The disease-associated r(GGGGCC)n repeat from the C9orf72 gene forms tract length-dependent uni- and multimolecular RNA G-quadruplex structures

J Biol Chem. 2013 Apr 5;288(14):9860-9866. doi: 10.1074/jbc.C113.452532. Epub 2013 Feb 19.

Abstract

Certain DNA and RNA sequences can form G-quadruplexes, which can affect promoter activity, genetic instability, RNA splicing, translation, and neurite mRNA localization. Amyotrophic lateral sclerosis and frontotemporal dementia were recently shown to be caused by expansion of a (GGGGCC)n·(GGCCCC)n repeat in the C9orf72 gene. Mutant r(GGGGCC)n-containing transcripts aggregate in nuclear foci possibly sequestering repeat-binding proteins, suggesting a toxic RNA pathogenesis. We demonstrate that the r(GGGGCC)n RNA but not the C-rich r(GGCCCC)n RNA forms extremely stable uni- and multimolecular parallel G-quadruplex structures (up to 95 °C). Multimolecular G-quadruplex formation is influenced by repeat number and RNA concentration. MBNL1, a splicing factor that is sequestered in myotonic dystrophy patients by binding to expanded r(CUG)n repeat hairpins, does not bind the C9orf72 repeats, but the splicing factor ASF/SF2 can bind the r(GGGGCC)n repeat. Because multimolecular G-quadruplexes are enhanced by repeat length, RNA-RNA interactions facilitated by G-quadruplex formation at expanded repeats might influence transcript aggregation and foci formation in amyotrophic lateral sclerosis-frontotemporal dementia cells. Tract length-dependent G-quadruplex formation by the C9orf72 RNA should be considered when assessing the role of this repeat in C9orf72 gene activity, protein binding, transcript foci formation, and translation of the C9orf72 product, including the noncanonical repeat-associated non-ATG translation (RAN translation) into pathologic dipeptide repeats, as well as any oligonucleotide repeat-based therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyotrophic Lateral Sclerosis / genetics
  • Amyotrophic Lateral Sclerosis / metabolism
  • C9orf72 Protein
  • Circular Dichroism
  • DNA Repeat Expansion
  • Frontotemporal Dementia / genetics
  • Frontotemporal Dementia / metabolism
  • G-Quadruplexes*
  • Humans
  • Ions
  • Neurodegenerative Diseases / metabolism
  • Nucleic Acid Conformation
  • Oligonucleotides / genetics
  • Peptides / chemistry
  • Protein Binding
  • Protein Isoforms
  • Proteins / chemistry*
  • Proteins / genetics*
  • RNA / chemistry
  • RNA / genetics
  • RNA Splicing

Substances

  • C9orf72 Protein
  • C9orf72 protein, human
  • Ions
  • Oligonucleotides
  • Peptides
  • Protein Isoforms
  • Proteins
  • RNA