Distinct roles for Nod2 protein and autocrine interleukin-1beta in muramyl dipeptide-induced mitogen-activated protein kinase activation and cytokine secretion in human macrophages

J Biol Chem. 2011 Jul 29;286(30):26440-9. doi: 10.1074/jbc.M111.237495. Epub 2011 Jun 9.

Abstract

Elucidating factors regulating Crohn's disease-associated nucleotide-binding oligomerization domain 2 (Nod2) responses is critical to understanding the mechanisms of intestinal immune homeostasis. Stimulation of primary monocyte-derived macrophages by muramyl dipeptide (MDP), a component of bacterial peptidoglycan and specific Nod2 ligand, produces cytokines, including IL-1β. We found that IL-1β blockade profoundly inhibits MDP-induced cytokine production in human monocyte-derived macrophages, demonstrating a key role for IL-1β autocrine secretion in Nod2-mediated responses. Importantly, although MAPK activation has previously been attributed directly to Nod2 signaling, we determined that the IL-1β autocrine loop is responsible for the majority of MDP-induced MAPK activation. Because the critical effects of IL-1β autocrine secretion on MAPK activation are observed as early as 10 min after Nod2 stimulation, we hypothesized that secretion of IL-1β from preexisting intracellular pro-IL-1β stores is necessary for optimal MDP-mediated cytokine induction. Consistently, we detected IL-1β secretion within 10 min of MDP treatment. Moreover, caspase-1 inhibition significantly attenuates MDP-mediated early MAPK activation. Importantly, selective JNK/p38 activation is sufficient to rescue the decreased cytokine secretion during Nod2 stimulation in the absence of autocrine IL-1β. Finally, we found that the IL-1β autocrine loop significantly enhances responses by a broad range of pattern recognition receptors. Taken together, MDP stimulation activates Nod2 to process and release preexisting pro-IL-1β stores in a caspase-1-dependent fashion; this secreted IL-1β, in turn, contributes to the majority of MDP-initiated MAPK activation and leads to subsequent cytokine secretion. Our findings clarify mechanisms of IL-1β contributions to Nod2 responses and elucidate the dominant role of IL-1β in MDP-initiated MAPK and cytokine secretion.

Publication types

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

MeSH terms

  • Acetylmuramyl-Alanyl-Isoglutamine / pharmacology*
  • Adjuvants, Immunologic / pharmacology*
  • Autocrine Communication / drug effects
  • Autocrine Communication / physiology*
  • Caspase 1 / genetics
  • Caspase 1 / metabolism
  • Caspase Inhibitors
  • Cell Line
  • Enzyme Activation / drug effects
  • Enzyme Activation / physiology
  • Humans
  • Interleukin-1beta / drug effects
  • Interleukin-1beta / genetics
  • Interleukin-1beta / metabolism*
  • Interleukin-1beta / physiology*
  • MAP Kinase Kinase 4 / genetics
  • MAP Kinase Kinase 4 / metabolism*
  • Macrophages / metabolism*
  • Nod2 Signaling Adaptor Protein / genetics
  • Nod2 Signaling Adaptor Protein / metabolism*
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • p38 Mitogen-Activated Protein Kinases / genetics
  • p38 Mitogen-Activated Protein Kinases / metabolism*

Substances

  • Adjuvants, Immunologic
  • Caspase Inhibitors
  • Interleukin-1beta
  • NOD2 protein, human
  • Nod2 Signaling Adaptor Protein
  • Acetylmuramyl-Alanyl-Isoglutamine
  • p38 Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase 4
  • Caspase 1