Arid1a deficiency sensitises pancreatic cancer to fatty acid synthase inhibition

Abstract Background Mutations in the AT‐rich interactive domain‐containing protein 1A (ARID1A) gene are frequently found in pancreatic cancer. However, the contribution of ARID1A inactivation to pancreatic tumorigenesis remains unclear. Previous work showed that depletion of Arid1a at early developm...

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Main Authors: Tzu‐Lei Kuo, Ya‐Chin Hou, Yan‐Shen Shan, Li‐Tzong Chen, Wen‐Chun Hung
Format: Article
Language:English
Published: Wiley 2025-07-01
Series:Clinical and Translational Medicine
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Online Access:https://doi.org/10.1002/ctm2.70394
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author Tzu‐Lei Kuo
Ya‐Chin Hou
Yan‐Shen Shan
Li‐Tzong Chen
Wen‐Chun Hung
author_facet Tzu‐Lei Kuo
Ya‐Chin Hou
Yan‐Shen Shan
Li‐Tzong Chen
Wen‐Chun Hung
author_sort Tzu‐Lei Kuo
collection DOAJ
description Abstract Background Mutations in the AT‐rich interactive domain‐containing protein 1A (ARID1A) gene are frequently found in pancreatic cancer. However, the contribution of ARID1A inactivation to pancreatic tumorigenesis remains unclear. Previous work showed that depletion of Arid1a at early developmental stages induces metabolic disturbance and diabetes mellitus in mice. Methods and Results In this study, we generated a genetically engineered mouse model harboring both K‐ras mutation and Arid1a depletion (KAR mice). We found that the combination of these two genetic alterations induces pancreatic tumor formation. Compared to tumors in K‐ras and Tp53‐mutant mice (KPC mice), KAR tumors showed increased immune cell infiltration and reduced stromal activation. Transcriptomic analysis revealed significant upregulation of fatty acid metabolism and fatty acid synthase (FASN) in KAR tumors, with ARID1A directly regulating Fasn expression. Pharmacological inhibition of FASN reduced tumor cell viability and slowed tumor progression in vivo. Analysis of clinical datasets showed an inverse correlation between ARID1A and FASN expression, with high FASN levels predicting worse patient survival. Conclusion ARID1A deficiency promotes fatty acid metabolism to accelerate pancreatic tumorigenesis. FASN is a potential therapeutic target for ARID1A‐deficient pancreatic cancer.Mutations in AT‐rich interactive domain‐containing protein 1A (ARID1A) gene are frequently found in pancreatic cancer. However, the contribution of ARID1A inactivation to pancreatic tumourigenesis is not well‐characterised. Previously, we generated genetically engineered mice with specific depletion of Arid1a gene in the pancreas and found that depletion of Arid1a at early developmental stage induced metabolic disturbance and diabetes mellitus. In this study, we established a mouse model with K‐ras mutation and Arid1a depletion (KAR mice) in the pancreas and showed that the combination of these two genetic alterations induced pancreatic tumour formation. Compared to the tumours developed in mice with K‐ras mutation and Tp53 deficiency (KPC mice), KAR tumours exhibited increased immune cell infiltration and reduced stromal activation. Our results demonstrated a significant upregulation of fatty acid metabolism and fatty acid synthase (FASN) in the KAR tumours, with ARID1A directly regulating FASN expression. Inhibition of FASN by chemical inhibitor reduced tumour cell viability and slowed tumour progression in mice. Clinical data revealed a negative correlation between ARID1A expression and FASN, with high FASN levels associated with worse patient survival. Collectively, ARID1A deficiency upregulates fatty acid metabolism to accelerate pancreatic tumourigenesis and FASN is a potential therapeutic target for ARID1A‐deficient pancreatic cancer. Key points ARID1A mutations drive metabolic reprogramming in pancreatic cancer. Co‐occurrence of K‐ras mutation and Arid1a loss induces tumor formation with distinct immune microenvironment features. FASN is upregulated by ARID1A deficiency and its inhibition suppresses tumor growth. Targeting FASN may benefit patients with ARID1A‐deficient pancreatic cancer.
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spelling doaj-art-7e5c99220e4146e0bf2cb4faff99fab72025-08-22T06:42:10ZengWileyClinical and Translational Medicine2001-13262025-07-01157n/an/a10.1002/ctm2.70394Arid1a deficiency sensitises pancreatic cancer to fatty acid synthase inhibitionTzu‐Lei Kuo0Ya‐Chin Hou1Yan‐Shen Shan2Li‐Tzong Chen3Wen‐Chun Hung4National Institute of Cancer Research, National Health Research Institutes Tainan TaiwanInstitute of Clinical Medicine, School of Medicine, National Cheng Kung University Tainan TaiwanInstitute of Clinical Medicine, School of Medicine, National Cheng Kung University Tainan TaiwanNational Institute of Cancer Research, National Health Research Institutes Tainan TaiwanNational Institute of Cancer Research, National Health Research Institutes Tainan TaiwanAbstract Background Mutations in the AT‐rich interactive domain‐containing protein 1A (ARID1A) gene are frequently found in pancreatic cancer. However, the contribution of ARID1A inactivation to pancreatic tumorigenesis remains unclear. Previous work showed that depletion of Arid1a at early developmental stages induces metabolic disturbance and diabetes mellitus in mice. Methods and Results In this study, we generated a genetically engineered mouse model harboring both K‐ras mutation and Arid1a depletion (KAR mice). We found that the combination of these two genetic alterations induces pancreatic tumor formation. Compared to tumors in K‐ras and Tp53‐mutant mice (KPC mice), KAR tumors showed increased immune cell infiltration and reduced stromal activation. Transcriptomic analysis revealed significant upregulation of fatty acid metabolism and fatty acid synthase (FASN) in KAR tumors, with ARID1A directly regulating Fasn expression. Pharmacological inhibition of FASN reduced tumor cell viability and slowed tumor progression in vivo. Analysis of clinical datasets showed an inverse correlation between ARID1A and FASN expression, with high FASN levels predicting worse patient survival. Conclusion ARID1A deficiency promotes fatty acid metabolism to accelerate pancreatic tumorigenesis. FASN is a potential therapeutic target for ARID1A‐deficient pancreatic cancer.Mutations in AT‐rich interactive domain‐containing protein 1A (ARID1A) gene are frequently found in pancreatic cancer. However, the contribution of ARID1A inactivation to pancreatic tumourigenesis is not well‐characterised. Previously, we generated genetically engineered mice with specific depletion of Arid1a gene in the pancreas and found that depletion of Arid1a at early developmental stage induced metabolic disturbance and diabetes mellitus. In this study, we established a mouse model with K‐ras mutation and Arid1a depletion (KAR mice) in the pancreas and showed that the combination of these two genetic alterations induced pancreatic tumour formation. Compared to the tumours developed in mice with K‐ras mutation and Tp53 deficiency (KPC mice), KAR tumours exhibited increased immune cell infiltration and reduced stromal activation. Our results demonstrated a significant upregulation of fatty acid metabolism and fatty acid synthase (FASN) in the KAR tumours, with ARID1A directly regulating FASN expression. Inhibition of FASN by chemical inhibitor reduced tumour cell viability and slowed tumour progression in mice. Clinical data revealed a negative correlation between ARID1A expression and FASN, with high FASN levels associated with worse patient survival. Collectively, ARID1A deficiency upregulates fatty acid metabolism to accelerate pancreatic tumourigenesis and FASN is a potential therapeutic target for ARID1A‐deficient pancreatic cancer. Key points ARID1A mutations drive metabolic reprogramming in pancreatic cancer. Co‐occurrence of K‐ras mutation and Arid1a loss induces tumor formation with distinct immune microenvironment features. FASN is upregulated by ARID1A deficiency and its inhibition suppresses tumor growth. Targeting FASN may benefit patients with ARID1A‐deficient pancreatic cancer.https://doi.org/10.1002/ctm2.70394ARID1Afatty acid metabolismfatty acid synthase (FASN)K‐ras mutationpancreatic cancertumour microenvironment
spellingShingle Tzu‐Lei Kuo
Ya‐Chin Hou
Yan‐Shen Shan
Li‐Tzong Chen
Wen‐Chun Hung
Arid1a deficiency sensitises pancreatic cancer to fatty acid synthase inhibition
Clinical and Translational Medicine
ARID1A
fatty acid metabolism
fatty acid synthase (FASN)
K‐ras mutation
pancreatic cancer
tumour microenvironment
title Arid1a deficiency sensitises pancreatic cancer to fatty acid synthase inhibition
title_full Arid1a deficiency sensitises pancreatic cancer to fatty acid synthase inhibition
title_fullStr Arid1a deficiency sensitises pancreatic cancer to fatty acid synthase inhibition
title_full_unstemmed Arid1a deficiency sensitises pancreatic cancer to fatty acid synthase inhibition
title_short Arid1a deficiency sensitises pancreatic cancer to fatty acid synthase inhibition
title_sort arid1a deficiency sensitises pancreatic cancer to fatty acid synthase inhibition
topic ARID1A
fatty acid metabolism
fatty acid synthase (FASN)
K‐ras mutation
pancreatic cancer
tumour microenvironment
url https://doi.org/10.1002/ctm2.70394
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