Unexpected kidney-restricted role for IL-17 receptor signaling in defense against systemic Candida albicans infection

JCI Insight. 2018 May 3;3(9):e98241. doi: 10.1172/jci.insight.98241.

Abstract

Kidney injury is a frequent outcome in patients with disseminated Candida albicans fungal infections. IL-17 receptor (IL-17R) signaling is critical for renal protection against disseminated candidiasis, but the identity and function of IL-17-responsive cells in mediating renal defense remains an active area of debate. Using BM chimeras, we found that IL-17R signaling is required only in nonhematopoietic cells for immunity to systemic C. albicans infection. Since renal tubular epithelial cells (RTEC) are highly responsive to IL-17 in vitro, we hypothesized that RTEC might be the dominant target of IL-17 activity in the infected kidney. We generated mice with a conditional deletion of IL-17 receptor A (Il17ra) in RTEC (Il17raΔRTEC). Strikingly, Il17raΔRTEC mice showed enhanced kidney damage and early mortality following systemic infection, very similar to Il17ra-/- animals. Increased susceptibility to candidiasis in Il17raΔRTEC mice was associated with diminished activation of the renal protective Kallikrein-kinin system (KKS), resulting in reduced apoptosis of kidney-resident cells during hyphal invasion. Moreover, protection was restored by treatment with bradykinin, the major end-product of KKS activation, which was mediated dominantly via bradykinin receptor b1. These data show that IL-17R signaling in RTEC is necessary and likely sufficient for IL-17-mediated renal defense against fatal systemic C. albicans infection.

Keywords: Cytokines; Fungal infections; Immunology; Infectious disease; Innate immunity.

Publication types

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

MeSH terms

  • Acute Kidney Injury / immunology*
  • Acute Kidney Injury / microbiology
  • Adoptive Transfer
  • Animals
  • Bradykinin / pharmacology
  • Candida albicans
  • Candidemia / immunology*
  • Epithelial Cells / metabolism
  • Female
  • Genetic Predisposition to Disease
  • Glomerular Basement Membrane / cytology
  • Glomerular Basement Membrane / metabolism*
  • Kallikrein-Kinin System / drug effects
  • Kallikrein-Kinin System / physiology
  • Kidney Tubules / metabolism
  • Male
  • Mice
  • Receptors, Antigen, T-Cell, alpha-beta / metabolism
  • Receptors, Antigen, T-Cell, gamma-delta / metabolism
  • Receptors, Interleukin-17 / genetics
  • Receptors, Interleukin-17 / immunology*
  • Receptors, Interleukin-17 / metabolism*
  • Signal Transduction / immunology*
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism

Substances

  • Il17ra protein, mouse
  • Receptors, Antigen, T-Cell, alpha-beta
  • Receptors, Antigen, T-Cell, gamma-delta
  • Receptors, Interleukin-17
  • Bradykinin