Omentin-1 inhibits the development of benign prostatic hyperplasia by attenuating local inflammation

Abstract Background Benign prostatic hyperplasia (BPH) is a prevalent disease affecting elderly men, with chronic inflammation being a critical factor in its development. Omentin-1, also known as intelectin-1 (ITLN-1), is an anti-inflammatory protein primarily found in the epithelial cells of the sm...

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Main Authors: Yi-Yi Wang, Guo-Qiang Zhu, Kun Xia, Hong-Bo Zeng, Yun-Hui He, Hui Xie, Zhen-Xing Wang, Ran Xu
Format: Article
Language:English
Published: BMC 2024-03-01
Series:Molecular Medicine
Subjects:
Online Access:https://doi.org/10.1186/s10020-024-00805-y
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author Yi-Yi Wang
Guo-Qiang Zhu
Kun Xia
Hong-Bo Zeng
Yun-Hui He
Hui Xie
Zhen-Xing Wang
Ran Xu
author_facet Yi-Yi Wang
Guo-Qiang Zhu
Kun Xia
Hong-Bo Zeng
Yun-Hui He
Hui Xie
Zhen-Xing Wang
Ran Xu
author_sort Yi-Yi Wang
collection DOAJ
description Abstract Background Benign prostatic hyperplasia (BPH) is a prevalent disease affecting elderly men, with chronic inflammation being a critical factor in its development. Omentin-1, also known as intelectin-1 (ITLN-1), is an anti-inflammatory protein primarily found in the epithelial cells of the small intestine. This study aimed to investigate the potential of ITLN-1 in mitigating BPH by modulating local inflammation in the prostate gland. Methods Our investigation involved two in vivo experimental models. Firstly, ITLN-1 knockout mice (Itln-1 −/− ) were used to study the absence of ITLN-1 in BPH development. Secondly, a testosterone propionate (TP)-induced BPH mouse model was treated with an ITLN-1 overexpressing adenovirus. We assessed BPH severity using prostate weight index and histological analysis, including H&E staining, immunohistochemistry, and enzyme-linked immunosorbent assay. In vitro, the impact of ITLN-1 on BPH-1 cell proliferation and inflammatory response was evaluated using cell proliferation assays and enzyme-linked immunosorbent assay. Results In vivo, Itln-1 −/− mice exhibited elevated prostate weight index, enlarged lumen area, and higher TNF-α levels compared to wild-type littermates. In contrast, ITLN-1 overexpression in TP-induced BPH mice resulted in reduced prostate weight index, lumen area, and TNF-α levels. In vitro studies indicated that ITLN-1 suppressed the proliferation of prostate epithelial cells and reduced TNF-α production in macrophages, suggesting a mechanism involving the inhibition of macrophage-mediated inflammation. Conclusion The study demonstrates that ITLN-1 plays a significant role in inhibiting the development of BPH by reducing local inflammation in the prostate gland. These findings highlight the potential of ITLN-1 as a therapeutic target in the management of BPH.
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spelling doaj.art-ed30143537cd4836a149a5a8a953b01e2024-03-24T12:23:57ZengBMCMolecular Medicine1528-36582024-03-0130111410.1186/s10020-024-00805-yOmentin-1 inhibits the development of benign prostatic hyperplasia by attenuating local inflammationYi-Yi Wang0Guo-Qiang Zhu1Kun Xia2Hong-Bo Zeng3Yun-Hui He4Hui Xie5Zhen-Xing Wang6Ran Xu7Department of Orthopedics, Movement System Injury and Repair Research Center, Xiangya Hospital, Central South UniversityDepartment of Orthopedics, Movement System Injury and Repair Research Center, Xiangya Hospital, Central South UniversityDepartment of Orthopedics, People’s Hospital of Ningxia Hui Autonomous RegionDepartment of Urology, The Second Xiangya Hospital, Central South UniversityDepartment of Urology, The Second Xiangya Hospital, Central South UniversityDepartment of Orthopedics, Movement System Injury and Repair Research Center, Xiangya Hospital, Central South UniversityDepartment of Orthopedics, Movement System Injury and Repair Research Center, Xiangya Hospital, Central South UniversityDepartment of Urology, The Second Xiangya Hospital, Central South UniversityAbstract Background Benign prostatic hyperplasia (BPH) is a prevalent disease affecting elderly men, with chronic inflammation being a critical factor in its development. Omentin-1, also known as intelectin-1 (ITLN-1), is an anti-inflammatory protein primarily found in the epithelial cells of the small intestine. This study aimed to investigate the potential of ITLN-1 in mitigating BPH by modulating local inflammation in the prostate gland. Methods Our investigation involved two in vivo experimental models. Firstly, ITLN-1 knockout mice (Itln-1 −/− ) were used to study the absence of ITLN-1 in BPH development. Secondly, a testosterone propionate (TP)-induced BPH mouse model was treated with an ITLN-1 overexpressing adenovirus. We assessed BPH severity using prostate weight index and histological analysis, including H&E staining, immunohistochemistry, and enzyme-linked immunosorbent assay. In vitro, the impact of ITLN-1 on BPH-1 cell proliferation and inflammatory response was evaluated using cell proliferation assays and enzyme-linked immunosorbent assay. Results In vivo, Itln-1 −/− mice exhibited elevated prostate weight index, enlarged lumen area, and higher TNF-α levels compared to wild-type littermates. In contrast, ITLN-1 overexpression in TP-induced BPH mice resulted in reduced prostate weight index, lumen area, and TNF-α levels. In vitro studies indicated that ITLN-1 suppressed the proliferation of prostate epithelial cells and reduced TNF-α production in macrophages, suggesting a mechanism involving the inhibition of macrophage-mediated inflammation. Conclusion The study demonstrates that ITLN-1 plays a significant role in inhibiting the development of BPH by reducing local inflammation in the prostate gland. These findings highlight the potential of ITLN-1 as a therapeutic target in the management of BPH.https://doi.org/10.1186/s10020-024-00805-yBenign prostatic hyperplasiaOmentin-1Intelectin-1InflammationProstate epithelial cellsMacrophages
spellingShingle Yi-Yi Wang
Guo-Qiang Zhu
Kun Xia
Hong-Bo Zeng
Yun-Hui He
Hui Xie
Zhen-Xing Wang
Ran Xu
Omentin-1 inhibits the development of benign prostatic hyperplasia by attenuating local inflammation
Molecular Medicine
Benign prostatic hyperplasia
Omentin-1
Intelectin-1
Inflammation
Prostate epithelial cells
Macrophages
title Omentin-1 inhibits the development of benign prostatic hyperplasia by attenuating local inflammation
title_full Omentin-1 inhibits the development of benign prostatic hyperplasia by attenuating local inflammation
title_fullStr Omentin-1 inhibits the development of benign prostatic hyperplasia by attenuating local inflammation
title_full_unstemmed Omentin-1 inhibits the development of benign prostatic hyperplasia by attenuating local inflammation
title_short Omentin-1 inhibits the development of benign prostatic hyperplasia by attenuating local inflammation
title_sort omentin 1 inhibits the development of benign prostatic hyperplasia by attenuating local inflammation
topic Benign prostatic hyperplasia
Omentin-1
Intelectin-1
Inflammation
Prostate epithelial cells
Macrophages
url https://doi.org/10.1186/s10020-024-00805-y
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