TLR3 regulates mycobacterial RNA-induced IL-10 production through the PI3K/AKT signaling pathway

Cell Signal. 2014 May;26(5):942-50. doi: 10.1016/j.cellsig.2014.01.015. Epub 2014 Jan 22.

Abstract

Cytokine induction in response to Mycobacterium tuberculosis (Mtb) infection is critical for pathogen control, by (i) mediating innate immune effector functions and (ii) instructing specific adaptive immunity. IL-10 is an important anti-inflammatory cytokine involved in pathogenesis of tuberculosis (TB). Here, we show that TLR3, a sensor of extracellular viral or host RNA with stable stem structures derived from infected or damaged cells, is essential for Mtb-induced IL-10 production. Upon Mycobacterium bovis Bacillus Calmette-Guérin (BCG) infection, TLR3(-/-) macrophages expressed lower IL-10 but higher IL-12p40 production, accompanied by reduced phosphorylation of AKT at Ser473. BCG-infected TLR3(-/-) mice exhibited reduced IL-10 but elevated IL-12 expression compared to controls. Moreover, higher numbers of splenic Th1 cells and reduced pulmonary bacterial burden and tissue damage were observed in BCG-infected TLR3(-/-) mice. Finally, BCG RNA induced IL-10 in macrophages via TLR3-mediated activation of PI3K/AKT. Our findings demonstrate a critical role of TLR3-mediated regulation in the pathogenesis of mycobacterial infection involving mycobacterial RNA, which induces IL-10 through the PI3K/AKT signaling pathway.

Keywords: Interleukin 10; Mycobacterium bovis BCG; Phosphoinositide 3-kinase (PI3K)/AKT; RNA; Toll-like receptor 3.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Interleukin-10 / metabolism*
  • Interleukin-12 Subunit p40 / metabolism
  • Macrophages / immunology
  • Macrophages / metabolism
  • Macrophages / microbiology
  • Mice
  • Mycobacterium bovis / genetics
  • Mycobacterium bovis / pathogenicity
  • Phosphatidylinositol 3-Kinase / metabolism*
  • Phosphorylation
  • Proto-Oncogene Proteins c-akt / metabolism*
  • RNA, Bacterial / metabolism*
  • Signal Transduction
  • Toll-Like Receptor 3 / deficiency
  • Toll-Like Receptor 3 / genetics
  • Toll-Like Receptor 3 / metabolism*

Substances

  • Interleukin-12 Subunit p40
  • RNA, Bacterial
  • Toll-Like Receptor 3
  • Interleukin-10
  • Phosphatidylinositol 3-Kinase
  • Proto-Oncogene Proteins c-akt