A Drosophila model system to assess the function of human monogenic podocyte mutations that cause nephrotic syndrome

Hum Mol Genet. 2017 Feb 15;26(4):768-780. doi: 10.1093/hmg/ddw428.

Abstract

Many genetic mutations have been identified as monogenic causes of nephrotic syndrome (NS), but important knowledge gaps exist in the roles of these genes in kidney cell biology and renal diseases. More animal models are needed to assess the functions of these genes in vivo, and to determine how they cause NS in a timely manner. Drosophila nephrocytes and human podocytes share striking similarities, but to what degree these known NS genes play conserved roles in nephrocytes remains unknown. Here we systematically studied 40 genes associated with NS, including 7 that have not previously been analysed for renal function in an animal model. We found that 85% of these genes are required for nephrocyte functions, suggesting that a majority of human genes known to be associated with NS play conserved roles in renal function from flies to humans. To investigate functional conservation in more detail, we focused on Cindr, the fly homolog of the human NS gene CD2AP. Silencing Cindr in nephrocytes led to dramatic nephrocyte functional impairment and shortened life span, as well as collapse of nephrocyte lacunar channels and effacement of nephrocyte slit diaphragms. These phenotypes could be rescued by expression of a wild-type human CD2AP gene, but not a mutant allele derived from a patient with CD2AP-associated NS. We conclude that the Drosophila nephrocyte can be used to elucidate clinically relevant molecular mechanisms underlying the pathogenesis of most monogenic forms of NS, and to efficiently generate personalized in vivo models of genetic renal diseases bearing patient-specific mutations.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics*
  • Animals
  • Cytoskeletal Proteins / genetics*
  • Disease Models, Animal
  • Drosophila Proteins / genetics*
  • Drosophila melanogaster / genetics
  • Gene Silencing
  • Humans
  • Kidney / physiopathology*
  • Microfilament Proteins / genetics*
  • Mutation
  • Nephrotic Syndrome / genetics*
  • Nephrotic Syndrome / physiopathology
  • Phenotype
  • Podocytes / metabolism
  • Podocytes / pathology

Substances

  • Adaptor Proteins, Signal Transducing
  • CD2-associated protein
  • Cindr protein, Drosophila
  • Cytoskeletal Proteins
  • Drosophila Proteins
  • Microfilament Proteins