Soluble RARRES1 induces podocyte apoptosis to promote glomerular disease progression

J Clin Invest. 2020 Oct 1;130(10):5523-5535. doi: 10.1172/JCI140155.

Abstract

Using the Nephrotic Syndrome Study Network Consortium data set and other publicly available transcriptomic data sets, we identified retinoic acid receptor responder protein 1 (RARRES1) as a gene whose expression positively correlated with renal function decline in human glomerular disease. The glomerular expression of RARRES1, which is largely restricted to podocytes, increased in focal segmental glomerulosclerosis (FSGS) and diabetic kidney disease (DKD). TNF-α was a potent inducer of RARRES1 expression in cultured podocytes, and transcriptomic analysis showed the enrichment of cell death pathway genes with RARRES1 overexpression. The overexpression of RARRES1 indeed induced podocyte apoptosis in vitro. Notably, this effect was dependent on its cleavage in the extracellular domain, as the mutation of its cleavage site abolished the apoptotic effect. Mechanistically, the soluble RARRES1 was endocytosed and interacted with and inhibited RIO kinase 1 (RIOK1), resulting in p53 activation and podocyte apoptosis. In mice, podocyte-specific overexpression of RARRES1 resulted in marked glomerular injury and albuminuria, while the overexpression of RARRES1 cleavage mutant had no effect. Conversely, podocyte-specific knockdown of Rarres1 in mice ameliorated glomerular injury in the setting of adriamycin-induced nephropathy. Our study demonstrates an important role and the mechanism of RARRES1 in podocyte injury in glomerular disease.

Keywords: Apoptosis; Cell Biology; Chronic kidney disease; Nephrology; Signal transduction.

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
  • Apoptosis
  • Cells, Cultured
  • Diabetic Nephropathies / etiology*
  • Diabetic Nephropathies / metabolism
  • Diabetic Nephropathies / pathology
  • Disease Models, Animal
  • Disease Progression
  • Gene Knockdown Techniques
  • Glomerulosclerosis, Focal Segmental / etiology*
  • Glomerulosclerosis, Focal Segmental / metabolism
  • Glomerulosclerosis, Focal Segmental / pathology
  • Humans
  • Kidney Glomerulus / metabolism
  • Kidney Glomerulus / pathology
  • Membrane Proteins / antagonists & inhibitors
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mice
  • Mice, Transgenic
  • Mutant Proteins / genetics
  • Mutant Proteins / metabolism
  • Podocytes / drug effects
  • Podocytes / metabolism*
  • Podocytes / pathology
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Signal Transduction
  • Solubility
  • Tumor Necrosis Factor-alpha / metabolism
  • Tumor Necrosis Factor-alpha / pharmacology
  • Up-Regulation

Substances

  • Membrane Proteins
  • Mutant Proteins
  • RARRES1 protein, human
  • RNA, Messenger
  • Rarres1 protein, mouse
  • Tumor Necrosis Factor-alpha