Cancer-associated fibroblasts induce sorafenib resistance of hepatocellular carcinoma cells through CXCL12/FOLR1

Abstract Background Due to the high drug resistance of hepatocellular carcinoma (HCC), sorafenib has limited efficacy in the treatment of advanced HCC. Cancer-associated fibroblasts (CAFs) play an important regulatory role in the induction of chemoresistance. This study aimed to clarify the mechanis...

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Main Authors: Jiali Zhao, En Lin, Zirui Bai, Yingbin Jia, Bo Wang, Yihua Dai, Wenfeng Zhuo, Guifang Zeng, Xialei Liu, Chaonong Cai, Peiping Li, Baojia Zou, Jian Li
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Language:English
Published: BMC 2023-12-01
Series:BMC Cancer
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Online Access:https://doi.org/10.1186/s12885-023-11613-8
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author Jiali Zhao
En Lin
Zirui Bai
Yingbin Jia
Bo Wang
Yihua Dai
Wenfeng Zhuo
Guifang Zeng
Xialei Liu
Chaonong Cai
Peiping Li
Baojia Zou
Jian Li
author_facet Jiali Zhao
En Lin
Zirui Bai
Yingbin Jia
Bo Wang
Yihua Dai
Wenfeng Zhuo
Guifang Zeng
Xialei Liu
Chaonong Cai
Peiping Li
Baojia Zou
Jian Li
author_sort Jiali Zhao
collection DOAJ
description Abstract Background Due to the high drug resistance of hepatocellular carcinoma (HCC), sorafenib has limited efficacy in the treatment of advanced HCC. Cancer-associated fibroblasts (CAFs) play an important regulatory role in the induction of chemoresistance. This study aimed to clarify the mechanism underlying CAF-mediated resistance to sorafenib in HCC. Methods Immunohistochemistry and immunofluorescence showed that the activation of CAFs was enhanced in HCC tissues. CAFs and paracancerous normal fibroblasts (NFs) were isolated from the cancer and paracancerous tissues of HCC, respectively. Cell cloning assays, ELISAs, and flow cytometry were used to detect whether CAFs induced sorafenib resistance in HCC cells via CXCL12. Western blotting and qPCR showed that CXCL12 induces sorafenib resistance in HCC cells by upregulating FOLR1. We investigated whether FOLR1 was the target molecule of CAFs regulating sorafenib resistance in HCC cells by querying gene expression data for human HCC specimens from the GEO database. Results High levels of activated CAFs were present in HCC tissues but not in paracancerous tissues. CAFs decreased the sensitivity of HCC cells to sorafenib. We found that CAFs secrete CXCL12, which upregulates FOLR1 in HCC cells to induce sorafenib resistance. Conclusions CAFs induce sorafenib resistance in HCC cells through CXCL12/FOLR1.
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spelling doaj-art-d62a3c6659d6470eba4631389bdadecc2025-08-20T03:06:01ZengBMCBMC Cancer1471-24072023-12-0123111110.1186/s12885-023-11613-8Cancer-associated fibroblasts induce sorafenib resistance of hepatocellular carcinoma cells through CXCL12/FOLR1Jiali Zhao0En Lin1Zirui Bai2Yingbin Jia3Bo Wang4Yihua Dai5Wenfeng Zhuo6Guifang Zeng7Xialei Liu8Chaonong Cai9Peiping Li10Baojia Zou11Jian Li12Department of Hepatobiliary Surgery, Fifth Affiliated Hospital of Sun Yat-Sen UniversityDepartment of Hepatobiliary Surgery, Fifth Affiliated Hospital of Sun Yat-Sen UniversityDepartment of Hepatobiliary Surgery, Fifth Affiliated Hospital of Sun Yat-Sen UniversityDepartment of Urology Surgery, Fifth Affiliated Hospital of Sun Yat-Sen UniversityDepartment of Hepatobiliary Surgery, Fifth Affiliated Hospital of Sun Yat-Sen UniversityDepartment of Anesthesiology, Fifth Affiliated Hospital of Sun Yat-Sen UniversityDepartment of Hepatobiliary Surgery, Fifth Affiliated Hospital of Sun Yat-Sen UniversityDepartment of Hepatobiliary Surgery, Fifth Affiliated Hospital of Sun Yat-Sen UniversityDepartment of Hepatobiliary Surgery, Fifth Affiliated Hospital of Sun Yat-Sen UniversityDepartment of Hepatobiliary Surgery, Fifth Affiliated Hospital of Sun Yat-Sen UniversityDepartment of Hepatobiliary Surgery, Fifth Affiliated Hospital of Sun Yat-Sen UniversityDepartment of Hepatobiliary Surgery, Fifth Affiliated Hospital of Sun Yat-Sen UniversityDepartment of Hepatobiliary Surgery, Fifth Affiliated Hospital of Sun Yat-Sen UniversityAbstract Background Due to the high drug resistance of hepatocellular carcinoma (HCC), sorafenib has limited efficacy in the treatment of advanced HCC. Cancer-associated fibroblasts (CAFs) play an important regulatory role in the induction of chemoresistance. This study aimed to clarify the mechanism underlying CAF-mediated resistance to sorafenib in HCC. Methods Immunohistochemistry and immunofluorescence showed that the activation of CAFs was enhanced in HCC tissues. CAFs and paracancerous normal fibroblasts (NFs) were isolated from the cancer and paracancerous tissues of HCC, respectively. Cell cloning assays, ELISAs, and flow cytometry were used to detect whether CAFs induced sorafenib resistance in HCC cells via CXCL12. Western blotting and qPCR showed that CXCL12 induces sorafenib resistance in HCC cells by upregulating FOLR1. We investigated whether FOLR1 was the target molecule of CAFs regulating sorafenib resistance in HCC cells by querying gene expression data for human HCC specimens from the GEO database. Results High levels of activated CAFs were present in HCC tissues but not in paracancerous tissues. CAFs decreased the sensitivity of HCC cells to sorafenib. We found that CAFs secrete CXCL12, which upregulates FOLR1 in HCC cells to induce sorafenib resistance. Conclusions CAFs induce sorafenib resistance in HCC cells through CXCL12/FOLR1.https://doi.org/10.1186/s12885-023-11613-8Cancer-associated fibroblastsHepatocellular carcinomaSorafenibResistance
spellingShingle Jiali Zhao
En Lin
Zirui Bai
Yingbin Jia
Bo Wang
Yihua Dai
Wenfeng Zhuo
Guifang Zeng
Xialei Liu
Chaonong Cai
Peiping Li
Baojia Zou
Jian Li
Cancer-associated fibroblasts induce sorafenib resistance of hepatocellular carcinoma cells through CXCL12/FOLR1
BMC Cancer
Cancer-associated fibroblasts
Hepatocellular carcinoma
Sorafenib
Resistance
title Cancer-associated fibroblasts induce sorafenib resistance of hepatocellular carcinoma cells through CXCL12/FOLR1
title_full Cancer-associated fibroblasts induce sorafenib resistance of hepatocellular carcinoma cells through CXCL12/FOLR1
title_fullStr Cancer-associated fibroblasts induce sorafenib resistance of hepatocellular carcinoma cells through CXCL12/FOLR1
title_full_unstemmed Cancer-associated fibroblasts induce sorafenib resistance of hepatocellular carcinoma cells through CXCL12/FOLR1
title_short Cancer-associated fibroblasts induce sorafenib resistance of hepatocellular carcinoma cells through CXCL12/FOLR1
title_sort cancer associated fibroblasts induce sorafenib resistance of hepatocellular carcinoma cells through cxcl12 folr1
topic Cancer-associated fibroblasts
Hepatocellular carcinoma
Sorafenib
Resistance
url https://doi.org/10.1186/s12885-023-11613-8
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