Loss of Carbamoyl Phosphate Synthetase 1 Potentiates Hepatocellular Carcinoma Metastasis by Reducing Aspartate Level

Abstract Hepatocellular carcinoma (HCC) is one of the most lethal cancers worldwide. Numerous studies have shown that metabolic reprogramming is crucial for the development of HCC. Carbamoyl phosphate synthase 1 (CPS1), a rate‐limiting enzyme in urea cycle, is an abundant protein in normal hepatocyt...

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Main Authors: Siyuan Chen, Qin Tang, Manqiu Hu, Sijie Song, Xiaohong Wu, You Zhou, Zihan Yang, Siqi Liao, Li Zhou, Qingliang Wang, Hongtao Liu, Mengsu Yang, Zhe‐Sheng Chen, Wei Zhao, Song He, Zhihang Zhou
Format: Article
Language:English
Published: Wiley 2024-12-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202402703
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author Siyuan Chen
Qin Tang
Manqiu Hu
Sijie Song
Xiaohong Wu
You Zhou
Zihan Yang
Siqi Liao
Li Zhou
Qingliang Wang
Hongtao Liu
Mengsu Yang
Zhe‐Sheng Chen
Wei Zhao
Song He
Zhihang Zhou
author_facet Siyuan Chen
Qin Tang
Manqiu Hu
Sijie Song
Xiaohong Wu
You Zhou
Zihan Yang
Siqi Liao
Li Zhou
Qingliang Wang
Hongtao Liu
Mengsu Yang
Zhe‐Sheng Chen
Wei Zhao
Song He
Zhihang Zhou
author_sort Siyuan Chen
collection DOAJ
description Abstract Hepatocellular carcinoma (HCC) is one of the most lethal cancers worldwide. Numerous studies have shown that metabolic reprogramming is crucial for the development of HCC. Carbamoyl phosphate synthase 1 (CPS1), a rate‐limiting enzyme in urea cycle, is an abundant protein in normal hepatocytes, however, lacking systemic research in HCC. It is found that CPS1 is low‐expressed in HCC tissues and circulating tumor cells, negatively correlated with HCC stage and prognosis. Further study reveals that CPS1 is a double‐edged sword. On the one hand, it inhibits the activity of phosphatidylcholine‐specific phospholipase C to block the biosynthesis of diacylglycerol (DAG), leading to the downregulation of the DAG/protein kinase C pathway to inhibit invasion and metastasis of cancer cells. On the other hand, CPS1 promotes cell proliferation by increasing intracellular S‐adenosylmethionin to enhance the m6A modification of solute carrier family 1 member 3 mRNA, a key transporter for aspartate intake. Finally, CPS1 overexpressing adeno‐associated virus can dampen HCC progression. Collectively, this results uncovered that CPS1 is a switch between HCC proliferation and metastasis by increasing intracellular aspartate level.
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spelling doaj-art-2e8952e540a94e2fa9db65bef10c5b9d2024-12-04T12:14:54ZengWileyAdvanced Science2198-38442024-12-011145n/an/a10.1002/advs.202402703Loss of Carbamoyl Phosphate Synthetase 1 Potentiates Hepatocellular Carcinoma Metastasis by Reducing Aspartate LevelSiyuan Chen0Qin Tang1Manqiu Hu2Sijie Song3Xiaohong Wu4You Zhou5Zihan Yang6Siqi Liao7Li Zhou8Qingliang Wang9Hongtao Liu10Mengsu Yang11Zhe‐Sheng Chen12Wei Zhao13Song He14Zhihang Zhou15Department of Gastroenterology The Second Affiliated Hospital of Chongqing Medical University Chongqing 400010 ChinaDepartment of Gastroenterology The Second Affiliated Hospital of Chongqing Medical University Chongqing 400010 ChinaDepartment of Gastroenterology The Second Affiliated Hospital of Chongqing Medical University Chongqing 400010 ChinaDepartment of Gastroenterology The Second Affiliated Hospital of Chongqing Medical University Chongqing 400010 ChinaDepartment of Gastroenterology The Second Affiliated Hospital of Chongqing Medical University Chongqing 400010 ChinaDepartment of Gastroenterology The Second Affiliated Hospital of Chongqing Medical University Chongqing 400010 ChinaDepartment of Biomedical Sciences and Tung Biomedical Sciences Center City University of Hong Kong 83 Tat Chee Avenue Kowloon Hong Kong SAR 999077 P. R. ChinaDepartment of Gastroenterology The Second Affiliated Hospital of Chongqing Medical University Chongqing 400010 ChinaDepartment of Gastroenterology The Second Affiliated Hospital of Chongqing Medical University Chongqing 400010 ChinaDepartment of Pathology The Second Affiliated Hospital of Chongqing Medical University Chongqing 400010 ChinaDepartment of Gastroenterology The Second Affiliated Hospital of Chongqing Medical University Chongqing 400010 ChinaDepartment of Biomedical Sciences and Tung Biomedical Sciences Center City University of Hong Kong 83 Tat Chee Avenue Kowloon Hong Kong SAR 999077 P. R. ChinaDepartment of Pharmaceutical Sciences Institute for Biotechnology College of Pharmacy and Health Sciences St. John's University Queens NY 11439 USASchool of Clinical Medicine The First Affiliated Hospital Chengdu Medical College Sichuan 610500 P. R. ChinaDepartment of Gastroenterology The Second Affiliated Hospital of Chongqing Medical University Chongqing 400010 ChinaDepartment of Gastroenterology The Second Affiliated Hospital of Chongqing Medical University Chongqing 400010 ChinaAbstract Hepatocellular carcinoma (HCC) is one of the most lethal cancers worldwide. Numerous studies have shown that metabolic reprogramming is crucial for the development of HCC. Carbamoyl phosphate synthase 1 (CPS1), a rate‐limiting enzyme in urea cycle, is an abundant protein in normal hepatocytes, however, lacking systemic research in HCC. It is found that CPS1 is low‐expressed in HCC tissues and circulating tumor cells, negatively correlated with HCC stage and prognosis. Further study reveals that CPS1 is a double‐edged sword. On the one hand, it inhibits the activity of phosphatidylcholine‐specific phospholipase C to block the biosynthesis of diacylglycerol (DAG), leading to the downregulation of the DAG/protein kinase C pathway to inhibit invasion and metastasis of cancer cells. On the other hand, CPS1 promotes cell proliferation by increasing intracellular S‐adenosylmethionin to enhance the m6A modification of solute carrier family 1 member 3 mRNA, a key transporter for aspartate intake. Finally, CPS1 overexpressing adeno‐associated virus can dampen HCC progression. Collectively, this results uncovered that CPS1 is a switch between HCC proliferation and metastasis by increasing intracellular aspartate level.https://doi.org/10.1002/advs.202402703aspartateCPS1m6AmetastasisPC‐PLC
spellingShingle Siyuan Chen
Qin Tang
Manqiu Hu
Sijie Song
Xiaohong Wu
You Zhou
Zihan Yang
Siqi Liao
Li Zhou
Qingliang Wang
Hongtao Liu
Mengsu Yang
Zhe‐Sheng Chen
Wei Zhao
Song He
Zhihang Zhou
Loss of Carbamoyl Phosphate Synthetase 1 Potentiates Hepatocellular Carcinoma Metastasis by Reducing Aspartate Level
Advanced Science
aspartate
CPS1
m6A
metastasis
PC‐PLC
title Loss of Carbamoyl Phosphate Synthetase 1 Potentiates Hepatocellular Carcinoma Metastasis by Reducing Aspartate Level
title_full Loss of Carbamoyl Phosphate Synthetase 1 Potentiates Hepatocellular Carcinoma Metastasis by Reducing Aspartate Level
title_fullStr Loss of Carbamoyl Phosphate Synthetase 1 Potentiates Hepatocellular Carcinoma Metastasis by Reducing Aspartate Level
title_full_unstemmed Loss of Carbamoyl Phosphate Synthetase 1 Potentiates Hepatocellular Carcinoma Metastasis by Reducing Aspartate Level
title_short Loss of Carbamoyl Phosphate Synthetase 1 Potentiates Hepatocellular Carcinoma Metastasis by Reducing Aspartate Level
title_sort loss of carbamoyl phosphate synthetase 1 potentiates hepatocellular carcinoma metastasis by reducing aspartate level
topic aspartate
CPS1
m6A
metastasis
PC‐PLC
url https://doi.org/10.1002/advs.202402703
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