Podocytopathy and Nephrotic Syndrome in Mice with Podocyte-Specific Deletion of the Asah1 Gene: Role of Ceramide Accumulation in Glomeruli

Am J Pathol. 2020 Jun;190(6):1211-1223. doi: 10.1016/j.ajpath.2020.02.008. Epub 2020 Mar 16.

Abstract

Lysosomal acid ceramidase (Ac) has been shown to be critical for ceramide hydrolysis and regulation of lysosome function and cellular homeostasis. In the present study, we generated a knockout mouse strain (Asah1fl/fl/PodoCre) with a podocyte-specific deletion of the α subunit (main catalytic subunit) of Ac. Although no significant morphologic changes in glomeruli were observed in these mice under light microscope, severe proteinuria and albuminuria were found in these podocyte-specific knockout mice compared with control genotype littermates. Transmission electron microscopic analysis showed that podocytes of the knockout mice had distinctive foot process effacement and microvillus formation. These functional and morphologic changes indicate the development of nephrotic syndrome in mice bearing the Asah1 podocyte-specific gene deletion. Ceramide accumulation determined by liquid chromatography-tandem mass spectrometry was demonstrated in isolated glomeruli of Asah1fl/fl/PodoCre mice compared with their littermates. By crossbreeding Asah1fl/fl/PodoCre mice with Smpd1-/- mice, we also produced a double knockout strain, Smpd1-/-/Asah1fl/fl/PodoCre, that also lacks Smpd1, the acid sphingomyelinase that hydrolyzes sphingomyelin to ceramide. These mice exhibited significantly lower levels of glomerular ceramide with decreased podocyte injury compared with Asah1fl/fl/PodoCre mice. These results strongly suggest that lysosomal Ac in podocytes is essential for the maintenance of the structural and functional integrity of podocytes.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Acid Ceramidase / genetics*
  • Acid Ceramidase / metabolism
  • Animals
  • Ceramides / metabolism*
  • Kidney Glomerulus / metabolism*
  • Kidney Glomerulus / pathology
  • Kidney Glomerulus / ultrastructure
  • Mice
  • Mice, Knockout
  • Microscopy, Electron, Transmission
  • Nephrotic Syndrome / genetics
  • Nephrotic Syndrome / metabolism*
  • Nephrotic Syndrome / pathology
  • Podocytes / metabolism*
  • Podocytes / pathology
  • Podocytes / ultrastructure

Substances

  • Ceramides
  • Acid Ceramidase
  • Asah1 protein, mouse