Cyclin G1 and TASCC regulate kidney epithelial cell G2-M arrest and fibrotic maladaptive repair

Sci Transl Med. 2019 Jan 23;11(476):eaav4754. doi: 10.1126/scitranslmed.aav4754.

Abstract

Fibrosis contributes to the progression of chronic kidney disease (CKD). Severe acute kidney injury can lead to CKD through proximal tubular cell (PTC) cycle arrest in the G2-M phase, with secretion of profibrotic factors. Here, we show that epithelial cells in the G2-M phase form target of rapamycin (TOR)-autophagy spatial coupling compartments (TASCCs), which promote profibrotic secretion similar to the senescence-associated secretory phenotype. Cyclin G1 (CG1), an atypical cyclin, promoted G2-M arrest in PTCs and up-regulated TASCC formation. PTC TASCC formation was also present in humans with CKD. Prevention of TASCC formation in cultured PTCs blocked secretion of profibrotic factors. PTC-specific knockout of a key TASCC component reduced the rate of kidney fibrosis progression in mice with CKD. CG1 induction and TASCC formation also occur in liver fibrosis. Deletion of CG1 reduced G2-M phase cells and TASCC formation in vivo. This study provides mechanistic evidence supporting how profibrotic G2-M arrest is induced in kidney injury and how G2-M-arrested PTCs promote fibrosis, identifying new therapeutic targets to mitigate kidney fibrosis.

Publication types

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

MeSH terms

  • Animals
  • Autophagy*
  • Cell Compartmentation*
  • Cell Cycle Checkpoints*
  • Cell Dedifferentiation
  • Cyclin G1 / metabolism*
  • Disease Models, Animal
  • Disease Progression
  • Epithelial Cells / metabolism
  • Epithelial Cells / pathology*
  • Fibrosis
  • Humans
  • Kidney / pathology*
  • Kidney Tubules, Proximal / pathology
  • LLC-PK1 Cells
  • Male
  • Mice
  • Renal Insufficiency, Chronic / pathology
  • Swine
  • TOR Serine-Threonine Kinases / metabolism*
  • Wound Healing*

Substances

  • Cyclin G1
  • TOR Serine-Threonine Kinases