Endothelial Epas1 Deficiency Is Sufficient To Promote Parietal Epithelial Cell Activation and FSGS in Experimental Hypertension

J Am Soc Nephrol. 2017 Dec;28(12):3563-3578. doi: 10.1681/ASN.2016090960. Epub 2017 Sep 19.

Abstract

FSGS, the most common primary glomerular disorder causing ESRD, is a complex disease that is only partially understood. Progressive sclerosis is a hallmark of FSGS, and genetic tracing studies have shown that parietal epithelial cells participate in the formation of sclerotic lesions. The loss of podocytes triggers a focal activation of parietal epithelial cells, which subsequently form cellular adhesions with the capillary tuft. However, in the absence of intrinsic podocyte alterations, the origin of the pathogenic signal that triggers parietal epithelial cell recruitment remains elusive. In this study, investigation of the role of the endothelial PAS domain-containing protein 1 (EPAS1), a regulatory α subunit of the hypoxia-inducible factor complex, during angiotensin II-induced hypertensive nephropathy provided novel insights into FSGS pathogenesis in the absence of a primary podocyte abnormality. We infused angiotensin II into endothelial-selective Epas1 knockout mice and their littermate controls. Although the groups presented with identical high BP, endothelial-specific Epas1 gene deletion accentuated albuminuria with severe podocyte lesions and recruitment of pathogenic parietal glomerular epithelial cells. These lesions and dysfunction of the glomerular filtration barrier were associated with FSGS in endothelial Epas1-deficient mice only. These results indicate that endothelial EPAS1 has a global protective role during glomerular hypertensive injuries without influencing the hypertensive effect of angiotensin II. Furthermore, these findings provide proof of principle that endothelial-derived signaling can trigger FSGS and illustrate the potential importance of the EPAS1 endothelial transcription factor in secondary FSGS.

Keywords: Pathophysiology of Renal Disease and Progression; endothelial cells; focal segmental glomerulosclerosis; glomerular endothelial cells; glomerular epithelial cells; hypertension.

MeSH terms

  • Albumins / analysis
  • Angiotensin II / metabolism
  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / deficiency
  • Basic Helix-Loop-Helix Transcription Factors / genetics*
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Blood Pressure
  • Cell Differentiation
  • Crosses, Genetic
  • Disease Progression
  • Epithelial Cells / cytology*
  • Epithelial Cells / metabolism
  • Gene Deletion
  • Gene Expression Regulation*
  • Glomerulosclerosis, Focal Segmental / metabolism*
  • Hypertension / metabolism*
  • Kidney Glomerulus / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Podocytes / metabolism
  • Telemetry

Substances

  • Albumins
  • Basic Helix-Loop-Helix Transcription Factors
  • Angiotensin II
  • endothelial PAS domain-containing protein 1