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Hexosamine biosynthetic pathway and O-GlcNAc-processing enzymes regulate daily rhythms in protein O-GlcNAcylation

Author

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  • Xianhui Liu

    (College of Agricultural and Environmental Sciences, University of California)

  • Ivana Blaženović

    (West Coast Metabolomics Center, University of California)

  • Adam J. Contreras

    (College of Agricultural and Environmental Sciences, University of California)

  • Thu M. Pham

    (College of Agricultural and Environmental Sciences, University of California)

  • Christine A. Tabuloc

    (College of Agricultural and Environmental Sciences, University of California)

  • Ying H. Li

    (College of Agricultural and Environmental Sciences, University of California)

  • Jian Ji

    (School of Food Science, State Key Laboratory of Food Science and Technology, National Engineering Research Center for Functional Foods, School of Food Science Synergetic Innovation Center of Food Safety and Nutrition, Jiangnan University)

  • Oliver Fiehn

    (West Coast Metabolomics Center, University of California)

  • Joanna C. Chiu

    (College of Agricultural and Environmental Sciences, University of California)

Abstract

The integration of circadian and metabolic signals is essential for maintaining robust circadian rhythms and ensuring efficient metabolism and energy use. Using Drosophila as an animal model, we show that cellular protein O-GlcNAcylation exhibits robust 24-hour rhythm and represents a key post-translational mechanism that regulates circadian physiology. We observe strong correlation between protein O-GlcNAcylation rhythms and clock-controlled feeding-fasting cycles, suggesting that O-GlcNAcylation rhythms are primarily driven by nutrient input. Interestingly, daily O-GlcNAcylation rhythms are severely dampened when we subject flies to time-restricted feeding at unnatural feeding time. This suggests the presence of clock-regulated buffering mechanisms that prevent excessive O-GlcNAcylation at non-optimal times of the day-night cycle. We show that this buffering mechanism is mediated by the expression and activity of GFAT, OGT, and OGA, which are regulated through integration of circadian and metabolic signals. Finally, we generate a mathematical model to describe the key factors that regulate daily O-GlcNAcylation rhythm.

Suggested Citation

  • Xianhui Liu & Ivana Blaženović & Adam J. Contreras & Thu M. Pham & Christine A. Tabuloc & Ying H. Li & Jian Ji & Oliver Fiehn & Joanna C. Chiu, 2021. "Hexosamine biosynthetic pathway and O-GlcNAc-processing enzymes regulate daily rhythms in protein O-GlcNAcylation," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-24301-7
    DOI: 10.1038/s41467-021-24301-7
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    Cited by:

    1. Haibo Zhang & Keke Xue & Wen Li & Xinyi Yang & Yusen Gou & Xiao Su & Feng Qian & Lei Sun, 2024. "Cullin5 drives experimental asthma exacerbations by modulating alveolar macrophage antiviral immunity," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. 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.

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