Receptor-mediated mitophagy regulates EPO production and protects against renal anemia

Elife. 2021 May 4:10:e64480. doi: 10.7554/eLife.64480.

Abstract

Erythropoietin (EPO) drives erythropoiesis and is secreted mainly by the kidney upon hypoxic or anemic stress. The paucity of EPO production in renal EPO-producing cells (REPs) causes renal anemia, one of the most common complications of chronic nephropathies. Although mitochondrial dysfunction is commonly observed in several renal and hematopoietic disorders, the mechanism by which mitochondrial quality control impacts renal anemia remains elusive. In this study, we showed that FUNDC1, a mitophagy receptor, plays a critical role in EPO-driven erythropoiesis induced by stresses. Mechanistically, EPO production is impaired in REPs in Fundc1-/- mice upon stresses, and the impairment is caused by the accumulation of damaged mitochondria, which consequently leads to the elevation of the reactive oxygen species (ROS) level and triggers inflammatory responses by up-regulating proinflammatory cytokines. These inflammatory factors promote the myofibroblastic transformation of REPs, resulting in the reduction of EPO production. We therefore provide a link between aberrant mitophagy and deficient EPO generation in renal anemia. Our results also suggest that the mitochondrial quality control safeguards REPs under stresses, which may serve as a potential therapeutic strategy for the treatment of renal anemia.

Keywords: Fundc1; cell biology; inflammation; mitophagy; mouse; renal EPO-producing cells; stress erythropoiesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anemia / prevention & control*
  • Animals
  • Erythropoiesis / genetics
  • Erythropoiesis / physiology
  • Erythropoietin / analysis
  • Erythropoietin / genetics
  • Erythropoietin / metabolism*
  • Gene Expression Regulation*
  • Kidney Diseases / classification
  • Kidney Diseases / prevention & control*
  • Membrane Proteins / genetics*
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mitochondrial Proteins / genetics*
  • Mitochondrial Proteins / metabolism
  • Mitophagy / genetics*
  • Mitophagy / physiology
  • Reactive Oxygen Species

Substances

  • Epo protein, mouse
  • FUNDC1 protein, mouse
  • Membrane Proteins
  • Mitochondrial Proteins
  • Reactive Oxygen Species
  • Erythropoietin

Associated data

  • GEO/GSE158361

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.