Endoglin aggravates peritoneal fibrosis by regulating the activation of TGF-β/ALK/Smads signaling

Background: Peritoneal fibrosis (PF) is an intractable complication in patients on long-term peritoneal dialysis (PD). Transforming growth factor-β (TGF-β) is a key pro-fibrogenic factor involved in PD-associated PF, and endoglin, as a coreceptor for TGF-β, plays a role in balancing the TGF-β signal...

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Main Authors: Qian Huang, Rui Xiao, Jing Lu, Yao Zhang, Liang Xu, Jie Gao, Jing Sun, Haiping Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-09-01
Series:Frontiers in Pharmacology
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Online Access:https://www.frontiersin.org/articles/10.3389/fphar.2022.973182/full
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author Qian Huang
Rui Xiao
Jing Lu
Yao Zhang
Liang Xu
Jie Gao
Jing Sun
Jing Sun
Haiping Wang
Haiping Wang
author_facet Qian Huang
Rui Xiao
Jing Lu
Yao Zhang
Liang Xu
Jie Gao
Jing Sun
Jing Sun
Haiping Wang
Haiping Wang
author_sort Qian Huang
collection DOAJ
description Background: Peritoneal fibrosis (PF) is an intractable complication in patients on long-term peritoneal dialysis (PD). Transforming growth factor-β (TGF-β) is a key pro-fibrogenic factor involved in PD-associated PF, and endoglin, as a coreceptor for TGF-β, plays a role in balancing the TGF-β signaling pathway. Here, we investigated whether endoglin could be a potential therapeutic target for PF.Methods:In vivo, we established PF model in SD rats by daily intraperitoneal injection of peritoneal dialysis fluids (PDF) containing 4.25% glucose for 6 weeks and downregulated endoglin expression by tail vein injection of AAV9-ENG on day 14 to assess the effect of endoglin on peritoneal morphology and markers related to fibrosis, angiogenesis, and epithelial-mesenchymal transition (EMT). In vitro, we treated human peritoneal mesothelial cells (HPMCs) transfected with ENG siRNA in high glucose medium to explore the potential mechanism of endoglin in PF.Results: Compared to control group, continuous exposure to biologically incompatible PDF induced exacerbated PF, accompanied by a significant increase in endoglin expression. Conversely, knockdown of endoglin ameliorated peritoneal injury characterized by increased peritoneal thickening and collagen deposition, angiogenesis, as well as EMT. Consistently, HPMCs cultured in high glucose medium underwent the EMT process and exhibited over-expression of fibronectin, collagen type I, vascular endothelial growth factor (VEGF), whereas these aforementioned alterations were alleviated after ENG siRNA transfection. In addition, we also found that ENG siRNA inhibited TGF-β-induced phosphorylation of Smad2/3 and Smad1/5/9 in HPMCs treated with high glucose (HG).Conclusion: Our findings confirmed for the first time that endoglin exacerbated PF by regulating the activation of TGF-β/ALK/Smads signaling, which will provide a novel potential therapeutic target in PF.
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spelling doaj-art-eab4cd1a93754b6a8e1a9f1230d4b3652025-08-20T02:34:24ZengFrontiers Media S.A.Frontiers in Pharmacology1663-98122022-09-011310.3389/fphar.2022.973182973182Endoglin aggravates peritoneal fibrosis by regulating the activation of TGF-β/ALK/Smads signalingQian Huang0Rui Xiao1Jing Lu2Yao Zhang3Liang Xu4Jie Gao5Jing Sun6Jing Sun7Haiping Wang8Haiping Wang9Department of Nephrology, Shandong Provincial Hospital, Shandong University, Jinan, ChinaDepartment of Nephrology, Shandong Provincial Hospital, Shandong University, Jinan, ChinaDepartment of Nephrology, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, ChinaDepartment of Nephrology, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, ChinaDepartment of Nephrology, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, ChinaDepartment of Nephrology, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, ChinaDepartment of Nephrology, Shandong Provincial Hospital, Shandong University, Jinan, ChinaDepartment of Nephrology, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, ChinaDepartment of Nephrology, Shandong Provincial Hospital, Shandong University, Jinan, ChinaDepartment of Nephrology, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, ChinaBackground: Peritoneal fibrosis (PF) is an intractable complication in patients on long-term peritoneal dialysis (PD). Transforming growth factor-β (TGF-β) is a key pro-fibrogenic factor involved in PD-associated PF, and endoglin, as a coreceptor for TGF-β, plays a role in balancing the TGF-β signaling pathway. Here, we investigated whether endoglin could be a potential therapeutic target for PF.Methods:In vivo, we established PF model in SD rats by daily intraperitoneal injection of peritoneal dialysis fluids (PDF) containing 4.25% glucose for 6 weeks and downregulated endoglin expression by tail vein injection of AAV9-ENG on day 14 to assess the effect of endoglin on peritoneal morphology and markers related to fibrosis, angiogenesis, and epithelial-mesenchymal transition (EMT). In vitro, we treated human peritoneal mesothelial cells (HPMCs) transfected with ENG siRNA in high glucose medium to explore the potential mechanism of endoglin in PF.Results: Compared to control group, continuous exposure to biologically incompatible PDF induced exacerbated PF, accompanied by a significant increase in endoglin expression. Conversely, knockdown of endoglin ameliorated peritoneal injury characterized by increased peritoneal thickening and collagen deposition, angiogenesis, as well as EMT. Consistently, HPMCs cultured in high glucose medium underwent the EMT process and exhibited over-expression of fibronectin, collagen type I, vascular endothelial growth factor (VEGF), whereas these aforementioned alterations were alleviated after ENG siRNA transfection. In addition, we also found that ENG siRNA inhibited TGF-β-induced phosphorylation of Smad2/3 and Smad1/5/9 in HPMCs treated with high glucose (HG).Conclusion: Our findings confirmed for the first time that endoglin exacerbated PF by regulating the activation of TGF-β/ALK/Smads signaling, which will provide a novel potential therapeutic target in PF.https://www.frontiersin.org/articles/10.3389/fphar.2022.973182/fullendoglinperitoneal fibrosisangiogenesisEMTTGF-β/ALK/Smads
spellingShingle Qian Huang
Rui Xiao
Jing Lu
Yao Zhang
Liang Xu
Jie Gao
Jing Sun
Jing Sun
Haiping Wang
Haiping Wang
Endoglin aggravates peritoneal fibrosis by regulating the activation of TGF-β/ALK/Smads signaling
Frontiers in Pharmacology
endoglin
peritoneal fibrosis
angiogenesis
EMT
TGF-β/ALK/Smads
title Endoglin aggravates peritoneal fibrosis by regulating the activation of TGF-β/ALK/Smads signaling
title_full Endoglin aggravates peritoneal fibrosis by regulating the activation of TGF-β/ALK/Smads signaling
title_fullStr Endoglin aggravates peritoneal fibrosis by regulating the activation of TGF-β/ALK/Smads signaling
title_full_unstemmed Endoglin aggravates peritoneal fibrosis by regulating the activation of TGF-β/ALK/Smads signaling
title_short Endoglin aggravates peritoneal fibrosis by regulating the activation of TGF-β/ALK/Smads signaling
title_sort endoglin aggravates peritoneal fibrosis by regulating the activation of tgf β alk smads signaling
topic endoglin
peritoneal fibrosis
angiogenesis
EMT
TGF-β/ALK/Smads
url https://www.frontiersin.org/articles/10.3389/fphar.2022.973182/full
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