Porphyromonas gingivalis manipulates complement and TLR signaling to uncouple bacterial clearance from inflammation and promote dysbiosis

Cell Host Microbe. 2014 Jun 11;15(6):768-78. doi: 10.1016/j.chom.2014.05.012.

Abstract

Certain low-abundance bacterial species, such as the periodontitis-associated oral bacterium Porphyromonas gingivalis, can subvert host immunity to remodel a normally symbiotic microbiota into a dysbiotic, disease-provoking state. However, such pathogens also exploit inflammation to thrive in dysbiotic conditions. How these bacteria evade immunity while maintaining inflammation is unclear. As previously reported, P. gingivalis remodels the oral microbiota into a dysbiotic state by exploiting complement. Now we show that in neutrophils P. gingivalis disarms a host-protective TLR2-MyD88 pathway via proteasomal degradation of MyD88, whereas it activates an alternate TLR2-Mal-PI3K pathway. This alternate TLR2-Mal-PI3K pathway blocks phagocytosis, provides "bystander" protection to otherwise susceptible bacteria, and promotes dysbiotic inflammation in vivo. This mechanism to disengage bacterial clearance from inflammation required an intimate crosstalk between TLR2 and the complement receptor C5aR and can contribute to the persistence of microbial communities that drive dysbiotic diseases.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacteroidaceae Infections / immunology
  • Complement System Proteins / immunology
  • Dysbiosis / immunology
  • Dysbiosis / microbiology*
  • Host-Pathogen Interactions / immunology
  • Mice
  • Mice, Mutant Strains
  • Myeloid Differentiation Factor 88 / genetics
  • Myeloid Differentiation Factor 88 / metabolism
  • Neutrophils / immunology
  • Neutrophils / microbiology
  • Periodontitis / immunology
  • Periodontitis / microbiology*
  • Phagocytosis
  • Phosphatidylinositol 3-Kinases / metabolism
  • Porphyromonas gingivalis / immunology
  • Porphyromonas gingivalis / pathogenicity*
  • Receptor, Anaphylatoxin C5a / genetics
  • Receptor, Anaphylatoxin C5a / immunology
  • Receptor, Anaphylatoxin C5a / metabolism*
  • Signal Transduction
  • Toll-Like Receptor 2 / genetics
  • Toll-Like Receptor 2 / immunology
  • Toll-Like Receptor 2 / metabolism*

Substances

  • C5AR1 protein, human
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • Receptor, Anaphylatoxin C5a
  • TLR2 protein, human
  • Tlr2 protein, mouse
  • Toll-Like Receptor 2
  • Complement System Proteins
  • Phosphatidylinositol 3-Kinases