Mycobacterium massiliense induces inflammatory responses in macrophages through Toll-like receptor 2 and c-Jun N-terminal kinase

J Clin Immunol. 2014 Feb;34(2):212-23. doi: 10.1007/s10875-013-9978-y. Epub 2014 Jan 9.

Abstract

Mycobacterium massiliense (Mmass) is an emerging, rapidly growing mycobacterium (RGM) that belongs to the M. abscessus (Mabc) group, albeit clearly differentiated from Mabc. Compared with M. tuberculosis, a well-characterized human pathogen, the host innate immune response against Mmass infection is largely unknown. In this study, we show that Mmass robustly activates mRNA and protein expression of tumor necrosis factor (TNF)-α and interleukin (IL)-6 in murine bone marrow-derived macrophages (BMDMs). Toll-like receptor (TLR)-2 and myeloid differentiation primary response gene 88 (MyD88), but neither TLR4 nor Dectin-1, are involved in Mmass-induced TNF-α or IL-6 production in BMDMs. Mmass infection also activates the mitogen-activated protein kinase (MAPKs; c-Jun N-terminal kinase (JNK), ERK1/2 and p38 MAPK) pathway. Mmass-induced TNF-α and IL-6 production was dependent on JNK activation, while they were unaffected by either the ERK1/2 or p38 pathway in BMDMs. Additionally, intracellular reactive oxygen species (ROS), NADPH oxidase-2, and nuclear factor-κB are required for Mmass-induced proinflammatory cytokine generation in macrophages. Furthermore, the S morphotype of Mmass showed lower overall induction of pro-inflammatory (TNF-α, IL-6, and IL-1β) and anti-inflammatory (IL-10) cytokines than the R morphotype, suggesting fewer immunogenic characteristics for this clinical strain. Together, these results suggest that Mmass-induced activation of host proinflammatory cytokines is mediated through TLR2-dependent JNK and ROS signaling pathways.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Cytokines / biosynthesis
  • Disease Models, Animal
  • Inflammation Mediators / metabolism
  • JNK Mitogen-Activated Protein Kinases / metabolism*
  • Lectins, C-Type / metabolism
  • Macrophages / immunology*
  • Macrophages / metabolism*
  • Membrane Glycoproteins / metabolism
  • Mice
  • Mice, Knockout
  • Mycobacterium / immunology*
  • Mycobacterium Infections / genetics
  • Mycobacterium Infections / immunology*
  • Mycobacterium Infections / metabolism*
  • Myeloid Differentiation Factor 88 / metabolism
  • NADPH Oxidase 2
  • NADPH Oxidases / metabolism
  • NF-kappa B / metabolism
  • Reactive Oxygen Species / metabolism
  • Signal Transduction
  • Toll-Like Receptor 2 / genetics
  • Toll-Like Receptor 2 / metabolism*

Substances

  • Cytokines
  • Inflammation Mediators
  • Lectins, C-Type
  • Membrane Glycoproteins
  • Myeloid Differentiation Factor 88
  • NF-kappa B
  • Reactive Oxygen Species
  • Toll-Like Receptor 2
  • dectin 1
  • Cybb protein, mouse
  • NADPH Oxidase 2
  • NADPH Oxidases
  • JNK Mitogen-Activated Protein Kinases