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ASI-RIM neuronal axis regulates systemic mitochondrial stress response via TGF-β signaling cascade

Author

Listed:
  • Zihao Wang

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

  • Qian Zhang

    (Chinese Academy of Sciences)

  • Yayun Jiang

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

  • Jun Zhou

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

  • Ye Tian

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

Abstract

Morphogens play a critical role in coordinating stress adaptation and aging across tissues, yet their involvement in neuronal mitochondrial stress responses and systemic effects remains unclear. In this study, we reveal that the transforming growth factor beta (TGF-β) DAF-7 is pivotal in mediating the intestinal mitochondrial unfolded protein response (UPRmt) in Caenorhabditis elegans under neuronal mitochondrial stress. Two ASI sensory neurons produce DAF-7, which targets DAF-1/TGF-β receptors on RIM interneurons to orchestrate a systemic UPRmt response. Remarkably, inducing mitochondrial stress specifically in ASI neurons activates intestinal UPRmt, extends lifespan, enhances pathogen resistance, and reduces both brood size and body fat levels. Furthermore, dopamine positively regulates this UPRmt activation, while GABA acts as a systemic suppressor. This study uncovers the intricate mechanisms of systemic mitochondrial stress regulation, emphasizing the vital role of TGF-β in metabolic adaptations that are crucial for organismal fitness and aging during neuronal mitochondrial stress.

Suggested Citation

  • Zihao Wang & Qian Zhang & Yayun Jiang & Jun Zhou & Ye Tian, 2024. "ASI-RIM neuronal axis regulates systemic mitochondrial stress response via TGF-β signaling cascade," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53093-9
    DOI: 10.1038/s41467-024-53093-9
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    References listed on IDEAS

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    1. Mark W. Pellegrino & Amrita M. Nargund & Natalia V. Kirienko & Reba Gillis & Christopher J. Fiorese & Cole M. Haynes, 2014. "Mitochondrial UPR-regulated innate immunity provides resistance to pathogen infection," Nature, Nature, vol. 516(7531), pages 414-417, December.
    2. Riekelt H. Houtkooper & Laurent Mouchiroud & Dongryeol Ryu & Norman Moullan & Elena Katsyuba & Graham Knott & Robert W. Williams & Johan Auwerx, 2013. "Mitonuclear protein imbalance as a conserved longevity mechanism," Nature, Nature, vol. 497(7450), pages 451-457, May.
    3. Nuria Flames & Oliver Hobert, 2009. "Gene regulatory logic of dopamine neuron differentiation," Nature, Nature, vol. 458(7240), pages 885-889, April.
    4. Steven L. McIntire & Richard J. Reimer & Kim Schuske & Robert H. Edwards & Erik M. Jorgensen, 1997. "Identification and characterization of the vesicular GABA transporter," Nature, Nature, vol. 389(6653), pages 870-876, October.
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