Tau-Mediated Disruption of the Spliceosome Triggers Cryptic RNA Splicing and Neurodegeneration in Alzheimer's Disease

Cell Rep. 2019 Oct 8;29(2):301-316.e10. doi: 10.1016/j.celrep.2019.08.104.

Abstract

In Alzheimer's disease (AD), spliceosomal proteins with critical roles in RNA processing aberrantly aggregate and mislocalize to Tau neurofibrillary tangles. We test the hypothesis that Tau-spliceosome interactions disrupt pre-mRNA splicing in AD. In human postmortem brain with AD pathology, Tau coimmunoprecipitates with spliceosomal components. In Drosophila, pan-neuronal Tau expression triggers reductions in multiple core and U1-specific spliceosomal proteins, and genetic disruption of these factors, including SmB, U1-70K, and U1A, enhances Tau-mediated neurodegeneration. We further show that loss of function in SmB, encoding a core spliceosomal protein, causes decreased survival, progressive locomotor impairment, and neuronal loss, independent of Tau toxicity. Lastly, RNA sequencing reveals a similar profile of mRNA splicing errors in SmB mutant and Tau transgenic flies, including intron retention and non-annotated cryptic splice junctions. In human brains, we confirm cryptic splicing errors in association with neurofibrillary tangle burden. Our results implicate spliceosome disruption and the resulting transcriptome perturbation in Tau-mediated neurodegeneration in AD.

Keywords: Alzheimer’s disease; RNA splicing; SmB; Tau; U1-70K; cryptic splicing; intron retention; neurodegeneration; neurofibrillary tangles; spliceosome.

Publication types

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

MeSH terms

  • Alzheimer Disease / complications
  • Alzheimer Disease / genetics*
  • Alzheimer Disease / pathology
  • Alzheimer Disease / physiopathology
  • Animals
  • Brain / metabolism
  • Brain / pathology
  • Brain / physiopathology
  • Drosophila / metabolism*
  • Drosophila Proteins / metabolism
  • Humans
  • Models, Biological
  • Motor Activity
  • Nerve Degeneration / complications
  • Nerve Degeneration / genetics*
  • Nerve Degeneration / physiopathology
  • RNA Splicing / genetics*
  • Ribonucleoproteins, Small Nuclear / metabolism
  • Spliceosomes / metabolism*
  • tau Proteins / metabolism*

Substances

  • Drosophila Proteins
  • Ribonucleoproteins, Small Nuclear
  • tau Proteins