O-GlcNAcylation of glutaminase isoform KGA inhibits ferroptosis through activation of glutaminolysis in hepatoblastoma

Abstract Hepatoblastoma (HB), the most common pediatric hepatic malignancy, exhibits an increasing incidence. Metabolism reprogramming represents a pivotal hallmark in the oncogenic transformation process, with glutamine emerging as a critical energy source for neoplastic cells, rivaling glucose. Ho...

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Main Authors: Sijia Fang, Guoqing Zhu, Yi Xie, Miao Ding, Ni Zhen, Jiabei Zhu, Siwei Mao, Xiaochen Tang, Han Wu, Qi Zhang, Aijia Zhang, Xin Ni, Qiuhui Pan, Ji Ma
Format: Article
Language:English
Published: Nature Publishing Group 2025-04-01
Series:Cell Death Discovery
Online Access:https://doi.org/10.1038/s41420-025-02464-2
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author Sijia Fang
Guoqing Zhu
Yi Xie
Miao Ding
Ni Zhen
Jiabei Zhu
Siwei Mao
Xiaochen Tang
Han Wu
Qi Zhang
Aijia Zhang
Xin Ni
Qiuhui Pan
Ji Ma
author_facet Sijia Fang
Guoqing Zhu
Yi Xie
Miao Ding
Ni Zhen
Jiabei Zhu
Siwei Mao
Xiaochen Tang
Han Wu
Qi Zhang
Aijia Zhang
Xin Ni
Qiuhui Pan
Ji Ma
author_sort Sijia Fang
collection DOAJ
description Abstract Hepatoblastoma (HB), the most common pediatric hepatic malignancy, exhibits an increasing incidence. Metabolism reprogramming represents a pivotal hallmark in the oncogenic transformation process, with glutamine emerging as a critical energy source for neoplastic cells, rivaling glucose. However, the mechanism by which glutamine is involved in the development of HB remains unclear. Our study identified glutamine metabolism as a crucial factor in the development of HB. The key enzyme of glutamine metabolism, kidney-type glutaminase (GLS1), is activated in HB and regulates cell proliferation. Mechanistically, the GLS1 subtype KGA, utilizing glutamate derived from glutaminolysis, enhances glutathione (GSH) synthesis, which in turn inhibits ferroptosis in HB cells. Importantly, the Thr563 residue of KGA undergoes O-GlcNAcylation, enhancing enzyme activity and stability, accelerating glutaminolysis, and promoting the proliferation of HB. This study demonstrated that enhanced glutaminolysis, driven by GLS1, is crucial for the development of HB by inhibiting ferroptosis. The O-GlcNAcylation of KGA isoform ensures its stability and glutaminase function in HB cells, which can serve as a promising therapeutic target for KGA-mediated glutaminolysis in HB.
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spelling doaj-art-b3a7b66cafba489988bbda5d3b4652df2025-08-20T03:10:09ZengNature Publishing GroupCell Death Discovery2058-77162025-04-0111111310.1038/s41420-025-02464-2O-GlcNAcylation of glutaminase isoform KGA inhibits ferroptosis through activation of glutaminolysis in hepatoblastomaSijia Fang0Guoqing Zhu1Yi Xie2Miao Ding3Ni Zhen4Jiabei Zhu5Siwei Mao6Xiaochen Tang7Han Wu8Qi Zhang9Aijia Zhang10Xin Ni11Qiuhui Pan12Ji Ma13Clinical Laboratory, Shanghai Children’s Medical Center, Shanghai Jiao Tong University School of MedicineClinical Laboratory, Shanghai Children’s Medical Center, Shanghai Jiao Tong University School of MedicineClinical Laboratory, Shanghai Children’s Medical Center, Shanghai Jiao Tong University School of MedicineClinical Laboratory, Shanghai Children’s Medical Center, Shanghai Jiao Tong University School of MedicineClinical Laboratory, Shanghai Children’s Medical Center, Shanghai Jiao Tong University School of MedicineClinical Laboratory, Shanghai Children’s Medical Center, Shanghai Jiao Tong University School of MedicineClinical Laboratory, Shanghai Children’s Medical Center, Shanghai Jiao Tong University School of MedicineClinical Laboratory, Shanghai Children’s Medical Center, Shanghai Jiao Tong University School of MedicineClinical Laboratory, Shanghai Children’s Medical Center, Shanghai Jiao Tong University School of MedicineClinical Laboratory, Shanghai Children’s Medical Center, Shanghai Jiao Tong University School of MedicineClinical Laboratory, Shanghai Children’s Medical Center, Shanghai Jiao Tong University School of MedicineBeijing Key Laboratory for Pediatric Diseases of Otolaryngology, Head and Neck Surgery, MOE Key Laboratory of Major Diseases in Children, Beijing Pediatric Research Institute, Beijing Children’s Hospital, Capital Medical University, National Center for Children’s Health (NCCH)Clinical Laboratory, Shanghai Children’s Medical Center, Shanghai Jiao Tong University School of MedicineClinical Laboratory, Shanghai Children’s Medical Center, Shanghai Jiao Tong University School of MedicineAbstract Hepatoblastoma (HB), the most common pediatric hepatic malignancy, exhibits an increasing incidence. Metabolism reprogramming represents a pivotal hallmark in the oncogenic transformation process, with glutamine emerging as a critical energy source for neoplastic cells, rivaling glucose. However, the mechanism by which glutamine is involved in the development of HB remains unclear. Our study identified glutamine metabolism as a crucial factor in the development of HB. The key enzyme of glutamine metabolism, kidney-type glutaminase (GLS1), is activated in HB and regulates cell proliferation. Mechanistically, the GLS1 subtype KGA, utilizing glutamate derived from glutaminolysis, enhances glutathione (GSH) synthesis, which in turn inhibits ferroptosis in HB cells. Importantly, the Thr563 residue of KGA undergoes O-GlcNAcylation, enhancing enzyme activity and stability, accelerating glutaminolysis, and promoting the proliferation of HB. This study demonstrated that enhanced glutaminolysis, driven by GLS1, is crucial for the development of HB by inhibiting ferroptosis. The O-GlcNAcylation of KGA isoform ensures its stability and glutaminase function in HB cells, which can serve as a promising therapeutic target for KGA-mediated glutaminolysis in HB.https://doi.org/10.1038/s41420-025-02464-2
spellingShingle Sijia Fang
Guoqing Zhu
Yi Xie
Miao Ding
Ni Zhen
Jiabei Zhu
Siwei Mao
Xiaochen Tang
Han Wu
Qi Zhang
Aijia Zhang
Xin Ni
Qiuhui Pan
Ji Ma
O-GlcNAcylation of glutaminase isoform KGA inhibits ferroptosis through activation of glutaminolysis in hepatoblastoma
Cell Death Discovery
title O-GlcNAcylation of glutaminase isoform KGA inhibits ferroptosis through activation of glutaminolysis in hepatoblastoma
title_full O-GlcNAcylation of glutaminase isoform KGA inhibits ferroptosis through activation of glutaminolysis in hepatoblastoma
title_fullStr O-GlcNAcylation of glutaminase isoform KGA inhibits ferroptosis through activation of glutaminolysis in hepatoblastoma
title_full_unstemmed O-GlcNAcylation of glutaminase isoform KGA inhibits ferroptosis through activation of glutaminolysis in hepatoblastoma
title_short O-GlcNAcylation of glutaminase isoform KGA inhibits ferroptosis through activation of glutaminolysis in hepatoblastoma
title_sort o glcnacylation of glutaminase isoform kga inhibits ferroptosis through activation of glutaminolysis in hepatoblastoma
url https://doi.org/10.1038/s41420-025-02464-2
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