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Neuronal PRDX-2-Mediated ROS Signaling Regulates Food Digestion via peripheral UPRmt Activation

Author

Listed:
  • Yating Liu

    (Yunnan University)

  • Qian Li

    (Yunnan University)

  • Guojing Tian

    (Yunnan University)

  • Xinyi Zhou

    (Yunnan University)

  • Panpan Chen

    (Yunnan University)

  • Bo Chen

    (Yunnan University)

  • Zhao Shan

    (Yunnan University)

  • Bin Qi

    (Yunnan University)

Abstract

All organisms depend on food digestion for survival, yet the brain-gut signaling mechanisms that regulate this process are not fully understood. Here, using an established C. elegans digestion model, we uncover a pathway in which neuronal ROS (free radicals) signal the intestine to suppress digestion. Genetic screening reveals that reducing genes responsible for maintaining ROS balance increases free radicals and decreases digestion. PRDX-2 knockout in olfactory neurons (AWC) elevates ROS and reduces digestive capacity, mediated by the neuropeptide NLP-1 and activation of the mitochondrial unfolded protein response (UPRmt) in the intestine. Additionally, over-expressing nlp-1 or ablating AWC neurons both trigger UPRmt and inhibit digestion. These findings reveal a brain-gut connection in which neuronal PRDX-2-mediated ROS signaling modulates food digestion, highlighting a critical role of free radicals in shutting down digestion to alleviate stress and reduce food consumption.

Suggested Citation

  • Yating Liu & Qian Li & Guojing Tian & Xinyi Zhou & Panpan Chen & Bo Chen & Zhao Shan & Bin Qi, 2024. "Neuronal PRDX-2-Mediated ROS Signaling Regulates Food Digestion via peripheral UPRmt Activation," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-55013-3
    DOI: 10.1038/s41467-024-55013-3
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    References listed on IDEAS

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    1. Fanrui Hao & Huimin Liu & Bin Qi, 2024. "Bacterial peptidoglycan acts as a digestive signal mediating host adaptation to diverse food resources in C. elegans," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Tomer Shpilka & YunGuang Du & Qiyuan Yang & Andrew Melber & Nandhitha Uma Naresh & Joshua Lavelle & Sookyung Kim & Pengpeng Liu & Hilla Weidberg & Rui Li & Jun Yu & Lihua Julie Zhu & Lara Strittmatter, 2021. "UPRmt scales mitochondrial network expansion with protein synthesis via mitochondrial import in Caenorhabditis elegans," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    3. Guang Li & Jianke Gong & Haoyun Lei & Jianfeng Liu & X. Z. Shawn Xu, 2016. "Promotion of behavior and neuronal function by reactive oxygen species in C. elegans," Nature Communications, Nature, vol. 7(1), pages 1-12, December.
    4. Zane B. Andrews & Zhong-Wu Liu & Nicholas Walllingford & Derek M. Erion & Erzsebet Borok & Jeffery M. Friedman & Matthias H. Tschöp & Marya Shanabrough & Gary Cline & Gerald I. Shulman & Anna Coppola , 2008. "UCP2 mediates ghrelin’s action on NPY/AgRP neurons by lowering free radicals," Nature, Nature, vol. 454(7206), pages 846-851, August.
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