F-box protein FBXO32 ubiquitinates and stabilizes D-type cyclins to drive cancer progression

Abstract D-type cyclins (hereafter, cyclin D) are central regulators orchestrating G1/S cell cycle transition. Accordingly, aberrant expression of cyclin D is strongly correlated with proliferation-related diseases such as cancer. However, the mechanisms regulating cyclin D turnover are incompletely...

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Main Authors: Feng Li, Hongqiang Yu, Yujun Zhang, Yuanhang Ma, Xinlei Chen, Jie Zhang, Liangbo Sun, Rui Guo, Ying Wu, Ping Zheng, Xiaojun Wang, Ping Bie, Fengtian He, Leida Zhang, Chuanming Xie, Haojun Xiong
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Language:English
Published: Nature Portfolio 2025-04-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-59407-9
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author Feng Li
Hongqiang Yu
Yujun Zhang
Yuanhang Ma
Xinlei Chen
Jie Zhang
Liangbo Sun
Rui Guo
Ying Wu
Ping Zheng
Xiaojun Wang
Ping Bie
Fengtian He
Leida Zhang
Chuanming Xie
Haojun Xiong
author_facet Feng Li
Hongqiang Yu
Yujun Zhang
Yuanhang Ma
Xinlei Chen
Jie Zhang
Liangbo Sun
Rui Guo
Ying Wu
Ping Zheng
Xiaojun Wang
Ping Bie
Fengtian He
Leida Zhang
Chuanming Xie
Haojun Xiong
author_sort Feng Li
collection DOAJ
description Abstract D-type cyclins (hereafter, cyclin D) are central regulators orchestrating G1/S cell cycle transition. Accordingly, aberrant expression of cyclin D is strongly correlated with proliferation-related diseases such as cancer. However, the mechanisms regulating cyclin D turnover are incompletely elucidated. Here we identify FBXO32, namely atrogin-1, as the E3 ubiquitin ligase that targets all three cyclin D for ubiquitination and stabilization. Specifically, FBXO32 catalyzes the lysine (Lys/K)27-linked polyubiquitination of cyclin D1 at the K58 site and subsequent stabilization. Moreover, GSK-3β inactivation-mediated dephosphorylation of cyclin D1 facilitates its interaction with FBXO32 and subsequent ubiquitination. Furthermore, FBXO32 exhibits tumor-promoting effect in mouse models and increased FBXO32 is associated with poor prognosis of cancer patients. Additionally, disrupting the FBXO32-cyclin D axis enhances the tumor-killing effect of cyclin-dependent kinase (CDK)4/6 inhibitor palbociclib. Collectively, these findings reveal that FBXO32 enhances the protein stability of cyclin D via K27-linked ubiquitination, and contributes to cancer progression and the limited response of cancer cells to CDK4/6 inhibitors.
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spelling doaj-art-3080bc4af35d4e958ec0dc2191c034d12025-08-20T01:47:32ZengNature PortfolioNature Communications2041-17232025-04-0116111910.1038/s41467-025-59407-9F-box protein FBXO32 ubiquitinates and stabilizes D-type cyclins to drive cancer progressionFeng Li0Hongqiang Yu1Yujun Zhang2Yuanhang Ma3Xinlei Chen4Jie Zhang5Liangbo Sun6Rui Guo7Ying Wu8Ping Zheng9Xiaojun Wang10Ping Bie11Fengtian He12Leida Zhang13Chuanming Xie14Haojun Xiong15Key Laboratory of Hepatobiliary and Pancreatic Surgery, Institute of Hepatobiliary Surgery, Southwest Hospital, Army Medical UniversityKey Laboratory of Hepatobiliary and Pancreatic Surgery, Institute of Hepatobiliary Surgery, Southwest Hospital, Army Medical UniversityKey Laboratory of Hepatobiliary and Pancreatic Surgery, Institute of Hepatobiliary Surgery, Southwest Hospital, Army Medical UniversityDepartment of General Surgery, Xinqiao Hospital, Army Medical UniversityKey Laboratory of Hepatobiliary and Pancreatic Surgery, Institute of Hepatobiliary Surgery, Southwest Hospital, Army Medical UniversityKey Laboratory of Hepatobiliary and Pancreatic Surgery, Institute of Hepatobiliary Surgery, Southwest Hospital, Army Medical UniversityDepartment of Clinical Biochemistry, Faculty of Pharmacy and Laboratory Medicine, Army Medical UniversityKey Laboratory of Hepatobiliary and Pancreatic Surgery, Institute of Hepatobiliary Surgery, Southwest Hospital, Army Medical UniversityKey Laboratory of Hepatobiliary and Pancreatic Surgery, Institute of Hepatobiliary Surgery, Southwest Hospital, Army Medical UniversityKey Laboratory of Hepatobiliary and Pancreatic Surgery, Institute of Hepatobiliary Surgery, Southwest Hospital, Army Medical UniversityKey Laboratory of Hepatobiliary and Pancreatic Surgery, Institute of Hepatobiliary Surgery, Southwest Hospital, Army Medical UniversityDepartment of Hepatobiliary and Pancreatic Surgery, The Third Affiliated Hospital of Chongqing Medical UniversityDepartment of Biochemistry and Molecular Biology, College of Basic Medical Sciences, Army Medical UniversityKey Laboratory of Hepatobiliary and Pancreatic Surgery, Institute of Hepatobiliary Surgery, Southwest Hospital, Army Medical UniversityKey Laboratory of Hepatobiliary and Pancreatic Surgery, Institute of Hepatobiliary Surgery, Southwest Hospital, Army Medical UniversityKey Laboratory of Hepatobiliary and Pancreatic Surgery, Institute of Hepatobiliary Surgery, Southwest Hospital, Army Medical UniversityAbstract D-type cyclins (hereafter, cyclin D) are central regulators orchestrating G1/S cell cycle transition. Accordingly, aberrant expression of cyclin D is strongly correlated with proliferation-related diseases such as cancer. However, the mechanisms regulating cyclin D turnover are incompletely elucidated. Here we identify FBXO32, namely atrogin-1, as the E3 ubiquitin ligase that targets all three cyclin D for ubiquitination and stabilization. Specifically, FBXO32 catalyzes the lysine (Lys/K)27-linked polyubiquitination of cyclin D1 at the K58 site and subsequent stabilization. Moreover, GSK-3β inactivation-mediated dephosphorylation of cyclin D1 facilitates its interaction with FBXO32 and subsequent ubiquitination. Furthermore, FBXO32 exhibits tumor-promoting effect in mouse models and increased FBXO32 is associated with poor prognosis of cancer patients. Additionally, disrupting the FBXO32-cyclin D axis enhances the tumor-killing effect of cyclin-dependent kinase (CDK)4/6 inhibitor palbociclib. Collectively, these findings reveal that FBXO32 enhances the protein stability of cyclin D via K27-linked ubiquitination, and contributes to cancer progression and the limited response of cancer cells to CDK4/6 inhibitors.https://doi.org/10.1038/s41467-025-59407-9
spellingShingle Feng Li
Hongqiang Yu
Yujun Zhang
Yuanhang Ma
Xinlei Chen
Jie Zhang
Liangbo Sun
Rui Guo
Ying Wu
Ping Zheng
Xiaojun Wang
Ping Bie
Fengtian He
Leida Zhang
Chuanming Xie
Haojun Xiong
F-box protein FBXO32 ubiquitinates and stabilizes D-type cyclins to drive cancer progression
Nature Communications
title F-box protein FBXO32 ubiquitinates and stabilizes D-type cyclins to drive cancer progression
title_full F-box protein FBXO32 ubiquitinates and stabilizes D-type cyclins to drive cancer progression
title_fullStr F-box protein FBXO32 ubiquitinates and stabilizes D-type cyclins to drive cancer progression
title_full_unstemmed F-box protein FBXO32 ubiquitinates and stabilizes D-type cyclins to drive cancer progression
title_short F-box protein FBXO32 ubiquitinates and stabilizes D-type cyclins to drive cancer progression
title_sort f box protein fbxo32 ubiquitinates and stabilizes d type cyclins to drive cancer progression
url https://doi.org/10.1038/s41467-025-59407-9
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