A low absolute number of expanded transcripts is involved in myotonic dystrophy type 1 manifestation in muscle

Hum Mol Genet. 2016 Apr 15;25(8):1648-62. doi: 10.1093/hmg/ddw042. Epub 2016 Feb 16.

Abstract

Muscular manifestation of myotonic dystrophy type 1 (DM1), a common inheritable degenerative multisystem disorder, is mainly caused by expression of RNA from a (CTG·CAG)n-expanded DM1 locus. Here, we report on comparative profiling of expression of normal and expanded endogenous or transgenic transcripts in skeletal muscle cells and biopsies from DM1 mouse models and patients in order to help us in understanding the role of this RNA-mediated toxicity. In tissue of HSA(LR) mice, the most intensely used 'muscle-only' model in the DM1 field, RNA from the α-actin (CTG)250 transgene was at least 1000-fold more abundant than that from the Dmpk gene, or the DMPK gene in humans. Conversely, the DMPK transgene in another line, DM500/DMSXL mice, was expressed ∼10-fold lower than the endogenous gene. Temporal regulation of expanded RNA expression differed between models. Onset of expression occurred remarkably late in HSA(LR) myoblasts during in vitro myogenesis whereas Dmpk or DMPK (trans)genes were expressed throughout proliferation and differentiation phases. Importantly, quantification of absolute transcript numbers revealed that normal and expanded Dmpk/DMPK transcripts in mouse models and DM1 patients are low-abundance RNA species. Northern blotting, reverse transcriptase-quantitative polymerase chain reaction, RNA-sequencing and fluorescent in situ hybridization analyses showed that they occur at an absolute number between one and a few dozen molecules per cell. Our findings refine the current RNA dominance theory for DM1 pathophysiology, as anomalous factor binding to expanded transcripts and formation of soluble or insoluble ribonucleoprotein aggregates must be nucleated by only few expanded DMPK transcripts and therefore be a small numbers game.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / genetics
  • Animals
  • Cells, Cultured
  • Disease Models, Animal
  • Female
  • Gene Expression Profiling / methods*
  • Gene Expression Regulation
  • Humans
  • Male
  • Mice
  • Muscle Development
  • Muscle, Skeletal / cytology*
  • Muscle, Skeletal / pathology
  • Myotonic Dystrophy / genetics*
  • Myotonic Dystrophy / pathology
  • Myotonin-Protein Kinase / genetics
  • Myotonin-Protein Kinase / metabolism
  • RNA, Messenger / genetics*
  • Trinucleotide Repeat Expansion*

Substances

  • Actins
  • RNA, Messenger
  • Myotonin-Protein Kinase