Flagellin-induced expression of CXCL10 mediates direct fungal killing and recruitment of NK cells to the cornea in response to Candida albicans infection

Eur J Immunol. 2014 Sep;44(9):2667-79. doi: 10.1002/eji.201444490. Epub 2014 Aug 14.

Abstract

We previously showed that topical flagellin induces profound mucosal innate protection in the cornea against microbial infection, a response involving multiple genes and cell types. In this study, we used a Candida albicans (CA)-C57BL/6 mouse keratitis model to delineate the contribution of CXCL10- and CXCR3-expressing cells in flagellin-induced protection. Flagellin pretreatment markedly enhanced CXCL10 expression at 6 h post CA infection (hpi), but significantly dampened CXCL10 expression at 24 hpi. At the cellular level, CXCL10 was expressed in the epithelia at 6 hpi in flagellin-pretreated corneas, and concentrated at lesion sites 24 hpi. CXCR3-expressing cells were detected in great numbers at 24 hpi, organized within clusters at the lesion sites in CA-infected corneas. CXCL10 or CXCR3 neutralization increased keratitis severity and dampened flagellin-induced protection. CXCR3-positive cells were identified as NK cells, the depletion of which resulted in severe CA keratitis. Contributions from NK T-cells were excluded by finding no change in flagellin-induced protection in Rag1 KO mice. Recombinant CXCL10 inhibited CA growth in vitro and accelerated fungal clearance and inflammation resolution in vivo. Taken together, our data indicate that epithelium-expressed CXCL10 plays a critical role in fungal clearance and that CXCR3-expressing NK cells contribute to CA eradication in mouse corneas.

Keywords: Antimicrobial peptides; CXCL10; Fungal keratitis; Innate immunity; Natural killer cells.

Publication types

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

MeSH terms

  • Animals
  • Candida albicans / immunology*
  • Candidiasis / genetics
  • Candidiasis / immunology*
  • Candidiasis / therapy
  • Chemokine CXCL10 / genetics
  • Chemokine CXCL10 / immunology*
  • Cornea / immunology*
  • Cornea / microbiology
  • Cornea / pathology
  • Flagellin* / chemistry
  • Flagellin* / immunology
  • Flagellin* / isolation & purification
  • Flagellin* / pharmacology
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / genetics
  • Gene Expression Regulation / immunology
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / immunology
  • Immunity, Cellular*
  • Immunity, Mucosal / drug effects
  • Immunity, Mucosal / genetics
  • Immunity, Mucosal / immunology
  • Keratitis / genetics
  • Keratitis / immunology*
  • Keratitis / microbiology
  • Keratitis / pathology
  • Keratitis / therapy
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / pathology
  • Mice
  • Mice, Knockout
  • Pseudomonas aeruginosa / chemistry*
  • Receptors, CXCR3 / genetics
  • Receptors, CXCR3 / immunology

Substances

  • Chemokine CXCL10
  • Cxcl10 protein, mouse
  • Cxcr3 protein, mouse
  • Homeodomain Proteins
  • Receptors, CXCR3
  • Flagellin
  • RAG-1 protein