Targeting PPARγ via SIAH1/2-mediated ubiquitin-proteasomal degradation as a new therapeutic approach in luminal-type bladder cancer

Abstract Bladder cancer (BC) is the second most prevalent genitourinary malignancy worldwide. Despite recent approvals of immune checkpoint inhibitors and targeted therapy for muscle invasive or recurrent BC, options remain limited for patients with non-muscle invasive BC (NMIBC) refractory to Bacil...

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Main Authors: Chih-Chieh Tu, Tsung-Han Hsieh, Cheng-Ying Chu, Yu-Chen Lin, Bo-Jyun Lin, Chun-Han Chen
Format: Article
Language:English
Published: Nature Publishing Group 2024-12-01
Series:Cell Death and Disease
Online Access:https://doi.org/10.1038/s41419-024-07298-x
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author Chih-Chieh Tu
Tsung-Han Hsieh
Cheng-Ying Chu
Yu-Chen Lin
Bo-Jyun Lin
Chun-Han Chen
author_facet Chih-Chieh Tu
Tsung-Han Hsieh
Cheng-Ying Chu
Yu-Chen Lin
Bo-Jyun Lin
Chun-Han Chen
author_sort Chih-Chieh Tu
collection DOAJ
description Abstract Bladder cancer (BC) is the second most prevalent genitourinary malignancy worldwide. Despite recent approvals of immune checkpoint inhibitors and targeted therapy for muscle invasive or recurrent BC, options remain limited for patients with non-muscle invasive BC (NMIBC) refractory to Bacillus Calmette-Guérin (BCG) and chemotherapy. NMIBC is more frequently classified as a luminal subtype, in which increased PPARγ activity is a key feature in promoting tumor growth and evasion of immunosurveillance. Cinobufotalin is one of the major compound of bufadienolides, the primary active components of toad venom that has been utilized in the clinical treatment of cancer. We herein focused on cinobufotalin, examining its anticancer activity and molecular mechanisms in luminal-type NMIBC. Our results newly reveal that cinobufotalin strongly suppresses the viability and proliferation of luminal BC cells with minimal cytotoxic effects on normal uroepithelial cells, and exhibits significant antitumor activity in a RT112 xenograft BC model. Mechanistically, our sub-G1-phase cell accumulation, Annexin V staining, caspase-3/8/9 activation, and PARP activation analyses show that cinobufotalin induces apoptosis in luminal-type BC cells. Cinobufotalin significantly inhibited the levels of PPARγ and its downstream targets, as well as lipid droplet formation and free fatty acid levels in RT112 cells. PPARγ overexpression rescued RT112 cells from cinobufotalin-induced apoptosis and mitigated the downregulation of FASN and PLIN4. Finally, we show seemingly for the first time that cinobufotalin promotes SIAH1/2-mediated proteasomal degradation of PPARγ in luminal BC cells. Together, these findings compellingly support the idea that cinobufotalin could be developed as a promising therapeutic agent for treating luminal-type NMIBC.
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spelling doaj-art-8dd32fd6ea714adda6f0d81931c1f6502024-12-22T12:50:54ZengNature Publishing GroupCell Death and Disease2041-48892024-12-01151211410.1038/s41419-024-07298-xTargeting PPARγ via SIAH1/2-mediated ubiquitin-proteasomal degradation as a new therapeutic approach in luminal-type bladder cancerChih-Chieh Tu0Tsung-Han Hsieh1Cheng-Ying Chu2Yu-Chen Lin3Bo-Jyun Lin4Chun-Han Chen5Department of Pharmacology, School of Medicine, College of Medicine, Taipei Medical UniversityPrecision Health Center, Taipei Medical UniversityCRISPR Gene Targeting Core, Taipei Medical UniversityDepartment of Pharmacology, School of Medicine, College of Medicine, Taipei Medical UniversityDepartment of Pharmacology, School of Medicine, College of Medicine, Taipei Medical UniversityDepartment of Pharmacology, School of Medicine, College of Medicine, Taipei Medical UniversityAbstract Bladder cancer (BC) is the second most prevalent genitourinary malignancy worldwide. Despite recent approvals of immune checkpoint inhibitors and targeted therapy for muscle invasive or recurrent BC, options remain limited for patients with non-muscle invasive BC (NMIBC) refractory to Bacillus Calmette-Guérin (BCG) and chemotherapy. NMIBC is more frequently classified as a luminal subtype, in which increased PPARγ activity is a key feature in promoting tumor growth and evasion of immunosurveillance. Cinobufotalin is one of the major compound of bufadienolides, the primary active components of toad venom that has been utilized in the clinical treatment of cancer. We herein focused on cinobufotalin, examining its anticancer activity and molecular mechanisms in luminal-type NMIBC. Our results newly reveal that cinobufotalin strongly suppresses the viability and proliferation of luminal BC cells with minimal cytotoxic effects on normal uroepithelial cells, and exhibits significant antitumor activity in a RT112 xenograft BC model. Mechanistically, our sub-G1-phase cell accumulation, Annexin V staining, caspase-3/8/9 activation, and PARP activation analyses show that cinobufotalin induces apoptosis in luminal-type BC cells. Cinobufotalin significantly inhibited the levels of PPARγ and its downstream targets, as well as lipid droplet formation and free fatty acid levels in RT112 cells. PPARγ overexpression rescued RT112 cells from cinobufotalin-induced apoptosis and mitigated the downregulation of FASN and PLIN4. Finally, we show seemingly for the first time that cinobufotalin promotes SIAH1/2-mediated proteasomal degradation of PPARγ in luminal BC cells. Together, these findings compellingly support the idea that cinobufotalin could be developed as a promising therapeutic agent for treating luminal-type NMIBC.https://doi.org/10.1038/s41419-024-07298-x
spellingShingle Chih-Chieh Tu
Tsung-Han Hsieh
Cheng-Ying Chu
Yu-Chen Lin
Bo-Jyun Lin
Chun-Han Chen
Targeting PPARγ via SIAH1/2-mediated ubiquitin-proteasomal degradation as a new therapeutic approach in luminal-type bladder cancer
Cell Death and Disease
title Targeting PPARγ via SIAH1/2-mediated ubiquitin-proteasomal degradation as a new therapeutic approach in luminal-type bladder cancer
title_full Targeting PPARγ via SIAH1/2-mediated ubiquitin-proteasomal degradation as a new therapeutic approach in luminal-type bladder cancer
title_fullStr Targeting PPARγ via SIAH1/2-mediated ubiquitin-proteasomal degradation as a new therapeutic approach in luminal-type bladder cancer
title_full_unstemmed Targeting PPARγ via SIAH1/2-mediated ubiquitin-proteasomal degradation as a new therapeutic approach in luminal-type bladder cancer
title_short Targeting PPARγ via SIAH1/2-mediated ubiquitin-proteasomal degradation as a new therapeutic approach in luminal-type bladder cancer
title_sort targeting pparγ via siah1 2 mediated ubiquitin proteasomal degradation as a new therapeutic approach in luminal type bladder cancer
url https://doi.org/10.1038/s41419-024-07298-x
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