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Early-adult methionine restriction reduces methionine sulfoxide and extends lifespan in Drosophila

Author

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  • Hina Kosakamoto

    (The University of Tokyo
    RIKEN Center for Biosystems Dynamics Research)

  • Fumiaki Obata

    (The University of Tokyo
    RIKEN Center for Biosystems Dynamics Research
    Kyoto University)

  • Junpei Kuraishi

    (The University of Tokyo)

  • Hide Aikawa

    (The University of Tokyo)

  • Rina Okada

    (RIKEN Center for Biosystems Dynamics Research)

  • Joshua N. Johnstone

    (Monash University)

  • Taro Onuma

    (The University of Tokyo
    RIKEN Center for Biosystems Dynamics Research)

  • Matthew D. W. Piper

    (Monash University)

  • Masayuki Miura

    (The University of Tokyo)

Abstract

Methionine restriction (MetR) extends lifespan in various organisms, but its mechanistic understanding remains incomplete. Whether MetR during a specific period of adulthood increases lifespan is not known. In Drosophila, MetR is reported to extend lifespan only when amino acid levels are low. Here, by using an exome-matched holidic medium, we show that decreasing Met levels to 10% extends Drosophila lifespan with or without decreasing total amino acid levels. MetR during the first four weeks of adult life only robustly extends lifespan. MetR in young flies induces the expression of many longevity-related genes, including Methionine sulfoxide reductase A (MsrA), which reduces oxidatively-damaged Met. MsrA induction is foxo-dependent and persists for two weeks after cessation of the MetR diet. Loss of MsrA attenuates lifespan extension by early-adulthood MetR. Our study highlights the age-dependency of the organismal response to specific nutrients and suggests that nutrient restriction during a particular period of life is sufficient for healthspan extension.

Suggested Citation

  • Hina Kosakamoto & Fumiaki Obata & Junpei Kuraishi & Hide Aikawa & Rina Okada & Joshua N. Johnstone & Taro Onuma & Matthew D. W. Piper & Masayuki Miura, 2023. "Early-adult methionine restriction reduces methionine sulfoxide and extends lifespan in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43550-2
    DOI: 10.1038/s41467-023-43550-2
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    References listed on IDEAS

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    1. Byung Cheon Lee & Alaattin Kaya & Siming Ma & Gwansu Kim & Maxim V. Gerashchenko & Sun Hee Yim & Zhen Hu & Lawrence G. Harshman & Vadim N. Gladyshev, 2014. "Methionine restriction extends lifespan of Drosophila melanogaster under conditions of low amino-acid status," Nature Communications, Nature, vol. 5(1), pages 1-12, May.
    2. Richard C. Grandison & Matthew D. W. Piper & Linda Partridge, 2009. "Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila," Nature, Nature, vol. 462(7276), pages 1061-1064, December.
    3. Judith Campisi & Pankaj Kapahi & Gordon J. Lithgow & Simon Melov & John C. Newman & Eric Verdin, 2019. "From discoveries in ageing research to therapeutics for healthy ageing," Nature, Nature, vol. 571(7764), pages 183-192, July.
    4. Fumiaki Obata & Masayuki Miura, 2015. "Enhancing S-adenosyl-methionine catabolism extends Drosophila lifespan," Nature Communications, Nature, vol. 6(1), pages 1-9, November.
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