OSGEP regulates islet β-cell function by modulating proinsulin translation and maintaining ER stress homeostasis in mice

Abstract Proinsulin translation and folding is crucial for glucose homeostasis. However, islet β-cell control of Proinsulin translation remains incompletely understood. Here, we identify OSGEP, an enzyme responsible for t6A37 modification of tRNANNU that tunes glucose metabolism in β-cells. Global O...

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Main Authors: Yujie Liu, Xuechun Yang, Jian Zhou, Haijun Yang, Ruimeng Yang, Peng Zhu, Rong Zhou, Tianyuan Wu, Yongchao Gao, Zhi Ye, Xi Li, Rong Liu, Wei Zhang, Honghao Zhou, Qing Li
Format: Article
Language:English
Published: Nature Portfolio 2024-12-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54905-8
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author Yujie Liu
Xuechun Yang
Jian Zhou
Haijun Yang
Ruimeng Yang
Peng Zhu
Rong Zhou
Tianyuan Wu
Yongchao Gao
Zhi Ye
Xi Li
Rong Liu
Wei Zhang
Honghao Zhou
Qing Li
author_facet Yujie Liu
Xuechun Yang
Jian Zhou
Haijun Yang
Ruimeng Yang
Peng Zhu
Rong Zhou
Tianyuan Wu
Yongchao Gao
Zhi Ye
Xi Li
Rong Liu
Wei Zhang
Honghao Zhou
Qing Li
author_sort Yujie Liu
collection DOAJ
description Abstract Proinsulin translation and folding is crucial for glucose homeostasis. However, islet β-cell control of Proinsulin translation remains incompletely understood. Here, we identify OSGEP, an enzyme responsible for t6A37 modification of tRNANNU that tunes glucose metabolism in β-cells. Global Osgep deletion causes glucose intolerance, while β-cell-specific deletion induces hyperglycemia and glucose intolerance due to impaired insulin activity. Transcriptomics and proteomics reveal activation of the unfolded protein response (UPR) and apoptosis signaling pathways in Osgep-deficient islets, linked to an increase in misfolded Proinsulin from reduced t6A37 modification. Osgep overexpression in pancreas rescues insulin secretion and mitigates diabetes in high-fat diet mice. Osgep enhances translational fidelity and alleviates UPR signaling, highlighting its potential as a therapeutic target for diabetes. Individuals carrying the C allele at rs74512655, which promotes OSGEP transcription, may show reduced susceptibility to T2DM. These findings show OSGEP is essential for islet β-cells and a potential diabetes therapy target.
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institution Kabale University
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publishDate 2024-12-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj-art-d0d7ff96412e4b99a9a6554eaecde2c52024-12-08T12:35:23ZengNature PortfolioNature Communications2041-17232024-12-0115111910.1038/s41467-024-54905-8OSGEP regulates islet β-cell function by modulating proinsulin translation and maintaining ER stress homeostasis in miceYujie Liu0Xuechun Yang1Jian Zhou2Haijun Yang3Ruimeng Yang4Peng Zhu5Rong Zhou6Tianyuan Wu7Yongchao Gao8Zhi Ye9Xi Li10Rong Liu11Wei Zhang12Honghao Zhou13Qing Li14Department of Clinical Pharmacology, Xiangya Hospital, Central South UniversityDepartment of Clinical Pharmacology, Xiangya Hospital, Central South UniversityDepartment of Clinical Pharmacology, Xiangya Hospital, Central South UniversityDepartment of Clinical Pharmacology, Xiangya Hospital, Central South UniversityDepartment of Clinical Pharmacology, Xiangya Hospital, Central South UniversityDepartment of Clinical Pharmacology, Xiangya Hospital, Central South UniversityDepartment of Clinical Pharmacology, Xiangya Hospital, Central South UniversityDepartment of Clinical Pharmacology, Xiangya Hospital, Central South UniversityDepartment of Clinical Pharmacology, Xiangya Hospital, Central South UniversityDepartment of Anesthesiology, Xiangya Hospital of Central South UniversityDepartment of Clinical Pharmacology, Xiangya Hospital, Central South UniversityDepartment of Clinical Pharmacology, Xiangya Hospital, Central South UniversityDepartment of Clinical Pharmacology, Xiangya Hospital, Central South UniversityDepartment of Clinical Pharmacology, Xiangya Hospital, Central South UniversityDepartment of Clinical Pharmacology, Xiangya Hospital, Central South UniversityAbstract Proinsulin translation and folding is crucial for glucose homeostasis. However, islet β-cell control of Proinsulin translation remains incompletely understood. Here, we identify OSGEP, an enzyme responsible for t6A37 modification of tRNANNU that tunes glucose metabolism in β-cells. Global Osgep deletion causes glucose intolerance, while β-cell-specific deletion induces hyperglycemia and glucose intolerance due to impaired insulin activity. Transcriptomics and proteomics reveal activation of the unfolded protein response (UPR) and apoptosis signaling pathways in Osgep-deficient islets, linked to an increase in misfolded Proinsulin from reduced t6A37 modification. Osgep overexpression in pancreas rescues insulin secretion and mitigates diabetes in high-fat diet mice. Osgep enhances translational fidelity and alleviates UPR signaling, highlighting its potential as a therapeutic target for diabetes. Individuals carrying the C allele at rs74512655, which promotes OSGEP transcription, may show reduced susceptibility to T2DM. These findings show OSGEP is essential for islet β-cells and a potential diabetes therapy target.https://doi.org/10.1038/s41467-024-54905-8
spellingShingle Yujie Liu
Xuechun Yang
Jian Zhou
Haijun Yang
Ruimeng Yang
Peng Zhu
Rong Zhou
Tianyuan Wu
Yongchao Gao
Zhi Ye
Xi Li
Rong Liu
Wei Zhang
Honghao Zhou
Qing Li
OSGEP regulates islet β-cell function by modulating proinsulin translation and maintaining ER stress homeostasis in mice
Nature Communications
title OSGEP regulates islet β-cell function by modulating proinsulin translation and maintaining ER stress homeostasis in mice
title_full OSGEP regulates islet β-cell function by modulating proinsulin translation and maintaining ER stress homeostasis in mice
title_fullStr OSGEP regulates islet β-cell function by modulating proinsulin translation and maintaining ER stress homeostasis in mice
title_full_unstemmed OSGEP regulates islet β-cell function by modulating proinsulin translation and maintaining ER stress homeostasis in mice
title_short OSGEP regulates islet β-cell function by modulating proinsulin translation and maintaining ER stress homeostasis in mice
title_sort osgep regulates islet β cell function by modulating proinsulin translation and maintaining er stress homeostasis in mice
url https://doi.org/10.1038/s41467-024-54905-8
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