Abundant transcriptomic alterations in the human cerebellum of patients with a C9orf72 repeat expansion

Acta Neuropathol. 2024 Apr 19;147(1):73. doi: 10.1007/s00401-024-02720-2.

Abstract

The most prominent genetic cause of both amyotrophic lateral sclerosis (ALS) and frontotemporal lobar degeneration (FTLD) is a repeat expansion in the gene C9orf72. Importantly, the transcriptomic consequences of the C9orf72 repeat expansion remain largely unclear. Here, we used short-read RNA sequencing (RNAseq) to profile the cerebellar transcriptome, detecting alterations in patients with a C9orf72 repeat expansion. We focused on the cerebellum, since key C9orf72-related pathologies are abundant in this neuroanatomical region, yet TDP-43 pathology and neuronal loss are minimal. Consistent with previous work, we showed a reduction in the expression of the C9orf72 gene and an elevation in homeobox genes, when comparing patients with the expansion to both patients without the C9orf72 repeat expansion and control subjects. Interestingly, we identified more than 1000 alternative splicing events, including 4 in genes previously associated with ALS and/or FTLD. We also found an increase of cryptic splicing in C9orf72 patients compared to patients without the expansion and controls. Furthermore, we demonstrated that the expression level of select RNA-binding proteins is associated with cryptic splice junction inclusion. Overall, this study explores the presence of widespread transcriptomic changes in the cerebellum, a region not confounded by severe neurodegeneration, in post-mortem tissue from C9orf72 patients.

Keywords: Amyotrophic lateral sclerosis; C9orf72; Cryptic exons; Frontotemporal lobar degeneration; Transcriptomics.

MeSH terms

  • Amyotrophic Lateral Sclerosis* / genetics
  • Amyotrophic Lateral Sclerosis* / metabolism
  • Amyotrophic Lateral Sclerosis* / pathology
  • C9orf72 Protein* / genetics
  • C9orf72 Protein* / metabolism
  • Cerebellum* / pathology
  • DNA Repeat Expansion / genetics
  • Frontotemporal Lobar Degeneration* / genetics
  • Frontotemporal Lobar Degeneration* / metabolism
  • Frontotemporal Lobar Degeneration* / pathology
  • Gene Expression Profiling
  • Humans
  • Transcriptome

Substances

  • C9orf72 Protein
  • C9orf72 protein, human