Analysis of Hydra PIWI proteins and piRNAs uncover early evolutionary origins of the piRNA pathway

Analysis of Hydra PIWI proteins and piRNAs uncover early evolutionary origins of the piRNA pathway
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DOI:
10.1016/j.ydbio.2013.12.007
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发表时间:
2014-02-01
影响因子:
2.7
通讯作者:
Kai, Toshie
Kai, Toshie
中科院分区:
生物学3区
文献类型:
--
作者:
Lim, Robyn S. M.;Anand, Amit;Kai, Toshie

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为了保持基因组的完整性,一种进化上保守的基于小RNA的沉默机制,涉及PIWI蛋白和PIWI相互作用RNA(PiRNAs),在动物中抑制潜在的有害转座子。尽管在双边动物中已经有了对PIWI蛋白的广泛研究,但这些蛋白仍有待于在古代门中进行检测。在这里,我们研究了海蛇的PIWI蛋白Hywi和Hyli,发现这两种PIWI蛋白在多能干细胞、生殖系干细胞和雌性生殖系中都有丰富的表达。Hywi和Hyli定位于nuage,一个与piRNA介导的转座子沉默有关的核周细胞器,以及其他保守的nuage和piRNA途径组件。我们的发现提供了非双侧的Nuage蛋白定位模式的第一个报告。Hydra PIWI蛋白具有对称的二甲基精氨酸:已知的修饰残基有助于PIWI蛋白定位到Nuage和适当的piRNA负载。PiRNA图谱表明,转座子是九头蛇中piRNA途径的主要靶标。我们的数据表明,通过乒乓球扩增周期的piRNA生物发生在Hydra中,Hywi和Hyli可能分别优先结合初级和次级piRNA。推测的piRNA簇是单向转录的,主要产生与转座子反义的piRNA。这些结果表明,PIWI蛋白的各种保守特征、piRNA途径以及它们与Nuage的关联可能在双侧动物进化之前就已经建立。(C)2013 Elsevier Inc.保留所有权利。
To preserve genome integrity, an evolutionarily conserved small RNA-based silencing mechanism involving PIWI proteins and PIWI-interacting RNAs (piRNAs) represses potentially deleterious transposons in animals. Although there has been extensive research into PIWI proteins in bilaterians, these proteins remain to be examined in ancient phyla. Here, we investigated the PIWI proteins Hywi and Hyli in the cnidarian Hydra, and found that both PIWI proteins are enriched in multipotent stem cells, germline stem cells, and in the female germline. Hywi and Hyli localize to the nuage, a perinuclear organelle that has been implicated in piRNA-mediated transposon silencing, together with other conserved nuage and piRNA pathway components. Our findings provide the first report of nuage protein localization patterns in a non-bilaterian. Hydra PIWI proteins possess symmetrical dimethylarginines: modified residues that are known to aid in PIWI protein localization to the nuage and proper piRNA loading. piRNA profiling suggests that transposons are the major targets of the piRNA pathway in Hydra. Our data suggest that piRNA biogenesis through the ping-pong amplification cycle occurs in Hydra and that Hywi and Hyli are likely to preferentially bind primary and secondary piRNAs, respectively. Presumptive piRNA clusters are unidirectionally transcribed and primarily give rise to piRNAs that are antisense to transposons. These results indicate that various conserved features of PIWI proteins, the piRNA pathway, and their associations with the nuage were likely established before the evolution of bilaterians. (C) 2013 Elsevier Inc. All rights reserved.