Angiogenin Mediates Cell-Autonomous Translational Control under Endoplasmic Reticulum Stress and Attenuates Kidney Injury

J Am Soc Nephrol. 2016 Mar;27(3):863-76. doi: 10.1681/ASN.2015020196. Epub 2015 Jul 20.

Abstract

Endoplasmic reticulum (ER) stress is involved in the pathophysiology of kidney disease and aging, but the molecular bases underlying the biologic outcomes on the evolution of renal disease remain mostly unknown. Angiogenin (ANG) is a ribonuclease that promotes cellular adaptation under stress but its contribution to ER stress signaling remains elusive. In this study, we investigated the ANG-mediated contribution to the signaling and biologic outcomes of ER stress in kidney injury. ANG expression was significantly higher in samples from injured human kidneys than in samples from normal human kidneys, and in mouse and rat kidneys, ANG expression was specifically induced under ER stress. In human renal epithelial cells, ER stress induced ANG expression in a manner dependent on the activity of transcription factor XBP1, and ANG promoted cellular adaptation to ER stress through induction of stress granules and inhibition of translation. Moreover, the severity of renal lesions induced by ER stress was dramatically greater in ANG knockout mice (Ang(-/-)) mice than in wild-type mice. These results indicate that ANG is a critical mediator of tissue adaptation to kidney injury and reveal a physiologically relevant ER stress-mediated adaptive translational control mechanism.

Keywords: acute renal failure; apoptosis; cell biology and structure; chronic allograft nephropathy; renal cell biology; renal epithelial cell.

Publication types

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

MeSH terms

  • Acute Kidney Injury / chemically induced
  • Acute Kidney Injury / pathology
  • Acute Kidney Injury / physiopathology*
  • Adaptation, Physiological
  • Animals
  • Apoptosis
  • Cells, Cultured
  • DNA-Binding Proteins / metabolism
  • Endoplasmic Reticulum Stress / physiology*
  • Endoribonucleases / genetics
  • Endoribonucleases / metabolism
  • Epithelial Cells
  • Gene Silencing
  • Humans
  • Kidney / pathology*
  • Kidney / physiopathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Poly(ADP-ribose) Polymerases / metabolism
  • Protein Biosynthesis / physiology*
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Regulatory Factor X Transcription Factors
  • Ribonuclease, Pancreatic / genetics
  • Ribonuclease, Pancreatic / metabolism*
  • Signal Transduction
  • Transcription Factors / metabolism
  • Transcription, Genetic
  • Tunicamycin
  • X-Box Binding Protein 1

Substances

  • DNA-Binding Proteins
  • Regulatory Factor X Transcription Factors
  • Transcription Factors
  • X-Box Binding Protein 1
  • XBP1 protein, human
  • Xbp1 protein, mouse
  • Xbp1 protein, rat
  • Tunicamycin
  • Poly(ADP-ribose) Polymerases
  • ERN1 protein, human
  • Protein Serine-Threonine Kinases
  • Endoribonucleases
  • angiogenin
  • Ribonuclease, Pancreatic