Activation of PERK/eIF2α/ATF4 signaling inhibits ERα expression in breast cancer

Approximately 70–80% of breast cancers rely on estrogen receptor alpha (ERα) for growth. The unfolded protein response (UPR), a cellular response to endoplasmic reticulum stress (ERS), is an important process crucial for oncogenic transformation. The effect of ERS on ERα expression and signaling rem...

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Main Authors: Yuanli Wu, Gang Wang, Ruixue Yang, Duanfang Zhou, Qingjuan Chen, Qiuya Wu, Bo Chen, Lie Yuan, Na Qu, Hongmei Wang, Moustapha Hassan, Ying Zhao, Mingpu Liu, Zhengze Shen, Weiying Zhou
Format: Article
Language:English
Published: Elsevier 2025-07-01
Series:Neoplasia: An International Journal for Oncology Research
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Online Access:http://www.sciencedirect.com/science/article/pii/S1476558625000442
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author Yuanli Wu
Gang Wang
Ruixue Yang
Duanfang Zhou
Qingjuan Chen
Qiuya Wu
Bo Chen
Lie Yuan
Na Qu
Hongmei Wang
Moustapha Hassan
Ying Zhao
Mingpu Liu
Zhengze Shen
Weiying Zhou
author_facet Yuanli Wu
Gang Wang
Ruixue Yang
Duanfang Zhou
Qingjuan Chen
Qiuya Wu
Bo Chen
Lie Yuan
Na Qu
Hongmei Wang
Moustapha Hassan
Ying Zhao
Mingpu Liu
Zhengze Shen
Weiying Zhou
author_sort Yuanli Wu
collection DOAJ
description Approximately 70–80% of breast cancers rely on estrogen receptor alpha (ERα) for growth. The unfolded protein response (UPR), a cellular response to endoplasmic reticulum stress (ERS), is an important process crucial for oncogenic transformation. The effect of ERS on ERα expression and signaling remains incompletely elucidated. Here, we focused on the regulatory mechanisms of ERS on ERα expression in ER-positive breast cancer (ER+ BC). Our results demonstrate that ERα protein and mRNA levels in ER+ BC cells are considerably reduced by the ERS inducers thapsigargin (TG) and brefeldin A (BFA) via the PERK/eIF2α/ATF4 signaling pathway. ChIP-qPCR and luciferase reporter gene analysis revealed that ERS induction facilitated ATF4 binding to the ESR1 (the gene encoding ERα) promoter region, thereby suppressing ESR1 promoter activity and inhibiting ERα expression. Furthermore, selective activation of PERK signaling or ATF4 overexpression attenuated ERα expression and tumor cell growth both in vitro and in vivo. In conclusion, our results demonstrate that ERS suppresses ERα expression transcriptionally via the PERK/eIF2α/ATF4 signaling. Our study provides insights into the treatment of ER+ BC by targeting ERα signaling through selective activation of the PERK branch of the UPR.
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spelling doaj-art-acd234a67df34251bdbdcb18319ea2522025-08-20T01:54:21ZengElsevierNeoplasia: An International Journal for Oncology Research1476-55862025-07-016510116510.1016/j.neo.2025.101165Activation of PERK/eIF2α/ATF4 signaling inhibits ERα expression in breast cancerYuanli Wu0Gang Wang1Ruixue Yang2Duanfang Zhou3Qingjuan Chen4Qiuya Wu5Bo Chen6Lie Yuan7Na Qu8Hongmei Wang9Moustapha Hassan10Ying Zhao11Mingpu Liu12Zhengze Shen13Weiying Zhou14Department of Pharmacology, College of Pharmacy, Chongqing Medical University, Chongqing, 400016, PR China; Chongqing Key Laboratory of Drug Metabolism, Chongqing Medical University, Chongqing, 400016, PR China; Key Laboratory for Biochemistry and Molecular Pharmacology of Chongqing, Chongqing Medical University, Chongqing, 400016, PR ChinaDepartment of Pharmacology, College of Pharmacy, Chongqing Medical University, Chongqing, 400016, PR China; Chongqing Key Laboratory of Drug Metabolism, Chongqing Medical University, Chongqing, 400016, PR China; Key Laboratory for Biochemistry and Molecular Pharmacology of Chongqing, Chongqing Medical University, Chongqing, 400016, PR ChinaDepartment of Pharmacology, College of Pharmacy, Chongqing Medical University, Chongqing, 400016, PR China; Chongqing Key Laboratory of Drug Metabolism, Chongqing Medical University, Chongqing, 400016, PR China; Key Laboratory for Biochemistry and Molecular Pharmacology of Chongqing, Chongqing Medical University, Chongqing, 400016, PR ChinaDepartment of Pharmacy, Women and Children’s Hospital of Chongqing Medical University/Chongqing Health Center for Women and Children, Chongqing, 401147, PR ChinaDepartment of Oncology, 3201 Hospital of Xi'an Jiaotong University Health Science Center, Hanzhong, 723000, Shaanxi, PR ChinaDepartment of Pharmacology, College of Pharmacy, Chongqing Medical University, Chongqing, 400016, PR China; Chongqing Key Laboratory of Drug Metabolism, Chongqing Medical University, Chongqing, 400016, PR China; Key Laboratory for Biochemistry and Molecular Pharmacology of Chongqing, Chongqing Medical University, Chongqing, 400016, PR ChinaDepartment of Pharmacology, College of Pharmacy, Chongqing Medical University, Chongqing, 400016, PR China; Chongqing Key Laboratory of Drug Metabolism, Chongqing Medical University, Chongqing, 400016, PR China; Key Laboratory for Biochemistry and Molecular Pharmacology of Chongqing, Chongqing Medical University, Chongqing, 400016, PR ChinaDepartment of Pharmacology, College of Pharmacy, Chongqing Medical University, Chongqing, 400016, PR China; Chongqing Key Laboratory of Drug Metabolism, Chongqing Medical University, Chongqing, 400016, PR China; Key Laboratory for Biochemistry and Molecular Pharmacology of Chongqing, Chongqing Medical University, Chongqing, 400016, PR ChinaDepartment of Pharmacology, College of Pharmacy, Chongqing Medical University, Chongqing, 400016, PR China; Chongqing Key Laboratory of Drug Metabolism, Chongqing Medical University, Chongqing, 400016, PR China; Key Laboratory for Biochemistry and Molecular Pharmacology of Chongqing, Chongqing Medical University, Chongqing, 400016, PR ChinaDepartment of Pharmacology, College of Pharmacy, Chongqing Medical University, Chongqing, 400016, PR China; Chongqing Key Laboratory of Drug Metabolism, Chongqing Medical University, Chongqing, 400016, PR China; Key Laboratory for Biochemistry and Molecular Pharmacology of Chongqing, Chongqing Medical University, Chongqing, 400016, PR China; Department of Pharmacy, The First Affiliated Hospital of Chongqing Medical University, Chongqing, PR ChinaExperimental Cancer Medicine, Division of Biomolecular and Cellular Medicine (BCM), Department of Laboratory Medicine, Karolinska Institutet, Huddinge, 14186, SwedenExperimental Cancer Medicine, Division of Biomolecular and Cellular Medicine (BCM), Department of Laboratory Medicine, Karolinska Institutet, Huddinge, 14186, SwedenDepartment of Pharmacology, College of Pharmacy, Chongqing Medical University, Chongqing, 400016, PR China; Chongqing Key Laboratory of Drug Metabolism, Chongqing Medical University, Chongqing, 400016, PR China; Key Laboratory for Biochemistry and Molecular Pharmacology of Chongqing, Chongqing Medical University, Chongqing, 400016, PR ChinaDepartment of Pharmacy, Yongchuan Hospital of Chongqing Medical University, Chongqing, 402160, PR China; Corresponding authors.Department of Pharmacology, College of Pharmacy, Chongqing Medical University, Chongqing, 400016, PR China; Chongqing Key Laboratory of Drug Metabolism, Chongqing Medical University, Chongqing, 400016, PR China; Key Laboratory for Biochemistry and Molecular Pharmacology of Chongqing, Chongqing Medical University, Chongqing, 400016, PR China; Corresponding authors.Approximately 70–80% of breast cancers rely on estrogen receptor alpha (ERα) for growth. The unfolded protein response (UPR), a cellular response to endoplasmic reticulum stress (ERS), is an important process crucial for oncogenic transformation. The effect of ERS on ERα expression and signaling remains incompletely elucidated. Here, we focused on the regulatory mechanisms of ERS on ERα expression in ER-positive breast cancer (ER+ BC). Our results demonstrate that ERα protein and mRNA levels in ER+ BC cells are considerably reduced by the ERS inducers thapsigargin (TG) and brefeldin A (BFA) via the PERK/eIF2α/ATF4 signaling pathway. ChIP-qPCR and luciferase reporter gene analysis revealed that ERS induction facilitated ATF4 binding to the ESR1 (the gene encoding ERα) promoter region, thereby suppressing ESR1 promoter activity and inhibiting ERα expression. Furthermore, selective activation of PERK signaling or ATF4 overexpression attenuated ERα expression and tumor cell growth both in vitro and in vivo. In conclusion, our results demonstrate that ERS suppresses ERα expression transcriptionally via the PERK/eIF2α/ATF4 signaling. Our study provides insights into the treatment of ER+ BC by targeting ERα signaling through selective activation of the PERK branch of the UPR.http://www.sciencedirect.com/science/article/pii/S1476558625000442Breast cancerESR1ERαEndoplasmic reticulum stressUnfolded protein responseATF4
spellingShingle Yuanli Wu
Gang Wang
Ruixue Yang
Duanfang Zhou
Qingjuan Chen
Qiuya Wu
Bo Chen
Lie Yuan
Na Qu
Hongmei Wang
Moustapha Hassan
Ying Zhao
Mingpu Liu
Zhengze Shen
Weiying Zhou
Activation of PERK/eIF2α/ATF4 signaling inhibits ERα expression in breast cancer
Neoplasia: An International Journal for Oncology Research
Breast cancer
ESR1
ERα
Endoplasmic reticulum stress
Unfolded protein response
ATF4
title Activation of PERK/eIF2α/ATF4 signaling inhibits ERα expression in breast cancer
title_full Activation of PERK/eIF2α/ATF4 signaling inhibits ERα expression in breast cancer
title_fullStr Activation of PERK/eIF2α/ATF4 signaling inhibits ERα expression in breast cancer
title_full_unstemmed Activation of PERK/eIF2α/ATF4 signaling inhibits ERα expression in breast cancer
title_short Activation of PERK/eIF2α/ATF4 signaling inhibits ERα expression in breast cancer
title_sort activation of perk eif2α atf4 signaling inhibits erα expression in breast cancer
topic Breast cancer
ESR1
ERα
Endoplasmic reticulum stress
Unfolded protein response
ATF4
url http://www.sciencedirect.com/science/article/pii/S1476558625000442
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