The Drosophila HP1 Homolog Rhino Is Required for Transposon Silencing and piRNA Production by Dual-Strand Clusters

Klattenhoff, Carla Andrea; Xi, Hualin Simon; Li, Chengjian; Lee, Soohyun; Xu, Jia; Khurana, Jaspreet S.; Zhang, Fan; Schultz, Nadine; Koppetsch, Birgit S.; Nowosielska, Anetta; Seitz, Hervé; Zamore, Phillip D.; Weng, Zhiping; Theurkauf, William E.

doi:10.1016/j.cell.2009.07.014

Cited by 397 publications

(569 citation statements)

References 59 publications

(99 reference statements)

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“…Chromatin preparation was carried out as described (19). Sonication used a Branson sonifier with a microprobe at 100% duty cycle and output setting 2.…”

Section: Methodsmentioning

confidence: 99%

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Drosophila Piwi functions downstream of piRNA production mediating a chromatin-based transposon silencing mechanism in female germ line

Wang

Elgin

2011

Proc. Natl. Acad. Sci. U.S.A.

209

232

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Transposon control is a critical process during reproduction. The PIWI family proteins can play a key role, using a piRNA-mediated slicing mechanism to suppress transposon activity posttranscriptionally. In Drosophila melanogaster , Piwi is predominantly localized in the nucleus and has been implicated in heterochromatin formation. Here, we use female germ-line–specific depletion to study Piwi function. This depletion of Piwi leads to infertility and to axis specification defects in the developing egg chambers; correspondingly, widespread loss of transposon silencing is observed. Germ-line Piwi does not appear to be required for piRNA production. Instead, Piwi requires Aubergine (and presumably secondary piRNA) for proper localization. A subset of transposons that show significant overexpression in germ-line Piwi-depleted ovaries exhibit a corresponding loss of HP1a and H3K9me2. Germ-line HP1a depletion also leads to a loss of transposon silencing, demonstrating the functional requirement for HP1a enrichment at these loci. Considering our results and those of others, we infer that germ-line Piwi functions downstream of piRNA production to promote silencing of some transposons via recruitment of HP1a. Thus, in addition to its better-known function in posttranscriptional silencing, piRNA also appears to function in a targeting mechanism for heterochromatin formation mediated by Piwi.

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“…Chromatin preparation was carried out as described (19). Sonication used a Branson sonifier with a microprobe at 100% duty cycle and output setting 2.…”

Section: Methodsmentioning

confidence: 99%

“…Despite recent progress, the mechanisms used by piRNA to promote silencing are not clear; evidence supporting both transcriptional and posttranscriptional silencing mechanisms has been reported (10,(18)(19)(20)(21). The fly genome codes for three PIWI family argonaute proteins used in the piRNA pathways are Piwi, Aub, and AGO3 (22).…”

mentioning

confidence: 99%

Drosophila Piwi functions downstream of piRNA production mediating a chromatin-based transposon silencing mechanism in female germ line

Wang

Elgin

2011

Proc. Natl. Acad. Sci. U.S.A.

209

232

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“…The stimulation of secondary piRNA biosynthesis by maternal aging does not result from increased levels of I-element piRNA precursors Several chromatin-associated proteins were reported to modulate the efficiency of piRNA biogenesis in the Drosophila germline at the level of transcription and/ or processing of the heterochromatic RNA precursors (Klattenhoff et al 2009;Rangan et al 2011;Zamparini et al 2011). We therefore asked whether the increased production of secondary piRNAs and its maternal inheritance could be due to modulation of transcription or chromatin modifications of defective I-elements in R H 3d ovaries compared with R L 3d ovaries.…”

Section: Ping-pong Amplification Can Occur Between Defective I-elemenmentioning

confidence: 99%

piRNA-mediated transgenerational inheritance of an acquired trait

et al. 2012

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The maintenance of genome integrity is an essential trait to the successful transmission of genetic information. In animal germ cells, piRNAs guide PIWI proteins to silence transposable elements (TEs) in order to maintain genome integrity. In insects, most TE silencing in the germline is achieved by secondary piRNAs that are produced by a feed-forward loop (the pingpong cycle), which requires the piRNA-directed cleavage of two types of RNAs: mRNAs of functional euchromatic TEs and heterochromatic transcripts that contain defective TE sequences. The first cleavage that initiates such an amplification loop remains poorly understood. Taking advantage of the existence of strains that are devoid of functional copies of the LINE-like I-element, we report here that in such Drosophila ovaries, the initiation of a ping-pong cycle is exclusively achieved by secondary I-element piRNAs that are produced in the ovary and deposited in the embryonic germline. This unusual secondary piRNA biogenesis, detected in the absence of functional I-element copies, results from the processing of sense and antisense transcripts of several different defective I-element. Once acquired, for instance after ancestor aging, this capacity to produce heterochromatic-only secondary piRNAs is partially transmitted through generations via maternal piRNAs. Furthermore, such piRNAs acting as ping-pong initiators in a chromatin-independent manner confer to the progeny a high capacity to repress the I-element mobility. Our study explains, at the molecular level, the basis for epigenetic memory of maternal immunity that protects females from hybrid dysgenesis caused by transposition of paternally inherited functional I-element.

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“…Large-scale sequencing of piRNA populations has revealed that individual TE families have distinct patterns of sense and antisense piRNAs (20,26). To determine whether the right half of the 1360 element has a distinguishing piRNA distribution that could indicate key sites for silencing, we mapped the piRNA read density from wild-type (wt) ovary piRNA data generated by Li et al (20), against the 1360 copy present in our construct, 1360{}1503.…”

Section: -Sensitive Silencing Is Observed In a Subset Of Euchromaticmentioning

confidence: 99%

Ectopic assembly of heterochromatin in Drosophila melanogaster triggered by transposable elements

Sentmanat

Elgin

2012

Proc. Natl. Acad. Sci. U.S.A.

104

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A persistent question in biology is how cis-acting sequence elements influence trans-acting factors and the local chromatin environment to modulate gene expression. We reported previously that the DNA transposon 1360 can enhance silencing of a reporter in a heterochromatic domain of Drosophila melanogaster. We have now generated a collection of variegating phiC31 landingpad insertion lines containing 1360 and a heat-shock protein 70 (hsp70)-driven white reporter to explore the mechanism of 1360-sensitive silencing. Many 1360-sensitive sites were identified, some in apparently euchromatic domains, although all are close to heterochromatic masses. One such site (line 1198; insertion near the base of chromosome arm 2L) has been investigated in detail. ChIP analysis shows 1360-dependent Heterochromatin Protein 1a (HP1a) accumulation at this otherwise euchromatic site. The phiC31 landing pad system allows different 1360 constructs to be swapped with the full-length element at the same genomic site to identify the sequences that mediate 1360-sensitive silencing. Short deletions over sites with homology to PIWI-interacting RNAs (piRNAs) are sufficient to compromise 1360-sensitive silencing. Similar results were obtained on replacing 1360 with Invader4 (a retrotransposon), suggesting that this phenomenon likely applies to a broader set of transposable elements. Our results suggest a model in which piRNA sequence elements behave as cis-acting targets for heterochromatin assembly, likely in the early embryo, where piRNA pathway components are abundant, with the heterochromatic state subsequently propagated by chromatin modifiers present in somatic tissue.epigenetics | position-effect variegation T ransposable elements (TEs) are major structural features of nearly all eukaryotic genomes, and can play a role as cisacting regulatory features with profound influence over the gene regulatory networks of their host (1). However, if left unchecked, the deleterious effects of TE mobilization can become insurmountable for the system, damaging genome integrity. Thus, silencing mechanisms that prevent TE mobilization are fundamental to the faithful propagation of genetic information. Position-effect variegation (PEV), a mosaic expression pattern resulting from silencing in some cells that normally express a gene, has frequently been used as an indicator of heterochromatic environments (2, 3). We reported previously that the DNA transposon 1360 can enhance reporter silencing in repeat-rich heterochromatic regions (4). To gain insight into the mechanisms involved, we sought to identify sequence elements present in 1360 that contribute to 1360-sensitive PEV, using an adjacent heat-shock protein 70 (hsp70)-driven white gene as the reporter.We used the phiC31 landing pad system, where phiC31 integrase mediates recombination between a landing pad (inserted in the genome) containing phage attachment (attP) sites and a donor construct containing bacterial attachment (attB) sites (5). This system allows us to maintain a constant genomic cont...

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The Drosophila HP1 Homolog Rhino Is Required for Transposon Silencing and piRNA Production by Dual-Strand Clusters

Cited by 397 publications

References 59 publications

Drosophila Piwi functions downstream of piRNA production mediating a chromatin-based transposon silencing mechanism in female germ line

Drosophila Piwi functions downstream of piRNA production mediating a chromatin-based transposon silencing mechanism in female germ line

piRNA-mediated transgenerational inheritance of an acquired trait

Ectopic assembly of heterochromatin in Drosophila melanogaster triggered by transposable elements

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