Periodontitis induced by Porphyromonas gingivalis drives impaired glucose metabolism in mice

Periodontitis has been demonstrated to be bidirectionally associated with diabetes and has been recognized as a complication of diabetes. As a periodontal pathogen, Porphyromonas gingivalis is a possible pathogen linking periodontal disease and systemic diseases. It has also been found to be involve...

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Main Authors: Ni Kang, Yong Zhang, Fei Xue, Jinyu Duan, Fan Chen, Yu Cai, Qingxian Luan
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-10-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2022.998600/full
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author Ni Kang
Ni Kang
Yong Zhang
Fei Xue
Jinyu Duan
Fan Chen
Yu Cai
Yu Cai
Qingxian Luan
author_facet Ni Kang
Ni Kang
Yong Zhang
Fei Xue
Jinyu Duan
Fan Chen
Yu Cai
Yu Cai
Qingxian Luan
author_sort Ni Kang
collection DOAJ
description Periodontitis has been demonstrated to be bidirectionally associated with diabetes and has been recognized as a complication of diabetes. As a periodontal pathogen, Porphyromonas gingivalis is a possible pathogen linking periodontal disease and systemic diseases. It has also been found to be involved in the occurrence and development of diabetes. In this study, 6-week-old male C57BL/6 mice were orally administered the P. gingivalis strain ATCC381 for 22 weeks. Histological analysis of the gingival tissue and quantified analysis of alveolar bone loss were performed to evaluate periodontal destruction. Body weight, fasting glucose, glucose tolerance test (GTT), and insulin tolerance test (ITT) were used to evaluate glucose metabolism disorder. We then analyzed the expression profiles of inflammatory cytokines and chemokines in gingival tissue, the liver, and adipose tissue, as well as in serum. The results showed that mice in the P. gingivalis-administered group developed apparent gingival inflammation and more alveolar bone loss compared to the control group. After 22 weeks of P. gingivalis infection, significant differences were observed at 30 and 60 min for the GTT and at 15 min for the ITT. P. gingivalis-administered mice showed an increase in the mRNA expression levels of the pro-inflammatory cytokines (TNF-α, IL-6, IL-17, and IL-23) and chemokines (CCL2, CCL8, and CXCL10) in the gingiva and serum. The expression levels of the glucose metabolism-related genes were also changed in the liver and adipose tissue. Our results indicate that oral administration of P. gingivalis can induce changes in the inflammatory cytokines and chemokines in the gingiva and blood, can lead to alveolar bone loss and to inflammatory changes in the liver and adipose tissues, and can promote glucose metabolism disorder in mice.
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spelling doaj.art-616cc619d291479a9a95412bdfdb82532022-12-22T04:13:03ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882022-10-011210.3389/fcimb.2022.998600998600Periodontitis induced by Porphyromonas gingivalis drives impaired glucose metabolism in miceNi Kang0Ni Kang1Yong Zhang2Fei Xue3Jinyu Duan4Fan Chen5Yu Cai6Yu Cai7Qingxian Luan8Department of Periodontology, Peking University School and Hospital of Stomatology and National Center of Stomatology and National Clinical Research Center for Oral Diseases and National Engineering Research Center of Oral Biomaterials and Digital Medical Devices and Beijing Key Laboratory of Digital Stomatology and Research Center of Engineering and Technology for Computerized Dentistry Ministry of Health and National Medical Products Administration (NMPA) Key Laboratory for Dental Materials, Beijing, ChinaCentral Laboratory, Peking University School and Hospital of Stomatology and National Center of Stomatology and National Clinical Research Center for Oral Diseases and National Engineering Research Center of Oral Biomaterials and Digital Medical Devices and Beijing Key Laboratory of Digital Stomatology and Research Center of Engineering and Technology for Computerized Dentistry Ministry of Health and National Medical Products Administration (NMPA) Key Laboratory for Dental Materials, Beijing, ChinaFirst Clinical Division, Peking University School and Hospital of Stomatology and National Center of Stomatology and National Clinical Research Center for Oral Diseases and National Engineering Research Center of Oral Biomaterials and Digital Medical Devices and Beijing Key Laboratory of Digital Stomatology and Research Center of Engineering and Technology for Computerized Dentistry Ministry of Health and National Medical Products Administration (NMPA) Key Laboratory for Dental Materials, Beijing, ChinaFirst Clinical Division, Peking University School and Hospital of Stomatology and National Center of Stomatology and National Clinical Research Center for Oral Diseases and National Engineering Research Center of Oral Biomaterials and Digital Medical Devices and Beijing Key Laboratory of Digital Stomatology and Research Center of Engineering and Technology for Computerized Dentistry Ministry of Health and National Medical Products Administration (NMPA) Key Laboratory for Dental Materials, Beijing, ChinaFirst Clinical Division, Peking University School and Hospital of Stomatology and National Center of Stomatology and National Clinical Research Center for Oral Diseases and National Engineering Research Center of Oral Biomaterials and Digital Medical Devices and Beijing Key Laboratory of Digital Stomatology and Research Center of Engineering and Technology for Computerized Dentistry Ministry of Health and National Medical Products Administration (NMPA) Key Laboratory for Dental Materials, Beijing, ChinaDepartment of Stomatology, People’s Hospital of Peking University, Beijing, ChinaDepartment of Periodontology, Peking University School and Hospital of Stomatology and National Center of Stomatology and National Clinical Research Center for Oral Diseases and National Engineering Research Center of Oral Biomaterials and Digital Medical Devices and Beijing Key Laboratory of Digital Stomatology and Research Center of Engineering and Technology for Computerized Dentistry Ministry of Health and National Medical Products Administration (NMPA) Key Laboratory for Dental Materials, Beijing, ChinaCentral Laboratory, Peking University School and Hospital of Stomatology and National Center of Stomatology and National Clinical Research Center for Oral Diseases and National Engineering Research Center of Oral Biomaterials and Digital Medical Devices and Beijing Key Laboratory of Digital Stomatology and Research Center of Engineering and Technology for Computerized Dentistry Ministry of Health and National Medical Products Administration (NMPA) Key Laboratory for Dental Materials, Beijing, ChinaDepartment of Periodontology, Peking University School and Hospital of Stomatology and National Center of Stomatology and National Clinical Research Center for Oral Diseases and National Engineering Research Center of Oral Biomaterials and Digital Medical Devices and Beijing Key Laboratory of Digital Stomatology and Research Center of Engineering and Technology for Computerized Dentistry Ministry of Health and National Medical Products Administration (NMPA) Key Laboratory for Dental Materials, Beijing, ChinaPeriodontitis has been demonstrated to be bidirectionally associated with diabetes and has been recognized as a complication of diabetes. As a periodontal pathogen, Porphyromonas gingivalis is a possible pathogen linking periodontal disease and systemic diseases. It has also been found to be involved in the occurrence and development of diabetes. In this study, 6-week-old male C57BL/6 mice were orally administered the P. gingivalis strain ATCC381 for 22 weeks. Histological analysis of the gingival tissue and quantified analysis of alveolar bone loss were performed to evaluate periodontal destruction. Body weight, fasting glucose, glucose tolerance test (GTT), and insulin tolerance test (ITT) were used to evaluate glucose metabolism disorder. We then analyzed the expression profiles of inflammatory cytokines and chemokines in gingival tissue, the liver, and adipose tissue, as well as in serum. The results showed that mice in the P. gingivalis-administered group developed apparent gingival inflammation and more alveolar bone loss compared to the control group. After 22 weeks of P. gingivalis infection, significant differences were observed at 30 and 60 min for the GTT and at 15 min for the ITT. P. gingivalis-administered mice showed an increase in the mRNA expression levels of the pro-inflammatory cytokines (TNF-α, IL-6, IL-17, and IL-23) and chemokines (CCL2, CCL8, and CXCL10) in the gingiva and serum. The expression levels of the glucose metabolism-related genes were also changed in the liver and adipose tissue. Our results indicate that oral administration of P. gingivalis can induce changes in the inflammatory cytokines and chemokines in the gingiva and blood, can lead to alveolar bone loss and to inflammatory changes in the liver and adipose tissues, and can promote glucose metabolism disorder in mice.https://www.frontiersin.org/articles/10.3389/fcimb.2022.998600/fullperiodontitisPorphyromonas gingivalis (P. gingivalis)glucose metabolisminflammationalveolar bone loss
spellingShingle Ni Kang
Ni Kang
Yong Zhang
Fei Xue
Jinyu Duan
Fan Chen
Yu Cai
Yu Cai
Qingxian Luan
Periodontitis induced by Porphyromonas gingivalis drives impaired glucose metabolism in mice
Frontiers in Cellular and Infection Microbiology
periodontitis
Porphyromonas gingivalis (P. gingivalis)
glucose metabolism
inflammation
alveolar bone loss
title Periodontitis induced by Porphyromonas gingivalis drives impaired glucose metabolism in mice
title_full Periodontitis induced by Porphyromonas gingivalis drives impaired glucose metabolism in mice
title_fullStr Periodontitis induced by Porphyromonas gingivalis drives impaired glucose metabolism in mice
title_full_unstemmed Periodontitis induced by Porphyromonas gingivalis drives impaired glucose metabolism in mice
title_short Periodontitis induced by Porphyromonas gingivalis drives impaired glucose metabolism in mice
title_sort periodontitis induced by porphyromonas gingivalis drives impaired glucose metabolism in mice
topic periodontitis
Porphyromonas gingivalis (P. gingivalis)
glucose metabolism
inflammation
alveolar bone loss
url https://www.frontiersin.org/articles/10.3389/fcimb.2022.998600/full
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