APOE Drives Glioma Progression by Modulating CCL5/CCR5 Signaling in the Tumor Microenvironment and Inducing M2 Macrophage Polarization

Background: Tumor-associated macrophages (TAMs) are pivotal in shaping the tumor microenvironment (TME) during cancer progression. Emerging evidence indicates that dysregulation of key signaling pathways in cancer cells drives the secretion of various cytokines, modulating TAMs function. This study...

Full description

Saved in:
Bibliographic Details
Main Authors: Wei Huang, Weimin Li, Xingyu Chen, Chengwei Xiang, Ke Luo
Format: Article
Language:English
Published: Elsevier 2025-05-01
Series:Immunobiology
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0171298525000294
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850130957042974720
author Wei Huang
Weimin Li
Xingyu Chen
Chengwei Xiang
Ke Luo
author_facet Wei Huang
Weimin Li
Xingyu Chen
Chengwei Xiang
Ke Luo
author_sort Wei Huang
collection DOAJ
description Background: Tumor-associated macrophages (TAMs) are pivotal in shaping the tumor microenvironment (TME) during cancer progression. Emerging evidence indicates that dysregulation of key signaling pathways in cancer cells drives the secretion of various cytokines, modulating TAMs function. This study aimed to explore how glioblastoma cells regulate macrophages and establish a TME conducive to tumor immune escape. Methods: In previous bioinformatics studies, we identified abnormally expressed genes in glioblastoma patients. Among them, the metabolism-related protein APOE garnered particular attention. We generated U87 and U251 cell lines with altered APOE expression to evaluate cancer cell invasion, migration, and inflammatory cytokine secretion through scratch assays, Transwell assays, and ELISA, respectively. Additionally, we established a co-culture system of cancer cells and monocytes THP-1 to assess the impact of shAPOE tumor cells on macrophage polarization using flow cytometry, Western blot, and immunofluorescence techniques. Result: Knockdown of APOE significantly reduced the viability, invasion, and migration capabilities of U87 and U251 cells. ELISA results also showed that APOE knockdown cells secreted higher levels of IL-6, IL-12, and TNF-α, while CCL5 and TGF-β secretion was markedly reduced. In macrophage studies, we observed that APOE knockdown altered the M1/M2 polarization ratio in THP-1 monocytes, with CCR5 inhibition further decreasing M2 macrophage proportions. Immunofluorescence analysis revealed that the reduction of M2 macrophages was dependent on APOE and CCL5. Conclusion: Our findings indicate that APOE knockdown suppresses glioblastoma cell migration, invasion, and CCL5 secretion, while enhancing the production of tumor-suppressive cytokines.
format Article
id doaj-art-a7fc3d55ff2746bfb54ad39a446b463e
institution OA Journals
issn 0171-2985
language English
publishDate 2025-05-01
publisher Elsevier
record_format Article
series Immunobiology
spelling doaj-art-a7fc3d55ff2746bfb54ad39a446b463e2025-08-20T02:32:33ZengElsevierImmunobiology0171-29852025-05-01230315289510.1016/j.imbio.2025.152895APOE Drives Glioma Progression by Modulating CCL5/CCR5 Signaling in the Tumor Microenvironment and Inducing M2 Macrophage PolarizationWei Huang0Weimin Li1Xingyu Chen2Chengwei Xiang3Ke Luo4Department of Neurosurgery, Suining Central Hospital, Suining city, Sichuan Province, ChinaDepartment of Neurosurgery, Suining Central Hospital, Suining city, Sichuan Province, ChinaDepartment of Neurosurgery, Suining Central Hospital, Suining city, Sichuan Province, ChinaDepartment of Neurosurgery, Suining Central Hospital, Suining city, Sichuan Province, ChinaDepartment of Neurosurgery, Suining Central Hospital, Suining city, Sichuan Province, China; Corresponding author at: Department of Neurosurgery, Suining Central Hospital, 27 Dongping North Road, Hedong New District, Chuanshan District, Suining City, Sichuan Province, China.Background: Tumor-associated macrophages (TAMs) are pivotal in shaping the tumor microenvironment (TME) during cancer progression. Emerging evidence indicates that dysregulation of key signaling pathways in cancer cells drives the secretion of various cytokines, modulating TAMs function. This study aimed to explore how glioblastoma cells regulate macrophages and establish a TME conducive to tumor immune escape. Methods: In previous bioinformatics studies, we identified abnormally expressed genes in glioblastoma patients. Among them, the metabolism-related protein APOE garnered particular attention. We generated U87 and U251 cell lines with altered APOE expression to evaluate cancer cell invasion, migration, and inflammatory cytokine secretion through scratch assays, Transwell assays, and ELISA, respectively. Additionally, we established a co-culture system of cancer cells and monocytes THP-1 to assess the impact of shAPOE tumor cells on macrophage polarization using flow cytometry, Western blot, and immunofluorescence techniques. Result: Knockdown of APOE significantly reduced the viability, invasion, and migration capabilities of U87 and U251 cells. ELISA results also showed that APOE knockdown cells secreted higher levels of IL-6, IL-12, and TNF-α, while CCL5 and TGF-β secretion was markedly reduced. In macrophage studies, we observed that APOE knockdown altered the M1/M2 polarization ratio in THP-1 monocytes, with CCR5 inhibition further decreasing M2 macrophage proportions. Immunofluorescence analysis revealed that the reduction of M2 macrophages was dependent on APOE and CCL5. Conclusion: Our findings indicate that APOE knockdown suppresses glioblastoma cell migration, invasion, and CCL5 secretion, while enhancing the production of tumor-suppressive cytokines.http://www.sciencedirect.com/science/article/pii/S0171298525000294GlioblastomaTumor microenvironmentAPOETumor-associated MacrophagesCCL5-CCR5 signaling pathwayImmunosuppressive Mechanisms
spellingShingle Wei Huang
Weimin Li
Xingyu Chen
Chengwei Xiang
Ke Luo
APOE Drives Glioma Progression by Modulating CCL5/CCR5 Signaling in the Tumor Microenvironment and Inducing M2 Macrophage Polarization
Immunobiology
Glioblastoma
Tumor microenvironment
APOE
Tumor-associated Macrophages
CCL5-CCR5 signaling pathway
Immunosuppressive Mechanisms
title APOE Drives Glioma Progression by Modulating CCL5/CCR5 Signaling in the Tumor Microenvironment and Inducing M2 Macrophage Polarization
title_full APOE Drives Glioma Progression by Modulating CCL5/CCR5 Signaling in the Tumor Microenvironment and Inducing M2 Macrophage Polarization
title_fullStr APOE Drives Glioma Progression by Modulating CCL5/CCR5 Signaling in the Tumor Microenvironment and Inducing M2 Macrophage Polarization
title_full_unstemmed APOE Drives Glioma Progression by Modulating CCL5/CCR5 Signaling in the Tumor Microenvironment and Inducing M2 Macrophage Polarization
title_short APOE Drives Glioma Progression by Modulating CCL5/CCR5 Signaling in the Tumor Microenvironment and Inducing M2 Macrophage Polarization
title_sort apoe drives glioma progression by modulating ccl5 ccr5 signaling in the tumor microenvironment and inducing m2 macrophage polarization
topic Glioblastoma
Tumor microenvironment
APOE
Tumor-associated Macrophages
CCL5-CCR5 signaling pathway
Immunosuppressive Mechanisms
url http://www.sciencedirect.com/science/article/pii/S0171298525000294
work_keys_str_mv AT weihuang apoedrivesgliomaprogressionbymodulatingccl5ccr5signalinginthetumormicroenvironmentandinducingm2macrophagepolarization
AT weiminli apoedrivesgliomaprogressionbymodulatingccl5ccr5signalinginthetumormicroenvironmentandinducingm2macrophagepolarization
AT xingyuchen apoedrivesgliomaprogressionbymodulatingccl5ccr5signalinginthetumormicroenvironmentandinducingm2macrophagepolarization
AT chengweixiang apoedrivesgliomaprogressionbymodulatingccl5ccr5signalinginthetumormicroenvironmentandinducingm2macrophagepolarization
AT keluo apoedrivesgliomaprogressionbymodulatingccl5ccr5signalinginthetumormicroenvironmentandinducingm2macrophagepolarization