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piRNAs are regulators of metabolic reprogramming in stem cells

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  • Patricia Rojas-Ríos

    (Université de Montpellier, CNRS
    Universidad de Sevilla)

  • Aymeric Chartier

    (Université de Montpellier, CNRS)

  • Camille Enjolras

    (Université de Montpellier, CNRS)

  • Julie Cremaschi

    (Université de Montpellier, CNRS)

  • Céline Garret

    (Université de Montpellier, CNRS)

  • Adel Boughlita

    (Université de Montpellier, CNRS)

  • Anne Ramat

    (Université de Montpellier, CNRS)

  • Martine Simonelig

    (Université de Montpellier, CNRS)

Abstract

Stem cells preferentially use glycolysis instead of oxidative phosphorylation and this metabolic rewiring plays an instructive role in their fate; however, the underlying molecular mechanisms remain largely unexplored. PIWI-interacting RNAs (piRNAs) and PIWI proteins have essential functions in a range of adult stem cells across species. Here, we show that piRNAs and the PIWI protein Aubergine (Aub) are instrumental in activating glycolysis in Drosophila female germline stem cells (GSCs). Higher glycolysis is required for GSC self-renewal and aub loss-of-function induces a metabolic switch in GSCs leading to their differentiation. Aub directly binds glycolytic mRNAs and Enolase mRNA regulation by Aub depends on its 5′UTR. Furthermore, mutations of a piRNA target site in Enolase 5′UTR lead to GSC loss. These data reveal an Aub/piRNA function in translational activation of glycolytic mRNAs in GSCs, and pinpoint a mechanism of regulation of metabolic reprogramming in stem cells based on small RNAs.

Suggested Citation

  • Patricia Rojas-Ríos & Aymeric Chartier & Camille Enjolras & Julie Cremaschi & Céline Garret & Adel Boughlita & Anne Ramat & Martine Simonelig, 2024. "piRNAs are regulators of metabolic reprogramming in stem cells," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52709-4
    DOI: 10.1038/s41467-024-52709-4
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    References listed on IDEAS

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    1. Rebecca Halbach & Pascal Miesen & Joep Joosten & Ezgi Taşköprü & Inge Rondeel & Bas Pennings & Chantal B. F. Vogels & Sarah H. Merkling & Constantianus J. Koenraadt & Louis Lambrechts & Ronald P. van , 2020. "A satellite repeat-derived piRNA controls embryonic development of Aedes," Nature, Nature, vol. 580(7802), pages 274-277, April.
    2. Robert J. Ross & Molly M. Weiner & Haifan Lin, 2014. "PIWI proteins and PIWI-interacting RNAs in the soma," Nature, Nature, vol. 505(7483), pages 353-359, January.
    3. Toby Lieber & Swathi P. Jeedigunta & Jonathan M. Palozzi & Ruth Lehmann & Thomas R. Hurd, 2019. "Mitochondrial fragmentation drives selective removal of deleterious mtDNA in the germline," Nature, Nature, vol. 570(7761), pages 380-384, June.
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