Distinct roles for Dectin-1 and TLR4 in the pathogenesis of Aspergillus fumigatus keratitis

PLoS Pathog. 2010 Jul 1;6(7):e1000976. doi: 10.1371/journal.ppat.1000976.

Abstract

Aspergillus species are a major worldwide cause of corneal ulcers, resulting in visual impairment and blindness in immunocompetent individuals. To enhance our understanding of the pathogenesis of Aspergillus keratitis, we developed a murine model in which red fluorescent protein (RFP)-expressing A. fumigatus (Af293.1RFP) conidia are injected into the corneal stroma, and disease progression and fungal survival are tracked over time. Using Mafia mice in which c-fms expressing macrophages and dendritic cells can be induced to undergo apoptosis, we demonstrated that the presence of resident corneal macrophages is essential for production of IL-1beta and CXCL1/KC, and for recruitment of neutrophils and mononuclear cells into the corneal stroma. We found that beta-glucan was highly expressed on germinating conidia and hyphae in the cornea stroma, and that both Dectin-1 and phospho-Syk were up-regulated in infected corneas. Additionally, we show that infected Dectin-1(-/-) corneas have impaired IL-1beta and CXCL1/KC production, resulting in diminished cellular infiltration and fungal clearance compared with control mice, especially during infection with clinical isolates expressing high beta-glucan. In contrast to Dectin 1(-/-) mice, cellular infiltration into infected TLR2(-/-), TLR4(-/-), and MD-2(-/-) mice corneas was unimpaired, indicating no role for these receptors in cell recruitment; however, fungal killing was significantly reduced in TLR4(-/-) mice, but not TLR2(-/-) or MD-2(-/-) mice. We also found that TRIF(-/-) and TIRAP(-/-) mice exhibited no fungal-killing defects, but that MyD88(-/-) and IL-1R1(-/-) mice were unable to regulate fungal growth. In conclusion, these data are consistent with a model in which beta-glucan on A.fumigatus germinating conidia activates Dectin-1 on corneal macrophages to produce IL-1beta, and CXCL1, which together with IL-1R1/MyD88-dependent activation, results in recruitment of neutrophils to the corneal stroma and TLR4-dependent fungal killing.

Publication types

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

MeSH terms

  • Animals
  • Aspergillus fumigatus / growth & development
  • Aspergillus fumigatus / pathogenicity*
  • Chemokine CXCL1 / biosynthesis
  • Corneal Stroma / microbiology
  • Corneal Stroma / pathology
  • Interleukin-1beta / biosynthesis
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Keratitis / microbiology*
  • Lectins, C-Type
  • Macrophages / physiology
  • Membrane Proteins / physiology*
  • Mice
  • Nerve Tissue Proteins / physiology*
  • Protein-Tyrosine Kinases / metabolism
  • Syk Kinase
  • Toll-Like Receptor 4 / physiology*
  • beta-Glucans / metabolism

Substances

  • Chemokine CXCL1
  • Cxcl1 protein, mouse
  • Interleukin-1beta
  • Intracellular Signaling Peptides and Proteins
  • Lectins, C-Type
  • Membrane Proteins
  • Nerve Tissue Proteins
  • Toll-Like Receptor 4
  • beta-Glucans
  • dectin 1
  • Protein-Tyrosine Kinases
  • Syk Kinase
  • Syk protein, mouse