Dental infection of Porphyromonas gingivalis exacerbates high fat diet-induced steatohepatitis in mice

J Gastroenterol. 2013 Nov;48(11):1259-70. doi: 10.1007/s00535-012-0738-1. Epub 2013 Jan 11.

Abstract

Background: We investigated the effects of dental infection with Porphyromonas gingivalis (P.g.), an important periodontal pathogen, on NASH progression, by feeding mice a high fat diet (HFD)and examining P.g. infection in the liver of NASH patients.

Methods: C57BL/6J mice were fed either chow-diet (CD) or HFD for 12 weeks, and then half of the mice in each group were infected with P.g. from the pulp chamber (HFD-P.g.(-), HFD-P.g.(+), CD-P.g.(-) and CD-P.g.(+)). Histological and immunohistochemical examinations, measurement of serum lipopolysaccharide (LPS) levels and ELISA for cytokines in the liver were performed. We then studied the effects of LPS from P.g. (P.g.-LPS) on palmitate-induced steatotic hepatocytes in vitro, and performed immunohistochemical detection of P.g. in liver biopsy specimens of NASH patients.

Results: Serum levels of LPS are upregulated in P.g.(+) groups. Steatosis of the liver developed in HFD groups, and foci of Mac2-positive macrophages were prominent in HFD-P.g.(+). P.g. was detected in Kupffer cells and hepatocytes. Interestingly, areas of fibrosis with proliferation of hepatic stellate cells and collagen formation were only observed in HFD-P.g.(+). In steatotic hepatocytes, expression of TLR2, one of the P.g.-LPS receptors, was upregulated. P.g.-LPS further increased mRNA levels of palmitate-induced inflammasome and proinflammatory cytokines in steatotic hepatocytes. We demonstrated for the first time that P.g. existed in the liver of NASH patients with advanced fibrosis.

Conclusions: Dental infection of P.g. may play an important role in NASH progression through upregulation of the P.g.-LPS-TLR2 pathway and activation of inflammasomes. Therefore, preventing and/or eliminating P.g. infection by dental therapy may have a beneficial impact on management of NASH.

MeSH terms

  • Adult
  • Aged
  • Animals
  • Bacteroidaceae Infections / complications*
  • Bacteroidaceae Infections / metabolism
  • Bacteroidaceae Infections / pathology
  • Biopsy
  • Cells, Cultured
  • Cytokines / biosynthesis
  • Cytokines / genetics
  • Diet, High-Fat / adverse effects*
  • Disease Models, Animal
  • Disease Progression
  • Fatty Liver / etiology*
  • Fatty Liver / metabolism
  • Fatty Liver / microbiology
  • Fatty Liver / pathology
  • Female
  • Gene Expression Regulation / drug effects
  • Hepatocytes / drug effects
  • Hepatocytes / metabolism
  • Hepatocytes / microbiology
  • Humans
  • Inflammasomes / biosynthesis
  • Inflammation Mediators / metabolism
  • Liver / metabolism
  • Liver / microbiology
  • Liver / pathology
  • Liver Cirrhosis / etiology
  • Liver Cirrhosis / metabolism
  • Liver Cirrhosis / microbiology
  • Liver Cirrhosis / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Middle Aged
  • Non-alcoholic Fatty Liver Disease
  • Palmitates / pharmacology
  • Periapical Granuloma / complications*
  • Porphyromonas gingivalis / isolation & purification*
  • RNA, Messenger / genetics
  • Toll-Like Receptor 2 / biosynthesis
  • Up-Regulation

Substances

  • Cytokines
  • Inflammasomes
  • Inflammation Mediators
  • Palmitates
  • RNA, Messenger
  • Tlr2 protein, mouse
  • Toll-Like Receptor 2