Overexpression of oncogenic polo-like kinase 1 disrupts the invasiveness, cell cycle, and apoptosis in synovial sarcoma

Abstract Background Synovial sarcoma (SS) is an aggressive malignant soft tissue sarcoma of undetermined tissue origin that harbors potential metastases and recurrences, leading to a poor prognosis. Polo-like kinase 1 (PLK1) is an essential member of the serine/threonine kinase family, which plays a...

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Main Authors: Jun Zhang, Zhong Li, Ming-Yu Xie, Ning Wang, Hao Liu, Feng Li, Li-Juan Pang, Yan Qi
Format: Article
Language:English
Published: BMC 2025-06-01
Series:Journal of Translational Medicine
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Online Access:https://doi.org/10.1186/s12967-025-06740-8
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author Jun Zhang
Zhong Li
Ming-Yu Xie
Ning Wang
Hao Liu
Feng Li
Li-Juan Pang
Yan Qi
author_facet Jun Zhang
Zhong Li
Ming-Yu Xie
Ning Wang
Hao Liu
Feng Li
Li-Juan Pang
Yan Qi
author_sort Jun Zhang
collection DOAJ
description Abstract Background Synovial sarcoma (SS) is an aggressive malignant soft tissue sarcoma of undetermined tissue origin that harbors potential metastases and recurrences, leading to a poor prognosis. Polo-like kinase 1 (PLK1) is an essential member of the serine/threonine kinase family, which plays a key role in cell cycle progression and other cellular processes. Therefore, PLK1 could act as a promising target for treating various cancers, including a low incidence of sarcoma. Methods SS paraffin-embedded tissue samples were selected to detect the expression of PLK1 and apoptosis- and autophagy-related proteins using immunohistochemistry. We analyzed the effects of low PLK1 expression on the SS cell cycle and function using the PLK1 inhibitor BI2536 in SW982 and SSX1 cells (cells with high expression of the SYT-SSX1 fusion gene). Western blotting was used to detect the expression of PLK1 and apoptotic proteins in different groups. Finally, the antitumor effects and safety of BI2536 were evaluated using xenograft tumor experiments in nude mice. Results In SS tissues, PLK1 was overexpressed and autophagy-related proteins were expressed at low levels, leading to poor prognosis. Suppressing PLK1 expression using the PLK1 inhibitor BI2536 decreased the proliferation, migration, and invasion abilities of SW982 and SYT-SSX1 cells and promoted the expression of the apoptotic protein Bax. Meanwhile, we confirmed that SS cell apoptosis increased and G2/M cycle arrest occurred after PLK1 expression was inhibited. We found that BI2536 significantly inhibited the growth of SS-xenografted tumors in nude mice, and the expression of stem cell-related factors significantly decreased. Conclusion PLK1 overexpression was closely associated with poor prognosis. Suppressing PLK1 expression significantly inhibited the growth, invasion, and migration of SS cells, promoted apoptosis, and blocked the G2/M phase of the cell cycle.
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spelling doaj-art-adba0808028c4f11939a2b5613ec86ba2025-08-20T02:37:35ZengBMCJournal of Translational Medicine1479-58762025-06-0123111410.1186/s12967-025-06740-8Overexpression of oncogenic polo-like kinase 1 disrupts the invasiveness, cell cycle, and apoptosis in synovial sarcomaJun Zhang0Zhong Li1Ming-Yu Xie2Ning Wang3Hao Liu4Feng Li5Li-Juan Pang6Yan Qi7Department of Pathology, The Third Hospital of Mianyang, Sichuan Mental Health CenterDepartment of Pathology, Xiongan Xuanwu HospitalDepartment of Pathology, Central People’s Hospital of Zhanjiang & Zhanjiang Central Hospital, Guangdong Medical UniversityDepartment of Pathology, Shihezi University School of Medicine & the First Affiliated Hospital to Shihezi University School of MedicineDepartment of Pathology, Central People’s Hospital of Zhanjiang & Zhanjiang Central Hospital, Guangdong Medical UniversityDepartment of Pathology, Central People’s Hospital of Zhanjiang & Zhanjiang Central Hospital, Guangdong Medical UniversityDepartment of Pathology, Central People’s Hospital of Zhanjiang & Zhanjiang Central Hospital, Guangdong Medical UniversityDepartment of Pathology, Central People’s Hospital of Zhanjiang & Zhanjiang Central Hospital, Guangdong Medical UniversityAbstract Background Synovial sarcoma (SS) is an aggressive malignant soft tissue sarcoma of undetermined tissue origin that harbors potential metastases and recurrences, leading to a poor prognosis. Polo-like kinase 1 (PLK1) is an essential member of the serine/threonine kinase family, which plays a key role in cell cycle progression and other cellular processes. Therefore, PLK1 could act as a promising target for treating various cancers, including a low incidence of sarcoma. Methods SS paraffin-embedded tissue samples were selected to detect the expression of PLK1 and apoptosis- and autophagy-related proteins using immunohistochemistry. We analyzed the effects of low PLK1 expression on the SS cell cycle and function using the PLK1 inhibitor BI2536 in SW982 and SSX1 cells (cells with high expression of the SYT-SSX1 fusion gene). Western blotting was used to detect the expression of PLK1 and apoptotic proteins in different groups. Finally, the antitumor effects and safety of BI2536 were evaluated using xenograft tumor experiments in nude mice. Results In SS tissues, PLK1 was overexpressed and autophagy-related proteins were expressed at low levels, leading to poor prognosis. Suppressing PLK1 expression using the PLK1 inhibitor BI2536 decreased the proliferation, migration, and invasion abilities of SW982 and SYT-SSX1 cells and promoted the expression of the apoptotic protein Bax. Meanwhile, we confirmed that SS cell apoptosis increased and G2/M cycle arrest occurred after PLK1 expression was inhibited. We found that BI2536 significantly inhibited the growth of SS-xenografted tumors in nude mice, and the expression of stem cell-related factors significantly decreased. Conclusion PLK1 overexpression was closely associated with poor prognosis. Suppressing PLK1 expression significantly inhibited the growth, invasion, and migration of SS cells, promoted apoptosis, and blocked the G2/M phase of the cell cycle.https://doi.org/10.1186/s12967-025-06740-8Synovial sarcomaPLK1BI2536InvasivenessCell cycleApoptosis
spellingShingle Jun Zhang
Zhong Li
Ming-Yu Xie
Ning Wang
Hao Liu
Feng Li
Li-Juan Pang
Yan Qi
Overexpression of oncogenic polo-like kinase 1 disrupts the invasiveness, cell cycle, and apoptosis in synovial sarcoma
Journal of Translational Medicine
Synovial sarcoma
PLK1
BI2536
Invasiveness
Cell cycle
Apoptosis
title Overexpression of oncogenic polo-like kinase 1 disrupts the invasiveness, cell cycle, and apoptosis in synovial sarcoma
title_full Overexpression of oncogenic polo-like kinase 1 disrupts the invasiveness, cell cycle, and apoptosis in synovial sarcoma
title_fullStr Overexpression of oncogenic polo-like kinase 1 disrupts the invasiveness, cell cycle, and apoptosis in synovial sarcoma
title_full_unstemmed Overexpression of oncogenic polo-like kinase 1 disrupts the invasiveness, cell cycle, and apoptosis in synovial sarcoma
title_short Overexpression of oncogenic polo-like kinase 1 disrupts the invasiveness, cell cycle, and apoptosis in synovial sarcoma
title_sort overexpression of oncogenic polo like kinase 1 disrupts the invasiveness cell cycle and apoptosis in synovial sarcoma
topic Synovial sarcoma
PLK1
BI2536
Invasiveness
Cell cycle
Apoptosis
url https://doi.org/10.1186/s12967-025-06740-8
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