TNF-α modulates cell proliferation via SOX4/TGF-β/Smad signaling in benign prostatic hyperplasia

Abstract Benign prostatic hyperplasia (BPH) is an age-related condition in men with a poorly defined etiology. Chronic inflammation is increasingly recognized as a key contributor to BPH progression; however, the underlying mechanisms remain incompletely understood. This study aimed to elucidate the...

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Main Authors: Jinze Li, Bo Chen, Yin Huang, Xinyang Liao, Jia You, Zeyu Chen, Shu Ning, Asmaa Reda, Junwei Zhao, Biao Ran, Jingxing Bai, Mengli Zhu, Yan Wang, Hongying Chen, Qiang Wei, Dehong Cao, Liangren Liu
Format: Article
Language:English
Published: Nature Publishing Group 2025-07-01
Series:Cell Death and Disease
Online Access:https://doi.org/10.1038/s41419-025-07783-x
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author Jinze Li
Bo Chen
Yin Huang
Xinyang Liao
Jia You
Zeyu Chen
Shu Ning
Asmaa Reda
Junwei Zhao
Biao Ran
Jingxing Bai
Mengli Zhu
Yan Wang
Hongying Chen
Qiang Wei
Dehong Cao
Liangren Liu
author_facet Jinze Li
Bo Chen
Yin Huang
Xinyang Liao
Jia You
Zeyu Chen
Shu Ning
Asmaa Reda
Junwei Zhao
Biao Ran
Jingxing Bai
Mengli Zhu
Yan Wang
Hongying Chen
Qiang Wei
Dehong Cao
Liangren Liu
author_sort Jinze Li
collection DOAJ
description Abstract Benign prostatic hyperplasia (BPH) is an age-related condition in men with a poorly defined etiology. Chronic inflammation is increasingly recognized as a key contributor to BPH progression; however, the underlying mechanisms remain incompletely understood. This study aimed to elucidate the role of a TNF-α-induced inflammatory microenvironment in regulating BPH progression. We demonstrated that TNF-α levels were significantly elevated in patients with BPH and positively correlated with key clinical characteristics. In vitro, TNF-α promoted the proliferation of prostatic cells. Mechanistically, TNF-α induced the overexpression of SOX4, which subsequently activated the TGF-β/Smad2/3 signaling axis, thereby enhancing cellular proliferation, promoting epithelial-mesenchymal transition (EMT), and exacerbating fibrosis. Importantly, metformin (Met) treatment reduced the expression levels of relevant inflammatory cytokines in the serum of BPH rats. Further analysis confirmed that Met inhibited the TGF-β/Smad2/3 signaling pathway by downregulating the expression of SOX4, thus suppressing cell proliferation, reversing EMT, alleviating fibrosis, and ultimately exerting anti-BPH effects. Collectively, our findings suggest that TNF-α promotes BPH progression via activation of the SOX4/TGF-β/Smad2/3 axis, while Met exerts therapeutic effects by targeting this pathway. These results highlight SOX4 as a potential therapeutic target for BPH and support the clinical potential of Met in BPH management.
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spelling doaj-art-17fb1c17c4694bdbbc38d7acb626edd62025-08-20T03:45:38ZengNature Publishing GroupCell Death and Disease2041-48892025-07-0116111510.1038/s41419-025-07783-xTNF-α modulates cell proliferation via SOX4/TGF-β/Smad signaling in benign prostatic hyperplasiaJinze Li0Bo Chen1Yin Huang2Xinyang Liao3Jia You4Zeyu Chen5Shu Ning6Asmaa Reda7Junwei Zhao8Biao Ran9Jingxing Bai10Mengli Zhu11Yan Wang12Hongying Chen13Qiang Wei14Dehong Cao15Liangren Liu16Department of Urology, Institute of Urology, West China Hospital, Sichuan UniversityDepartment of Urology, Institute of Urology, West China Hospital, Sichuan UniversityDepartment of Urology, Institute of Urology, West China Hospital, Sichuan UniversityDepartment of Urology, Institute of Urology, West China Hospital, Sichuan UniversityNingbo Clinical Pathological Diagnosis CenterDepartment of Urology, Institute of Urology, West China Hospital, Sichuan UniversityDepartment of Urologic Surgery, School of Medicine, University of California DavisComputational Biology and Bioinformatics, Zoology Department, Faculty of Science, Benha UniversityDepartment of Biochemistry and Molecular Medicine, UC Davis NCI-designated Comprehensive Cancer Center, University of California DavisDepartment of Urology, Institute of Urology, West China Hospital, Sichuan UniversityDepartment of Urology, Institute of Urology, West China Hospital, Sichuan UniversityCore Facilities of West China Hospital, Sichuan UniversityCore Facilities of West China Hospital, Sichuan UniversityCore Facilities of West China Hospital, Sichuan UniversityDepartment of Urology, Institute of Urology, West China Hospital, Sichuan UniversityDepartment of Urology, Institute of Urology, West China Hospital, Sichuan UniversityDepartment of Urology, Institute of Urology, West China Hospital, Sichuan UniversityAbstract Benign prostatic hyperplasia (BPH) is an age-related condition in men with a poorly defined etiology. Chronic inflammation is increasingly recognized as a key contributor to BPH progression; however, the underlying mechanisms remain incompletely understood. This study aimed to elucidate the role of a TNF-α-induced inflammatory microenvironment in regulating BPH progression. We demonstrated that TNF-α levels were significantly elevated in patients with BPH and positively correlated with key clinical characteristics. In vitro, TNF-α promoted the proliferation of prostatic cells. Mechanistically, TNF-α induced the overexpression of SOX4, which subsequently activated the TGF-β/Smad2/3 signaling axis, thereby enhancing cellular proliferation, promoting epithelial-mesenchymal transition (EMT), and exacerbating fibrosis. Importantly, metformin (Met) treatment reduced the expression levels of relevant inflammatory cytokines in the serum of BPH rats. Further analysis confirmed that Met inhibited the TGF-β/Smad2/3 signaling pathway by downregulating the expression of SOX4, thus suppressing cell proliferation, reversing EMT, alleviating fibrosis, and ultimately exerting anti-BPH effects. Collectively, our findings suggest that TNF-α promotes BPH progression via activation of the SOX4/TGF-β/Smad2/3 axis, while Met exerts therapeutic effects by targeting this pathway. These results highlight SOX4 as a potential therapeutic target for BPH and support the clinical potential of Met in BPH management.https://doi.org/10.1038/s41419-025-07783-x
spellingShingle Jinze Li
Bo Chen
Yin Huang
Xinyang Liao
Jia You
Zeyu Chen
Shu Ning
Asmaa Reda
Junwei Zhao
Biao Ran
Jingxing Bai
Mengli Zhu
Yan Wang
Hongying Chen
Qiang Wei
Dehong Cao
Liangren Liu
TNF-α modulates cell proliferation via SOX4/TGF-β/Smad signaling in benign prostatic hyperplasia
Cell Death and Disease
title TNF-α modulates cell proliferation via SOX4/TGF-β/Smad signaling in benign prostatic hyperplasia
title_full TNF-α modulates cell proliferation via SOX4/TGF-β/Smad signaling in benign prostatic hyperplasia
title_fullStr TNF-α modulates cell proliferation via SOX4/TGF-β/Smad signaling in benign prostatic hyperplasia
title_full_unstemmed TNF-α modulates cell proliferation via SOX4/TGF-β/Smad signaling in benign prostatic hyperplasia
title_short TNF-α modulates cell proliferation via SOX4/TGF-β/Smad signaling in benign prostatic hyperplasia
title_sort tnf α modulates cell proliferation via sox4 tgf β smad signaling in benign prostatic hyperplasia
url https://doi.org/10.1038/s41419-025-07783-x
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