ACACA depletion activates the cPLA2–arachidonic acid–NF-κB axis to drive inflammatory reprogramming in androgen receptor-independent prostate cancer

Abstract Background Acetyl-CoA carboxylase alpha (ACACA) is a key enzyme in fatty acid biosynthesis and a proposed therapeutic target in prostate cancer. However, its role in androgen receptor-independent prostate cancer (ARIPC), an aggressive and treatment-resistant subtype, remains unclear. This s...

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Main Authors: Shaoyou Liu, Yupeng Chen, Jian Chen, Jinchuang Li, Zhenguo Liang, Xinyue Mei, Yuanfa Feng, Zhaodong Han, Funeng Jiang, Yongding Wu, Huijing Tan, Hongwei Luo, Huichan He, Jiarun Lai, Weide Zhong
Format: Article
Language:English
Published: BMC 2025-07-01
Series:Cell Communication and Signaling
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Online Access:https://doi.org/10.1186/s12964-025-02363-0
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author Shaoyou Liu
Yupeng Chen
Jian Chen
Jinchuang Li
Zhenguo Liang
Xinyue Mei
Yuanfa Feng
Zhaodong Han
Funeng Jiang
Yongding Wu
Huijing Tan
Hongwei Luo
Huichan He
Jiarun Lai
Weide Zhong
author_facet Shaoyou Liu
Yupeng Chen
Jian Chen
Jinchuang Li
Zhenguo Liang
Xinyue Mei
Yuanfa Feng
Zhaodong Han
Funeng Jiang
Yongding Wu
Huijing Tan
Hongwei Luo
Huichan He
Jiarun Lai
Weide Zhong
author_sort Shaoyou Liu
collection DOAJ
description Abstract Background Acetyl-CoA carboxylase alpha (ACACA) is a key enzyme in fatty acid biosynthesis and a proposed therapeutic target in prostate cancer. However, its role in androgen receptor-independent prostate cancer (ARIPC), an aggressive and treatment-resistant subtype, remains unclear. This study aimed to investigate the effects of ACACA depletion on ARIPC, with a focus on inflammation and metastasis. Methods ACACA expression patterns were analyzed across multiple metastatic castration-resistant prostate cancer (mCRPC) datasets. In ARIPC cell lines, ACACA was inhibited via both shRNA and the pharmacological inhibitor TOFA. Transcriptomic, metabolomic, and single-cell RNA sequencing data were used to identify downstream changes. Inflammatory signaling was assessed by qPCR, western blotting, and immunofluorescence. Cell migration was evaluated via wound healing and transwell assays, and the metastatic potential was examined in a mouse tail vein injection model. The roles of arachidonic acid (AA), cytosolic phospholipase A2 (cPLA2), and NF-κB signaling were further tested through targeted inhibition. Results ACACA expression was reduced in ARIPC and was negatively correlated with inflammatory pathways. Its inhibition upregulated proinflammatory cytokines and chemokines, elevated AA and eicosanoid levels, and increased cPLA2 expression. Single-cell RNA sequencing confirmed NF-κB signaling enrichment in ACACA-low tumor cells. Mechanistically, elevated AA activated NF-κB signaling. ACACA depletion enhanced cell migration and metastasis, along with macrophage infiltration. Inhibiting cPLA2 or NF-κB signaling reversed these effects. Conclusions This study reveals a previously unrecognized tumor-promoting effect of ACACA depletion in ARIPC. Targeting ACACA in this context enhances inflammation and metastasis via arachidonic acid-mediated activation of NF-κB signaling. These findings highlight a context dependent, tumor-promoting role of ACACA inhibition and underscore the need for combinational strategies to avoid potential adverse outcomes in metabolic therapies. Trial registration Not applicable. Graphical Abstract
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issn 1478-811X
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publisher BMC
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series Cell Communication and Signaling
spelling doaj-art-07998ac977094d8fa9d0ec6c0bf50dd22025-08-20T03:43:01ZengBMCCell Communication and Signaling1478-811X2025-07-0123111910.1186/s12964-025-02363-0ACACA depletion activates the cPLA2–arachidonic acid–NF-κB axis to drive inflammatory reprogramming in androgen receptor-independent prostate cancerShaoyou Liu0Yupeng Chen1Jian Chen2Jinchuang Li3Zhenguo Liang4Xinyue Mei5Yuanfa Feng6Zhaodong Han7Funeng Jiang8Yongding Wu9Huijing Tan10Hongwei Luo11Huichan He12Jiarun Lai13Weide Zhong14Guangdong Provincial Key Laboratory of Urology, The First Affiliated Hospital of Guangzhou Medical UniversityDepartment of Urology, The Second Affiliated Hospital, School of Medicine, South China University of TechnologyGuangdong Provincial Key Laboratory of Urology, The First Affiliated Hospital of Guangzhou Medical UniversityDepartment of Urology, The Second Affiliated Hospital, School of Medicine, South China University of TechnologyDepartment of Urology, Guangzhou First People’s Hospital, Guangzhou Medical UniversityGuangzhou National LaboratoryGuangdong Provincial Key Laboratory of Urology, The First Affiliated Hospital of Guangzhou Medical UniversityDepartment of Urology, The Second Affiliated Hospital, School of Medicine, South China University of TechnologyDepartment of Urology, The Second Affiliated Hospital, School of Medicine, South China University of TechnologyDepartment of Urology, The Second Affiliated Hospital, School of Medicine, South China University of TechnologyDepartment of Urology, The Second Affiliated Hospital, School of Medicine, South China University of TechnologyGuangdong Provincial Institute of Nephrology, Nanfang Hospital, Southern Medical UniversityGuangdong Provincial Key Laboratory of Urology, The First Affiliated Hospital of Guangzhou Medical UniversityGuangdong Provincial Key Laboratory of Urology, The First Affiliated Hospital of Guangzhou Medical UniversityGuangdong Provincial Key Laboratory of Urology, The First Affiliated Hospital of Guangzhou Medical UniversityAbstract Background Acetyl-CoA carboxylase alpha (ACACA) is a key enzyme in fatty acid biosynthesis and a proposed therapeutic target in prostate cancer. However, its role in androgen receptor-independent prostate cancer (ARIPC), an aggressive and treatment-resistant subtype, remains unclear. This study aimed to investigate the effects of ACACA depletion on ARIPC, with a focus on inflammation and metastasis. Methods ACACA expression patterns were analyzed across multiple metastatic castration-resistant prostate cancer (mCRPC) datasets. In ARIPC cell lines, ACACA was inhibited via both shRNA and the pharmacological inhibitor TOFA. Transcriptomic, metabolomic, and single-cell RNA sequencing data were used to identify downstream changes. Inflammatory signaling was assessed by qPCR, western blotting, and immunofluorescence. Cell migration was evaluated via wound healing and transwell assays, and the metastatic potential was examined in a mouse tail vein injection model. The roles of arachidonic acid (AA), cytosolic phospholipase A2 (cPLA2), and NF-κB signaling were further tested through targeted inhibition. Results ACACA expression was reduced in ARIPC and was negatively correlated with inflammatory pathways. Its inhibition upregulated proinflammatory cytokines and chemokines, elevated AA and eicosanoid levels, and increased cPLA2 expression. Single-cell RNA sequencing confirmed NF-κB signaling enrichment in ACACA-low tumor cells. Mechanistically, elevated AA activated NF-κB signaling. ACACA depletion enhanced cell migration and metastasis, along with macrophage infiltration. Inhibiting cPLA2 or NF-κB signaling reversed these effects. Conclusions This study reveals a previously unrecognized tumor-promoting effect of ACACA depletion in ARIPC. Targeting ACACA in this context enhances inflammation and metastasis via arachidonic acid-mediated activation of NF-κB signaling. These findings highlight a context dependent, tumor-promoting role of ACACA inhibition and underscore the need for combinational strategies to avoid potential adverse outcomes in metabolic therapies. Trial registration Not applicable. Graphical Abstracthttps://doi.org/10.1186/s12964-025-02363-0ACACAARIPCArachidonic acid metabolismMetastasisInflammationNF-κB
spellingShingle Shaoyou Liu
Yupeng Chen
Jian Chen
Jinchuang Li
Zhenguo Liang
Xinyue Mei
Yuanfa Feng
Zhaodong Han
Funeng Jiang
Yongding Wu
Huijing Tan
Hongwei Luo
Huichan He
Jiarun Lai
Weide Zhong
ACACA depletion activates the cPLA2–arachidonic acid–NF-κB axis to drive inflammatory reprogramming in androgen receptor-independent prostate cancer
Cell Communication and Signaling
ACACA
ARIPC
Arachidonic acid metabolism
Metastasis
Inflammation
NF-κB
title ACACA depletion activates the cPLA2–arachidonic acid–NF-κB axis to drive inflammatory reprogramming in androgen receptor-independent prostate cancer
title_full ACACA depletion activates the cPLA2–arachidonic acid–NF-κB axis to drive inflammatory reprogramming in androgen receptor-independent prostate cancer
title_fullStr ACACA depletion activates the cPLA2–arachidonic acid–NF-κB axis to drive inflammatory reprogramming in androgen receptor-independent prostate cancer
title_full_unstemmed ACACA depletion activates the cPLA2–arachidonic acid–NF-κB axis to drive inflammatory reprogramming in androgen receptor-independent prostate cancer
title_short ACACA depletion activates the cPLA2–arachidonic acid–NF-κB axis to drive inflammatory reprogramming in androgen receptor-independent prostate cancer
title_sort acaca depletion activates the cpla2 arachidonic acid nf κb axis to drive inflammatory reprogramming in androgen receptor independent prostate cancer
topic ACACA
ARIPC
Arachidonic acid metabolism
Metastasis
Inflammation
NF-κB
url https://doi.org/10.1186/s12964-025-02363-0
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