Endosulfan promotes cell growth, migration and invasion via CCL5/CCR5 axis in MCF-7 cells

Endosulfan, recognized as an endocrine disruptor, has emerged as an important risk factor for human breast cancer. The chemokine ligand 5 (CCL5) and its receptor CCR5 constitute a biological axis, that is implicated in tumorigenesis and cancer progression. However, the role of the CCL5/CCR5 axis in...

Full description

Saved in:
Bibliographic Details
Main Authors: Zeming Liu, Xiaolin Ding, Boxiang Zhang, Yue Pang, Yuhui Wang, Dan Xu, Hailong Wang
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0147651324014209
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850168598527475712
author Zeming Liu
Xiaolin Ding
Boxiang Zhang
Yue Pang
Yuhui Wang
Dan Xu
Hailong Wang
author_facet Zeming Liu
Xiaolin Ding
Boxiang Zhang
Yue Pang
Yuhui Wang
Dan Xu
Hailong Wang
author_sort Zeming Liu
collection DOAJ
description Endosulfan, recognized as an endocrine disruptor, has emerged as an important risk factor for human breast cancer. The chemokine ligand 5 (CCL5) and its receptor CCR5 constitute a biological axis, that is implicated in tumorigenesis and cancer progression. However, the role of the CCL5/CCR5 axis in breast cancer when exposure to endosulfan remains unclear. The present study aimed to determine the significance of the CCL5/CCR5 axis in the carcinogenic effects of endosulfan in human breast cancer MCF-7 cells. The results showed that endosulfan significantly promoted cell proliferation, increased the rate of colony formation, and enhanced cell migration ability in a dose-dependent manner by activating the PI3K/AKT signaling pathway, which were rescued by the specific inhibitor (LY-294002) for PI3K/AKT signaling pathway. We utilized Cytoscape software to construct protein-protein interaction (PPI) network when exposure to endosulfan, and identified 47 highly connected genes in the network diagram centered on CCL5. Endosulfan significantly increased the secretion of CCL5 and the expression levels of CCL5/CCR5, which were reversed by CCR5 inhibitor (HY-13004). HY-13004 significantly counteracted the effects of endosulfan on colony formation, cell migration and the activation of PI3K/AKT signaling pathway. Endosulfan markedly altered the expression levels of epithelial-mesenchymal transition (EMT) biomarkers and enhanced transwell migration and invasion capabilities of MCF-7 cells, which were inhibited by HY-13004, similar to the effects observed with LY-294002. Collectively, our findings suggest that endosulfan activates the PI3K/AKT signaling pathway to promote cell growth, and induces EMT, thereby enhancing cell migration and invasion via the CCL5/CCR5 axis in MCF-7 cells.
format Article
id doaj-art-ebe4146828b8474ba08d6ad1d07b95e1
institution OA Journals
issn 0147-6513
language English
publishDate 2024-12-01
publisher Elsevier
record_format Article
series Ecotoxicology and Environmental Safety
spelling doaj-art-ebe4146828b8474ba08d6ad1d07b95e12025-08-20T02:20:56ZengElsevierEcotoxicology and Environmental Safety0147-65132024-12-0128811734410.1016/j.ecoenv.2024.117344Endosulfan promotes cell growth, migration and invasion via CCL5/CCR5 axis in MCF-7 cellsZeming Liu0Xiaolin Ding1Boxiang Zhang2Yue Pang3Yuhui Wang4Dan Xu5Hailong Wang6Institute of Environmental Systems Biology, Environment Science and Engineering College, Dalian Maritime University, Linghai Road 1, Dalian 116026, PR ChinaInstitute of Environmental Systems Biology, Environment Science and Engineering College, Dalian Maritime University, Linghai Road 1, Dalian 116026, PR ChinaInstitute of Environmental Systems Biology, Environment Science and Engineering College, Dalian Maritime University, Linghai Road 1, Dalian 116026, PR ChinaInstitute of Environmental Systems Biology, Environment Science and Engineering College, Dalian Maritime University, Linghai Road 1, Dalian 116026, PR ChinaInstitute of Environmental Systems Biology, Environment Science and Engineering College, Dalian Maritime University, Linghai Road 1, Dalian 116026, PR ChinaInstitute of Environmental Systems Biology, Environment Science and Engineering College, Dalian Maritime University, Linghai Road 1, Dalian 116026, PR China; Corresponding authors.Department of Clinical Epidemiology and Evidence-based Medicine, First Hospital of China Medical University, Shenyang 110016, PR China; Corresponding authors.Endosulfan, recognized as an endocrine disruptor, has emerged as an important risk factor for human breast cancer. The chemokine ligand 5 (CCL5) and its receptor CCR5 constitute a biological axis, that is implicated in tumorigenesis and cancer progression. However, the role of the CCL5/CCR5 axis in breast cancer when exposure to endosulfan remains unclear. The present study aimed to determine the significance of the CCL5/CCR5 axis in the carcinogenic effects of endosulfan in human breast cancer MCF-7 cells. The results showed that endosulfan significantly promoted cell proliferation, increased the rate of colony formation, and enhanced cell migration ability in a dose-dependent manner by activating the PI3K/AKT signaling pathway, which were rescued by the specific inhibitor (LY-294002) for PI3K/AKT signaling pathway. We utilized Cytoscape software to construct protein-protein interaction (PPI) network when exposure to endosulfan, and identified 47 highly connected genes in the network diagram centered on CCL5. Endosulfan significantly increased the secretion of CCL5 and the expression levels of CCL5/CCR5, which were reversed by CCR5 inhibitor (HY-13004). HY-13004 significantly counteracted the effects of endosulfan on colony formation, cell migration and the activation of PI3K/AKT signaling pathway. Endosulfan markedly altered the expression levels of epithelial-mesenchymal transition (EMT) biomarkers and enhanced transwell migration and invasion capabilities of MCF-7 cells, which were inhibited by HY-13004, similar to the effects observed with LY-294002. Collectively, our findings suggest that endosulfan activates the PI3K/AKT signaling pathway to promote cell growth, and induces EMT, thereby enhancing cell migration and invasion via the CCL5/CCR5 axis in MCF-7 cells.http://www.sciencedirect.com/science/article/pii/S0147651324014209Breast cancerCCL5CCR5PI3K/AKTEMT
spellingShingle Zeming Liu
Xiaolin Ding
Boxiang Zhang
Yue Pang
Yuhui Wang
Dan Xu
Hailong Wang
Endosulfan promotes cell growth, migration and invasion via CCL5/CCR5 axis in MCF-7 cells
Ecotoxicology and Environmental Safety
Breast cancer
CCL5
CCR5
PI3K/AKT
EMT
title Endosulfan promotes cell growth, migration and invasion via CCL5/CCR5 axis in MCF-7 cells
title_full Endosulfan promotes cell growth, migration and invasion via CCL5/CCR5 axis in MCF-7 cells
title_fullStr Endosulfan promotes cell growth, migration and invasion via CCL5/CCR5 axis in MCF-7 cells
title_full_unstemmed Endosulfan promotes cell growth, migration and invasion via CCL5/CCR5 axis in MCF-7 cells
title_short Endosulfan promotes cell growth, migration and invasion via CCL5/CCR5 axis in MCF-7 cells
title_sort endosulfan promotes cell growth migration and invasion via ccl5 ccr5 axis in mcf 7 cells
topic Breast cancer
CCL5
CCR5
PI3K/AKT
EMT
url http://www.sciencedirect.com/science/article/pii/S0147651324014209
work_keys_str_mv AT zemingliu endosulfanpromotescellgrowthmigrationandinvasionviaccl5ccr5axisinmcf7cells
AT xiaolinding endosulfanpromotescellgrowthmigrationandinvasionviaccl5ccr5axisinmcf7cells
AT boxiangzhang endosulfanpromotescellgrowthmigrationandinvasionviaccl5ccr5axisinmcf7cells
AT yuepang endosulfanpromotescellgrowthmigrationandinvasionviaccl5ccr5axisinmcf7cells
AT yuhuiwang endosulfanpromotescellgrowthmigrationandinvasionviaccl5ccr5axisinmcf7cells
AT danxu endosulfanpromotescellgrowthmigrationandinvasionviaccl5ccr5axisinmcf7cells
AT hailongwang endosulfanpromotescellgrowthmigrationandinvasionviaccl5ccr5axisinmcf7cells