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

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 me...

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Main Authors: Zihao Wang, Qian Zhang, Yayun Jiang, Jun Zhou, Ye Tian
Format: Article
Language:English
Published: Nature Portfolio 2024-10-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-53093-9
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author Zihao Wang
Qian Zhang
Yayun Jiang
Jun Zhou
Ye Tian
author_facet Zihao Wang
Qian Zhang
Yayun Jiang
Jun Zhou
Ye Tian
author_sort Zihao Wang
collection DOAJ
description 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.
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spelling doaj-art-8496a76e2a734e1688a9aae33f97dde42025-08-20T02:17:50ZengNature PortfolioNature Communications2041-17232024-10-0115111310.1038/s41467-024-53093-9ASI-RIM neuronal axis regulates systemic mitochondrial stress response via TGF-β signaling cascadeZihao Wang0Qian Zhang1Yayun Jiang2Jun Zhou3Ye Tian4State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of SciencesState Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of SciencesState Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of SciencesState Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of SciencesState Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of SciencesAbstract 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.https://doi.org/10.1038/s41467-024-53093-9
spellingShingle Zihao Wang
Qian Zhang
Yayun Jiang
Jun Zhou
Ye Tian
ASI-RIM neuronal axis regulates systemic mitochondrial stress response via TGF-β signaling cascade
Nature Communications
title ASI-RIM neuronal axis regulates systemic mitochondrial stress response via TGF-β signaling cascade
title_full ASI-RIM neuronal axis regulates systemic mitochondrial stress response via TGF-β signaling cascade
title_fullStr ASI-RIM neuronal axis regulates systemic mitochondrial stress response via TGF-β signaling cascade
title_full_unstemmed ASI-RIM neuronal axis regulates systemic mitochondrial stress response via TGF-β signaling cascade
title_short ASI-RIM neuronal axis regulates systemic mitochondrial stress response via TGF-β signaling cascade
title_sort asi rim neuronal axis regulates systemic mitochondrial stress response via tgf β signaling cascade
url https://doi.org/10.1038/s41467-024-53093-9
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AT yayunjiang asirimneuronalaxisregulatessystemicmitochondrialstressresponseviatgfbsignalingcascade
AT junzhou asirimneuronalaxisregulatessystemicmitochondrialstressresponseviatgfbsignalingcascade
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