AGEs-RAGE manipulates tumor intrinsic pERK/Sp1/IL6 pathway and reprograms macrophage to promote intrahepatic cholangiocarcinoma progression

Tumors often exhibit oxygen deprivation and enhanced glucose uptake, leading to glycolysis. Advanced glycation end products (AGEs) protein modifications induced by hyperglycemia—activate signaling pathways that promote cancer progression upon binding to its receptor (RAGE). In this study, AGEs-treat...

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Main Authors: Juan Zhang, Biyang Jing, Xiaojian Ni, Youpei Lin, Jiaomeng Pan, MaoPei Chen, Boheng Zhang, Lan Zhang, Ningling Ge, Ruyuan Deng, Xiao Wang, Guohe Song
Format: Article
Language:English
Published: Elsevier 2025-10-01
Series:Translational Oncology
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Online Access:http://www.sciencedirect.com/science/article/pii/S1936523325001779
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author Juan Zhang
Biyang Jing
Xiaojian Ni
Youpei Lin
Jiaomeng Pan
MaoPei Chen
Boheng Zhang
Lan Zhang
Ningling Ge
Ruyuan Deng
Xiao Wang
Guohe Song
author_facet Juan Zhang
Biyang Jing
Xiaojian Ni
Youpei Lin
Jiaomeng Pan
MaoPei Chen
Boheng Zhang
Lan Zhang
Ningling Ge
Ruyuan Deng
Xiao Wang
Guohe Song
author_sort Juan Zhang
collection DOAJ
description Tumors often exhibit oxygen deprivation and enhanced glucose uptake, leading to glycolysis. Advanced glycation end products (AGEs) protein modifications induced by hyperglycemia—activate signaling pathways that promote cancer progression upon binding to its receptor (RAGE). In this study, AGEs-treatment enhanced the growth, invasion and migration of intrahepatic cholangiocarcinoma cells (ICC), while increasing IL-6 expression and secretion. Meanwhile, AGEs stimulated the expression of RAGE, specificity protein 1 (Sp1), and the phosphorylation of extracellular signal-regulated kinase (ERK) in a dose-dependent manner. However, these effects were attenuated by RAGE antibody blockade, RAGE knockdown, the ERK inhibitor U0126, or Sp1-specific siRNA. Furthermore, the supernatant of AGEs-treated RBE cells induced M2 polarization of THP-1 macrophages. Thus, AGEs promote ICC progression partly through the pERK/Sp1/IL-6 pathway and M2 macrophage polarization. These findings highlight underscore the role of the AGEs-RAGE axis in driving ICC progression via pERK/Sp1/IL-6 signaling.
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issn 1936-5233
language English
publishDate 2025-10-01
publisher Elsevier
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series Translational Oncology
spelling doaj-art-755a00dff3f04a1dae08e567da1f0b8a2025-08-20T03:31:11ZengElsevierTranslational Oncology1936-52332025-10-016010244610.1016/j.tranon.2025.102446AGEs-RAGE manipulates tumor intrinsic pERK/Sp1/IL6 pathway and reprograms macrophage to promote intrahepatic cholangiocarcinoma progressionJuan Zhang0Biyang Jing1Xiaojian Ni2Youpei Lin3Jiaomeng Pan4MaoPei Chen5Boheng Zhang6Lan Zhang7Ningling Ge8Ruyuan Deng9Xiao Wang10Guohe Song11Department of Hepatobiliary Oncology, Liver Cancer Institute, Key Laboratory of Carcinogenesis and Cancer Invasion, Ministry of Education, Shanghai 200032, ChinaSchool of Mathematical Sciences and Center for Statistical Science, Peking University, Beijing 100871, ChinaDepartment of Biliary Surgery and Biliary Tract Disease, Biliary Tract Disease Institute and Cancer Center, Zhongshan Hospital, Fudan University, Shanghai Biliary Tract Minimal Invasive Surgery and Materials Engineering Research Center, Shanghai 200032, ChinaDepartment of Hepatobiliary Surgery and Liver Transplantation, Key Laboratory of Carcinogenesis and Cancer Invasion, Ministry of Education, Liver Cancer Institute, Zhongshan Hospital, Fudan University, Shanghai 200032, ChinaDepartment of Hepatobiliary Surgery and Liver Transplantation, Key Laboratory of Carcinogenesis and Cancer Invasion, Ministry of Education, Liver Cancer Institute, Zhongshan Hospital, Fudan University, Shanghai 200032, ChinaDepartment of Hepatobiliary Oncology, Liver Cancer Institute, Key Laboratory of Carcinogenesis and Cancer Invasion, Ministry of Education, Shanghai 200032, ChinaDepartment of Hepatobiliary Oncology, Zhongshan Hospital, Fudan University (Xiamen Branch), Xiamen Clinical Research Center for Cancer Therapy, Clinical Research Center for Precision medicine of abdominal tumor of Fujian Province, Xiamen City, Fujian Province 361015, ChinaDepartment of Hepatobiliary Oncology, Liver Cancer Institute, Key Laboratory of Carcinogenesis and Cancer Invasion, Ministry of Education, Shanghai 200032, ChinaDepartment of Hepatobiliary Oncology, Liver Cancer Institute, Key Laboratory of Carcinogenesis and Cancer Invasion, Ministry of Education, Shanghai 200032, ChinaDepartment of Gastroenterology, Zhongshan Hospital, Fudan University, Shanghai 200032, China; Corresponding authors.Shanghai Institute of Endocrine and Metabolic Diseases, Department of Endocrine and Metabolic Diseases, Shanghai Clinical Center for Endocrine and Metabolic Diseases, Ruijin Hospital, Shanghai Jiao tong University School of Medicine, Shanghai 200025, PR China; Corresponding authors.Department of Hepatobiliary Surgery and Liver Transplantation, Key Laboratory of Carcinogenesis and Cancer Invasion, Ministry of Education, Liver Cancer Institute, Zhongshan Hospital, Fudan University, Shanghai 200032, China; Corresponding authors.Tumors often exhibit oxygen deprivation and enhanced glucose uptake, leading to glycolysis. Advanced glycation end products (AGEs) protein modifications induced by hyperglycemia—activate signaling pathways that promote cancer progression upon binding to its receptor (RAGE). In this study, AGEs-treatment enhanced the growth, invasion and migration of intrahepatic cholangiocarcinoma cells (ICC), while increasing IL-6 expression and secretion. Meanwhile, AGEs stimulated the expression of RAGE, specificity protein 1 (Sp1), and the phosphorylation of extracellular signal-regulated kinase (ERK) in a dose-dependent manner. However, these effects were attenuated by RAGE antibody blockade, RAGE knockdown, the ERK inhibitor U0126, or Sp1-specific siRNA. Furthermore, the supernatant of AGEs-treated RBE cells induced M2 polarization of THP-1 macrophages. Thus, AGEs promote ICC progression partly through the pERK/Sp1/IL-6 pathway and M2 macrophage polarization. These findings highlight underscore the role of the AGEs-RAGE axis in driving ICC progression via pERK/Sp1/IL-6 signaling.http://www.sciencedirect.com/science/article/pii/S1936523325001779Advanced glycation end productsReceptor for advanced glycation end productsExtracellular signal-regulated kinaseSpecificity protein 1IL-6Intrahepatic cholangiocarcinoma
spellingShingle Juan Zhang
Biyang Jing
Xiaojian Ni
Youpei Lin
Jiaomeng Pan
MaoPei Chen
Boheng Zhang
Lan Zhang
Ningling Ge
Ruyuan Deng
Xiao Wang
Guohe Song
AGEs-RAGE manipulates tumor intrinsic pERK/Sp1/IL6 pathway and reprograms macrophage to promote intrahepatic cholangiocarcinoma progression
Translational Oncology
Advanced glycation end products
Receptor for advanced glycation end products
Extracellular signal-regulated kinase
Specificity protein 1
IL-6
Intrahepatic cholangiocarcinoma
title AGEs-RAGE manipulates tumor intrinsic pERK/Sp1/IL6 pathway and reprograms macrophage to promote intrahepatic cholangiocarcinoma progression
title_full AGEs-RAGE manipulates tumor intrinsic pERK/Sp1/IL6 pathway and reprograms macrophage to promote intrahepatic cholangiocarcinoma progression
title_fullStr AGEs-RAGE manipulates tumor intrinsic pERK/Sp1/IL6 pathway and reprograms macrophage to promote intrahepatic cholangiocarcinoma progression
title_full_unstemmed AGEs-RAGE manipulates tumor intrinsic pERK/Sp1/IL6 pathway and reprograms macrophage to promote intrahepatic cholangiocarcinoma progression
title_short AGEs-RAGE manipulates tumor intrinsic pERK/Sp1/IL6 pathway and reprograms macrophage to promote intrahepatic cholangiocarcinoma progression
title_sort ages rage manipulates tumor intrinsic perk sp1 il6 pathway and reprograms macrophage to promote intrahepatic cholangiocarcinoma progression
topic Advanced glycation end products
Receptor for advanced glycation end products
Extracellular signal-regulated kinase
Specificity protein 1
IL-6
Intrahepatic cholangiocarcinoma
url http://www.sciencedirect.com/science/article/pii/S1936523325001779
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