A Novel Class of Somatic Small RNAs Similar to Germ Cell Pachytene PIWI-interacting Small RNAs

Ortogero, Nicole; Schuster, Andrew; Oliver, Daniel; Riordan, Connor R.; Hong, Annie; Hennig, Grant W.; Luong, Dickson; Bao, Jianqiang; Bhetwal, Bhupal P.; Ro, Seungil; McCarrey, John R.; Yan, Wei

doi:10.1074/jbc.m114.613232

Cited by 26 publications

(14 citation statements)

References 45 publications

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“…Pre-pachytene piRNAs are typically 26–28 nt in length and prefer uracil and adenine at their 1st and 10th nucleotides, respectively. The pachytene piRNAs, however, expressed after the pre-pachytene piRNAs, are typically 30 nt long and only have a preference for uracil at their first nucleotide [22]. The majority of the dysregulated piRNAs displayed pachytene piRNA characteristics, indicating that they originate during the later stages of spermatogenesis (Fig.…”

Section: Resultsmentioning

confidence: 99%

Ancestral vinclozolin exposure alters the epigenetic transgenerational inheritance of sperm small noncoding RNAs

2016

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Exposure to the agricultural fungicide vinclozolin during gestation promotes a higher incidence of various diseases in the subsequent unexposed F3 and F4 generations. This phenomenon is termed epigenetic transgenerational inheritance and has been shown to in part involve alterations in DNA methylation, but the role of other epigenetic mechanisms remains unknown. The current study investigated the alterations in small noncoding RNA (sncRNA) in the sperm from F3 generation control and vinclozolin lineage rats. Over 200 differentially expressed sncRNAs were identified and the tRNA-derived sncRNAs, namely 5′ halves of mature tRNAs (5′ halves), displayed the most dramatic changes. Gene targets of the altered miRNAs and tRNA 5′ halves revealed associations between the altered sncRNAs and differentially DNA methylated regions. Dysregulated sncRNAs appear to correlate with mRNA profiles associated with the previously observed vinclozolin-induced disease phenotypes. Data suggest potential connections between sperm-borne RNAs and the vinclozolin-induced epigenetic transgenerational inheritance phenomenon.

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Section: Resultsmentioning

confidence: 99%

Ancestral vinclozolin exposure alters the epigenetic transgenerational inheritance of sperm small noncoding RNAs

2016

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“…Prepachytene piRNAs are typically 26–28 nt in length and have a strong preference towards uracil and adenine at their first and 10th nucleotide positions, respectively. In contrast, pachytene piRNAs are typically 30 nt in length and only possess a preference for adenine at their first nucleotide [62]. Based on these characteristics, we assessed whether the piRNAs found in total sperm samples were prepachytene or pachytene in origin.…”

Section: Resultsmentioning

confidence: 99%

SpermBase: A Database for Sperm-Borne RNA Contents

Schuster

Tang

Xie

et al. 2016

Biology of Reproduction

109

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Since their discovery approximately three decades ago, sperm-borne RNAs, both large/small and coding/noncoding, have been reported in multiple organisms, and some have been implicated in spermatogenesis, early development, and epigenetic inheritance. Despite these advances, isolation, quantification, and annotation of sperm-borne RNAs remain nontrivial. The yields and subspecies of sperm-borne RNAs isolated from sperm can vary drastically depending on the methods used, and no cross-species analyses of sperm RNA contents have ever been conducted using a standardized sperm RNA isolation protocol. To address these issues, we developed a simple RNA isolation method that is applicable to sperm of various species, thus allowing for reliable interspecies comparisons. Based on RNASeq analyses, we established SpermBase (www.spermbase.org), a database dedicated to sperm-borne RNA profiling of multiple species. Currently, SpermBase contains large and small RNA expression data for mouse, rat, rabbit, and human total sperm and sperm heads. By analyzing large and small RNAs for conserved features, we found that many sperm-borne RNA species were conserved across all four species analyzed, and among the conserved small RNAs, sperm-borne tRNA-derived small noncoding RNAs and miRNAs can target a large number of genes known to be critical for early development.

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“…same genomic loci that give rise to pachytene piRNAs, yet with different genetic requirements for their biogenesis, have recently been described in a variety of somatic cell types (Ortogero et al 2014). In addition, dicer-dependent endogenous small interfering RNAs are produced from some piRNA clusters (Watanabe et al 2008).…”

Section: Discussionmentioning

confidence: 99%

piRNAs derived from ancient viral processed pseudogenes as transgenerational sequence-specific immune memory in mammals

Parrish

Fujino

Shiromoto

et al. 2015

RNA

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Endogenous bornavirus-like nucleoprotein elements (EBLNs) are sequences within vertebrate genomes derived from reverse transcription and integration of ancient bornaviral nucleoprotein mRNA via the host retrotransposon machinery. While species with EBLNs appear relatively resistant to bornaviral disease, the nature of this association is unclear. We hypothesized that EBLNs could give rise to antiviral interfering RNA in the form of PIWI-interacting RNAs (piRNAs), a class of small RNA known to silence transposons but not exogenous viruses. We found that in both rodents and primates, which acquired their EBLNs independently some 25-40 million years ago, EBLNs are present within piRNA-generating regions of the genome far more often than expected by chance alone (P = 8 × 10 −3 -6 × 10 −8 ). Three of the seven human EBLNs fall within annotated piRNA clusters and two marmoset EBLNs give rise to bona fide piRNAs. In both rats and mice, at least two of the five EBLNs give rise to abundant piRNAs in the male gonad. While no EBLNs are syntenic between rodent and primate, some of the piRNA clusters containing EBLNs are; thus we deduce that EBLNs were integrated into existing piRNA clusters. All true piRNAs derived from EBLNs are antisense relative to the proposed ancient bornaviral nucleoprotein mRNA. These observations are consistent with a role for EBLN-derived piRNA-like RNAs in interfering with ancient bornaviral infection. They raise the hypothesis that retrotransposon-dependent virus-to-host gene flow could engender RNA-mediated, sequence-specific antiviral immune memory in metazoans analogous to the CRISPR/Cas system in prokaryotes.

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A Novel Class of Somatic Small RNAs Similar to Germ Cell Pachytene PIWI-interacting Small RNAs

Cited by 26 publications

References 45 publications

Ancestral vinclozolin exposure alters the epigenetic transgenerational inheritance of sperm small noncoding RNAs

Ancestral vinclozolin exposure alters the epigenetic transgenerational inheritance of sperm small noncoding RNAs

SpermBase: A Database for Sperm-Borne RNA Contents

piRNAs derived from ancient viral processed pseudogenes as transgenerational sequence-specific immune memory in mammals

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