A satellite repeat-derived piRNA controls embryonic development of Aedes

Halbach, Rebecca; Miesen, Pascal; Joosten, Joep; Taşköprü, Ezgi; Rondeel, Inge; Pennings, Bas; Vogels, Chantal B.F.; Merkling, Sarah H.; Koenraadt, Constantianus J. M.; Lambrechts, Louis; Rij, Ronald P. van

doi:10.1038/s41586-020-2159-2

Cited by 83 publications

(125 citation statements)

References 89 publications

(149 reference statements)

Supporting

Mentioning

116

Contrasting

Order By: Relevance

“…Samples were resolved on 10% polyacrylamide gels and blotted to nitrocellulose membranes. The following antibodies, generated in our laboratory, were used for western blotting: rabbit-anti-Ago3, -Piwi4, -Piwi5 and -Piwi6 (all at 1:500) (34,58). Figure 3A.…”

Section: Co-immunoprecipitation and Western Blotmentioning

confidence: 99%

“…Size preferences of somatically expressed PIWI proteinsSize distribution of piRNA-sized (24-33 nt) small RNA reads in Ago3-(A), Piwi4-(B), Piwi5-(C), and Piwi6-IP (D) sequencing libraries. Piwi4-IP is dominated by two very abundantly expressed piRNAs (tapiR1/2-30 and 29 nt in size, respectively), that are involved in the degradation of maternally provided transcripts during embryonic development in mosquitoes(58). Counts are raw, unmapped reads from our previously published data(34,58).…”

mentioning

confidence: 99%

See 1 more Smart Citation

Endogenous piRNA-guided slicing triggers responder and trailer piRNA production from viral RNA inAedes aegyptimosquitoes

Joosten

Overheul

Rij

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

ABSTRACTPIWI interacting (pi)RNAs are small RNAs mostly known to protect the genomes of animal germlines against transposable elements. In Drosophila, piRNA-mediated cleavage of transposon RNA triggers the release of a responder piRNAs via the ping-pong amplification cycle. Responder piRNA 3’ end formation by the endonuclease Zucchini is coupled to the production of downstream trailer piRNAs, expanding the repertoire of piRNAs that target transposons. Intriguingly, in Aedes aegypti mosquitoes, somatic piRNAs are produced from viral RNA, implying a role of viral (v)piRNAs in antiviral immunity. Knowledge on how vpiRNA 3’ ends are formed and whether viral RNA is subjected to trailer piRNA production, however, is lacking. To address these questions, we analyzed small RNA sequencing libraries from Ae. aegypti cells. We found that virus- and transposon-derived piRNAs have sharply defined 3’ ends, and that uridine residues are enriched directly downstream of dominant piRNA sequences, both of which are characteristic features of Zucchini-like cleavage of precursor piRNAs. Next, we designed a piRNA reporter system based on Sindbis virus recombinants that harbor target sites for abundant endogenous piRNAs. These piRNAs guide cleavage of the viral RNA, which is subsequently processed into abundant responder piRNAs. Using this reporter virus system, we identified the Ae. aegypti orthologs of Zucchini, which is required for sharp 3’ end formation of responder piRNAs, and Nibbler, a 3’-5’ exonuclease involved in the trimming of a subset of piRNAs and miRNAs. Furthermore, we found that cleavage of viral RNA triggers the production of trailer piRNAs, thus expanding the piRNA sequence pool that is able to target viral RNA. Our results have important implications for understanding how autonomous piRNA production from viral RNA can be triggered by just a few cleavage events by genome-encoded piRNAs.

show abstract

Section: Co-immunoprecipitation and Western Blotmentioning

confidence: 99%

mentioning

confidence: 99%

Endogenous piRNA-guided slicing triggers responder and trailer piRNA production from viral RNA inAedes aegyptimosquitoes

Joosten

Overheul

Rij

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Although some Drosophila piRNAs have been suggested to regulate embryonic development by degrading maternally deposited transcripts in the zygote which has also now been observed in Ae. aegypti [ 96 , 97 , 98 , 99 ], more of the Ae. aegypti piRNAs have been mapped to protein-coding genes abundantly expressed in the soma [ 100 , 101 ].…”

Section: Genome Transposon Composition and Germline Specificity Ofmentioning

confidence: 99%

“…aegypti discussed a mosquito piRNA cluster analogous to the Drosophila flamenco cluster [ 137 ], but we believe greater insight into mosquito piRNA cluster evolution is gained through multiple-species comparisons that include piRNAs from Cu. quinquefasciatus [ 46 , 96 ].…”

Section: The Pirna Clusters Of Drosophila and Cmentioning

confidence: 99%

“…For example, cross-species piRNA cluster comparisons lead to the discovery of a conserved piRNA Cluster Locus (piRCL) composed of satellite DNA repeats in culicine mosquitoes [ 46 , 96 ]. Among the major anopheline and culicine mosquitoes, this piRCL is found near two genes of unknown function ( Figure 3 B(iii)) and did not appear to be restricted to any tissue or cell type [ 46 ].…”

Section: The Pirna Clusters Of Drosophila and Cmentioning

confidence: 99%

See 1 more Smart Citation

Diverse Defenses: A Perspective Comparing Dipteran Piwi-piRNA Pathways

Gamez

Srivastav

Akbari

et al. 2020

Cells

View full text Add to dashboard Cite

Animals face the dual threat of virus infections hijacking cellular function and transposons proliferating in germline genomes. For insects, the deeply conserved RNA interference (RNAi) pathways and other chromatin regulators provide an important line of defense against both viruses and transposons. For example, this innate immune system displays adaptiveness to new invasions by generating cognate small RNAs for targeting gene silencing measures against the viral and genomic intruders. However, within the Dipteran clade of insects, Drosophilid fruit flies and Culicids mosquitoes have evolved several unique mechanistic aspects of their RNAi defenses to combat invading transposons and viruses, with the Piwi-piRNA arm of the RNAi pathways showing the greatest degree of novel evolution. Whereas central features of Piwi-piRNA pathways are conserved between Drosophilids and Culicids, multiple lineage-specific innovations have arisen that may reflect distinct genome composition differences and specific ecological and physiological features dividing these two branches of Dipterans. This perspective review focuses on the most recent findings illuminating the Piwi/piRNA pathway distinctions between fruit flies and mosquitoes, and raises open questions that need to be addressed in order to ameliorate human diseases caused by pathogenic viruses that mosquitoes transmit as vectors.

show abstract

Small RNAs in epigenetic inheritance: from mechanisms to trait transmission

Cecere

2021

FEBS Letters

View full text Add to dashboard Cite

Inherited information is transmitted to progeny primarily by the genome through the gametes. However, in recent years, epigenetic inheritance has been demonstrated in several organisms, including animals. Although it is clear that certain post-translational histone modifications, DNA methylation, and noncoding RNAs regulate epigenetic inheritance, the molecular mechanisms responsible for epigenetic inheritance are incompletely understood. This review focuses on the role of small RNAs in transmitting epigenetic information across generations in animals. Examples of documented cases of transgenerational epigenetic inheritance are discussed, from the silencing of transgenes to the inheritance of complex traits, such as fertility, stress responses, infections, and behavior. Experimental evidence supporting the idea that small RNAs are epigenetic molecules capable of transmitting traits across generations is highlighted, focusing on the mechanisms by which small RNAs achieve such a function. Just as the role of small RNAs in epigenetic processes is redefining the concept of inheritance, so too our understanding of the molecular pathways and mechanisms that govern epigenetic inheritance in animals is radically changing.

show abstract

A satellite repeat-derived piRNA controls embryonic development of Aedes

Cited by 83 publications

References 89 publications

Endogenous piRNA-guided slicing triggers responder and trailer piRNA production from viral RNA inAedes aegyptimosquitoes

Endogenous piRNA-guided slicing triggers responder and trailer piRNA production from viral RNA inAedes aegyptimosquitoes

Diverse Defenses: A Perspective Comparing Dipteran Piwi-piRNA Pathways

Small RNAs in epigenetic inheritance: from mechanisms to trait transmission

Contact Info

Product

Resources

About