Pro-atherogenic lung and oral pathogens induce an inflammatory response in human and mouse mast cells

J Cell Mol Med. 2009 Jan;13(1):103-13. doi: 10.1111/j.1582-4934.2008.00285.x.

Abstract

A broad variety of microbes are present in atherosclerotic plaques and chronic bacterial infection increases the risk of atherosclerosis by mechanisms that have remained vague. One possible mechanism is that bacteria or bacterial products activate plaque mast cells that are known to participate in the pathogenesis of atherosclerosis. Here, we show by real-time PCR analysis and ELISA that Chlamydia pneumoniae (Cpn) and a periodontal pathogen, Aggregatibacter actinomycetemcomitans (Aa), both induce a time and concentration-dependent expression and secretion of interleukin 8 (IL-8), tumour necrosis factor-alpha (TNF-alpha) and monocyte chemoattractant protein-1 (MCP-1) by cultured human peripheral blood-derived mast cells, but not anti-inflammatory molecules, such as IL-10 or transforming growth factor beta 1 (TGF-beta 1). The IL-8 and MCP-1 responses were immediate, whereas the onset of TNF-alpha secretion was delayed. The Cpn-mediated pro-inflammatory effect was attenuated when the bacteria were inactivated by UV-treatment. Human monocyte-derived macrophages that were pre-infected with Cpn also induced a significant pro-inflammatory response in human mast cells, both in cocultures and when preconditioned media from Cpn-infected macrophages were used. Intranasal and intravenous administration of live Cpn and Aa, respectively induced an accumulation of activated mast cells in the aortic sinus of apolipoprotein E-deficient mice, however, with varying responses in the systemic levels of lipopolysaccharide (LPS) and TNF-alpha. Pro-atherogenic Cpn and Aa induce a pro-inflammatory response in cultured human connective tissue-type mast cells and activation of mouse aortic mast cells in vivo.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Atherosclerosis / immunology
  • Atherosclerosis / microbiology*
  • Atherosclerosis / pathology
  • Cell Degranulation
  • Cells, Cultured
  • Chemokine CCL2 / genetics
  • Chemokine CCL2 / metabolism
  • Chlamydophila Infections / immunology
  • Chlamydophila Infections / microbiology
  • Chlamydophila Infections / pathology
  • Chlamydophila pneumoniae / immunology*
  • Chlamydophila pneumoniae / pathogenicity
  • Coculture Techniques
  • Cytokines / metabolism*
  • Humans
  • Interleukin-8 / genetics
  • Interleukin-8 / metabolism
  • Lipopolysaccharides / blood
  • Macrophages / microbiology
  • Mast Cells / immunology*
  • Mast Cells / microbiology
  • Mice
  • Pasteurellaceae / immunology*
  • Pasteurellaceae / pathogenicity
  • Pasteurellaceae Infections / immunology
  • Pasteurellaceae Infections / microbiology
  • Pasteurellaceae Infections / pathology
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Sinus of Valsalva / immunology
  • Sinus of Valsalva / pathology
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • CCL2 protein, human
  • Ccl2 protein, mouse
  • Chemokine CCL2
  • Cytokines
  • Interleukin-8
  • Lipopolysaccharides
  • RNA, Messenger
  • Tumor Necrosis Factor-alpha