TRPV1 Promotes Periodontitis Tissue Inflammation and Oxidative Damage by Regulating STAT3 Signaling Pathway.

IF 3.4 3区 医学 Q1 DENTISTRY, ORAL SURGERY & MEDICINE
Mingzhu Yu, Huan Tian, Ruqing Lu, Ni Quan, Ling Qian
{"title":"TRPV1 Promotes Periodontitis Tissue Inflammation and Oxidative Damage by Regulating STAT3 Signaling Pathway.","authors":"Mingzhu Yu, Huan Tian, Ruqing Lu, Ni Quan, Ling Qian","doi":"10.1111/jre.13368","DOIUrl":null,"url":null,"abstract":"<p><strong>Aims: </strong>Periodontitis is a chronic disease affecting adult oral health. Transient receptor potential vanilloid 1 (TRPV1) expression is shown to upregulate in many inflammatory diseases. Nevertheless, its biological potential along with the molecular mechanism in periodontitis is unclear. Our study aimed to explore the biological role and underlying signaling pathway of TRPV1 in periodontitis.</p><p><strong>Methods: </strong>In the current research, human periodontal ligament stem cells (hPDLSCs) were stimulated by lipopolysaccharide (LPS) to induce inflammatory conditions in vitro. In vivo, the periodontitis mouse model was built by ligating the gingival sulcus of male C57BL/6J mice. Thereafter, the proliferation, apoptosis, inflammation, and oxidative stress-related processes were assessed.</p><p><strong>Results: </strong>We found that LPS induced apoptosis and inflammation in hPDLCs, along with oxidative stress, while simultaneously inhibiting hPDLC proliferation (p < 0.05). Notably, TRPV1 expression was elevated in LPS-treated hPDLSCs and gingival samples from patients with periodontitis. Interestingly, the increase in TRPV1 expression induced by Capsaicin, a TRPV1 agonist, inhibited cell proliferation while promoting LPS-stimulated apoptosis, inflammation, and oxidative stress in hPDLSCs (p < 0.01). In contrast, inhibition of TRPV1 expression using Capsazepine, a TRPV1 inhibitor, produced opposite effects (p < 0.01). In vivo experiments revealed that inhibition of TRPV1 attenuated ligation-induced periodontitis in mice, as evidenced by enhanced oxidative stress, inflammatory response, and elevated apoptosis (p < 0.01). Additionally, rescue assays indicated that TRPV1 promoted periodontitis-associated tissue inflammation and oxidative damage via activating the STAT3 signaling pathway (p < 0.01).</p><p><strong>Conclusion: </strong>Our study demonstrates that TRPV1 expression is high in periodontitis and facilitates periodontitis-associated tissue inflammation and oxidative damage by regulating STAT3 signaling pathway, which implies that TRPV1 may represent a new therapeutic target for periodontitis.</p>","PeriodicalId":16715,"journal":{"name":"Journal of periodontal research","volume":" ","pages":""},"PeriodicalIF":3.4000,"publicationDate":"2024-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of periodontal research","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1111/jre.13368","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"DENTISTRY, ORAL SURGERY & MEDICINE","Score":null,"Total":0}
引用次数: 0

Abstract

Aims: Periodontitis is a chronic disease affecting adult oral health. Transient receptor potential vanilloid 1 (TRPV1) expression is shown to upregulate in many inflammatory diseases. Nevertheless, its biological potential along with the molecular mechanism in periodontitis is unclear. Our study aimed to explore the biological role and underlying signaling pathway of TRPV1 in periodontitis.

Methods: In the current research, human periodontal ligament stem cells (hPDLSCs) were stimulated by lipopolysaccharide (LPS) to induce inflammatory conditions in vitro. In vivo, the periodontitis mouse model was built by ligating the gingival sulcus of male C57BL/6J mice. Thereafter, the proliferation, apoptosis, inflammation, and oxidative stress-related processes were assessed.

Results: We found that LPS induced apoptosis and inflammation in hPDLCs, along with oxidative stress, while simultaneously inhibiting hPDLC proliferation (p < 0.05). Notably, TRPV1 expression was elevated in LPS-treated hPDLSCs and gingival samples from patients with periodontitis. Interestingly, the increase in TRPV1 expression induced by Capsaicin, a TRPV1 agonist, inhibited cell proliferation while promoting LPS-stimulated apoptosis, inflammation, and oxidative stress in hPDLSCs (p < 0.01). In contrast, inhibition of TRPV1 expression using Capsazepine, a TRPV1 inhibitor, produced opposite effects (p < 0.01). In vivo experiments revealed that inhibition of TRPV1 attenuated ligation-induced periodontitis in mice, as evidenced by enhanced oxidative stress, inflammatory response, and elevated apoptosis (p < 0.01). Additionally, rescue assays indicated that TRPV1 promoted periodontitis-associated tissue inflammation and oxidative damage via activating the STAT3 signaling pathway (p < 0.01).

Conclusion: Our study demonstrates that TRPV1 expression is high in periodontitis and facilitates periodontitis-associated tissue inflammation and oxidative damage by regulating STAT3 signaling pathway, which implies that TRPV1 may represent a new therapeutic target for periodontitis.

求助全文
约1分钟内获得全文 求助全文
来源期刊
Journal of periodontal research
Journal of periodontal research 医学-牙科与口腔外科
CiteScore
6.90
自引率
5.70%
发文量
103
审稿时长
6-12 weeks
期刊介绍: The Journal of Periodontal Research is an international research periodical the purpose of which is to publish original clinical and basic investigations and review articles concerned with every aspect of periodontology and related sciences. Brief communications (1-3 journal pages) are also accepted and a special effort is made to ensure their rapid publication. Reports of scientific meetings in periodontology and related fields are also published. One volume of six issues is published annually.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信