IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-41759-9.html
   My bibliography  Save this article

Multi-omics profiling reveals rhythmic liver function shaped by meal timing

Author

Listed:
  • Rongfeng Huang

    (Army Medical University)

  • Jianghui Chen

    (Army Medical University)

  • Meiyu Zhou

    (Army Medical University)

  • Haoran Xin

    (Army Medical University)

  • Sin Man Lam

    (Chinese Academy of Sciences
    LipidALL Technologies Company Limited)

  • Xiaoqing Jiang

    (Army Medical University)

  • Jie Li

    (Army Medical University)

  • Fang Deng

    (Army Medical University)

  • Guanghou Shui

    (Chinese Academy of Sciences)

  • Zhihui Zhang

    (Army Medical University)

  • Min-Dian Li

    (Army Medical University)

Abstract

Post-translational modifications (PTMs) couple feed-fast cycles to diurnal rhythms. However, it remains largely uncharacterized whether and how meal timing organizes diurnal rhythms beyond the transcriptome. Here, we systematically profile the daily rhythms of the proteome, four PTMs (phosphorylation, ubiquitylation, succinylation and N-glycosylation) and the lipidome in the liver from young female mice subjected to either day/sleep time-restricted feeding (DRF) or night/wake time-restricted feeding (NRF). We detect robust daily rhythms among different layers of omics with phosphorylation the most nutrient-responsive and succinylation the least. Integrative analyses reveal that clock regulation of fatty acid metabolism represents a key diurnal feature that is reset by meal timing, as indicated by the rhythmic phosphorylation of the circadian repressor PERIOD2 at Ser971 (PER2-pSer971). We confirm that PER2-pSer971 is activated by nutrient availability in vivo. Together, this dataset represents a comprehensive resource detailing the proteomic and lipidomic responses by the liver to alterations in meal timing.

Suggested Citation

  • Rongfeng Huang & Jianghui Chen & Meiyu Zhou & Haoran Xin & Sin Man Lam & Xiaoqing Jiang & Jie Li & Fang Deng & Guanghou Shui & Zhihui Zhang & Min-Dian Li, 2023. "Multi-omics profiling reveals rhythmic liver function shaped by meal timing," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41759-9
    DOI: 10.1038/s41467-023-41759-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-41759-9
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-41759-9?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. Ying Xu & Quasar S. Padiath & Robert E. Shapiro & Christopher R. Jones & Susan C. Wu & Noriko Saigoh & Kazumasa Saigoh & Louis J. Ptáček & Ying-Hui Fu, 2005. "Functional consequences of a CKIδ mutation causing familial advanced sleep phase syndrome," Nature, Nature, vol. 434(7033), pages 640-644, March.
    2. Yunzhi Wang & Lei Song & Mingwei Liu & Rui Ge & Quan Zhou & Wanlin Liu & Ruiyang Li & Jingbo Qie & Bei Zhen & Yi Wang & Fuchu He & Jun Qin & Chen Ding, 2018. "A proteomics landscape of circadian clock in mouse liver," Nature Communications, Nature, vol. 9(1), pages 1-16, December.
    3. Sihao Liu & Jonathan D. Brown & Kristopher J. Stanya & Edwin Homan & Mathias Leidl & Karen Inouye & Prerna Bhargava & Matthew R. Gangl & Lingling Dai & Ben Hatano & Gökhan S. Hotamisligil & Alan Sagha, 2013. "A diurnal serum lipid integrates hepatic lipogenesis and peripheral fatty acid use," Nature, Nature, vol. 502(7472), pages 550-554, October.
    4. Han Cho & Xuan Zhao & Megumi Hatori & Ruth T. Yu & Grant D. Barish & Michael T. Lam & Ling-Wa Chong & Luciano DiTacchio & Annette R. Atkins & Christopher K. Glass & Christopher Liddle & Johan Auwerx &, 2012. "Regulation of circadian behaviour and metabolism by REV-ERB-α and REV-ERB-β," Nature, Nature, vol. 485(7396), pages 123-127, May.
    5. Fynn M. Hansen & Maria C. Tanzer & Franziska Brüning & Isabell Bludau & Che Stafford & Brenda A. Schulman & Maria S. Robles & Ozge Karayel & Matthias Mann, 2021. "Data-independent acquisition method for ubiquitinome analysis reveals regulation of circadian biology," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    6. Yang An & Baoshi Yuan & Pancheng Xie & Yue Gu & Zhiwei Liu & Tao Wang & Zhihao Li & Ying Xu & Yi Liu, 2022. "Author Correction: Decoupling PER phosphorylation, stability and rhythmic expression from circadian clock function by abolishing PER-CK1 interaction," Nature Communications, Nature, vol. 13(1), pages 1-1, December.
    7. Yang An & Baoshi Yuan & Pancheng Xie & Yue Gu & Zhiwei Liu & Tao Wang & Zhihao Li & Ying Xu & Yi Liu, 2022. "Decoupling PER phosphorylation, stability and rhythmic expression from circadian clock function by abolishing PER-CK1 interaction," Nature Communications, Nature, vol. 13(1), pages 1-17, 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. Yang An & Baoshi Yuan & Pancheng Xie & Yue Gu & Zhiwei Liu & Tao Wang & Zhihao Li & Ying Xu & Yi Liu, 2022. "Decoupling PER phosphorylation, stability and rhythmic expression from circadian clock function by abolishing PER-CK1 interaction," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Yanying Wang & Jing Wang & Xiaoyu Li & Xushen Xiong & Jianyi Wang & Ziheng Zhou & Xiaoxiao Zhu & Yang Gu & Dan Dominissini & Lei He & Yong Tian & Chengqi Yi & Zusen Fan, 2021. "N1-methyladenosine methylation in tRNA drives liver tumourigenesis by regulating cholesterol metabolism," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    3. Meghan H. Murray & Aurore Cecile Valfort & Thomas Koelblen & Céline Ronin & Fabrice Ciesielski & Arindam Chatterjee & Giri Babu Veerakanellore & Bahaa Elgendy & John K. Walker & Lamees Hegazy & Thomas, 2022. "Structural basis of synthetic agonist activation of the nuclear receptor REV-ERB," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    4. Jiyeon Lee & Julie M. Dimitry & Jong Hee Song & Minsoo Son & Patrick W. Sheehan & Melvin W. King & G. Travis Tabor & Young Ah Goo & Mitchell A. Lazar & Leonard Petrucelli & Erik S. Musiek, 2023. "Microglial REV-ERBα regulates inflammation and lipid droplet formation to drive tauopathy in male mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    5. Xiaodi Hu & Mingwei Sun & Qian Chen & Yixia Zhao & Na Liang & Siyuan Wang & Pengbin Yin & Yuanping Yang & Sin Man Lam & Qianying Zhang & Alimujiang Tudiyusufu & Yingying Gu & Xin Wan & Meihong Chen & , 2023. "Skeletal muscle-secreted DLPC orchestrates systemic energy homeostasis by enhancing adipose browning," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    6. Qixin Wang & Isaac Kirubakaran Sundar & Joseph H. Lucas & Jun-Gyu Park & Aitor Nogales & Luis Martinez-Sobrido & Irfan Rahman, 2023. "Circadian clock molecule REV-ERBα regulates lung fibrotic progression through collagen stabilization," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    7. Ke Shui & Chenwei Wang & Xuedi Zhang & Shanshan Ma & Qinyu Li & Wanshan Ning & Weizhi Zhang & Miaomiao Chen & Di Peng & Hui Hu & Zheng Fang & Anyuan Guo & Guanjun Gao & Mingliang Ye & Luoying Zhang & , 2023. "Small-sample learning reveals propionylation in determining global protein homeostasis," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    8. Liam C. Hunt & Vishwajeeth Pagala & Anna Stephan & Boer Xie & Kiran Kodali & Kanisha Kavdia & Yong-Dong Wang & Abbas Shirinifard & Michelle Curley & Flavia A. Graca & Yingxue Fu & Suresh Poudel & Yuxi, 2023. "An adaptive stress response that confers cellular resilience to decreased ubiquitination," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    9. Henson, Michael A., 2013. "Multicellular models of intercellular synchronization in circadian neural networks," Chaos, Solitons & Fractals, Elsevier, vol. 50(C), pages 48-64.
    10. Li, Ying & Liu, Zengrong, 2015. "Dynamical mechanism of Bmal1/Rev-erbα loop in circadian clock," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 430(C), pages 126-135.
    11. Yi Yang & Qun Fang, 2024. "Prediction of glycopeptide fragment mass spectra by deep learning," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    12. Samuel A. Druzak & Matteo Tardelli & Suzanne G. Mays & Mireille El Bejjani & Xulie Mo & Kristal M. Maner-Smith & Thomas Bowen & Michael L. Cato & Matthew C. Tillman & Akiko Sugiyama & Yang Xie & Haian, 2023. "Ligand dependent interaction between PC-TP and PPARδ mitigates diet-induced hepatic steatosis in male mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    13. Tomasz Pałka & Przemysław Pajor & Anna Katarzyna Tyka & Wanda Pilch & Agata Cebula & Aneta Teległów & Marek Strzała & Marcin Maciejczyk, 2021. "Time-of-Day Effects on Anaerobic Power and Concentration of Selected Hormones in Blind Men," IJERPH, MDPI, vol. 18(17), pages 1-12, September.
    14. Ulises H. Guzman & Henriette Aksnes & Rasmus Ree & Nicolai Krogh & Magnus E. Jakobsson & Lars J. Jensen & Thomas Arnesen & Jesper V. Olsen, 2023. "Loss of N-terminal acetyltransferase A activity induces thermally unstable ribosomal proteins and increases their turnover in Saccharomyces cerevisiae," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    15. Yasuko O. Abe & Hikari Yoshitane & Dae Wook Kim & Satoshi Kawakami & Michinori Koebis & Kazuki Nakao & Atsu Aiba & Jae Kyoung Kim & Yoshitaka Fukada, 2022. "Rhythmic transcription of Bmal1 stabilizes the circadian timekeeping system in mammals," Nature Communications, Nature, vol. 13(1), pages 1-12, 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_s41467-023-41759-9. 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.