PIWI-interacting RNAs (piRNAs) target transcripts by sequence complementarity serving as guides for RNA slicing in animal germ cells. The piRNA pathway is increasingly recognized as critical for essential cellular functions such as germline development and reproduction. In the ovary, as much as 11% of piRNAs map to protein-coding genes. Here, we show that ovarian mRNAs and long non-coding RNAs (lncRNAs) are processed into piRNAs that can direct other transcripts into the piRNA biogenesis pathway. Targeting piRNAs fuel transcripts either into the ping-pong cycle of piRNA amplification or into the machinery of phased piRNA biogenesis, thereby creating networks of inter-regulating transcripts. RNAs of the same network share related genomic repeats. These repeats give rise to piRNAs, which target other transcripts and lead to a cascade of concerted RNA slicing. While ping-pong networks are based on repeats of several hundred nucleotides, networks that rely on phased piRNA biogenesis operate through short ~40-nucleotides long repeats, which we named snetDNAs. Interestingly, snetDNAs are recurring in evolution from insects to mammals. Our study brings to light a new type of conserved regulatory pathway, the snetDNA-pathway, by which short sequences can include independent genes and lncRNAs in the same biological pathway.
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http://dx.doi.org/10.3390/cells9061491 | DOI Listing |
Nat Rev Mol Cell Biol
January 2025
RNA Therapeutics Institute and Howard Hughes Medical Institute, University of Massachusetts Chan Medical School, Worcester, MA, USA.
Small non-coding RNAs can be categorized into two main classes: structural RNAs and regulatory RNAs. Structural RNAs, which are abundant and ubiquitously expressed, have essential roles in the maturation of pre-mRNAs, modification of rRNAs and the translation of coding transcripts. By contrast, regulatory RNAs are often expressed in a developmental-specific, tissue-specific or cell-type-specific manner and exert precise control over gene expression.
View Article and Find Full Text PDFNoncoding RNA
December 2024
Department of Chemistry and Chemical Biology, Northeastern University, Boston, MA 02115, USA.
RNA metabolism is focused on RNA molecules and encompasses all the crucial processes an RNA molecule may or will undergo throughout its life cycle. It is an essential cellular process that allows all cells to function effectively. The transcriptomic landscape of a cell is shaped by the processes such as RNA biosynthesis, maturation (RNA processing, folding, and modification), intra- and inter-cellular transport, transcriptional and post-transcriptional regulation, modification, catabolic decay, and retrograde signaling, all of which are interconnected and are essential for cellular RNA homeostasis.
View Article and Find Full Text PDFFEBS J
December 2024
Laboratory of Germline Biology, Graduate School of Frontier Biosciences, Osaka University, Suita, Japan.
Discovered two decades ago, PIWI-interacting RNAs (piRNAs) are crucial for silencing transposable elements (TEs) in animal gonads, thereby protecting the germline genome from harmful transposition, and ensuring species continuity. Silencing of TEs is achieved through transcriptional and post-transcriptional suppression by piRNAs and the PIWI clade of Argonaute proteins within non-membrane structured organelle. These structures are composed of proteins involved in piRNA processing, including PIWIs and other proteins by distinct functional motifs such as the Tudor domain, LOTUS, and intrinsic disordered regions (IDRs).
View Article and Find Full Text PDFSci Rep
December 2024
Department of Structural and Functional Biology, Institute of Biosciences, Sao Paulo State University (UNESP), Botucatu, SP, 18618-689, Brazil.
Front Cell Dev Biol
November 2024
Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
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