ACSL3 is an unfavorable prognostic marker in cholangiocarcinoma patients and confers ferroptosis resistance in cholangiocarcinoma cells

Abstract Cholangiocarcinoma (CCA) is a bile duct malignancy. Our previous comprehensive analysis showed that ferroptosis-related genes can stratify CCA patients into low-risk and high-risk groups based on survival time. Here, we explored the role of ferroptosis in CCA by analyzing mRNA expression in...

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Main Authors: Apiwit Sae-Fung, Nawaporn Vinayavekhin, Bengt Fadeel, Siriporn Jitkaew
Format: Article
Language:English
Published: Nature Portfolio 2024-12-01
Series:npj Precision Oncology
Online Access:https://doi.org/10.1038/s41698-024-00783-8
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author Apiwit Sae-Fung
Nawaporn Vinayavekhin
Bengt Fadeel
Siriporn Jitkaew
author_facet Apiwit Sae-Fung
Nawaporn Vinayavekhin
Bengt Fadeel
Siriporn Jitkaew
author_sort Apiwit Sae-Fung
collection DOAJ
description Abstract Cholangiocarcinoma (CCA) is a bile duct malignancy. Our previous comprehensive analysis showed that ferroptosis-related genes can stratify CCA patients into low-risk and high-risk groups based on survival time. Here, we explored the role of ferroptosis in CCA by analyzing mRNA expression in CCA patients from public databases. We identified acyl-CoA synthetase long chain family member 3 (ACSL3) as a potential ferroptosis suppressor in high-risk CCA patients. Using a panel of CCA cell lines, we confirmed ACSL3 upregulation in CCA cell lines associated with high-risk CCA, correlating this with resistance to the ferroptosis inducer RSL3. Lipidomic analysis revealed increased monounsaturated fatty acid (MUFA)-containing phospholipids in resistant cell lines. ACSL3 silencing sensitized these cells to RSL3. Resistance to ferroptosis was also dependent on exogenous MUFAs and was enhanced by lipid droplet biogenesis inhibition. These findings highlight ACSL3 as a promising target for therapeutic strategies aimed at overcoming ferroptosis resistance in CCA.
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issn 2397-768X
language English
publishDate 2024-12-01
publisher Nature Portfolio
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series npj Precision Oncology
spelling doaj-art-cc181eb5ddd841d5ae849fb6ef0e9dde2025-08-20T01:59:39ZengNature Portfolionpj Precision Oncology2397-768X2024-12-018111410.1038/s41698-024-00783-8ACSL3 is an unfavorable prognostic marker in cholangiocarcinoma patients and confers ferroptosis resistance in cholangiocarcinoma cellsApiwit Sae-Fung0Nawaporn Vinayavekhin1Bengt Fadeel2Siriporn Jitkaew3Graduate Program in Clinical Biochemistry and Molecular Medicine, Department of Clinical Chemistry, Faculty of Allied Health Sciences, Chulalongkorn UniversityCenter of Excellence in Natural Products Chemistry, Department of Chemistry, Faculty of Science, Chulalongkorn UniversityDivision of Molecular Toxicology, Institute of Environmental Medicine, Karolinska InstitutetCenter of Excellence for Cancer and Inflammation, Department of Clinical Chemistry, Faculty of Allied Health Sciences, Chulalongkorn UniversityAbstract Cholangiocarcinoma (CCA) is a bile duct malignancy. Our previous comprehensive analysis showed that ferroptosis-related genes can stratify CCA patients into low-risk and high-risk groups based on survival time. Here, we explored the role of ferroptosis in CCA by analyzing mRNA expression in CCA patients from public databases. We identified acyl-CoA synthetase long chain family member 3 (ACSL3) as a potential ferroptosis suppressor in high-risk CCA patients. Using a panel of CCA cell lines, we confirmed ACSL3 upregulation in CCA cell lines associated with high-risk CCA, correlating this with resistance to the ferroptosis inducer RSL3. Lipidomic analysis revealed increased monounsaturated fatty acid (MUFA)-containing phospholipids in resistant cell lines. ACSL3 silencing sensitized these cells to RSL3. Resistance to ferroptosis was also dependent on exogenous MUFAs and was enhanced by lipid droplet biogenesis inhibition. These findings highlight ACSL3 as a promising target for therapeutic strategies aimed at overcoming ferroptosis resistance in CCA.https://doi.org/10.1038/s41698-024-00783-8
spellingShingle Apiwit Sae-Fung
Nawaporn Vinayavekhin
Bengt Fadeel
Siriporn Jitkaew
ACSL3 is an unfavorable prognostic marker in cholangiocarcinoma patients and confers ferroptosis resistance in cholangiocarcinoma cells
npj Precision Oncology
title ACSL3 is an unfavorable prognostic marker in cholangiocarcinoma patients and confers ferroptosis resistance in cholangiocarcinoma cells
title_full ACSL3 is an unfavorable prognostic marker in cholangiocarcinoma patients and confers ferroptosis resistance in cholangiocarcinoma cells
title_fullStr ACSL3 is an unfavorable prognostic marker in cholangiocarcinoma patients and confers ferroptosis resistance in cholangiocarcinoma cells
title_full_unstemmed ACSL3 is an unfavorable prognostic marker in cholangiocarcinoma patients and confers ferroptosis resistance in cholangiocarcinoma cells
title_short ACSL3 is an unfavorable prognostic marker in cholangiocarcinoma patients and confers ferroptosis resistance in cholangiocarcinoma cells
title_sort acsl3 is an unfavorable prognostic marker in cholangiocarcinoma patients and confers ferroptosis resistance in cholangiocarcinoma cells
url https://doi.org/10.1038/s41698-024-00783-8
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AT nawapornvinayavekhin acsl3isanunfavorableprognosticmarkerincholangiocarcinomapatientsandconfersferroptosisresistanceincholangiocarcinomacells
AT bengtfadeel acsl3isanunfavorableprognosticmarkerincholangiocarcinomapatientsandconfersferroptosisresistanceincholangiocarcinomacells
AT siripornjitkaew acsl3isanunfavorableprognosticmarkerincholangiocarcinomapatientsandconfersferroptosisresistanceincholangiocarcinomacells