RNA-binding protein HuR inhibition induces multiple programmed cell death in breast and prostate cancer

Abstract The RNA-binding protein Hu antigen R (HuR) plays a pivotal role in cancer progression, and previous studies have demonstrated its involvement in suppressing cell death in cancer. However, the precise mechanisms underlying HuR inhibition-induced cell death remain elusive. Here, we investigat...

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Main Authors: Lanjing Wei, Sung Hae Kim, Ahlam M. Armaly, Jeffrey Aubé, Liang Xu, Xiaoqing Wu
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Cell Communication and Signaling
Subjects:
Online Access:https://doi.org/10.1186/s12964-024-01916-z
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author Lanjing Wei
Sung Hae Kim
Ahlam M. Armaly
Jeffrey Aubé
Liang Xu
Xiaoqing Wu
author_facet Lanjing Wei
Sung Hae Kim
Ahlam M. Armaly
Jeffrey Aubé
Liang Xu
Xiaoqing Wu
author_sort Lanjing Wei
collection DOAJ
description Abstract The RNA-binding protein Hu antigen R (HuR) plays a pivotal role in cancer progression, and previous studies have demonstrated its involvement in suppressing cell death in cancer. However, the precise mechanisms underlying HuR inhibition-induced cell death remain elusive. Here, we investigated the impacts of HuR functional inhibition via the small molecule inhibitor KH-3 on cell proliferation, colony formation, and cell death across multiple cancer cell lines, with an emphasis on breast and prostate cancers. KH-3 treatment induced apoptotic cell death of various cancer cell lines, as well as autophagy-associated cell death and ferroptosis. Remarkably, KH-3-induced cell death was partially rescued by an autophagy inhibitor and a ferroptosis inhibitor. The anti-tumor effects of KH-3 were further validated in two mouse xenograft models of human prostate cancer. Mechanistically, KH-3 reduced the expression of HuR targets involved in apoptosis and ferroptosis suppression, including cFLIP and SLC7A11, respectively. Moreover, cFLIP silencing enhanced Caspase-8 activation as well as PARP cleavage in both breast cancer and prostate cancer cells. Both KH-3-induced pharmacological HuR inhibition and RNA interference-mediated HuR knockdown reduced the expression of SLC7A11. Additionally, KH-3 also reduced XIAP and Survivin, enhancing the activation of multiple caspases and leading to apoptosis. This study highlights the critical roles of HuR in programmed cell death regulation, advocating HuR inhibition as a promising anti-tumor strategy for cell-death-inducing cancer therapy.
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spelling doaj-art-81353faa4ece45169487dba6f78ea5352024-12-08T12:38:05ZengBMCCell Communication and Signaling1478-811X2024-12-0122111410.1186/s12964-024-01916-zRNA-binding protein HuR inhibition induces multiple programmed cell death in breast and prostate cancerLanjing Wei0Sung Hae Kim1Ahlam M. Armaly2Jeffrey Aubé3Liang Xu4Xiaoqing Wu5Bioengineering Program, The University of KansasDepartment of Molecular Biosciences, The University of KansasDivision of Chemical Biology and Medicinal Chemistry, UNC Eshelman School of Pharmacy, The University of North CarolinaDivision of Chemical Biology and Medicinal Chemistry, UNC Eshelman School of Pharmacy, The University of North CarolinaDepartment of Molecular Biosciences, The University of KansasDepartment of Molecular Biosciences, The University of KansasAbstract The RNA-binding protein Hu antigen R (HuR) plays a pivotal role in cancer progression, and previous studies have demonstrated its involvement in suppressing cell death in cancer. However, the precise mechanisms underlying HuR inhibition-induced cell death remain elusive. Here, we investigated the impacts of HuR functional inhibition via the small molecule inhibitor KH-3 on cell proliferation, colony formation, and cell death across multiple cancer cell lines, with an emphasis on breast and prostate cancers. KH-3 treatment induced apoptotic cell death of various cancer cell lines, as well as autophagy-associated cell death and ferroptosis. Remarkably, KH-3-induced cell death was partially rescued by an autophagy inhibitor and a ferroptosis inhibitor. The anti-tumor effects of KH-3 were further validated in two mouse xenograft models of human prostate cancer. Mechanistically, KH-3 reduced the expression of HuR targets involved in apoptosis and ferroptosis suppression, including cFLIP and SLC7A11, respectively. Moreover, cFLIP silencing enhanced Caspase-8 activation as well as PARP cleavage in both breast cancer and prostate cancer cells. Both KH-3-induced pharmacological HuR inhibition and RNA interference-mediated HuR knockdown reduced the expression of SLC7A11. Additionally, KH-3 also reduced XIAP and Survivin, enhancing the activation of multiple caspases and leading to apoptosis. This study highlights the critical roles of HuR in programmed cell death regulation, advocating HuR inhibition as a promising anti-tumor strategy for cell-death-inducing cancer therapy.https://doi.org/10.1186/s12964-024-01916-zHuRCell deathBreast cancerProstate cancerMouse tumor models
spellingShingle Lanjing Wei
Sung Hae Kim
Ahlam M. Armaly
Jeffrey Aubé
Liang Xu
Xiaoqing Wu
RNA-binding protein HuR inhibition induces multiple programmed cell death in breast and prostate cancer
Cell Communication and Signaling
HuR
Cell death
Breast cancer
Prostate cancer
Mouse tumor models
title RNA-binding protein HuR inhibition induces multiple programmed cell death in breast and prostate cancer
title_full RNA-binding protein HuR inhibition induces multiple programmed cell death in breast and prostate cancer
title_fullStr RNA-binding protein HuR inhibition induces multiple programmed cell death in breast and prostate cancer
title_full_unstemmed RNA-binding protein HuR inhibition induces multiple programmed cell death in breast and prostate cancer
title_short RNA-binding protein HuR inhibition induces multiple programmed cell death in breast and prostate cancer
title_sort rna binding protein hur inhibition induces multiple programmed cell death in breast and prostate cancer
topic HuR
Cell death
Breast cancer
Prostate cancer
Mouse tumor models
url https://doi.org/10.1186/s12964-024-01916-z
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