Inhibition of soluble epoxide hydrolase reverses bone loss in periodontitis by upregulating EMCN and inhibiting osteoclasts

Abstract Background Improving the microenvironment to augment endogenous regenerative potential has emerged as a fundamental concept for stimulating and expediting periodontal tissue repair and regeneration. Previous studies have demonstrated that TPPU, a soluble epoxide hydrolase inhibitor (sEHi),...

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Main Authors: Juanjuan Li, Ni Kou, Xiaoli Shi, Lingwenyao Kong, Weixian Chen, Xueping Yang, Yanrong Zhao, Jie Zhao, Fu Wang
Format: Article
Language:English
Published: BMC 2024-11-01
Series:Stem Cell Research & Therapy
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Online Access:https://doi.org/10.1186/s13287-024-04054-y
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author Juanjuan Li
Ni Kou
Xiaoli Shi
Lingwenyao Kong
Weixian Chen
Xueping Yang
Yanrong Zhao
Jie Zhao
Fu Wang
author_facet Juanjuan Li
Ni Kou
Xiaoli Shi
Lingwenyao Kong
Weixian Chen
Xueping Yang
Yanrong Zhao
Jie Zhao
Fu Wang
author_sort Juanjuan Li
collection DOAJ
description Abstract Background Improving the microenvironment to augment endogenous regenerative potential has emerged as a fundamental concept for stimulating and expediting periodontal tissue repair and regeneration. Previous studies have demonstrated that TPPU, a soluble epoxide hydrolase inhibitor (sEHi), mediates the suppression of inflammatory bone loss in periodontitis models. However, the underlying mechanisms remain largely elusive. Methods In this study, we constructed a human umbilical vein endothelial cell (HUVEC) and periodontal ligament stem cell (PDLSC) coculture system in vitro and tested the anti-inflammatory effect of TPPU under inflammatory conditions. The roles of HIF-1α and Endomucin (EMCN) in the anti-inflammatory effects of TPPU were analyzed. The effects of TPPU on osteogenesis and osteoclastogenesis in cocultured cells were examined. The in vivo periodontitis model further verified the effects of TPPU on inhibiting neutrophil adhesion and inflammation and inhibiting osteoclasts. Results Our in vitro experiments demonstrated that TPPU enhances the interaction between mesenchymal stem cells and vascular endothelial cells to enhance anti-inflammatory and osteogenic differentiation effects and revealed a new anti-inflammatory mechanism of TPPU involving the upregulation of EMCN in endothelial cells to prevent lymphocyte recruitment. We also confirmed that TPPU inhibits osteoclast activity. Our in vivo findings showed that TPPU inhibits osteoclast activity and neutrophil adhesion and enhances periodontal tissue repair and regeneration. Conclusions TPPU promotes local regeneration in periodontitis by inhibiting inflammation and bone resorption. Thus, targeting soluble epoxide hydrolase represents an endogenous regenerative strategy for periodontitis treatment.
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spelling doaj-art-4e75c5c1ca12434599a5e61cee1c7b262025-08-20T02:51:43ZengBMCStem Cell Research & Therapy1757-65122024-11-0115111410.1186/s13287-024-04054-yInhibition of soluble epoxide hydrolase reverses bone loss in periodontitis by upregulating EMCN and inhibiting osteoclastsJuanjuan Li0Ni Kou1Xiaoli Shi2Lingwenyao Kong3Weixian Chen4Xueping Yang5Yanrong Zhao6Jie Zhao7Fu Wang8School of Stomatology, Dalian Medical UniversitySchool of Stomatology, Dalian Medical UniversitySchool of Stomatology, Dalian Medical UniversitySchool of Stomatology, Dalian Medical UniversitySchool of Stomatology, Dalian Medical UniversitySchool of Stomatology, Dalian Medical UniversitySchool of Stomatology, Dalian Medical UniversityNational-Local Joint Engineering Research Center for Drug-Research and Development (R&D) of Neurodegenerative Diseases, Dalian Medical UniversitySchool of Stomatology, Dalian Medical UniversityAbstract Background Improving the microenvironment to augment endogenous regenerative potential has emerged as a fundamental concept for stimulating and expediting periodontal tissue repair and regeneration. Previous studies have demonstrated that TPPU, a soluble epoxide hydrolase inhibitor (sEHi), mediates the suppression of inflammatory bone loss in periodontitis models. However, the underlying mechanisms remain largely elusive. Methods In this study, we constructed a human umbilical vein endothelial cell (HUVEC) and periodontal ligament stem cell (PDLSC) coculture system in vitro and tested the anti-inflammatory effect of TPPU under inflammatory conditions. The roles of HIF-1α and Endomucin (EMCN) in the anti-inflammatory effects of TPPU were analyzed. The effects of TPPU on osteogenesis and osteoclastogenesis in cocultured cells were examined. The in vivo periodontitis model further verified the effects of TPPU on inhibiting neutrophil adhesion and inflammation and inhibiting osteoclasts. Results Our in vitro experiments demonstrated that TPPU enhances the interaction between mesenchymal stem cells and vascular endothelial cells to enhance anti-inflammatory and osteogenic differentiation effects and revealed a new anti-inflammatory mechanism of TPPU involving the upregulation of EMCN in endothelial cells to prevent lymphocyte recruitment. We also confirmed that TPPU inhibits osteoclast activity. Our in vivo findings showed that TPPU inhibits osteoclast activity and neutrophil adhesion and enhances periodontal tissue repair and regeneration. Conclusions TPPU promotes local regeneration in periodontitis by inhibiting inflammation and bone resorption. Thus, targeting soluble epoxide hydrolase represents an endogenous regenerative strategy for periodontitis treatment.https://doi.org/10.1186/s13287-024-04054-ySoluble epoxide hydrolase inhibitorTPPUPeriodontitisTissue regenerationEMCN
spellingShingle Juanjuan Li
Ni Kou
Xiaoli Shi
Lingwenyao Kong
Weixian Chen
Xueping Yang
Yanrong Zhao
Jie Zhao
Fu Wang
Inhibition of soluble epoxide hydrolase reverses bone loss in periodontitis by upregulating EMCN and inhibiting osteoclasts
Stem Cell Research & Therapy
Soluble epoxide hydrolase inhibitor
TPPU
Periodontitis
Tissue regeneration
EMCN
title Inhibition of soluble epoxide hydrolase reverses bone loss in periodontitis by upregulating EMCN and inhibiting osteoclasts
title_full Inhibition of soluble epoxide hydrolase reverses bone loss in periodontitis by upregulating EMCN and inhibiting osteoclasts
title_fullStr Inhibition of soluble epoxide hydrolase reverses bone loss in periodontitis by upregulating EMCN and inhibiting osteoclasts
title_full_unstemmed Inhibition of soluble epoxide hydrolase reverses bone loss in periodontitis by upregulating EMCN and inhibiting osteoclasts
title_short Inhibition of soluble epoxide hydrolase reverses bone loss in periodontitis by upregulating EMCN and inhibiting osteoclasts
title_sort inhibition of soluble epoxide hydrolase reverses bone loss in periodontitis by upregulating emcn and inhibiting osteoclasts
topic Soluble epoxide hydrolase inhibitor
TPPU
Periodontitis
Tissue regeneration
EMCN
url https://doi.org/10.1186/s13287-024-04054-y
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