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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
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    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
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