Induced pluripotent stem cell models of progranulin-deficient frontotemporal dementia uncover specific reversible neuronal defects

Cell Rep. 2012 Oct 25;2(4):789-98. doi: 10.1016/j.celrep.2012.09.007. Epub 2012 Oct 11.

Abstract

The pathogenic mechanisms of frontotemporal dementia (FTD) remain poorly understood. Here we generated multiple induced pluripotent stem cell lines from a control subject, a patient with sporadic FTD, and an FTD patient with a novel heterozygous GRN mutation (progranulin [PGRN] S116X). In neurons and microglia differentiated from PGRN S116X induced pluripotent stem cells, the levels of intracellular and secreted PGRN were reduced, establishing patient-specific cellular models of PGRN haploinsufficiency. Through a systematic screen of inducers of cellular stress, we found that PGRN S116X neurons, but not sporadic FTD neurons, exhibited increased sensitivity to staurosporine and other kinase inhibitors. Moreover, the serine/threonine kinase S6K2, a component of the phosphatidylinositol 3-kinase and mitogen-activated protein kinase pathways, was specifically downregulated in PGRN S116X neurons. Both increased sensitivity to kinase inhibitors and reduced S6K2 were rescued by PGRN expression. Our findings identify cell-autonomous, reversible defects in patient neurons with PGRN deficiency, and provide a compelling model for studying PGRN-dependent pathogenic mechanisms and testing potential therapies.

Publication types

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

MeSH terms

  • Cell Line
  • Down-Regulation
  • Frontotemporal Dementia / metabolism*
  • Frontotemporal Dementia / pathology
  • Haploinsufficiency
  • Heterozygote
  • Humans
  • Induced Pluripotent Stem Cells / cytology*
  • Induced Pluripotent Stem Cells / metabolism
  • Intercellular Signaling Peptides and Proteins / deficiency
  • Intercellular Signaling Peptides and Proteins / genetics
  • Intercellular Signaling Peptides and Proteins / metabolism*
  • Microglia / metabolism
  • Mitogen-Activated Protein Kinases / metabolism
  • Mutation
  • Neurons / drug effects
  • Neurons / metabolism*
  • Phosphatidylinositol 3-Kinase / metabolism
  • Progranulins
  • Protein Kinase Inhibitors / pharmacology
  • Ribosomal Protein S6 Kinases, 70-kDa / metabolism
  • Staurosporine / pharmacology

Substances

  • GRN protein, human
  • Intercellular Signaling Peptides and Proteins
  • Progranulins
  • Protein Kinase Inhibitors
  • Phosphatidylinositol 3-Kinase
  • Ribosomal Protein S6 Kinases, 70-kDa
  • Mitogen-Activated Protein Kinases
  • Staurosporine

Associated data

  • GEO/GSE40378