Mechanical signal modulates prostate cancer immune escape by USP8-mediated ubiquitination-dependent degradation of PD-L1 and MHC-1

Abstract The tumor environment of prostate cancer (PCa) tissues of high Gleason score has been proved to be more immune suppressive and has higher extracellular matrix (ECM) stiffness, but whether ECM mechanical stiffness is the cause of higher ability of invasiveness and immune escape of PCa with h...

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Main Authors: Zhi-Bin Ke, Jia-Yin Chen, Yu-Ting Xue, Bin Lin, Qi Huang, Xu-Yun Huang, Dong-Ning Chen, Shao-Hao Chen, Xiao-Jian Ye, Qing-Shui Zheng, Yong Wei, Xue-Yi Xue, Ning Xu
Format: Article
Language:English
Published: Nature Publishing Group 2025-05-01
Series:Cell Death and Disease
Online Access:https://doi.org/10.1038/s41419-025-07736-4
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author Zhi-Bin Ke
Jia-Yin Chen
Yu-Ting Xue
Bin Lin
Qi Huang
Xu-Yun Huang
Dong-Ning Chen
Shao-Hao Chen
Xiao-Jian Ye
Qing-Shui Zheng
Yong Wei
Xue-Yi Xue
Ning Xu
author_facet Zhi-Bin Ke
Jia-Yin Chen
Yu-Ting Xue
Bin Lin
Qi Huang
Xu-Yun Huang
Dong-Ning Chen
Shao-Hao Chen
Xiao-Jian Ye
Qing-Shui Zheng
Yong Wei
Xue-Yi Xue
Ning Xu
author_sort Zhi-Bin Ke
collection DOAJ
description Abstract The tumor environment of prostate cancer (PCa) tissues of high Gleason score has been proved to be more immune suppressive and has higher extracellular matrix (ECM) stiffness, but whether ECM mechanical stiffness is the cause of higher ability of invasiveness and immune escape of PCa with high Gleason score remains uncertain. In this study, we showed that higher polyacrylamide hydrogels (PAAG) stiffness resulted in the progression and immune escape of PCa via integrin β1/FAK/YAP axis. The translocation of YAP into cell nucleus to bind to TEAD2 promoted the transcriptional activation of USP8. NBR1 could be ubiquitinated, and then degraded, via interacting with P62/SQSTM1 and through autophagy-lysosome pathway. Increased expression of USP8 promoted the abundance of NBR1 via K63-linked de-ubiquitination and PD-L1 via K48-linked de-ubiquitination in response to high PAAG stiffness. NBR1-mediated selective autophagy accelerated the degradation of MHC-1 of PCa. The USP8 inhibitor presented a potential application value in sensitizing immunotherapy of PCa. Taken together, we identified a USP8-mediated de-ubiquitination mechanism that involves in the process of high PAAG stiffness-mediated high expression of PD-L1 and low expression of MHC-1 of PCa cells, which provided a rationale of immunotherapy sensitization of PCa via USP8 inhibition.
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spelling doaj-art-06950d1778f548c28e4977f9b5283f4b2025-08-20T01:53:20ZengNature Publishing GroupCell Death and Disease2041-48892025-05-0116111910.1038/s41419-025-07736-4Mechanical signal modulates prostate cancer immune escape by USP8-mediated ubiquitination-dependent degradation of PD-L1 and MHC-1Zhi-Bin Ke0Jia-Yin Chen1Yu-Ting Xue2Bin Lin3Qi Huang4Xu-Yun Huang5Dong-Ning Chen6Shao-Hao Chen7Xiao-Jian Ye8Qing-Shui Zheng9Yong Wei10Xue-Yi Xue11Ning Xu12Department of Urology, Urology Research Institute, the First Affiliated Hospital, Fujian Medical UniversityDepartment of Urology, Urology Research Institute, the First Affiliated Hospital, Fujian Medical UniversityDepartment of Urology, Urology Research Institute, the First Affiliated Hospital, Fujian Medical UniversityDepartment of Urology, Urology Research Institute, the First Affiliated Hospital, Fujian Medical UniversityDepartment of Urology, Urology Research Institute, the First Affiliated Hospital, Fujian Medical UniversityDepartment of Urology, Urology Research Institute, the First Affiliated Hospital, Fujian Medical UniversityDepartment of Urology, Urology Research Institute, the First Affiliated Hospital, Fujian Medical UniversityDepartment of Urology, Urology Research Institute, the First Affiliated Hospital, Fujian Medical UniversityDepartment of Ultrasonography, the First Affiliated Hospital, Fujian Medical UniversityDepartment of Urology, Urology Research Institute, the First Affiliated Hospital, Fujian Medical UniversityDepartment of Urology, Urology Research Institute, the First Affiliated Hospital, Fujian Medical UniversityDepartment of Urology, Urology Research Institute, the First Affiliated Hospital, Fujian Medical UniversityDepartment of Urology, Urology Research Institute, the First Affiliated Hospital, Fujian Medical UniversityAbstract The tumor environment of prostate cancer (PCa) tissues of high Gleason score has been proved to be more immune suppressive and has higher extracellular matrix (ECM) stiffness, but whether ECM mechanical stiffness is the cause of higher ability of invasiveness and immune escape of PCa with high Gleason score remains uncertain. In this study, we showed that higher polyacrylamide hydrogels (PAAG) stiffness resulted in the progression and immune escape of PCa via integrin β1/FAK/YAP axis. The translocation of YAP into cell nucleus to bind to TEAD2 promoted the transcriptional activation of USP8. NBR1 could be ubiquitinated, and then degraded, via interacting with P62/SQSTM1 and through autophagy-lysosome pathway. Increased expression of USP8 promoted the abundance of NBR1 via K63-linked de-ubiquitination and PD-L1 via K48-linked de-ubiquitination in response to high PAAG stiffness. NBR1-mediated selective autophagy accelerated the degradation of MHC-1 of PCa. The USP8 inhibitor presented a potential application value in sensitizing immunotherapy of PCa. Taken together, we identified a USP8-mediated de-ubiquitination mechanism that involves in the process of high PAAG stiffness-mediated high expression of PD-L1 and low expression of MHC-1 of PCa cells, which provided a rationale of immunotherapy sensitization of PCa via USP8 inhibition.https://doi.org/10.1038/s41419-025-07736-4
spellingShingle Zhi-Bin Ke
Jia-Yin Chen
Yu-Ting Xue
Bin Lin
Qi Huang
Xu-Yun Huang
Dong-Ning Chen
Shao-Hao Chen
Xiao-Jian Ye
Qing-Shui Zheng
Yong Wei
Xue-Yi Xue
Ning Xu
Mechanical signal modulates prostate cancer immune escape by USP8-mediated ubiquitination-dependent degradation of PD-L1 and MHC-1
Cell Death and Disease
title Mechanical signal modulates prostate cancer immune escape by USP8-mediated ubiquitination-dependent degradation of PD-L1 and MHC-1
title_full Mechanical signal modulates prostate cancer immune escape by USP8-mediated ubiquitination-dependent degradation of PD-L1 and MHC-1
title_fullStr Mechanical signal modulates prostate cancer immune escape by USP8-mediated ubiquitination-dependent degradation of PD-L1 and MHC-1
title_full_unstemmed Mechanical signal modulates prostate cancer immune escape by USP8-mediated ubiquitination-dependent degradation of PD-L1 and MHC-1
title_short Mechanical signal modulates prostate cancer immune escape by USP8-mediated ubiquitination-dependent degradation of PD-L1 and MHC-1
title_sort mechanical signal modulates prostate cancer immune escape by usp8 mediated ubiquitination dependent degradation of pd l1 and mhc 1
url https://doi.org/10.1038/s41419-025-07736-4
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