IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-31268-6.html
   My bibliography  Save this article

Global stable-isotope tracing metabolomics reveals system-wide metabolic alternations in aging Drosophila

Author

Listed:
  • Ruohong Wang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yandong Yin

    (Chinese Academy of Sciences)

  • Jingshu Li

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Hongmiao Wang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Wanting Lv

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yang Gao

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Tangci Wang

    (Chinese Academy of Sciences)

  • Yedan Zhong

    (Chinese Academy of Sciences)

  • Zhiwei Zhou

    (Chinese Academy of Sciences)

  • Yuping Cai

    (Chinese Academy of Sciences)

  • Xiaoyang Su

    (Rutgers University
    Rutgers University)

  • Nan Liu

    (Chinese Academy of Sciences)

  • Zheng-Jiang Zhu

    (Chinese Academy of Sciences)

Abstract

System-wide metabolic homeostasis is crucial for maintaining physiological functions of living organisms. Stable-isotope tracing metabolomics allows to unravel metabolic activity quantitatively by measuring the isotopically labeled metabolites, but has been largely restricted by coverage. Delineating system-wide metabolic homeostasis at the whole-organism level remains challenging. Here, we develop a global isotope tracing metabolomics technology to measure labeled metabolites with a metabolome-wide coverage. Using Drosophila as an aging model organism, we probe the in vivo tracing kinetics with quantitative information on labeling patterns, extents and rates on a metabolome-wide scale. We curate a system-wide metabolic network to characterize metabolic homeostasis and disclose a system-wide loss of metabolic coordinations that impacts both intra- and inter-tissue metabolic homeostasis significantly during Drosophila aging. Importantly, we reveal an unappreciated metabolic diversion from glycolysis to serine metabolism and purine metabolism as Drosophila aging. The developed technology facilitates a system-level understanding of metabolic regulation in living organisms.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31268-6
    DOI: 10.1038/s41467-022-31268-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-31268-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-31268-6?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. Sílvia F. Henriques & Darshan B. Dhakan & Lúcia Serra & Ana Patrícia Francisco & Zita Carvalho-Santos & Célia Baltazar & Ana Paula Elias & Margarida Anjos & Tong Zhang & Oliver D. K. Maddocks & Carlos, 2020. "Metabolic cross-feeding in imbalanced diets allows gut microbes to improve reproduction and alter host behaviour," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    2. Won Dong Lee & Dzmitry Mukha & Elina Aizenshtein & Tomer Shlomi, 2019. "Spatial-fluxomics provides a subcellular-compartmentalized view of reductive glutamine metabolism in cancer cells," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    3. 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.
    4. Fumiaki Obata & Masayuki Miura, 2015. "Enhancing S-adenosyl-methionine catabolism extends Drosophila lifespan," Nature Communications, Nature, vol. 6(1), pages 1-9, November.
    5. Xiaotao Shen & Ruohong Wang & Xin Xiong & Yandong Yin & Yuping Cai & Zaijun Ma & Nan Liu & Zheng-Jiang Zhu, 2019. "Metabolic reaction network-based recursive metabolite annotation for untargeted metabolomics," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    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. 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.
    3. 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.
    4. Mahmoud A. Bassal & Saumya E. Samaraweera & Kelly Lim & Brooks A. Benard & Sheree Bailey & Satinder Kaur & Paul Leo & John Toubia & Chloe Thompson-Peach & Tran Nguyen & Kyaw Ze Ya Maung & Debora A. Ca, 2022. "Germline mutations in mitochondrial complex I reveal genetic and targetable vulnerability in IDH1-mutant acute myeloid leukaemia," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    5. Xiaotao Shen & Hong Yan & Chuchu Wang & Peng Gao & Caroline H. Johnson & Michael P. Snyder, 2022. "TidyMass an object-oriented reproducible analysis framework for LC–MS data," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    6. Ren Dodge & Eric W. Jones & Haolong Zhu & Benjamin Obadia & Daniel J. Martinez & Chenhui Wang & Andrés Aranda-Díaz & Kevin Aumiller & Zhexian Liu & Marco Voltolini & Eoin L. Brodie & Kerwyn Casey Huan, 2023. "A symbiotic physical niche in Drosophila melanogaster regulates stable association of a multi-species gut microbiota," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    7. 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.
    8. Hanyu Rao & Changwei Liu & Aiting Wang & Chunxiao Ma & Yue Xu & Tianbao Ye & Wenqiong Su & Peijun Zhou & Wei-Qiang Gao & Li Li & Xianting Ding, 2023. "SETD2 deficiency accelerates sphingomyelin accumulation and promotes the development of renal cancer," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    9. K. E. Huus & T. T. Hoang & A. Creus-Cuadros & M. Cirstea & S. L. Vogt & K. Knuff-Janzen & P. J. Sansonetti & P. Vonaesch & B. B. Finlay, 2021. "Cross-feeding between intestinal pathobionts promotes their overgrowth during undernutrition," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    10. 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.
    11. Mingdu Luo & Yandong Yin & Zhiwei Zhou & Haosong Zhang & Xi Chen & Hongmiao Wang & Zheng-Jiang Zhu, 2023. "A mass spectrum-oriented computational method for ion mobility-resolved untargeted metabolomics," Nature Communications, Nature, vol. 14(1), pages 1-15, 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:13:y:2022:i:1:d:10.1038_s41467-022-31268-6. 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.