p53 enhances elesclomol-Cu-induced cuproptosis in hepatocellular carcinoma via FDXR-mediated FDX1 upregulation

BackgroundCuproptosis, a novel cell death pathway mediated by ferredoxin 1 (FDX1) and protein lipoylation, has emerged as a valuable target in cancer therapy. Although the findings of previous research have indicated a potential correlation between p53 and cuproptosis, the precise role and underlyin...

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Main Authors: Xiao Liu, Honglin Qu, Jingmin Li, Xuhong Sun, Zhenlin Wang, Dong Wang, Xianyong Bai, Xiaoyan Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-06-01
Series:Frontiers in Oncology
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Online Access:https://www.frontiersin.org/articles/10.3389/fonc.2025.1584811/full
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author Xiao Liu
Honglin Qu
Jingmin Li
Xuhong Sun
Zhenlin Wang
Dong Wang
Xianyong Bai
Xiaoyan Li
author_facet Xiao Liu
Honglin Qu
Jingmin Li
Xuhong Sun
Zhenlin Wang
Dong Wang
Xianyong Bai
Xiaoyan Li
author_sort Xiao Liu
collection DOAJ
description BackgroundCuproptosis, a novel cell death pathway mediated by ferredoxin 1 (FDX1) and protein lipoylation, has emerged as a valuable target in cancer therapy. Although the findings of previous research have indicated a potential correlation between p53 and cuproptosis, the precise role and underlying mechanisms of p53 in cuproptosis, particularly within the context of hepatocellular carcinoma (HCC), remain unclear.MethodsTo evaluate cuproptosis, three HCC cell lines (HepG2, PLC/PRF/5, and Hep3B2.1-7) with distinct p53 statuses were treated with elesclomol-Cu. p53 overexpression/knockdown, siRNA-mediated ferredoxin reductase (FDXR)/FDX1 knockdown, and the p53 activators CP-31398 and nutlin-3 were employed to elucidate the associated molecular mechanisms. Cell viability, protein expression [FDX1, dihydrolipoyl transacetylase (DLAT), FDXR], and DLAT oligomerization were assessed via Cell Counting Kit-8 (CCK-8), western blotting, and immunofluorescence analyses. A PLC/PRF/5 xenograft mouse model was used to assess combined the therapeutic efficacy of elesclomol-Cu and CP-31398.ResultsElesclomol-Cu triggered cuproptosis in HCC cells, as evidenced by a dose-dependent suppression of proliferation, FDX1 upregulation, DLAT oligomerization, and rescue by the copper chelator tetrathiomolybdate (TTM). p53 activation enhanced FDXR expression, promoting FDX1 upregulation and subsequent DLAT oligomerization, thereby sensitizing HCC cells to elesclomol-Cu, whereas FDXR knockdown reversed these effects, demonstrating its role in p53-mediated potentiation of cuproptosis sensitivity. In mutant p53-R249S cells, CP-31398 functioned synergistically with elesclomol-Cu to suppress proliferation. In vivo, elesclomol-Cu and CP-31398 combination therapy significantly reduced tumor growth and Ki67 expression whilst upregulating FDXR levels.ConclusionsThese findings revealed that p53 enhances elesclomol-Cu-induced cuproptosis in HCC via FDXR-mediated FDX1 upregulation. This study provides mechanistic insights into p53’s role in cuproptosis and may serve as a basis for targeting copper metabolism in therapeutic strategies for HCC.
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spelling doaj-art-3c415ac9d4b641f0bf64fa8e97c322d82025-08-20T03:29:26ZengFrontiers Media S.A.Frontiers in Oncology2234-943X2025-06-011510.3389/fonc.2025.15848111584811p53 enhances elesclomol-Cu-induced cuproptosis in hepatocellular carcinoma via FDXR-mediated FDX1 upregulationXiao Liu0Honglin Qu1Jingmin Li2Xuhong Sun3Zhenlin Wang4Dong Wang5Xianyong Bai6Xiaoyan Li7Department of Histology and Embryology, School of Basic Medical Sciences, Binzhou Medical University, Yantai, ChinaDepartment of Human Anatomy, School of Basic Medical Sciences, Binzhou Medical University, Yantai, ChinaInstitute of Neurobiology, School of Basic Medical Sciences, Binzhou Medical University, Yantai, ChinaDepartment of Introduction to Medicine, School of Basic Medical Sciences, Binzhou Medical University, Yantai, ChinaDepartment of Histology and Embryology, School of Basic Medical Sciences, Binzhou Medical University, Yantai, ChinaDepartment of Histology and Embryology, School of Basic Medical Sciences, Binzhou Medical University, Yantai, ChinaDepartment of Histology and Embryology, School of Basic Medical Sciences, Binzhou Medical University, Yantai, ChinaDepartment of Introduction to Medicine, School of Basic Medical Sciences, Binzhou Medical University, Yantai, ChinaBackgroundCuproptosis, a novel cell death pathway mediated by ferredoxin 1 (FDX1) and protein lipoylation, has emerged as a valuable target in cancer therapy. Although the findings of previous research have indicated a potential correlation between p53 and cuproptosis, the precise role and underlying mechanisms of p53 in cuproptosis, particularly within the context of hepatocellular carcinoma (HCC), remain unclear.MethodsTo evaluate cuproptosis, three HCC cell lines (HepG2, PLC/PRF/5, and Hep3B2.1-7) with distinct p53 statuses were treated with elesclomol-Cu. p53 overexpression/knockdown, siRNA-mediated ferredoxin reductase (FDXR)/FDX1 knockdown, and the p53 activators CP-31398 and nutlin-3 were employed to elucidate the associated molecular mechanisms. Cell viability, protein expression [FDX1, dihydrolipoyl transacetylase (DLAT), FDXR], and DLAT oligomerization were assessed via Cell Counting Kit-8 (CCK-8), western blotting, and immunofluorescence analyses. A PLC/PRF/5 xenograft mouse model was used to assess combined the therapeutic efficacy of elesclomol-Cu and CP-31398.ResultsElesclomol-Cu triggered cuproptosis in HCC cells, as evidenced by a dose-dependent suppression of proliferation, FDX1 upregulation, DLAT oligomerization, and rescue by the copper chelator tetrathiomolybdate (TTM). p53 activation enhanced FDXR expression, promoting FDX1 upregulation and subsequent DLAT oligomerization, thereby sensitizing HCC cells to elesclomol-Cu, whereas FDXR knockdown reversed these effects, demonstrating its role in p53-mediated potentiation of cuproptosis sensitivity. In mutant p53-R249S cells, CP-31398 functioned synergistically with elesclomol-Cu to suppress proliferation. In vivo, elesclomol-Cu and CP-31398 combination therapy significantly reduced tumor growth and Ki67 expression whilst upregulating FDXR levels.ConclusionsThese findings revealed that p53 enhances elesclomol-Cu-induced cuproptosis in HCC via FDXR-mediated FDX1 upregulation. This study provides mechanistic insights into p53’s role in cuproptosis and may serve as a basis for targeting copper metabolism in therapeutic strategies for HCC.https://www.frontiersin.org/articles/10.3389/fonc.2025.1584811/fullp53cuproptosisferredoxin reductaseelesclomol-Cuferredoxin 1dihydrolipoyl transacetylase
spellingShingle Xiao Liu
Honglin Qu
Jingmin Li
Xuhong Sun
Zhenlin Wang
Dong Wang
Xianyong Bai
Xiaoyan Li
p53 enhances elesclomol-Cu-induced cuproptosis in hepatocellular carcinoma via FDXR-mediated FDX1 upregulation
Frontiers in Oncology
p53
cuproptosis
ferredoxin reductase
elesclomol-Cu
ferredoxin 1
dihydrolipoyl transacetylase
title p53 enhances elesclomol-Cu-induced cuproptosis in hepatocellular carcinoma via FDXR-mediated FDX1 upregulation
title_full p53 enhances elesclomol-Cu-induced cuproptosis in hepatocellular carcinoma via FDXR-mediated FDX1 upregulation
title_fullStr p53 enhances elesclomol-Cu-induced cuproptosis in hepatocellular carcinoma via FDXR-mediated FDX1 upregulation
title_full_unstemmed p53 enhances elesclomol-Cu-induced cuproptosis in hepatocellular carcinoma via FDXR-mediated FDX1 upregulation
title_short p53 enhances elesclomol-Cu-induced cuproptosis in hepatocellular carcinoma via FDXR-mediated FDX1 upregulation
title_sort p53 enhances elesclomol cu induced cuproptosis in hepatocellular carcinoma via fdxr mediated fdx1 upregulation
topic p53
cuproptosis
ferredoxin reductase
elesclomol-Cu
ferredoxin 1
dihydrolipoyl transacetylase
url https://www.frontiersin.org/articles/10.3389/fonc.2025.1584811/full
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