Adaptation to P Element Transposon Invasion in Drosophila melanogaster

Khurana, Jaspreet S.; Wang, Jie; Xu, Jia; Koppetsch, Birgit S.; Thomson, Travis; Nowosielska, Anetta; Li, Chengjian; Zamore, Phillip D.; Weng, Zhiping; Theurkauf, William E.

doi:10.1016/j.cell.2011.11.042

Cited by 235 publications

(308 citation statements)

References 58 publications

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“…When higher amounts of piRNAs are maternally deposited, as in the R H lineage described here, almost full repression can be reached in the first generation (SF H females). Note however that, as recently reported (Khurana et al 2011), P-M dysgenic females, lacking any P-element piRNA can, at the end of their life, produce enough piRNAs to completely repress their P-elements.…”

Section: Discussionsupporting

confidence: 59%

“…1). Khurana et al (2011) have recently described another kind of ancestor aging memory in the P-M hybrid dysgenesis system, which is based on the mobilization of resident functional elements like the Ivk-element into piRNA clusters in aged dysgenic female ovaries. However, the P-M dysgenic aging effect is not reversible and leads to de novo piRNA production in the progeny of aged females in contrast to the piRNA-dependent aging memory here described.…”

Section: Discussionmentioning

confidence: 99%

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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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Section: Discussionsupporting

confidence: 59%

Section: Discussionmentioning

confidence: 99%

piRNA-mediated transgenerational inheritance of an acquired trait

et al. 2012

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“…et al 2011). It has been proposed that piRNA clusters may serve as a trap for new retrotransposon copies (Girard and Hannon 2008;Khurana et al 2011), thus providing an opportunity for the host cells to generate piRNAs with sequences identical to, or most similar to, the active copies. Our knock-in insertion of EGFP-neo into a piRNA cluster mimicked a retrotransposon insertion, and the resulting piRNA generation and silencing of the reporter genes support this hypothesis.…”

Section: Discussionmentioning

confidence: 99%

Targeted gene silencing in mouse germ cells by insertion of a homologous DNA into a piRNA generating locus

et al. 2012

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In germ cells, early embryos, and stem cells of animals, PIWI-interacting RNAs (piRNAs) have an important role in silencing retrotransposons, which are vicious genomic parasites, through transcriptional and post-transcriptional mechanisms. To examine whether the piRNA pathway can be used to silence genes of interest in germ cells, we have generated knock-in mice in which a foreign DNA fragment was inserted into a region generating pachytene piRNAs. The knock-in sequence was transcribed, and the resulting RNA was processed to yield piRNAs in postnatal testes. When reporter genes possessing a sequence complementary to portions of the knock-in sequence were introduced, they were greatly repressed after the time of pachytene piRNA generation. This repression mainly occurred at the post-transcriptional level, as degradation of the reporter RNAs was accelerated. Our results show that the piRNA pathway can be used as a tool for sequence-specific gene silencing in germ cells and support the idea that the piRNA generating regions serve as traps for retrotransposons, enabling the host cell to generate piRNAs against active retrotransposons.

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“…However, when new transposons are acquired by the piRNA cluster, new inserts either tansposition into the cluster randomly or with a preference for the loci, but do not integrate in any specific logical sequence. Because of the randomness associated with new additions to piRNA clusters, adaption into pRNA clusters is less efficient than adaption into CRISPR loci [80].…”

Section: Differences In Crispr-cas and Pirnamentioning

confidence: 99%

“…PiRNAs function to control the gene expression of the host, through mRNA regulation, histone modification direction, and chromatin structures [80]. PiRNA performs these functions independently of its role in transposon silencing.…”

Section: Differences In Crispr-cas and Pirnamentioning

confidence: 99%

Diversity, evolution, and therapeutic applications of small RNAs in prokaryotic and eukaryotic immune systems

Cooper

Overstreet

2014

Physics of Life Reviews

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Recent evidence supports that prokaryotes exhibit adaptive immunity in the form of CRISPR (Clustered Regularly Interspersed Short Palindromic Repeats) and Cas (CRISPR associated proteins). The CRISPR-Cas system confers resistance to exogenous genetic elements such as phages and plasmids by allowing for the recognition and silencing of these genetic elements. Moreover, CRISPR-Cas serves as a memory of past exposures. This suggests that the evolution of the immune system has counterparts among the prokaryotes, not exclusively among eukaryotes. Mathematical models have been proposed which simulate the evolutionary patterns of CRISPR, however large gaps in our understanding of CRISPR-Cas function and evolution still exist. The CRISPR-Cas system is analogous to small RNAs involved in resistance mechanisms throughout the tree of life, and a deeper understanding of the evolution of small RNA pathways is necessary before the relationship between these convergent systems is to be determined. Presented in this review are novel RNAi therapies based on CRISPR-Cas analogs and the potential for future therapies based on CRISPR-Cas system components.

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Adaptation to P Element Transposon Invasion in Drosophila melanogaster

Cited by 235 publications

References 58 publications

piRNA-mediated transgenerational inheritance of an acquired trait

piRNA-mediated transgenerational inheritance of an acquired trait

Targeted gene silencing in mouse germ cells by insertion of a homologous DNA into a piRNA generating locus

Diversity, evolution, and therapeutic applications of small RNAs in prokaryotic and eukaryotic immune systems

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