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ORIGINAL RESEARCH article

Front. Cell Dev. Biol.
Sec. Stem Cell Research
Volume 12 - 2024 | doi: 10.3389/fcell.2024.1450227
This article is part of the Research Topic Functional Implications of Piwi Proteins and piRNAs in Stem Cell Maintenance and Development View all articles

Essential functions of RNA helicase Vasa in maintaining germline stem cells and piRNA-guided Stellate silencing in Drosophila spermatogenesis

Provisionally accepted
Vladimir E. Adashev Vladimir E. Adashev 1Alexei A. Kotov Alexei A. Kotov 1Sergei S. Bazylev Sergei S. Bazylev 1Ilia A. Kombarov Ilia A. Kombarov 1Oxana M. Olenkina Oxana M. Olenkina 2Aleksei S. Shatskikh Aleksei S. Shatskikh 1Ludmila V. Olenina Ludmila V. Olenina 1*
  • 1 Koltzov Institute of Developmental Biology, Russian Academy of Sciences, Moscow, Moscow Oblast, Russia
  • 2 Kurchatov Institute, Moscow, Moscow Oblast, Russia

The final, formatted version of the article will be published soon.

    DEAD-box RNA helicase Vasa is required for gonad development and fertility in multiple animals. Vasa is implicated in many crucial aspects of Drosophila oogenesis, including translation regulation, primordial germ cell specification, piRNA silencing of transposable elements, and maintenance of germline stem cells (GSCs). However, data about Vasa functions in Drosophila spermatogenesis remain controversial. Here we showed that loss-of-function vasa mutations led to failures of GSC maintenance in the testes, a severe loss of total germ cell content, and a cessation of male fertility over time. Defects in GSC maintenance in vasa mutant testes were not associated with an increasing frequency of programmed cell death, indicating that a premature loss of GSCs occurred via entering differentiation. We found that Vasa is implicated in the positive regulation of rhino expression both in the testes and ovaries. The introduction of a transgene copy of rhino, encoding a nuclear component of piRNA pathway machinery, in vasa mutant background allowed us to restore premeiotic stages of spermatogenesis, including the maintenance of GSCs and the development of spermatogonia and spermatocytes. However, piRNA-guided repression of Stellate genes in spermatocytes of vasa mutant testes with additional rhino copy was not restored, and male fertility was disrupted. Our study uncovered a novel mechanistic link involving Vasa and Rhino in a regulatory network that mediates GSC maintenance but is dispensable for the perfect biogenesis of Su(Ste) piRNAs in testes. Thus, we have shown that Vasa functions in spermatogenesis are essential at two distinct developmental stages: in GSCs for their maintenance and in spermatocytes for piRNA-mediated silencing of Stellate genes.

    Keywords: piRNA pathway, Germline stem cells, DEAD-box RNA helicase, Spermatogenesis, male fertility

    Received: 17 Jun 2024; Accepted: 29 Jul 2024.

    Copyright: © 2024 Adashev, Kotov, Bazylev, Kombarov, Olenkina, Shatskikh and Olenina. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

    * Correspondence: Ludmila V. Olenina, Koltzov Institute of Developmental Biology, Russian Academy of Sciences, Moscow, 119991, Moscow Oblast, Russia

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