Akkermansia muciniphila reduces Porphyromonas gingivalis-induced inflammation and periodontal bone destruction

Olivier Huck, Hannah Mulhall, George Rubin, Zev Kizelnik, Radha Iyer, John D. Perpich, Nasreen Haque, Patrice D. Cani, Willem M. de Vos, Salomon Amar*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Aim: Akkermansia muciniphila is a beneficial gut commensal, whose anti-inflammatory properties have recently been demonstrated. This study aimed to evaluate the effect of A. muciniphila on Porphyromonas gingivalis elicited inflammation. Material and Methods: In lean and obese mice, A. muciniphila was administered in P. gingivalis-induced calvarial abscess and in experimental periodontitis model (EIP). Bone destruction and inflammation were evaluated by histomorphometric analysis. In vitro, A. muciniphila was co-cultured with P. gingivalis, growth and virulence factor expression was evaluated. Bone marrow macrophages (BMMϕ) and gingival epithelial cells (TIGK) were exposed to both bacterial strains, and the expression of inflammatory mediators, as well as tight junction markers, was analysed. Results: In a model of calvarial infection, A. muciniphila decreased inflammatory cell infiltration and bone destruction. In EIP, treatment with A. muciniphila resulted in a decreased alveolar bone loss. In vitro, the addition of A. muciniphila to P. gingivalis-infected BMMϕ increased anti-inflammatory IL-10 and decreased IL-12. Additionally, A. muciniphila exposure increases the expression of junctional integrity markers such as integrin-β1, E-cadherin and ZO-1 in TIGK cells. A. muciniphila co-culture with P. gingivalis reduced gingipains mRNA expression. Discussion: This study demonstrated the protective effects of A. muciniphila administration and may open consideration to its use as an adjunctive therapeutic agent to periodontal treatment.

Original languageEnglish
Pages (from-to)202-212
JournalJournal of Clinical Periodontology
Volume47
Issue number2
Early online date1 Nov 2019
DOIs
Publication statusPublished - Feb 2020

Fingerprint

Osteitis
Porphyromonas gingivalis
Periodontitis
Cadherins
Anti-Inflammatory Agents
Theoretical Models
Bone Marrow
Macrophages
Alveolar Bone Loss
Obese Mice
Tight Junctions
Virulence Factors
Interleukin-12
Coculture Techniques
Integrins
Interleukin-10
Abscess
Intercellular Signaling Peptides and Proteins
Epithelial Cells
Inflammation

Keywords

  • infection
  • inflammation
  • periodontitis
  • probiotic

Cite this

Huck, Olivier ; Mulhall, Hannah ; Rubin, George ; Kizelnik, Zev ; Iyer, Radha ; Perpich, John D. ; Haque, Nasreen ; Cani, Patrice D. ; de Vos, Willem M. ; Amar, Salomon. / Akkermansia muciniphila reduces Porphyromonas gingivalis-induced inflammation and periodontal bone destruction. In: Journal of Clinical Periodontology. 2020 ; Vol. 47, No. 2. pp. 202-212.
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title = "Akkermansia muciniphila reduces Porphyromonas gingivalis-induced inflammation and periodontal bone destruction",
abstract = "Aim: Akkermansia muciniphila is a beneficial gut commensal, whose anti-inflammatory properties have recently been demonstrated. This study aimed to evaluate the effect of A. muciniphila on Porphyromonas gingivalis elicited inflammation. Material and Methods: In lean and obese mice, A. muciniphila was administered in P. gingivalis-induced calvarial abscess and in experimental periodontitis model (EIP). Bone destruction and inflammation were evaluated by histomorphometric analysis. In vitro, A. muciniphila was co-cultured with P. gingivalis, growth and virulence factor expression was evaluated. Bone marrow macrophages (BMMϕ) and gingival epithelial cells (TIGK) were exposed to both bacterial strains, and the expression of inflammatory mediators, as well as tight junction markers, was analysed. Results: In a model of calvarial infection, A. muciniphila decreased inflammatory cell infiltration and bone destruction. In EIP, treatment with A. muciniphila resulted in a decreased alveolar bone loss. In vitro, the addition of A. muciniphila to P. gingivalis-infected BMMϕ increased anti-inflammatory IL-10 and decreased IL-12. Additionally, A. muciniphila exposure increases the expression of junctional integrity markers such as integrin-β1, E-cadherin and ZO-1 in TIGK cells. A. muciniphila co-culture with P. gingivalis reduced gingipains mRNA expression. Discussion: This study demonstrated the protective effects of A. muciniphila administration and may open consideration to its use as an adjunctive therapeutic agent to periodontal treatment.",
keywords = "infection, inflammation, periodontitis, probiotic",
author = "Olivier Huck and Hannah Mulhall and George Rubin and Zev Kizelnik and Radha Iyer and Perpich, {John D.} and Nasreen Haque and Cani, {Patrice D.} and {de Vos}, {Willem M.} and Salomon Amar",
year = "2020",
month = "2",
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language = "English",
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Huck, O, Mulhall, H, Rubin, G, Kizelnik, Z, Iyer, R, Perpich, JD, Haque, N, Cani, PD, de Vos, WM & Amar, S 2020, 'Akkermansia muciniphila reduces Porphyromonas gingivalis-induced inflammation and periodontal bone destruction', Journal of Clinical Periodontology, vol. 47, no. 2, pp. 202-212. https://doi.org/10.1111/jcpe.13214

Akkermansia muciniphila reduces Porphyromonas gingivalis-induced inflammation and periodontal bone destruction. / Huck, Olivier; Mulhall, Hannah; Rubin, George; Kizelnik, Zev; Iyer, Radha; Perpich, John D.; Haque, Nasreen; Cani, Patrice D.; de Vos, Willem M.; Amar, Salomon.

In: Journal of Clinical Periodontology, Vol. 47, No. 2, 02.2020, p. 202-212.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Akkermansia muciniphila reduces Porphyromonas gingivalis-induced inflammation and periodontal bone destruction

AU - Huck, Olivier

AU - Mulhall, Hannah

AU - Rubin, George

AU - Kizelnik, Zev

AU - Iyer, Radha

AU - Perpich, John D.

AU - Haque, Nasreen

AU - Cani, Patrice D.

AU - de Vos, Willem M.

AU - Amar, Salomon

PY - 2020/2

Y1 - 2020/2

N2 - Aim: Akkermansia muciniphila is a beneficial gut commensal, whose anti-inflammatory properties have recently been demonstrated. This study aimed to evaluate the effect of A. muciniphila on Porphyromonas gingivalis elicited inflammation. Material and Methods: In lean and obese mice, A. muciniphila was administered in P. gingivalis-induced calvarial abscess and in experimental periodontitis model (EIP). Bone destruction and inflammation were evaluated by histomorphometric analysis. In vitro, A. muciniphila was co-cultured with P. gingivalis, growth and virulence factor expression was evaluated. Bone marrow macrophages (BMMϕ) and gingival epithelial cells (TIGK) were exposed to both bacterial strains, and the expression of inflammatory mediators, as well as tight junction markers, was analysed. Results: In a model of calvarial infection, A. muciniphila decreased inflammatory cell infiltration and bone destruction. In EIP, treatment with A. muciniphila resulted in a decreased alveolar bone loss. In vitro, the addition of A. muciniphila to P. gingivalis-infected BMMϕ increased anti-inflammatory IL-10 and decreased IL-12. Additionally, A. muciniphila exposure increases the expression of junctional integrity markers such as integrin-β1, E-cadherin and ZO-1 in TIGK cells. A. muciniphila co-culture with P. gingivalis reduced gingipains mRNA expression. Discussion: This study demonstrated the protective effects of A. muciniphila administration and may open consideration to its use as an adjunctive therapeutic agent to periodontal treatment.

AB - Aim: Akkermansia muciniphila is a beneficial gut commensal, whose anti-inflammatory properties have recently been demonstrated. This study aimed to evaluate the effect of A. muciniphila on Porphyromonas gingivalis elicited inflammation. Material and Methods: In lean and obese mice, A. muciniphila was administered in P. gingivalis-induced calvarial abscess and in experimental periodontitis model (EIP). Bone destruction and inflammation were evaluated by histomorphometric analysis. In vitro, A. muciniphila was co-cultured with P. gingivalis, growth and virulence factor expression was evaluated. Bone marrow macrophages (BMMϕ) and gingival epithelial cells (TIGK) were exposed to both bacterial strains, and the expression of inflammatory mediators, as well as tight junction markers, was analysed. Results: In a model of calvarial infection, A. muciniphila decreased inflammatory cell infiltration and bone destruction. In EIP, treatment with A. muciniphila resulted in a decreased alveolar bone loss. In vitro, the addition of A. muciniphila to P. gingivalis-infected BMMϕ increased anti-inflammatory IL-10 and decreased IL-12. Additionally, A. muciniphila exposure increases the expression of junctional integrity markers such as integrin-β1, E-cadherin and ZO-1 in TIGK cells. A. muciniphila co-culture with P. gingivalis reduced gingipains mRNA expression. Discussion: This study demonstrated the protective effects of A. muciniphila administration and may open consideration to its use as an adjunctive therapeutic agent to periodontal treatment.

KW - infection

KW - inflammation

KW - periodontitis

KW - probiotic

U2 - 10.1111/jcpe.13214

DO - 10.1111/jcpe.13214

M3 - Article

VL - 47

SP - 202

EP - 212

JO - Journal of Clinical Periodontology

JF - Journal of Clinical Periodontology

SN - 0303-6979

IS - 2

ER -