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Nutrient-dependent regulation of a stable intron modulates germline mitochondrial quality control

Author

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  • Annabel Qi En Ng

    (1 Research Link National University of Singapore)

  • Seow Neng Chan

    (1 Research Link National University of Singapore)

  • Jun Wei Pek

    (1 Research Link National University of Singapore
    National University of Singapore)

Abstract

Mitochondria are inherited exclusively from the mothers and are required for the proper development of embryos. Hence, germline mitochondrial quality is highly regulated during oogenesis to ensure oocyte viability. How nutrient availability influences germline mitochondrial quality control is unclear. Here we find that fasting leads to the accumulation of mitochondrial clumps and oogenesis arrest in Drosophila. Fasting induces the downregulation of the DIP1-Clueless pathway, leading to an increase in the expression of a stable intronic sequence RNA called sisR-1. Mechanistically, sisR-1 localizes to the mitochondrial clumps to inhibit the poly-ubiquitination of the outer mitochondrial protein Porin/VDAC1, thereby suppressing p62-mediated mitophagy. Alleviation of the fasting-induced high sisR-1 levels by either sisR-1 RNAi or refeeding leads to mitophagy, the resumption of oogenesis and an improvement in oocyte quality. Thus, our study provides a possible mechanism by which fasting can improve oocyte quality by modulating the mitochondrial quality control pathway. Of note, we uncover that the sisR-1 response also regulates mitochondrial clumping and oogenesis during protein deprivation, heat shock and aging, suggesting a broader role for this mechanism in germline mitochondrial quality control.

Suggested Citation

  • Annabel Qi En Ng & Seow Neng Chan & Jun Wei Pek, 2024. "Nutrient-dependent regulation of a stable intron modulates germline mitochondrial quality control," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45651-y
    DOI: 10.1038/s41467-024-45651-y
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    References listed on IDEAS

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    1. Julie Parenteau & Laurine Maignon & Mélodie Berthoumieux & Mathieu Catala & Vanessa Gagnon & Sherif Abou Elela, 2019. "Introns are mediators of cell response to starvation," Nature, Nature, vol. 565(7741), pages 612-617, January.
    2. 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.
    3. Jeffrey T. Morgan & Gerald R. Fink & David P. Bartel, 2019. "Excised linear introns regulate growth in yeast," Nature, Nature, vol. 565(7741), pages 606-611, January.
    4. Jing Ting Wong & Farzanah Akhbar & Amanda Yunn Ee Ng & Mandy Li-Ian Tay & Gladys Jing En Loi & Jun Wei Pek, 2017. "DIP1 modulates stem cell homeostasis in Drosophila through regulation of sisR-1," Nature Communications, Nature, vol. 8(1), pages 1-12, December.
    5. Sibiao Yue & Lei Wang & George N. DeMartino & FangZhou Zhao & Yi Liu & Matthew H. Sieber, 2022. "Highly conserved shifts in ubiquitin-proteasome system (UPS) activity drive mitochondrial remodeling during quiescence," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
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