Cyclic di-AMP alleviates periodontitis by activating PI3K/Akt/Nrf2 pathways

Emerging research demonstrates the regulatory effects of c-di-AMP, a bacterial-derived small molecule secondary messenger, on host immune responses and promoting resistance against infection-related diseases. This study aims to elucidate the role of c-di-AMP in the occurrence and development of peri...

Full description

Saved in:
Bibliographic Details
Main Authors: Kaihua Luo, Qinrui Wu, Zhengyi Li, Yajie Wu, Zhifei Su, Fangjie Zhou, Qinyang Li, Biao Ren, Yuqing Li, Jiyao Li, Xian Peng
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-03-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2025.1560155/full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850051236660772864
author Kaihua Luo
Kaihua Luo
Qinrui Wu
Qinrui Wu
Zhengyi Li
Yajie Wu
Yajie Wu
Zhifei Su
Zhifei Su
Fangjie Zhou
Fangjie Zhou
Qinyang Li
Qinyang Li
Biao Ren
Yuqing Li
Jiyao Li
Jiyao Li
Xian Peng
author_facet Kaihua Luo
Kaihua Luo
Qinrui Wu
Qinrui Wu
Zhengyi Li
Yajie Wu
Yajie Wu
Zhifei Su
Zhifei Su
Fangjie Zhou
Fangjie Zhou
Qinyang Li
Qinyang Li
Biao Ren
Yuqing Li
Jiyao Li
Jiyao Li
Xian Peng
author_sort Kaihua Luo
collection DOAJ
description Emerging research demonstrates the regulatory effects of c-di-AMP, a bacterial-derived small molecule secondary messenger, on host immune responses and promoting resistance against infection-related diseases. This study aims to elucidate the role of c-di-AMP in the occurrence and development of periodontitis. Using model of ligation-induced periodontitis, we observed that c-di-AMP effectively alleviated alveolar bone resorption. Transcriptomic sequencing in mice gingival tissues demonstrated that treatment with c-di-AMP led to a significant upregulation of the PI3K/Akt signaling pathway and its key components, including Akt3. Concurrently, we observed an upregulation of the cGMP/PKG signaling pathway. To validate our findings, we treated gingival epithelial cells with c-di-AMP and confirmed the activation of the PI3K/Akt pathway by c-di-AMP in gingival epithelial cells. Under LPS-induced inflammation, c-di-AMP significantly suppressed the release of inflammatory factors (such as IL-6 and TNF-α) from gingival epithelial cells. Moreover, key components of the PI3K/Akt pathway, including Akt, and downstream inflammation regulatory gene Nrf2, were upregulated, which were also confirmed at the protein level. Collectively, this study demonstrates that c-di-AMP definitely plays a role in alleviating periodontitis. Our findings highlight the mechanisms by which c-di-AMP modulates periodontitis, including activating the PI3K/Akt pathway and potentially involving the cGMP/PKG pathway, ultimately contributing to improved immune defense and maintenance of bone homeostasis.
format Article
id doaj-art-dd36b07d19fd4231ba1d40c80f096076
institution DOAJ
issn 2235-2988
language English
publishDate 2025-03-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Cellular and Infection Microbiology
spelling doaj-art-dd36b07d19fd4231ba1d40c80f0960762025-08-20T02:53:13ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882025-03-011510.3389/fcimb.2025.15601551560155Cyclic di-AMP alleviates periodontitis by activating PI3K/Akt/Nrf2 pathwaysKaihua Luo0Kaihua Luo1Qinrui Wu2Qinrui Wu3Zhengyi Li4Yajie Wu5Yajie Wu6Zhifei Su7Zhifei Su8Fangjie Zhou9Fangjie Zhou10Qinyang Li11Qinyang Li12Biao Ren13Yuqing Li14Jiyao Li15Jiyao Li16Xian Peng17State Key Laboratory of Oral Diseases & National Center for Stomatology & National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Cariology and Endodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaState Key Laboratory of Oral Diseases & National Center for Stomatology & National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Cariology and Endodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaState Key Laboratory of Oral Diseases & National Center for Stomatology & National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaState Key Laboratory of Oral Diseases & National Center for Stomatology & National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Cariology and Endodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaState Key Laboratory of Oral Diseases & National Center for Stomatology & National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Cariology and Endodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaState Key Laboratory of Oral Diseases & National Center for Stomatology & National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Cariology and Endodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaState Key Laboratory of Oral Diseases & National Center for Stomatology & National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Cariology and Endodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaState Key Laboratory of Oral Diseases & National Center for Stomatology & National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaState Key Laboratory of Oral Diseases & National Center for Stomatology & National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaState Key Laboratory of Oral Diseases & National Center for Stomatology & National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Cariology and Endodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaState Key Laboratory of Oral Diseases & National Center for Stomatology & National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, ChinaEmerging research demonstrates the regulatory effects of c-di-AMP, a bacterial-derived small molecule secondary messenger, on host immune responses and promoting resistance against infection-related diseases. This study aims to elucidate the role of c-di-AMP in the occurrence and development of periodontitis. Using model of ligation-induced periodontitis, we observed that c-di-AMP effectively alleviated alveolar bone resorption. Transcriptomic sequencing in mice gingival tissues demonstrated that treatment with c-di-AMP led to a significant upregulation of the PI3K/Akt signaling pathway and its key components, including Akt3. Concurrently, we observed an upregulation of the cGMP/PKG signaling pathway. To validate our findings, we treated gingival epithelial cells with c-di-AMP and confirmed the activation of the PI3K/Akt pathway by c-di-AMP in gingival epithelial cells. Under LPS-induced inflammation, c-di-AMP significantly suppressed the release of inflammatory factors (such as IL-6 and TNF-α) from gingival epithelial cells. Moreover, key components of the PI3K/Akt pathway, including Akt, and downstream inflammation regulatory gene Nrf2, were upregulated, which were also confirmed at the protein level. Collectively, this study demonstrates that c-di-AMP definitely plays a role in alleviating periodontitis. Our findings highlight the mechanisms by which c-di-AMP modulates periodontitis, including activating the PI3K/Akt pathway and potentially involving the cGMP/PKG pathway, ultimately contributing to improved immune defense and maintenance of bone homeostasis.https://www.frontiersin.org/articles/10.3389/fcimb.2025.1560155/fullc-di-AMPPI3K/Akt signaling pathwaysecond-messenger systemsperiodontitishost-pathogen interactionsmicrobial dysbiosis
spellingShingle Kaihua Luo
Kaihua Luo
Qinrui Wu
Qinrui Wu
Zhengyi Li
Yajie Wu
Yajie Wu
Zhifei Su
Zhifei Su
Fangjie Zhou
Fangjie Zhou
Qinyang Li
Qinyang Li
Biao Ren
Yuqing Li
Jiyao Li
Jiyao Li
Xian Peng
Cyclic di-AMP alleviates periodontitis by activating PI3K/Akt/Nrf2 pathways
Frontiers in Cellular and Infection Microbiology
c-di-AMP
PI3K/Akt signaling pathway
second-messenger systems
periodontitis
host-pathogen interactions
microbial dysbiosis
title Cyclic di-AMP alleviates periodontitis by activating PI3K/Akt/Nrf2 pathways
title_full Cyclic di-AMP alleviates periodontitis by activating PI3K/Akt/Nrf2 pathways
title_fullStr Cyclic di-AMP alleviates periodontitis by activating PI3K/Akt/Nrf2 pathways
title_full_unstemmed Cyclic di-AMP alleviates periodontitis by activating PI3K/Akt/Nrf2 pathways
title_short Cyclic di-AMP alleviates periodontitis by activating PI3K/Akt/Nrf2 pathways
title_sort cyclic di amp alleviates periodontitis by activating pi3k akt nrf2 pathways
topic c-di-AMP
PI3K/Akt signaling pathway
second-messenger systems
periodontitis
host-pathogen interactions
microbial dysbiosis
url https://www.frontiersin.org/articles/10.3389/fcimb.2025.1560155/full
work_keys_str_mv AT kaihualuo cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT kaihualuo cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT qinruiwu cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT qinruiwu cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT zhengyili cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT yajiewu cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT yajiewu cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT zhifeisu cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT zhifeisu cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT fangjiezhou cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT fangjiezhou cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT qinyangli cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT qinyangli cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT biaoren cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT yuqingli cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT jiyaoli cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT jiyaoli cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways
AT xianpeng cyclicdiampalleviatesperiodontitisbyactivatingpi3kaktnrf2pathways