multiple developmental stages in Drosophila melanogaster. Furthermore, the heterochromatic states of genes depend not only on the number of and distance from adjacent TEs, but also on the likelihood that their nearest TEs are targeted by piRNAs. These variations in chromatin status probably have functional consequences, causing genes near TEs to have lower expression. Importantly, we found stronger selection against TEs that lead to higher H3K9me enrichment of adjacent genes, demonstrating the pervasive evolutionary consequences of TE-induced epigenetic silencing. Because of the intrinsic biological mechanism of piRNA amplification, spread of TE heterochromatin could result in the theoretically required synergistic deleterious effects of TE insertions for stable containment of TE copy number. The indirect deleterious impact of piRNA-mediated epigenetic silencing of TEs is a previously unexplored, yet important, element for the evolutionary dynamics of TEs.

Dataset Information

A novel organelle, the piNG-body, in the nuage of Drosophila male germ cells is associated with piRNA-mediated gene silencing.

Publications

A novel organelle, the piNG-body, in the nuage of Drosophila male germ cells is associated with piRNA-mediated gene silencing.

Similar Datasets

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