Dissecting the Causal Mechanism of X-Linked Dystonia-Parkinsonism by Integrating Genome and Transcriptome Assembly

Cell. 2018 Feb 22;172(5):897-909.e21. doi: 10.1016/j.cell.2018.02.011.

Abstract

X-linked Dystonia-Parkinsonism (XDP) is a Mendelian neurodegenerative disease that is endemic to the Philippines and is associated with a founder haplotype. We integrated multiple genome and transcriptome assembly technologies to narrow the causal mutation to the TAF1 locus, which included a SINE-VNTR-Alu (SVA) retrotransposition into intron 32 of the gene. Transcriptome analyses identified decreased expression of the canonical cTAF1 transcript among XDP probands, and de novo assembly across multiple pluripotent stem-cell-derived neuronal lineages discovered aberrant TAF1 transcription that involved alternative splicing and intron retention (IR) in proximity to the SVA that was anti-correlated with overall TAF1 expression. CRISPR/Cas9 excision of the SVA rescued this XDP-specific transcriptional signature and normalized TAF1 expression in probands. These data suggest an SVA-mediated aberrant transcriptional mechanism associated with XDP and may provide a roadmap for layered technologies and integrated assembly-based analyses for other unsolved Mendelian disorders.

Keywords: DYT3; Parkinson’s disease; SVA; TAF1; XDP; dystonia; genome assembly; intron retention; retrotransposon; transcriptome assembly.

Publication types

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

MeSH terms

  • Alternative Splicing / genetics
  • Alu Elements / genetics
  • Base Sequence
  • CRISPR-Cas Systems / genetics
  • Cohort Studies
  • Dystonic Disorders / genetics*
  • Family
  • Female
  • Genetic Diseases, X-Linked / genetics*
  • Genetic Loci
  • Genome, Human*
  • Haplotypes / genetics
  • High-Throughput Nucleotide Sequencing
  • Histone Acetyltransferases / genetics
  • Histone Acetyltransferases / metabolism
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Introns / genetics
  • Male
  • Minisatellite Repeats / genetics
  • Models, Genetic
  • Nerve Degeneration / genetics
  • Nerve Degeneration / pathology
  • Neural Stem Cells / metabolism
  • Neurons / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Short Interspersed Nucleotide Elements
  • TATA-Binding Protein Associated Factors / genetics
  • TATA-Binding Protein Associated Factors / metabolism
  • Transcription Factor TFIID / genetics
  • Transcription Factor TFIID / metabolism
  • Transcriptome / genetics*

Substances

  • RNA, Messenger
  • TATA-Binding Protein Associated Factors
  • Transcription Factor TFIID
  • Histone Acetyltransferases
  • TATA-binding protein associated factor 250 kDa

Supplementary concepts

  • Dystonia 3, Torsion, X-Linked