Long-read targeted sequencing uncovers clinicopathological associations for C9orf72-linked diseases

Brain. 2021 May 7;144(4):1082-1088. doi: 10.1093/brain/awab006.

Abstract

To examine the length of a hexanucleotide expansion in C9orf72, which represents the most frequent genetic cause of frontotemporal lobar degeneration and motor neuron disease, we employed a targeted amplification-free long-read sequencing technology: No-Amp sequencing. In our cross-sectional study, we assessed cerebellar tissue from 28 well-characterized C9orf72 expansion carriers. We obtained 3507 on-target circular consensus sequencing reads, of which 814 bridged the C9orf72 repeat expansion (23%). Importantly, we observed a significant correlation between expansion sizes obtained using No-Amp sequencing and Southern blotting (P = 5.0 × 10-4). Interestingly, we also detected a significant survival advantage for individuals with smaller expansions (P = 0.004). Additionally, we uncovered that smaller expansions were significantly associated with higher levels of C9orf72 transcripts containing intron 1b (P = 0.003), poly(GP) proteins (P = 1.3 × 10- 5), and poly(GA) proteins (P = 0.005). Thorough examination of the composition of the expansion revealed that its GC content was extremely high (median: 100%) and that it was mainly composed of GGGGCC repeats (median: 96%), suggesting that expanded C9orf72 repeats are quite pure. Taken together, our findings demonstrate that No-Amp sequencing is a powerful tool that enables the discovery of relevant clinicopathological associations, highlighting the important role played by the cerebellar size of the expanded repeat in C9orf72-linked diseases.

Keywords: C9orf72; amyotrophic lateral sclerosis; frontotemporal lobar degeneration; long-read sequencing; motor neuron disease.

Publication types

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

MeSH terms

  • Aged
  • C9orf72 Protein / genetics*
  • Cerebellum / metabolism
  • Cross-Sectional Studies
  • DNA Repeat Expansion / genetics
  • Female
  • Humans
  • Male
  • Middle Aged
  • Neurodegenerative Diseases / genetics*
  • Sequence Analysis, DNA / methods*

Substances

  • C9orf72 Protein
  • C9orf72 protein, human