Activation of NOD2 in vivo induces IL-1beta production in the eye via caspase-1 but results in ocular inflammation independently of IL-1 signaling

J Leukoc Biol. 2008 Aug;84(2):529-36. doi: 10.1189/jlb.0108015. Epub 2008 May 21.

Abstract

Nucleotide-binding and oligomerization domain 2 (NOD2) belongs to the emerging Nod-like receptor (NLR) family considered important in innate immunity. Mutations in NOD2 cause Blau syndrome, an inherited inflammation of eye, joints, and skin. Mutations in a homologous region of another NLR member, NALP3, cause autoinflammation, wherein IL-1beta plays a critical role. Here, we tested the hypothesis that IL-1beta is a downstream mediator of NOD2-dependent ocular inflammation. We used a mouse model of NOD2-dependent ocular inflammation induced by muramyl dipeptide (MDP), the minimal bacterial motif sensed by NOD2. We report that MDP-induced ocular inflammation generates IL-1beta and IL-18 within the eye in a NOD2- and caspase-1-dependent manner. Surprisingly, two critical measures of ocular inflammation, leukocyte rolling and leukocyte intravascular adherence, appear to be completely independent of IL-1 signaling effects, as caspase-1 and IL-1R1-deficient mice still developed ocular inflammation in response to MDP. In contrast to the eye, a diminished neutrophil response was observed in an in vivo model of MDP-induced peritonitis in caspase-1-deficient mice, suggesting that IL-1beta is not essential in NOD2-dependent ocular inflammation, but it is involved, in part, in systemic inflammation triggered by NOD2 activation. This disparity may be influenced by IL-1R antagonist (IL-1Ra), as we observed differential IL-1Ra levels in the eye versus plasma at baseline levels and in response to MDP treatment. This report reveals a new in vivo function of NOD2 within the eye yet importantly, distinguishes NOD2-dependent from NALP3-dependent inflammation, as ocular inflammation in mice occurred independently of IL-1beta.

Publication types

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

MeSH terms

  • Acetylmuramyl-Alanyl-Isoglutamine / toxicity
  • Adaptor Proteins, Signal Transducing / genetics*
  • Animals
  • Apoptosis Regulatory Proteins / genetics*
  • Caspase 1 / metabolism*
  • Disease Models, Animal
  • Eye / enzymology
  • Eye / physiopathology*
  • Eye Diseases / chemically induced
  • Eye Diseases / genetics
  • Eye Diseases / physiopathology
  • Female
  • Inflammation / chemically induced
  • Inflammation / genetics*
  • Inflammation / physiopathology*
  • Interleukin-1beta / biosynthesis
  • Interleukin-1beta / physiology*
  • Mice
  • Mice, Inbred BALB C
  • Nod2 Signaling Adaptor Protein / genetics*

Substances

  • Adaptor Proteins, Signal Transducing
  • Apoptosis Regulatory Proteins
  • Interleukin-1beta
  • NALP1 protein, mouse
  • Nod2 Signaling Adaptor Protein
  • Nod2 protein, mouse
  • Acetylmuramyl-Alanyl-Isoglutamine
  • Caspase 1