TRIM65 as a key regulator of ferroptosis and glycolysis in lactate-driven renal tubular injury and diabetic kidney disease

Summary: Recent studies have highlighted the critical role of renal tubular epithelial cell (TEC) damage in the progression of diabetic kidney disease (DKD), where lactate accumulation is closely associated with TEC injury despite unclear mechanisms. This study demonstrates that TRIM65 knockout exac...

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Main Authors: Guangyan Yang, Xiaomai Liu, Yanchun Li, Lixing Li, Jiaqing Xiang, Zhen Liang, Meixiu Jiang, Shu Yang
Format: Article
Language:English
Published: Elsevier 2025-08-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124725008629
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author Guangyan Yang
Xiaomai Liu
Yanchun Li
Lixing Li
Jiaqing Xiang
Zhen Liang
Meixiu Jiang
Shu Yang
author_facet Guangyan Yang
Xiaomai Liu
Yanchun Li
Lixing Li
Jiaqing Xiang
Zhen Liang
Meixiu Jiang
Shu Yang
author_sort Guangyan Yang
collection DOAJ
description Summary: Recent studies have highlighted the critical role of renal tubular epithelial cell (TEC) damage in the progression of diabetic kidney disease (DKD), where lactate accumulation is closely associated with TEC injury despite unclear mechanisms. This study demonstrates that TRIM65 knockout exacerbates diabetic kidney damage, while TEC-specific overexpression of TRIM65 ameliorates injury. Mechanistically, TRIM65 suppresses ferroptosis by targeting iron-responsive element binding protein 2 (IREB2) for ubiquitin-mediated degradation while also inhibiting glycolysis through ubiquitination and degradation of pyruvate dehydrogenase kinase 4, a key glycolytic regulator. Notably, lactate promotes p300-mediated lactylation of TRIM65 at lysine 206 (K206), which reduces ubiquitin ligase activity. Supplementation of wild-type TRIM65 reverses kidney damage in knockout mice, and overexpression of the lactylation-defective K206R mutant further enhances protective effects against DKD. These findings reveal that lactate-induced lactylation of TRIM65 at K206 impairs its dual regulatory roles in inhibiting ferroptosis and glycolysis, thereby driving DKD progression and identifying therapeutic targets.
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spelling doaj-art-e1cae2d15a49493bbc17106fd4e010dc2025-08-20T03:58:11ZengElsevierCell Reports2211-12472025-08-0144811609110.1016/j.celrep.2025.116091TRIM65 as a key regulator of ferroptosis and glycolysis in lactate-driven renal tubular injury and diabetic kidney diseaseGuangyan Yang0Xiaomai Liu1Yanchun Li2Lixing Li3Jiaqing Xiang4Zhen Liang5Meixiu Jiang6Shu Yang7Department of Geriatrics, The First Affiliated Hospital of Southern University of Science and Technology, Shenzhen, Guangdong 518020, China; Guangdong Provincial Clinical Research Center for Geriatrics, Shenzhen Clinical Research Center for Geriatrics, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University, The First Affiliated Hospital, Southern University of Science and Technology), Shenzhen, Guangdong 518020, ChinaDepartment of Geriatrics, The First Affiliated Hospital of Southern University of Science and Technology, Shenzhen, Guangdong 518020, China; Guangdong Provincial Clinical Research Center for Geriatrics, Shenzhen Clinical Research Center for Geriatrics, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University, The First Affiliated Hospital, Southern University of Science and Technology), Shenzhen, Guangdong 518020, ChinaDepartment of Geriatrics, The First Affiliated Hospital of Southern University of Science and Technology, Shenzhen, Guangdong 518020, China; Guangdong Provincial Clinical Research Center for Geriatrics, Shenzhen Clinical Research Center for Geriatrics, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University, The First Affiliated Hospital, Southern University of Science and Technology), Shenzhen, Guangdong 518020, ChinaDepartment of Geriatrics, The First Affiliated Hospital of Southern University of Science and Technology, Shenzhen, Guangdong 518020, China; Guangdong Provincial Clinical Research Center for Geriatrics, Shenzhen Clinical Research Center for Geriatrics, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University, The First Affiliated Hospital, Southern University of Science and Technology), Shenzhen, Guangdong 518020, ChinaDepartment of Geriatrics, The First Affiliated Hospital of Southern University of Science and Technology, Shenzhen, Guangdong 518020, China; Guangdong Provincial Clinical Research Center for Geriatrics, Shenzhen Clinical Research Center for Geriatrics, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University, The First Affiliated Hospital, Southern University of Science and Technology), Shenzhen, Guangdong 518020, ChinaDepartment of Geriatrics, Peking University Shenzhen Hospital, Shenzhen, Guangdong 518036, China; Corresponding authorThe National Engineering Research Center for Bioengineering Drugs and the Technologies, Institute of Translational Medicine, Jiangxi Medical College, Nanchang University, Nanchang, Jiangxi 330031, China; Corresponding authorDepartment of Geriatrics, The First Affiliated Hospital of Southern University of Science and Technology, Shenzhen, Guangdong 518020, China; Guangdong Provincial Clinical Research Center for Geriatrics, Shenzhen Clinical Research Center for Geriatrics, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University, The First Affiliated Hospital, Southern University of Science and Technology), Shenzhen, Guangdong 518020, China; Department of Geriatrics, Peking University Shenzhen Hospital, Shenzhen, Guangdong 518036, China; Corresponding authorSummary: Recent studies have highlighted the critical role of renal tubular epithelial cell (TEC) damage in the progression of diabetic kidney disease (DKD), where lactate accumulation is closely associated with TEC injury despite unclear mechanisms. This study demonstrates that TRIM65 knockout exacerbates diabetic kidney damage, while TEC-specific overexpression of TRIM65 ameliorates injury. Mechanistically, TRIM65 suppresses ferroptosis by targeting iron-responsive element binding protein 2 (IREB2) for ubiquitin-mediated degradation while also inhibiting glycolysis through ubiquitination and degradation of pyruvate dehydrogenase kinase 4, a key glycolytic regulator. Notably, lactate promotes p300-mediated lactylation of TRIM65 at lysine 206 (K206), which reduces ubiquitin ligase activity. Supplementation of wild-type TRIM65 reverses kidney damage in knockout mice, and overexpression of the lactylation-defective K206R mutant further enhances protective effects against DKD. These findings reveal that lactate-induced lactylation of TRIM65 at K206 impairs its dual regulatory roles in inhibiting ferroptosis and glycolysis, thereby driving DKD progression and identifying therapeutic targets.http://www.sciencedirect.com/science/article/pii/S2211124725008629CP: Molecular biologyCP: Metabolism
spellingShingle Guangyan Yang
Xiaomai Liu
Yanchun Li
Lixing Li
Jiaqing Xiang
Zhen Liang
Meixiu Jiang
Shu Yang
TRIM65 as a key regulator of ferroptosis and glycolysis in lactate-driven renal tubular injury and diabetic kidney disease
Cell Reports
CP: Molecular biology
CP: Metabolism
title TRIM65 as a key regulator of ferroptosis and glycolysis in lactate-driven renal tubular injury and diabetic kidney disease
title_full TRIM65 as a key regulator of ferroptosis and glycolysis in lactate-driven renal tubular injury and diabetic kidney disease
title_fullStr TRIM65 as a key regulator of ferroptosis and glycolysis in lactate-driven renal tubular injury and diabetic kidney disease
title_full_unstemmed TRIM65 as a key regulator of ferroptosis and glycolysis in lactate-driven renal tubular injury and diabetic kidney disease
title_short TRIM65 as a key regulator of ferroptosis and glycolysis in lactate-driven renal tubular injury and diabetic kidney disease
title_sort trim65 as a key regulator of ferroptosis and glycolysis in lactate driven renal tubular injury and diabetic kidney disease
topic CP: Molecular biology
CP: Metabolism
url http://www.sciencedirect.com/science/article/pii/S2211124725008629
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