The 40S ribosomal subunit recycling complex modulates mitochondrial dynamics and endoplasmic reticulum - mitochondria tethering at mitochondrial fission/fusion hotspots

Abstract The 40S ribosomal subunit recycling pathway is an integral link in the cellular quality control network, occurring after translational errors have been corrected by the ribosome-associated quality control (RQC) machinery. Despite our understanding of its role, the impact of translation qual...

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Main Authors: Foozhan Tahmasebinia, Yinglu Tang, Rushi Tang, Yi Zhang, Will Bonderer, Maisa de Oliveira, Bretton Laboret, Songjie Chen, Ruiqi Jian, Lihua Jiang, Michael Snyder, Chun-Hong Chen, Yawei Shen, Qing Liu, Boxiang Liu, Zhihao Wu
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-56346-3
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author Foozhan Tahmasebinia
Yinglu Tang
Rushi Tang
Yi Zhang
Will Bonderer
Maisa de Oliveira
Bretton Laboret
Songjie Chen
Ruiqi Jian
Lihua Jiang
Michael Snyder
Chun-Hong Chen
Yawei Shen
Qing Liu
Boxiang Liu
Zhihao Wu
author_facet Foozhan Tahmasebinia
Yinglu Tang
Rushi Tang
Yi Zhang
Will Bonderer
Maisa de Oliveira
Bretton Laboret
Songjie Chen
Ruiqi Jian
Lihua Jiang
Michael Snyder
Chun-Hong Chen
Yawei Shen
Qing Liu
Boxiang Liu
Zhihao Wu
author_sort Foozhan Tahmasebinia
collection DOAJ
description Abstract The 40S ribosomal subunit recycling pathway is an integral link in the cellular quality control network, occurring after translational errors have been corrected by the ribosome-associated quality control (RQC) machinery. Despite our understanding of its role, the impact of translation quality control on cellular metabolism remains poorly understood. Here, we reveal a conserved role of the 40S ribosomal subunit recycling (USP10-G3BP1) complex in regulating mitochondrial dynamics and function. The complex binds to fission-fusion proteins located at mitochondrial hotspots, regulating the functional assembly of endoplasmic reticulum-mitochondria contact sites (ERMCSs). Furthermore, it alters the activity of mTORC1/2 pathways, suggesting a link between quality control and energy fluctuations. Effective communication is essential for resolving proteostasis-related stresses. Our study illustrates that the USP10-G3BP1 complex acts as a hub that interacts with various pathways to adapt to environmental stimuli promptly. It advances our molecular understanding of RQC regulation and helps explain the pathogenesis of human proteostasis and mitochondrial dysfunction diseases.
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issn 2041-1723
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publishDate 2025-01-01
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spelling doaj-art-b0dd61f8154b48c5807bdd2ee685f8bb2025-01-26T12:42:51ZengNature PortfolioNature Communications2041-17232025-01-0116112410.1038/s41467-025-56346-3The 40S ribosomal subunit recycling complex modulates mitochondrial dynamics and endoplasmic reticulum - mitochondria tethering at mitochondrial fission/fusion hotspotsFoozhan Tahmasebinia0Yinglu Tang1Rushi Tang2Yi Zhang3Will Bonderer4Maisa de Oliveira5Bretton Laboret6Songjie Chen7Ruiqi Jian8Lihua Jiang9Michael Snyder10Chun-Hong Chen11Yawei Shen12Qing Liu13Boxiang Liu14Zhihao Wu15Department of Biological Sciences, Dedman College of Humanities and Sciences, Southern Methodist UniversityDepartment of Biological Sciences, Dedman College of Humanities and Sciences, Southern Methodist UniversityDepartment of Pharmacy and Pharmaceutical Sciences, Faculty of Science, National University of SingaporeDepartment of Biological Sciences, Dedman College of Humanities and Sciences, Southern Methodist UniversityDepartment of Biological Sciences, Dedman College of Humanities and Sciences, Southern Methodist UniversityDepartment of Biological Sciences, Dedman College of Humanities and Sciences, Southern Methodist UniversityDepartment of Biological Sciences, Dedman College of Humanities and Sciences, Southern Methodist UniversityDepartment of Genetics, Stanford University School of MedicineDepartment of Genetics, Stanford University School of MedicineDepartment of Genetics, Stanford University School of MedicineDepartment of Genetics, Stanford University School of MedicineNational Institute of Infectious Diseases and Vaccinology, NHRIDepartment of Biological Sciences, Clemson UniversityDepartment of Biological Sciences, Clemson UniversityDepartment of Pharmacy and Pharmaceutical Sciences, Faculty of Science, National University of SingaporeDepartment of Biological Sciences, Dedman College of Humanities and Sciences, Southern Methodist UniversityAbstract The 40S ribosomal subunit recycling pathway is an integral link in the cellular quality control network, occurring after translational errors have been corrected by the ribosome-associated quality control (RQC) machinery. Despite our understanding of its role, the impact of translation quality control on cellular metabolism remains poorly understood. Here, we reveal a conserved role of the 40S ribosomal subunit recycling (USP10-G3BP1) complex in regulating mitochondrial dynamics and function. The complex binds to fission-fusion proteins located at mitochondrial hotspots, regulating the functional assembly of endoplasmic reticulum-mitochondria contact sites (ERMCSs). Furthermore, it alters the activity of mTORC1/2 pathways, suggesting a link between quality control and energy fluctuations. Effective communication is essential for resolving proteostasis-related stresses. Our study illustrates that the USP10-G3BP1 complex acts as a hub that interacts with various pathways to adapt to environmental stimuli promptly. It advances our molecular understanding of RQC regulation and helps explain the pathogenesis of human proteostasis and mitochondrial dysfunction diseases.https://doi.org/10.1038/s41467-025-56346-3
spellingShingle Foozhan Tahmasebinia
Yinglu Tang
Rushi Tang
Yi Zhang
Will Bonderer
Maisa de Oliveira
Bretton Laboret
Songjie Chen
Ruiqi Jian
Lihua Jiang
Michael Snyder
Chun-Hong Chen
Yawei Shen
Qing Liu
Boxiang Liu
Zhihao Wu
The 40S ribosomal subunit recycling complex modulates mitochondrial dynamics and endoplasmic reticulum - mitochondria tethering at mitochondrial fission/fusion hotspots
Nature Communications
title The 40S ribosomal subunit recycling complex modulates mitochondrial dynamics and endoplasmic reticulum - mitochondria tethering at mitochondrial fission/fusion hotspots
title_full The 40S ribosomal subunit recycling complex modulates mitochondrial dynamics and endoplasmic reticulum - mitochondria tethering at mitochondrial fission/fusion hotspots
title_fullStr The 40S ribosomal subunit recycling complex modulates mitochondrial dynamics and endoplasmic reticulum - mitochondria tethering at mitochondrial fission/fusion hotspots
title_full_unstemmed The 40S ribosomal subunit recycling complex modulates mitochondrial dynamics and endoplasmic reticulum - mitochondria tethering at mitochondrial fission/fusion hotspots
title_short The 40S ribosomal subunit recycling complex modulates mitochondrial dynamics and endoplasmic reticulum - mitochondria tethering at mitochondrial fission/fusion hotspots
title_sort 40s ribosomal subunit recycling complex modulates mitochondrial dynamics and endoplasmic reticulum mitochondria tethering at mitochondrial fission fusion hotspots
url https://doi.org/10.1038/s41467-025-56346-3
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