Early maturation and distinct tau pathology in induced pluripotent stem cell-derived neurons from patients with MAPT mutations

Brain. 2015 Nov;138(Pt 11):3345-59. doi: 10.1093/brain/awv222. Epub 2015 Jul 27.

Abstract

Tauopathies, such as Alzheimer's disease, some cases of frontotemporal dementia, corticobasal degeneration and progressive supranuclear palsy, are characterized by aggregates of the microtubule-associated protein tau, which are linked to neuronal death and disease development and can be caused by mutations in the MAPT gene. Six tau isoforms are present in the adult human brain and they differ by the presence of 3(3R) or 4(4R) C-terminal repeats. Only the shortest 3R isoform is present in foetal brain. MAPT mutations found in human disease affect tau binding to microtubules or the 3R:4R isoform ratio by altering exon 10 splicing. We have differentiated neurons from induced pluripotent stem cells derived from fibroblasts of controls and patients with N279K and P301L MAPT mutations. Induced pluripotent stem cell-derived neurons recapitulate developmental tau expression, showing the adult brain tau isoforms after several months in culture. Both N279K and P301L neurons exhibit earlier electrophysiological maturation and altered mitochondrial transport compared to controls. Specifically, the N279K neurons show abnormally premature developmental 4R tau expression, including changes in the 3R:4R isoform ratio and AT100-hyperphosphorylated tau aggregates, while P301L neurons are characterized by contorted processes with varicosity-like structures, some containing both alpha-synuclein and 4R tau. The previously unreported faster maturation of MAPT mutant human neurons, the developmental expression of 4R tau and the morphological alterations may contribute to disease development.

Keywords: FTDP-17T; IPSC-derived neurons; MAPT gene mutations; microtubule-associated protein tau; neurofibrillary tangles.

Publication types

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

MeSH terms

  • Adult
  • Aged
  • Case-Control Studies
  • Cell Line
  • Cells, Cultured
  • Female
  • Gene Expression Regulation, Developmental*
  • Humans
  • Immunohistochemistry
  • Induced Pluripotent Stem Cells / cytology
  • Induced Pluripotent Stem Cells / metabolism*
  • Induced Pluripotent Stem Cells / pathology
  • Infant, Newborn
  • Male
  • Microscopy, Confocal
  • Microtubules / metabolism
  • Middle Aged
  • Neurons / cytology
  • Neurons / metabolism*
  • Neurons / pathology
  • Patch-Clamp Techniques
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • RNA, Messenger / metabolism*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Tauopathies
  • alpha-Synuclein / metabolism
  • tau Proteins / genetics*
  • tau Proteins / metabolism

Substances

  • MAPT protein, human
  • Protein Isoforms
  • RNA, Messenger
  • alpha-Synuclein
  • tau Proteins