Von Hippel-Lindau Acts as a Metabolic Switch Controlling Nephron Progenitor Differentiation

J Am Soc Nephrol. 2019 Jul;30(7):1192-1205. doi: 10.1681/ASN.2018111170. Epub 2019 May 29.

Abstract

Background: Nephron progenitors, the cell population that give rise to the functional unit of the kidney, are metabolically active and self-renew under glycolytic conditions. A switch from glycolysis to mitochondrial respiration drives these cells toward differentiation, but the mechanisms that control this switch are poorly defined. Studies have demonstrated that kidney formation is highly dependent on oxygen concentration, which is largely regulated by von Hippel-Lindau (VHL; a protein component of a ubiquitin ligase complex) and hypoxia-inducible factors (a family of transcription factors activated by hypoxia).

Methods: To explore VHL as a regulator defining nephron progenitor self-renewal versus differentiation, we bred Six2-TGCtg mice with VHLlox/lox mice to generate mice with a conditional deletion of VHL from Six2+ nephron progenitors. We used histologic, immunofluorescence, RNA sequencing, and metabolic assays to characterize kidneys from these mice and controls during development and up to postnatal day 21.

Results: By embryonic day 15.5, kidneys of nephron progenitor cell-specific VHL knockout mice begin to exhibit reduced maturation of nephron progenitors. Compared with controls, VHL knockout kidneys are smaller and developmentally delayed by postnatal day 1, and have about half the number of glomeruli at postnatal day 21. VHL knockout nephron progenitors also exhibit persistent Six2 and Wt1 expression, as well as decreased mitochondrial respiration and prolonged reliance on glycolysis.

Conclusions: Our findings identify a novel role for VHL in mediating nephron progenitor differentiation through metabolic regulation, and suggest that VHL is required for normal kidney development.

Keywords: Cellular differentiation; Glycolysis; HIF-1α metabolism; Nephron progenitors; VHL.

Publication types

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

MeSH terms

  • Animals
  • Cell Differentiation
  • Gene Expression Regulation
  • Glycolysis
  • Homeodomain Proteins / physiology
  • Mice
  • Mitochondria / metabolism
  • Nephrons / cytology*
  • Stem Cells / cytology*
  • Transcription Factors / physiology
  • Von Hippel-Lindau Tumor Suppressor Protein / physiology*

Substances

  • Homeodomain Proteins
  • Six2 protein, mouse
  • Transcription Factors
  • Von Hippel-Lindau Tumor Suppressor Protein
  • VHL protein, mouse