Thrombospondin-1 production is enhanced by Porphyromonas gingivalis lipopolysaccharide in THP-1 cells

PLoS One. 2014 Dec 12;9(12):e115107. doi: 10.1371/journal.pone.0115107. eCollection 2014.

Abstract

Periodontitis is a chronic inflammatory disease caused by gram-negative anaerobic bacteria. Monocytes and macrophages stimulated by periodontopathic bacteria induce inflammatory mediators that cause tooth-supporting structure destruction and alveolar bone resorption. In this study, using a DNA microarray, we identified the enhanced gene expression of thrombospondin-1 (TSP-1) in human monocytic cells stimulated by Porphyromonas gingivalis lipopolysaccharide (LPS). TSP-1 is a multifunctional extracellular matrix protein that is upregulated during the inflammatory process. Recent studies have suggested that TSP-1 is associated with rheumatoid arthritis, diabetes mellitus, and osteoclastogenesis. TSP-1 is secreted from neutrophils, monocytes, and macrophages, which mediate immune responses at inflammatory regions. However, TSP-1 expression in periodontitis and the mechanisms underlying TSP-1 expression in human monocytic cells remain unknown. Here using real-time RT-PCR, we demonstrated that TSP-1 mRNA expression level was significantly upregulated in inflamed periodontitis gingival tissues and in P. gingivalis LPS-stimulated human monocytic cell line THP-1 cells. TSP-1 was expressed via Toll-like receptor (TLR) 2 and TLR4 pathways. In P. gingivalis LPS stimulation, TSP-1 expression was dependent upon TLR2 through the activation of NF-κB signaling. Furthermore, IL-17F synergistically enhanced P. gingivalis LPS-induced TSP-1 production. These results suggest that modulation of TSP-1 expression by P. gingivalis plays an important role in the progression and chronicity of periodontitis. It may also contribute a new target molecule for periodontal therapy.

MeSH terms

  • Cell Line, Tumor
  • Cytokines / biosynthesis
  • Cytokines / genetics
  • Gene Expression / drug effects
  • Humans
  • Lipopolysaccharides / pharmacology*
  • Microarray Analysis
  • Monocytes / drug effects*
  • Monocytes / metabolism*
  • NF-kappa B p50 Subunit / metabolism
  • Periodontitis / metabolism*
  • Periodontitis / microbiology
  • Porphyromonas gingivalis / chemistry
  • Porphyromonas gingivalis / metabolism*
  • RNA, Messenger / biosynthesis
  • Thrombospondin 1 / biosynthesis*
  • Thrombospondin 1 / genetics
  • Toll-Like Receptors / metabolism
  • Up-Regulation / drug effects

Substances

  • Cytokines
  • Lipopolysaccharides
  • NF-kappa B p50 Subunit
  • RNA, Messenger
  • Thrombospondin 1
  • Toll-Like Receptors

Grants and funding

This work was supported by JSPS KAKENHI Grant Number 25463213, 25293424, 26861805. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.