Radiofrequency ablation plays double role in immunosuppression and activation of PBMCs in recurrent hepatocellular carcinoma

BackgroundRadiofrequency ablation (RFA) is the primary curative treatment for hepatocellular carcinoma (HCC) patients who are not eligible for surgery. However, the effects of RFA on the global tumor immune response remain unclear.MethodIn this study, we examined the phenotypic and functional change...

Full description

Bibliographic Details
Main Authors: Yang Zhao, Tongwang Yang, Yabo Ouyang, Wei Rao, Kai Liu, Jiasheng Zheng, Fudong Lv, Ying Shi, Feng Wang, Dongjie Liu, Luxin Qiao, Zhenying Xia, Yushi Zhang, Dexi Chen, Wenjing Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2024.1339213/full
_version_ 1827370459689123840
author Yang Zhao
Yang Zhao
Tongwang Yang
Tongwang Yang
Yabo Ouyang
Yabo Ouyang
Wei Rao
Kai Liu
Kai Liu
Jiasheng Zheng
Fudong Lv
Ying Shi
Ying Shi
Feng Wang
Dongjie Liu
Dongjie Liu
Luxin Qiao
Luxin Qiao
Zhenying Xia
Yushi Zhang
Dexi Chen
Dexi Chen
Dexi Chen
Wenjing Wang
Wenjing Wang
author_facet Yang Zhao
Yang Zhao
Tongwang Yang
Tongwang Yang
Yabo Ouyang
Yabo Ouyang
Wei Rao
Kai Liu
Kai Liu
Jiasheng Zheng
Fudong Lv
Ying Shi
Ying Shi
Feng Wang
Dongjie Liu
Dongjie Liu
Luxin Qiao
Luxin Qiao
Zhenying Xia
Yushi Zhang
Dexi Chen
Dexi Chen
Dexi Chen
Wenjing Wang
Wenjing Wang
author_sort Yang Zhao
collection DOAJ
description BackgroundRadiofrequency ablation (RFA) is the primary curative treatment for hepatocellular carcinoma (HCC) patients who are not eligible for surgery. However, the effects of RFA on the global tumor immune response remain unclear.MethodIn this study, we examined the phenotypic and functional changes in peripheral blood mononuclear cells (PBMCs) from recurrent HCC patients who had undergone two RFA treatments using mass cytometry and high-throughput mRNA assays. ResultsWe observed significant increase in monocytes and decrease in T cell subpopulations three days after the first RFA treatment and three days after the second RFA treatment. The down-regulation of GZMB, GZMH, GZMK, and CD8A, which are involved in the cytotoxic function of T cells, was observed following RFA. Furthermore, the population of CD8 effector and memory T cells (CD8 Teff and CD8 Tem) significantly decreased after RFA. The expression of CD5 and CD161 in various T cell subpopulations also showed significant reductions. Additionally, elevated secretion of VEGF was observed in monocytes, B cells, regulatory T cells (Tregs), and CD4 naive T cells. ConclusionIn recurrent HCC patients, serum components derived from radiofrequency therapy can enhance the antigen-presenting capacity of monocytes. However, they also inhibit the anti-cancer immune response by reducing the population of CD8 effector and memory T cells and suppressing the activation of T cells, as well as down-regulating the expression of CD161 and CD5 in various T cell subpopulations. These tumor-derived components also contribute to an immunosuppressive microenvironment by promoting the secretion of VEGF in monocytes, Tregs, B cells, and CD4 naive T cells.
first_indexed 2024-03-08T10:14:38Z
format Article
id doaj.art-6eaf9cff89c54b47beba70bf1b4970cc
institution Directory Open Access Journal
issn 1664-3224
language English
last_indexed 2024-03-08T10:14:38Z
publishDate 2024-01-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Immunology
spelling doaj.art-6eaf9cff89c54b47beba70bf1b4970cc2024-01-29T04:27:35ZengFrontiers Media S.A.Frontiers in Immunology1664-32242024-01-011510.3389/fimmu.2024.13392131339213Radiofrequency ablation plays double role in immunosuppression and activation of PBMCs in recurrent hepatocellular carcinomaYang Zhao0Yang Zhao1Tongwang Yang2Tongwang Yang3Yabo Ouyang4Yabo Ouyang5Wei Rao6Kai Liu7Kai Liu8Jiasheng Zheng9Fudong Lv10Ying Shi11Ying Shi12Feng Wang13Dongjie Liu14Dongjie Liu15Luxin Qiao16Luxin Qiao17Zhenying Xia18Yushi Zhang19Dexi Chen20Dexi Chen21Dexi Chen22Wenjing Wang23Wenjing Wang24Department of Urology, Peking Union Medical College Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Beijing, ChinaThe Affiliated Hospital of Qingdao University, Organ Transplantation Center, Qingdao, Shandong, ChinaBeijing YouAn Hospital, Capital Medical University, Beijing Institute of Hepatology, Beijing, ChinaBeijing Engineering Research Center for Precision Medicine and Transformation of Hepatitis and Liver Cancer, Beijing, ChinaBeijing YouAn Hospital, Capital Medical University, Beijing Institute of Hepatology, Beijing, ChinaBeijing Engineering Research Center for Precision Medicine and Transformation of Hepatitis and Liver Cancer, Beijing, ChinaThe Affiliated Hospital of Qingdao University, Organ Transplantation Center, Qingdao, Shandong, ChinaBeijing YouAn Hospital, Capital Medical University, Beijing Institute of Hepatology, Beijing, ChinaBeijing Engineering Research Center for Precision Medicine and Transformation of Hepatitis and Liver Cancer, Beijing, ChinaBeijing YouAn Hospital, Capital Medical University, Beijing Institute of Hepatology, Beijing, ChinaBeijing YouAn Hospital, Capital Medical University, Beijing Institute of Hepatology, Beijing, ChinaBeijing YouAn Hospital, Capital Medical University, Beijing Institute of Hepatology, Beijing, ChinaBeijing Engineering Research Center for Precision Medicine and Transformation of Hepatitis and Liver Cancer, Beijing, ChinaThe Affiliated Hospital of Qingdao University, Organ Transplantation Center, Qingdao, Shandong, ChinaBeijing YouAn Hospital, Capital Medical University, Beijing Institute of Hepatology, Beijing, ChinaBeijing Engineering Research Center for Precision Medicine and Transformation of Hepatitis and Liver Cancer, Beijing, ChinaBeijing YouAn Hospital, Capital Medical University, Beijing Institute of Hepatology, Beijing, ChinaBeijing Engineering Research Center for Precision Medicine and Transformation of Hepatitis and Liver Cancer, Beijing, ChinaThe Affiliated Hospital of Qingdao University, Organ Transplantation Center, Qingdao, Shandong, ChinaDepartment of Urology, Peking Union Medical College Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Beijing, ChinaThe Affiliated Hospital of Qingdao University, Organ Transplantation Center, Qingdao, Shandong, ChinaBeijing YouAn Hospital, Capital Medical University, Beijing Institute of Hepatology, Beijing, ChinaBeijing Engineering Research Center for Precision Medicine and Transformation of Hepatitis and Liver Cancer, Beijing, ChinaBeijing YouAn Hospital, Capital Medical University, Beijing Institute of Hepatology, Beijing, ChinaBeijing Engineering Research Center for Precision Medicine and Transformation of Hepatitis and Liver Cancer, Beijing, ChinaBackgroundRadiofrequency ablation (RFA) is the primary curative treatment for hepatocellular carcinoma (HCC) patients who are not eligible for surgery. However, the effects of RFA on the global tumor immune response remain unclear.MethodIn this study, we examined the phenotypic and functional changes in peripheral blood mononuclear cells (PBMCs) from recurrent HCC patients who had undergone two RFA treatments using mass cytometry and high-throughput mRNA assays. ResultsWe observed significant increase in monocytes and decrease in T cell subpopulations three days after the first RFA treatment and three days after the second RFA treatment. The down-regulation of GZMB, GZMH, GZMK, and CD8A, which are involved in the cytotoxic function of T cells, was observed following RFA. Furthermore, the population of CD8 effector and memory T cells (CD8 Teff and CD8 Tem) significantly decreased after RFA. The expression of CD5 and CD161 in various T cell subpopulations also showed significant reductions. Additionally, elevated secretion of VEGF was observed in monocytes, B cells, regulatory T cells (Tregs), and CD4 naive T cells. ConclusionIn recurrent HCC patients, serum components derived from radiofrequency therapy can enhance the antigen-presenting capacity of monocytes. However, they also inhibit the anti-cancer immune response by reducing the population of CD8 effector and memory T cells and suppressing the activation of T cells, as well as down-regulating the expression of CD161 and CD5 in various T cell subpopulations. These tumor-derived components also contribute to an immunosuppressive microenvironment by promoting the secretion of VEGF in monocytes, Tregs, B cells, and CD4 naive T cells. https://www.frontiersin.org/articles/10.3389/fimmu.2024.1339213/fullmass cytometryradiofrequency ablationrecurrent hepatocellular carcinomaPBMCimmunosuppresion
spellingShingle Yang Zhao
Yang Zhao
Tongwang Yang
Tongwang Yang
Yabo Ouyang
Yabo Ouyang
Wei Rao
Kai Liu
Kai Liu
Jiasheng Zheng
Fudong Lv
Ying Shi
Ying Shi
Feng Wang
Dongjie Liu
Dongjie Liu
Luxin Qiao
Luxin Qiao
Zhenying Xia
Yushi Zhang
Dexi Chen
Dexi Chen
Dexi Chen
Wenjing Wang
Wenjing Wang
Radiofrequency ablation plays double role in immunosuppression and activation of PBMCs in recurrent hepatocellular carcinoma
Frontiers in Immunology
mass cytometry
radiofrequency ablation
recurrent hepatocellular carcinoma
PBMC
immunosuppresion
title Radiofrequency ablation plays double role in immunosuppression and activation of PBMCs in recurrent hepatocellular carcinoma
title_full Radiofrequency ablation plays double role in immunosuppression and activation of PBMCs in recurrent hepatocellular carcinoma
title_fullStr Radiofrequency ablation plays double role in immunosuppression and activation of PBMCs in recurrent hepatocellular carcinoma
title_full_unstemmed Radiofrequency ablation plays double role in immunosuppression and activation of PBMCs in recurrent hepatocellular carcinoma
title_short Radiofrequency ablation plays double role in immunosuppression and activation of PBMCs in recurrent hepatocellular carcinoma
title_sort radiofrequency ablation plays double role in immunosuppression and activation of pbmcs in recurrent hepatocellular carcinoma
topic mass cytometry
radiofrequency ablation
recurrent hepatocellular carcinoma
PBMC
immunosuppresion
url https://www.frontiersin.org/articles/10.3389/fimmu.2024.1339213/full
work_keys_str_mv AT yangzhao radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT yangzhao radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT tongwangyang radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT tongwangyang radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT yaboouyang radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT yaboouyang radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT weirao radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT kailiu radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT kailiu radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT jiashengzheng radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT fudonglv radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT yingshi radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT yingshi radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT fengwang radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT dongjieliu radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT dongjieliu radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT luxinqiao radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT luxinqiao radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT zhenyingxia radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT yushizhang radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT dexichen radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT dexichen radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT dexichen radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT wenjingwang radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma
AT wenjingwang radiofrequencyablationplaysdoubleroleinimmunosuppressionandactivationofpbmcsinrecurrenthepatocellularcarcinoma