Inpp5e suppresses polycystic kidney disease via inhibition of PI3K/Akt-dependent mTORC1 signaling

Hum Mol Genet. 2016 Jun 1;25(11):2295-2313. doi: 10.1093/hmg/ddw097. Epub 2016 Apr 7.

Abstract

Polycystic kidney disease (PKD) is a common cause of renal failure with few effective treatments. INPP5E is an inositol polyphosphate 5-phosphatase that dephosphorylates phosphoinositide 3-kinase (PI3K)-generated PI(3,4,5)P3 and is mutated in ciliopathy syndromes. Germline Inpp5e deletion is embryonically lethal, attributed to cilia stability defects, and is associated with polycystic kidneys. However, the molecular mechanisms responsible for PKD development upon Inpp5e loss remain unknown. Here, we show conditional inactivation of Inpp5e in mouse kidney epithelium results in severe PKD and renal failure, associated with a partial reduction in cilia number and hyperactivation of PI3K/Akt and downstream mammalian target of rapamycin complex 1 (mTORC1) signaling. Treatment with an mTORC1 inhibitor improved kidney morphology and function, but did not affect cilia number or length. Therefore, we identify Inpp5e as an essential inhibitor of the PI3K/Akt/mTORC1 signaling axis in renal epithelial cells, and demonstrate a critical role for Inpp5e-dependent mTORC1 regulation in PKD suppression.

MeSH terms

  • Animals
  • Ciliopathies / drug therapy
  • Ciliopathies / genetics
  • Ciliopathies / pathology
  • Disease Models, Animal
  • Elafin / genetics
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Epithelial Cells / pathology
  • Germ-Line Mutation
  • Humans
  • Kidney / drug effects
  • Kidney / metabolism*
  • Kidney / pathology
  • Mechanistic Target of Rapamycin Complex 1
  • Mice
  • Multiprotein Complexes / antagonists & inhibitors
  • Multiprotein Complexes / genetics*
  • Phosphoric Monoester Hydrolases / antagonists & inhibitors
  • Phosphoric Monoester Hydrolases / genetics*
  • Polycystic Kidney Diseases / drug therapy
  • Polycystic Kidney Diseases / genetics*
  • Polycystic Kidney Diseases / pathology
  • Proto-Oncogene Proteins c-akt / genetics
  • Sequence Deletion
  • Signal Transduction / drug effects
  • Sirolimus / administration & dosage
  • TOR Serine-Threonine Kinases / antagonists & inhibitors
  • TOR Serine-Threonine Kinases / genetics*

Substances

  • Elafin
  • Multiprotein Complexes
  • PI3 protein, human
  • Mechanistic Target of Rapamycin Complex 1
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases
  • Phosphoric Monoester Hydrolases
  • phosphoinositide 5-phosphatase
  • Sirolimus