Familial Alzheimer's disease-associated presenilin-1 alters cerebellar activity and calcium homeostasis

J Clin Invest. 2014 Apr;124(4):1552-67. doi: 10.1172/JCI66407. Epub 2014 Feb 24.

Abstract

Familial Alzheimer's disease (FAD) is characterized by autosomal dominant heritability and early disease onset. Mutations in the gene encoding presenilin-1 (PS1) are found in approximately 80% of cases of FAD, with some of these patients presenting cerebellar damage with amyloid plaques and ataxia with unclear pathophysiology. A Colombian kindred carrying the PS1-E280A mutation is the largest known cohort of PS1-FAD patients. Here, we investigated PS1-E280A-associated cerebellar dysfunction and found that it occurs early in PS1-E208A carriers, while cerebellar signs are highly prevalent in patients with dementia. Postmortem analysis of cerebella of PS1-E280A carrier revealed greater Purkinje cell (PC) loss and more abnormal mitochondria compared with controls. In PS1-E280A tissue, ER/mitochondria tethering was impaired, Ca2+ channels IP3Rs and CACNA1A were downregulated, and Ca2+-dependent mitochondrial transport proteins MIRO1 and KIF5C were reduced. Accordingly, expression of PS1-E280A in a neuronal cell line altered ER/mitochondria tethering and transport compared with that in cells expressing wild-type PS1. In a murine model of PS1-FAD, animals exhibited mild ataxia and reduced PC simple spike activity prior to cerebellar β-amyloid deposition. Our data suggest that impaired calcium homeostasis and mitochondrial dysfunction in PS1-FAD PCs reduces their activity and contributes to motor coordination deficits prior to Aβ aggregation and dementia. We propose that PS1-E280A affects both Ca2+ homeostasis and Aβ precursor processing, leading to FAD and neurodegeneration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Alzheimer Disease / genetics*
  • Alzheimer Disease / metabolism*
  • Alzheimer Disease / pathology
  • Amino Acid Substitution
  • Amyloid beta-Protein Precursor / metabolism
  • Animals
  • Calcium / metabolism*
  • Case-Control Studies
  • Cell Line
  • Cerebellum / metabolism*
  • Cerebellum / pathology
  • Disease Models, Animal
  • Endoplasmic Reticulum / pathology
  • Female
  • Genes, Dominant
  • Heterozygote
  • Homeostasis
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Mutant Strains
  • Mice, Transgenic
  • Middle Aged
  • Mitochondria / metabolism
  • Mitochondria / pathology
  • Models, Neurological
  • Mutation, Missense*
  • Presenilin-1 / genetics*
  • Presenilin-1 / metabolism*
  • Purkinje Cells / metabolism

Substances

  • Amyloid beta-Protein Precursor
  • PSEN1 protein, human
  • Presenilin-1
  • presenilin 1, mouse
  • Calcium