CARD9 mediates Dectin-1-induced ERK activation by linking Ras-GRF1 to H-Ras for antifungal immunity

J Exp Med. 2014 Oct 20;211(11):2307-21. doi: 10.1084/jem.20132349. Epub 2014 Sep 29.

Abstract

Dectin-1 functions as a pattern recognition receptor for sensing fungal infection. It has been well-established that Dectin-1 induces innate immune responses through caspase recruitment domain-containing protein 9 (CARD9)-mediated NF-κB activation. In this study, we find that CARD9 is dispensable for NF-κB activation induced by Dectin-1 ligands, such as curdlan or Candida albicans yeast. In contrast, we find that CARD9 regulates H-Ras activation by linking Ras-GRF1 to H-Ras, which mediates Dectin-1-induced extracellular signal-regulated protein kinase (ERK) activation and proinflammatory responses when stimulated by their ligands. Mechanistically, Dectin-1 engagement initiates spleen tyrosine kinase (Syk)-dependent Ras-GRF1 phosphorylation, and the phosphorylated Ras-GRF1 recruits and activates H-Ras through forming a complex with CARD9, which leads to activation of ERK downstream. Finally, we show that inhibiting ERK activation significantly accelerates the death of C. albicans-infected mice, and this inhibitory effect is dependent on CARD9. Together, our studies reveal a molecular mechanism by which Dectin-1 induces H-Ras activation that leads to ERK activation for host innate immune responses against fungal infection.

Publication types

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

MeSH terms

  • Animals
  • CARD Signaling Adaptor Proteins / genetics
  • CARD Signaling Adaptor Proteins / metabolism*
  • Candida albicans / drug effects
  • Candida albicans / genetics
  • Candida albicans / immunology
  • Candidiasis / genetics
  • Candidiasis / immunology
  • Candidiasis / metabolism
  • Candidiasis / mortality
  • Enzyme Activation / drug effects
  • Extracellular Signal-Regulated MAP Kinases / metabolism*
  • Female
  • Fungi / drug effects
  • Fungi / genetics
  • Fungi / immunology*
  • Humans
  • Immunity, Innate
  • Lectins, C-Type / genetics
  • Lectins, C-Type / metabolism*
  • Mice
  • Mice, Knockout
  • Multiprotein Complexes / metabolism
  • Mycoses / genetics
  • Mycoses / immunology*
  • Mycoses / metabolism*
  • Mycoses / mortality
  • NF-kappa B / metabolism
  • Protein Binding
  • Signal Transduction
  • beta-Glucans / pharmacology
  • ras Proteins / genetics
  • ras Proteins / metabolism*
  • ras-GRF1 / metabolism*

Substances

  • CARD Signaling Adaptor Proteins
  • CARD9 protein, human
  • Lectins, C-Type
  • Multiprotein Complexes
  • NF-kappa B
  • beta-Glucans
  • dectin 1
  • ras-GRF1
  • Extracellular Signal-Regulated MAP Kinases
  • ras Proteins