IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43550-2.html
   My bibliography  Save this article

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

Author

Listed:
  • 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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43550-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-43550-2?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Hyo Sub Choi & Ajay Bhat & Marshall B. Howington & Megan L. Schaller & Rebecca L. Cox & Shijiao Huang & Safa Beydoun & Hillary A. Miller & Angela M. Tuckowski & Joy Mecano & Elizabeth S. Dean & Lindy , 2023. "FMO rewires metabolism to promote longevity through tryptophan and one carbon metabolism in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Ruohong Wang & Yandong Yin & Jingshu Li & Hongmiao Wang & Wanting Lv & Yang Gao & Tangci Wang & Yedan Zhong & Zhiwei Zhou & Yuping Cai & Xiaoyang Su & Nan Liu & Zheng-Jiang Zhu, 2022. "Global stable-isotope tracing metabolomics reveals system-wide metabolic alternations in aging Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Grace Y. Liu & Patrick Jouandin & Raymond E. Bahng & Norbert Perrimon & David M. Sabatini, 2024. "An evolutionary mechanism to assimilate new nutrient sensors into the mTORC1 pathway," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    4. Scott, Andrew J., 2023. "The economics of longevity – An introduction," The Journal of the Economics of Ageing, Elsevier, vol. 24(C).
    5. Juewon Kim & Yunju Jo & Donghyun Cho & Dongryeol Ryu, 2022. "L-threonine promotes healthspan by expediting ferritin-dependent ferroptosis inhibition in C. elegans," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Joae Joung & Yekang Heo & Yeonju Kim & Jaejin Kim & Haebeen Choi & Taerang Jeon & Yeji Jang & Eun-Jung Kim & Sang Heon Lee & Jae Myoung Suh & Stephen J. Elledge & Mi-Sung Kim & Chanhee Kang, 2025. "Cell enlargement modulated by GATA4 and YAP instructs the senescence-associated secretory phenotype," Nature Communications, Nature, vol. 16(1), pages 1-19, December.
    7. Ziwei Dai & Weiyan Zheng & Jason W. Locasale, 2022. "Amino acid variability, tradeoffs and optimality in human diet," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    8. Old, Jonathan & Scott, Andrew, 2023. "Healthy ageing trends in England between 2002 to 2018: Improving but slowing and unequal," Department of Economics, Working Paper Series qt759110mx, Department of Economics, Institute for Business and Economic Research, UC Berkeley.
    9. Chenxi Liu & Ning Tian & Pei Chang & Wei Zhang, 2024. "Mating reconciles fitness and fecundity by switching diet preference in flies," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    10. Cristal M. Hill & Diana C. Albarado & Lucia G. Coco & Redin A. Spann & Md Shahjalal Khan & Emily Qualls-Creekmore & David H. Burk & Susan J. Burke & J. Jason Collier & Sangho Yu & David H. McDougal & , 2022. "FGF21 is required for protein restriction to extend lifespan and improve metabolic health in male mice," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    11. Jinjie Duan & Wenhui Dong & Guangyan Wang & Wenjing Xiu & Guangyin Pu & Jingwen Xu & Chenji Ye & Xu Zhang & Yi Zhu & Chunjiong Wang, 2023. "Senescence-associated 13-HODE production promotes age-related liver steatosis by directly inhibiting catalase activity," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    12. Rupesh S. Patel & Rodrigo Romero & Emma V. Watson & Anthony C. Liang & Megan Burger & Peter M. K. Westcott & Kim L. Mercer & Roderick T. Bronson & Eric C. Wooten & Arjun Bhutkar & Tyler Jacks & Stephe, 2022. "A GATA4-regulated secretory program suppresses tumors through recruitment of cytotoxic CD8 T cells," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    13. Noha Sharafeldin & Martha L. Slattery & Qi Liu & Conrado Franco-Villalobos & Bette J. Caan & John D. Potter & Yutaka Yasui, 2017. "Multiple Gene-Environment Interactions on the Angiogenesis Gene-Pathway Impact Rectal Cancer Risk and Survival," IJERPH, MDPI, vol. 14(10), pages 1, September.
    14. Zi Wang & Lina Zou & Yiyan Zhang & Mengnan Zhu & Shuxian Zhang & Di Wu & Jianfeng Lan & Xiao Zang & Qi Wang & Hanxin Zhang & Zixing Wu & Huanhu Zhu & Di Chen, 2023. "ACS-20/FATP4 mediates the anti-ageing effect of dietary restriction in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    15. Célia Alecki & Javeria Rizwan & Phuong Le & Suleima Jacob-Tomas & Mario Fernandez Comaduran & Morgane Verbrugghe & Jia Ming Stella Xu & Sandra Minotti & James Lynch & Jeetayu Biswas & Tad Wu & Heather, 2024. "Localized molecular chaperone synthesis maintains neuronal dendrite proteostasis," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    16. Qing Zou & Yingsi Lai & Zhao-Rong Lun, 2023. "Exploring the Association between Oxygen Concentration and Life Expectancy in China: A Quantitative Analysis," IJERPH, MDPI, vol. 20(2), pages 1-13, January.
    17. Juewon Kim & Yunju Jo & Gyumin Lim & Yosep Ji & Jong-Hwa Roh & Wan-Gi Kim & Hyon-Seung Yi & Dong Wook Choi & Donghyun Cho & Dongryeol Ryu, 2024. "A microbiota-derived metabolite, 3-phenyllactic acid, prolongs healthspan by enhancing mitochondrial function and stress resilience via SKN-1/ATFS-1 in C. elegans," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    18. Jin-Hyuck Jeong & Jun-Seok Han & Youngae Jung & Seung-Min Lee & So-Hyun Park & Mooncheol Park & Min-Gi Shin & Nami Kim & Mi Sun Kang & Seokho Kim & Kwang-Pyo Lee & Ki-Sun Kwon & Chun-A. Kim & Yong Ryo, 2023. "A new AMPK isoform mediates glucose-restriction induced longevity non-cell autonomously by promoting membrane fluidity," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    19. Seoyeon Lee & Mohammad Naimul Islam & Kaveh Boostanpour & Dvir Aran & Guangchun Jin & Stephanie Christenson & Michael A. Matthay & Walter L. Eckalbar & Daryle J. DePianto & Joseph R. Arron & Liam Mage, 2021. "Molecular programs of fibrotic change in aging human lung," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    20. Christopher Livelo & Yiming Guo & Farah Abou Daya & Vasanthi Rajasekaran & Shweta Varshney & Hiep D. Le & Stephen Barnes & Satchidananda Panda & Girish C. Melkani, 2023. "Time-restricted feeding promotes muscle function through purine cycle and AMPK signaling in Drosophila obesity models," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43550-2. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.