A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila

Saito, Kuniaki; Inagaki, Sachi; Mituyama, Toutai; Kawamura, Yuta; Ono, Yukiteru; Sakota, Eri; Kotani, Hazuki; Asai, Kiyoshi; Siomi, Haruhiko; Siomi, Mikiko C.

doi:10.1038/nature08501

Cited by 411 publications

(570 citation statements)

References 29 publications

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“…For a subset of PRMRs whose proteins are needed at later stages, their mRNAs could be transcribed at an earlier time point and are stabilized by the formation of a senseantisense duplex, and this phenomenon is more popular at post-meiotic stages than early ones. Whether MRPRs themselves have regulatory function during spermatogenesis remains as an open question, although some indication has been reported (Saito et al 2009). …”

Section: Discussionmentioning

confidence: 99%

piRNA profiling during specific stages of mouse spermatogenesis

Gan

Lin²,

Zhang³

et al. 2011

RNA

111

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PIWI-interacting RNAs (piRNAs) are a class of small RNAs abundantly expressed in animal gonads. piRNAs that map to retrotransposons are generated by a ''ping-pong'' amplification loop to suppress the activity of retrotransposons. However, the biogenesis and function of other categories of piRNAs have yet to be investigated. In this study, we first profiled the expression of small RNAs in type A spermatogonia, pachytene spermatocytes, and round spermatids by deep sequencing. We then focused on the computational analysis of the potential piRNAs generated in the present study as well as other published sets. piRNAs mapping to retrotransposons, mRNAs, and intergenic regions had different length distributions and were differentially regulated in spermatogenesis. piRNA-generating mRNAs (PRMRs), whose expression positively correlated with their piRNA products, constituted one-third of the protein-coding genes and were evolutionarily conserved and enriched with splicing isoforms and antisense transcripts. PRMRs with piRNAs preferentially mapped to CDSs and 39 UTRs partitioned into three clusters differentially expressed during spermatogenesis and enriched with unique sets of functional annotation terms related to housekeeping activities as well as spermatogenesis-specific processes. Intergenic piRNAs were divided into 2992 clusters probably representing novel transcriptional units that have not been reported. The transcripts of a large number of genes involved in spermatogenesis are the precursors of piRNAs, and these genes are intricately regulated by alternative splicing and antisense transcripts. piRNAs, whose regulatory role in gene expression awaits to be identified, are clearly products of a novel regulatory process that needs to be defined.

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Section: Discussionmentioning

confidence: 99%

piRNA profiling during specific stages of mouse spermatogenesis

Gan

Lin²,

Zhang³

et al. 2011

RNA

111

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“…In the Drosophila melanogaster female gonad, two distinct piRNA pathways have been identified that drive transposon silencing in the germ line and the soma, respectively (13)(14)(15). In the germ line, piRNA biogenesis involves both primary processing and a secondary amplification pathway (ping-pong amplification) (8,9,16), whereas piRNAs in the soma are generated solely from primary transcripts (primary pathway) (14,15,17).…”

mentioning

confidence: 99%

“…In the germ line, piRNA biogenesis involves both primary processing and a secondary amplification pathway (ping-pong amplification) (8,9,16), whereas piRNAs in the soma are generated solely from primary transcripts (primary pathway) (14,15,17).…”

mentioning

confidence: 99%

“…Although Aub and AGO3 are restricted to the germ-line cytoplasm, Piwi localizes predominantly in the nucleus, while still present in the cytoplasm of both the germ line and the ovarian soma (8,10,23). Correspondingly, Piwi appears to be a key component of both germ line and somatic piRNA pathways (14,15). Aub and AGO3 are the enzymes that generate the 5′ end of secondary piRNAs (8,9).…”

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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.

216

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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“…Primary piRNA processing has been reported in a Drosophila ovarian somatic cell line where Piwi, but not Aub or AGO3, is expressed Saito et al 2009). The genomic loci for these ovarian somatic cell piRNAs are flamenco and traffic jam (tj), a large Maf gene (Saito et al 2009).…”

Section: Introductionmentioning

confidence: 99%

Identification of piRNAs in the central nervous system

Lee¹,

Banerjee²,

Zhou³

et al. 2011

RNA

259

290

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Piwi-interacting RNAs (piRNAs) are small noncoding RNAs generated by a conserved pathway. Their most widely studied function involves restricting transposable elements, particularly in the germline, where piRNAs are highly abundant. Increasingly, another set of piRNAs derived from intergenic regions appears to have a role in the regulation of mRNA from early embryos and gonads. We report a more widespread expression of a limited set of piRNAs and particularly focus on their expression in the hippocampus. Deep sequencing of extracted RNA from the mouse hippocampus revealed a set of small RNAs in the size range of piRNAs. These were confirmed by their presence in the piRNA database as well as coimmunoprecipitation with MIWI. Their expression was validated by Northern blot and in situ hybridization in cultured hippocampal neurons, where signal from one piRNA extended to the dendritic compartment. Antisense suppression of this piRNA suggested a role in spine morphogenesis. Possible targets include genes, which control spine shape by a distinctive mechanism in comparison to microRNAs.

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A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila

Cited by 411 publications

References 29 publications

piRNA profiling during specific stages of mouse spermatogenesis

piRNA profiling during specific stages of mouse spermatogenesis

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

Identification of piRNAs in the central nervous system

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