MBNL1 and CUGBP1 modify expanded CUG-induced toxicity in a Drosophila model of myotonic dystrophy type 1

Hum Mol Genet. 2006 Jul 1;15(13):2138-45. doi: 10.1093/hmg/ddl137. Epub 2006 May 24.

Abstract

Myotonic dystrophy type 1 (DM1) is a neuromuscular disorder caused by a CTG expansion in the 3' UTR of the dystrophia myotonica protein kinase (DMPK) gene. It has been hypothesized that the pathogenesis in DM1 is triggered by a toxic gain of function of the expanded DMPK RNA. This expanded RNA is retained in nuclear foci where it sequesters and induces alterations in the levels of RNA-binding proteins (RNA-BP). To model DM1 and study the implication of RNA-BP in CUG-induced toxicity, we have generated a Drosophila DM1 model expressing a non-coding mRNA containing 480 interrupted CUG repeats; i.e. [(CUG)20CUCGA]24. This (iCUG)480 transcript accumulates in nuclear foci and its expression leads to muscle wasting and degeneration in Drosophila. We also report that altering the levels of two RNA-BP known to be involved in DM1 pathogenesis, MBNL1 and CUGBP1, modify the (iCUG)480 degenerative phenotypes. Expanded CUG-induced toxicity in Drosophila is suppressed when MBNL1 expression levels are increased, and enhanced when MBNL1 levels are reduced. In addition, (iCUG)480 also causes a decrease in the levels of soluble MBNL1 that is sequestered in the CUG-containing nuclear foci. In contrast, increasing the levels of CUGBP1 worsens (iCUG)480-induced degeneration even though CUGBP1 distribution is not altered by the expression of the expanded triplet repeat. Our data supports a mechanism for DM1 pathogenesis in which decreased levels of MBNL and increased levels of CUGBP mediate the RNA-induced toxicity observed in DM1. Perhaps more importantly, they also provide proof of the principle that CUG-induced muscle toxicity can be suppressed.

Publication types

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

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Blotting, Northern
  • CELF1 Protein
  • Cell Nucleus / metabolism
  • Disease Models, Animal
  • Drosophila melanogaster / genetics*
  • Drosophila melanogaster / metabolism
  • Drosophila melanogaster / ultrastructure
  • Eye / metabolism
  • Eye / ultrastructure
  • Humans
  • In Situ Hybridization
  • Microscopy, Electron, Scanning
  • Muscles / metabolism
  • Muscles / ultrastructure
  • Myotonic Dystrophy / genetics*
  • Myotonic Dystrophy / metabolism
  • Myotonic Dystrophy / pathology
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / physiology*
  • Trinucleotide Repeat Expansion / genetics*

Substances

  • CELF1 Protein
  • CELF1 protein, human
  • MBNL1 protein, human
  • RNA, Messenger
  • RNA-Binding Proteins