IL-17C/IL-17 Receptor E Signaling in CD4+ T Cells Promotes TH17 Cell-Driven Glomerular Inflammation

J Am Soc Nephrol. 2018 Apr;29(4):1210-1222. doi: 10.1681/ASN.2017090949. Epub 2018 Feb 26.

Abstract

The IL-17 cytokine family and the cognate receptors thereof have a unique role in organ-specific autoimmunity. Most studies have focused on the founding member of the IL-17 family, IL-17A, as the central mediator of diseases. Indeed, although pathogenic functions have been ascribed to IL-17A and IL-17F in the context of immune-mediated glomerular diseases, the specific functions of the other IL-17 family members in immunity and inflammatory kidney diseases is largely unknown. Here, we report that compared with healthy controls, patients with acute Anti-neutrophil cytoplasmatic antibody (ANCA)-associated crescentic glomerulonephritis (GN) had significantly elevated serum levels of IL-17C (but not IL-17A, F, or E). In mouse models of crescentic GN (nephrotoxic nephritis) and pristane-induced lupus nephritis, deficiency in IL-17C significantly ameliorated the course of GN in terms of renal tissue injury and kidney function. Deficiency of the unique IL-17C receptor IL-17 receptor E (IL-17RE) provided similar protection against crescentic GN. These protective effects associated with a reduced TH17 response. Bone marrow transplantation experiments revealed that IL-17C is produced by tissue-resident cells, but not by lymphocytes. Finally, IL-17RE was highly expressed by CD4+ TH17 cells, and loss of this expression prevented the TH17 responses and subsequent tissue injury in crescentic GN. Our findings indicate that IL-17C promotes TH17 cell responses and immune-mediated kidney disease via IL-17RE expressed on CD4+ TH17 cells. Targeting the IL-17C/IL-17RE pathway may present an intriguing therapeutic strategy for TH17-induced autoimmune disorders.

Keywords: ANCA; Th17 response; cytokines; glomerulonephritis; immunology; lupus nephritis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Antineutrophil Cytoplasmic / immunology
  • Autoimmune Diseases / blood
  • Autoimmune Diseases / immunology*
  • Autoimmune Diseases / pathology
  • Autoimmune Diseases / prevention & control
  • CD4-Positive T-Lymphocytes / immunology*
  • Glomerulonephritis / blood
  • Glomerulonephritis / immunology*
  • Glomerulonephritis / pathology
  • Glomerulonephritis / prevention & control
  • Humans
  • Interleukin-17 / biosynthesis
  • Interleukin-17 / blood*
  • Interleukin-17 / deficiency
  • Interleukin-17 / genetics
  • Interleukin-17 / physiology*
  • Kidney / immunology
  • Kidney / pathology
  • Lupus Nephritis / chemically induced
  • Lupus Nephritis / immunology
  • Lupus Nephritis / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Molecular Targeted Therapy
  • RNA, Messenger / biosynthesis
  • Radiation Chimera
  • Receptors, Interleukin-17 / biosynthesis
  • Receptors, Interleukin-17 / deficiency
  • Receptors, Interleukin-17 / genetics
  • Receptors, Interleukin-17 / physiology*
  • Terpenes / toxicity
  • Th17 Cells / immunology*
  • Up-Regulation

Substances

  • Antibodies, Antineutrophil Cytoplasmic
  • IL17C protein, human
  • Il17a protein, mouse
  • Il17c protein, mouse
  • Interleukin-17
  • RNA, Messenger
  • Receptors, Interleukin-17
  • Terpenes
  • pristane