Huang S et al. (2021), A Review of Discovery Profiling of PIWI-Interac...

ECB-ART-48902

Int J Mol Sci 2021 Oct 16;2220:. doi: 10.3390/ijms222011166.

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A Review of Discovery Profiling of PIWI-Interacting RNAs and Their Diverse Functions in Metazoans.

Huang S , Yoshitake K , Asakawa S .

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PIWI-interacting RNAs (piRNAs) are a class of small non-coding RNAs (sncRNAs) that perform crucial biological functions in metazoans and defend against transposable elements (TEs) in germ lines. Recently, ubiquitously expressed piRNAs were discovered in soma and germ lines using small RNA sequencing (sRNA-seq) in humans and animals, providing new insights into the diverse functions of piRNAs. However, the role of piRNAs has not yet been fully elucidated, and sRNA-seq studies continue to reveal different piRNA activities in the genome. In this review, we summarize a set of simplified processes for piRNA analysis in order to provide a useful guide for researchers to perform piRNA research suitable for their study objectives. These processes can help expand the functional research on piRNAs from previously reported sRNA-seq results in metazoans. Ubiquitously expressed piRNAs have been discovered in the soma and germ lines in Annelida, Cnidaria, Echinodermata, Crustacea, Arthropoda, and Mollusca, but they are limited to germ lines in Chordata. The roles of piRNAs in TE silencing, gene expression regulation, epigenetic regulation, embryonic development, immune response, and associated diseases will continue to be discovered via sRNA-seq.

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	Figure 1. Overview of common pipeline for PIWI-interacting RNA (piRNA) discovery and functional analysis in metazoans. The raw data of small RNA sequencing (sRNA-seq) were trimmed using adapters, quality control was performed, and the data were subsequently filtered by read lengths. Generally, microRNAs (miRNAs) and small interfering RNAs (siRNAs) are 20–25 nt in length, transfer RNAs (tRNAs) are typically ~80 nt in length, and small nuclear RNAs (snRNAs) and circular RNAs (circRNAs) are more than 100 nt in length, whereas piRNAs normally have lengths of 24–31 nt. However, species-specific piRNAs of 21 nt with a 5′ uridine (21U-RNAs) binding to p53-responsive gene 1 (PRG-1) and 22 nt piRNAs with a 5′ guanosine (22G-RNAs) loaded onto worm-specific Argonautes (WAGOs) were detected in C. elegans [50,51,52]. In the preprocessing step, the potential piRNAs and piRNA isoforms with a length of 18–35 nt were preserved for subsequent known RNA mapping and filtration. The remaining putative piRNA reads were processed for piRNA analysis using multiple tools and databases.
	Figure 2. Discovery of piRNAs in metazoans. In the same taxa, the proportion of TEs increases with the genome size, whereas the number of piRNA species does not increase with the size of the genome or the proportion of TEs.
	Figure 3. piRNA biogenesis and its functional roles in metazoans. In most cases, the piRNA pathway begins with transcription of piRNA clusters, which is mediated by RNA polymerase II (pol II), to generate the respective precursor piRNA (pre-piRNA) transcripts in the nucleus and drive them to cytoplasm where primary and second piRNA biogenesis takes place. The primary transcripts of piRNA clusters are shortened into piRNA intermediates and subsequently loaded onto PIWI proteins and trimmed from the 3′ end to the size of mature piRNAs and then 2′-O-methylated. The mature piRNAs interact with PIWI proteins to form piRISC, which serves various functions in the nucleus and cytoplasm. piRISC is translocated to the nucleus and targets the nascent transcripts through sequence complementarity. Upon binding, PIWI recruits the epigenetic modifier heterochromatin protein 1 (HP1a) and histone methyltransferase (HMT) to a methyl group on unmethylated histone 3 lysine 9 (H3K9) to inhibit pol II transcription, effectively silencing transcription of the gene or TE. The piRNA pathway may also start with a transcript of a protein-coding gene, viral DNA (vDNA), or an invasive viral RNA in the cytoplasm in order to silence the transcript through the ping-pong amplification loop.

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Aravin, Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. 2001, Pubmed