The RNA binding protein Arid5a drives IL-17-dependent autoantibody-induced glomerulonephritis

J Exp Med. 2024 Sep 2;221(9):e20240656. doi: 10.1084/jem.20240656. Epub 2024 Jul 26.

Abstract

Autoantibody-mediated glomerulonephritis (AGN) arises from dysregulated renal inflammation, with urgent need for improved treatments. IL-17 is implicated in AGN and drives pathology in a kidney-intrinsic manner via renal tubular epithelial cells (RTECs). Nonetheless, downstream signaling mechanisms provoking kidney pathology are poorly understood. A noncanonical RNA binding protein (RBP), Arid5a, was upregulated in human and mouse AGN. Arid5a-/- mice were refractory to AGN, with attenuated myeloid infiltration and impaired expression of IL-17-dependent cytokines and transcription factors (C/EBPβ, C/EBPδ). Transcriptome-wide RIP-Seq revealed that Arid5a inducibly interacts with conventional IL-17 target mRNAs, including CEBPB and CEBPD. Unexpectedly, many Arid5a RNA targets corresponded to translational regulation and RNA processing pathways, including rRNAs. Indeed, global protein synthesis was repressed in Arid5a-deficient cells, and C/EBPs were controlled at the level of protein rather than RNA accumulation. IL-17 prompted Arid5a nuclear export and association with 18S rRNA, a 40S ribosome constituent. Accordingly, IL-17-dependent renal autoimmunity is driven by Arid5a at the level of ribosome interactions and translation.

Publication types

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

MeSH terms

  • Animals
  • Autoantibodies* / immunology
  • CCAAT-Enhancer-Binding Protein-beta / genetics
  • CCAAT-Enhancer-Binding Protein-beta / metabolism
  • CCAAT-Enhancer-Binding Protein-delta / genetics
  • CCAAT-Enhancer-Binding Protein-delta / metabolism
  • DNA-Binding Proteins* / genetics
  • DNA-Binding Proteins* / metabolism
  • Glomerulonephritis* / genetics
  • Glomerulonephritis* / immunology
  • Glomerulonephritis* / metabolism
  • Glomerulonephritis* / pathology
  • Humans
  • Interleukin-17* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / immunology
  • RNA-Binding Proteins / metabolism
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism

Substances

  • Interleukin-17
  • Transcription Factors
  • Autoantibodies
  • Arid5a protein, mouse
  • DNA-Binding Proteins
  • CCAAT-Enhancer-Binding Protein-beta
  • CCAAT-Enhancer-Binding Protein-delta
  • ARID5A protein, human
  • Cebpd protein, mouse
  • RNA-Binding Proteins
  • Cebpb protein, mouse
  • RNA, Messenger