Identifying the target, mechanism, and agonist of α-ketoglutaric acid in delaying mesenchymal stem cell senescence

Summary: α-ketoglutaric acid (AKG), a tricarboxylic acid cycle metabolite central to aerobic metabolism and longevity, retains unresolved anti-aging protein targets. Here, we demonstrate that reduced isocitrate dehydrogenase 1 (IDH1) expression during senescence lowers AKG production, accelerating t...

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Main Authors: Zhao Cui, Jiameng Li, Caifeng Li, Shiwen Deng, Wei Liu, Tong Lei, Junxian Cao, Ziyi Wang, Xiaoxu Wang, Shuhua Ma, Yinhua Zhu, Hongjun Yang, Peng Chen
Format: Article
Language:English
Published: Elsevier 2025-07-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124725006886
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author Zhao Cui
Jiameng Li
Caifeng Li
Shiwen Deng
Wei Liu
Tong Lei
Junxian Cao
Ziyi Wang
Xiaoxu Wang
Shuhua Ma
Yinhua Zhu
Hongjun Yang
Peng Chen
author_facet Zhao Cui
Jiameng Li
Caifeng Li
Shiwen Deng
Wei Liu
Tong Lei
Junxian Cao
Ziyi Wang
Xiaoxu Wang
Shuhua Ma
Yinhua Zhu
Hongjun Yang
Peng Chen
author_sort Zhao Cui
collection DOAJ
description Summary: α-ketoglutaric acid (AKG), a tricarboxylic acid cycle metabolite central to aerobic metabolism and longevity, retains unresolved anti-aging protein targets. Here, we demonstrate that reduced isocitrate dehydrogenase 1 (IDH1) expression during senescence lowers AKG production, accelerating the aging of mesenchymal stem cells (MSCs). Exogenous AKG or IDH1 overexpression restores AKG levels, enabling 2-oxoglutarate and Fe(II)-dependent oxygenase domain-containing protein 1 (OGFOD1)-catalyzed hydroxylation of ribosomal protein S23 (RPS23) at proline 62. Mechanistically, AKG stabilizes the OGFOD1-RPS23 complex, enhancing translation accuracy to limit misfolded protein accumulation while sustaining synthesis rates, thereby balancing proteostasis. The natural flavonoid scutellarin (Scu), identified as an IDH1 agonist, elevates AKG to delay MSC senescence. In aged mice, Scu improves cognitive function, reduces osteoporosis and skin aging, and suppresses senescence-associated secretory phenotype. Our findings identify the AKG-IDH1-RPS23 axis as a regulator of stem cell senescence and we propose metabolic reprogramming strategies for anti-aging therapies.
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spelling doaj-art-59765c41a9b64fcea020d87cac96c1dd2025-08-20T02:35:36ZengElsevierCell Reports2211-12472025-07-0144711591710.1016/j.celrep.2025.115917Identifying the target, mechanism, and agonist of α-ketoglutaric acid in delaying mesenchymal stem cell senescenceZhao Cui0Jiameng Li1Caifeng Li2Shiwen Deng3Wei Liu4Tong Lei5Junxian Cao6Ziyi Wang7Xiaoxu Wang8Shuhua Ma9Yinhua Zhu10Hongjun Yang11Peng Chen12Experimental Research Center, China Academy of Chinese Medical Sciences, Beijing 100700, China; Laboratory of Cardiovascular Diseases, Xiyuan Hospital of China Academy of Chinese Medical Sciences, Beijing 100091, ChinaThe First Affiliated Hospital of Guangzhou Medical University, Guangzhou 510120, China; CAS Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety, Chinese Academy of Sciences and National Center for Nanoscience and Technology of China, Beijing 100190, ChinaExperimental Research Center, China Academy of Chinese Medical Sciences, Beijing 100700, ChinaExperimental Research Center, China Academy of Chinese Medical Sciences, Beijing 100700, ChinaExperimental Research Center, China Academy of Chinese Medical Sciences, Beijing 100700, ChinaInstitute of Basic Theory for Chinese Medicine, China Academy of Chinese Medical Sciences, Beijing 100700, ChinaExperimental Research Center, China Academy of Chinese Medical Sciences, Beijing 100700, ChinaExperimental Research Center, China Academy of Chinese Medical Sciences, Beijing 100700, ChinaAstraZeneca Pharmaceuticals LP, Gaithersburg, MD 20878, USAExperimental Research Center, China Academy of Chinese Medical Sciences, Beijing 100700, ChinaBeijing Advanced Innovation Center for Food Nutrition and Human Health, Department of Nutrition and Health, China Agricultural University, Beijing 100193, ChinaExperimental Research Center, China Academy of Chinese Medical Sciences, Beijing 100700, China; Corresponding authorExperimental Research Center, China Academy of Chinese Medical Sciences, Beijing 100700, China; Corresponding authorSummary: α-ketoglutaric acid (AKG), a tricarboxylic acid cycle metabolite central to aerobic metabolism and longevity, retains unresolved anti-aging protein targets. Here, we demonstrate that reduced isocitrate dehydrogenase 1 (IDH1) expression during senescence lowers AKG production, accelerating the aging of mesenchymal stem cells (MSCs). Exogenous AKG or IDH1 overexpression restores AKG levels, enabling 2-oxoglutarate and Fe(II)-dependent oxygenase domain-containing protein 1 (OGFOD1)-catalyzed hydroxylation of ribosomal protein S23 (RPS23) at proline 62. Mechanistically, AKG stabilizes the OGFOD1-RPS23 complex, enhancing translation accuracy to limit misfolded protein accumulation while sustaining synthesis rates, thereby balancing proteostasis. The natural flavonoid scutellarin (Scu), identified as an IDH1 agonist, elevates AKG to delay MSC senescence. In aged mice, Scu improves cognitive function, reduces osteoporosis and skin aging, and suppresses senescence-associated secretory phenotype. Our findings identify the AKG-IDH1-RPS23 axis as a regulator of stem cell senescence and we propose metabolic reprogramming strategies for anti-aging therapies.http://www.sciencedirect.com/science/article/pii/S2211124725006886CP: MetabolismCP: Stem cell research
spellingShingle Zhao Cui
Jiameng Li
Caifeng Li
Shiwen Deng
Wei Liu
Tong Lei
Junxian Cao
Ziyi Wang
Xiaoxu Wang
Shuhua Ma
Yinhua Zhu
Hongjun Yang
Peng Chen
Identifying the target, mechanism, and agonist of α-ketoglutaric acid in delaying mesenchymal stem cell senescence
Cell Reports
CP: Metabolism
CP: Stem cell research
title Identifying the target, mechanism, and agonist of α-ketoglutaric acid in delaying mesenchymal stem cell senescence
title_full Identifying the target, mechanism, and agonist of α-ketoglutaric acid in delaying mesenchymal stem cell senescence
title_fullStr Identifying the target, mechanism, and agonist of α-ketoglutaric acid in delaying mesenchymal stem cell senescence
title_full_unstemmed Identifying the target, mechanism, and agonist of α-ketoglutaric acid in delaying mesenchymal stem cell senescence
title_short Identifying the target, mechanism, and agonist of α-ketoglutaric acid in delaying mesenchymal stem cell senescence
title_sort identifying the target mechanism and agonist of α ketoglutaric acid in delaying mesenchymal stem cell senescence
topic CP: Metabolism
CP: Stem cell research
url http://www.sciencedirect.com/science/article/pii/S2211124725006886
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