DUX4 expression in FSHD muscle cells: how could such a rare protein cause a myopathy?

J Cell Mol Med. 2013 Jan;17(1):76-89. doi: 10.1111/j.1582-4934.2012.01647.x. Epub 2012 Dec 4.

Abstract

Facioscapulohumeral muscular dystrophy (FSHD) is one of the most frequent hereditary muscle disorders. It is linked to contractions of the D4Z4 repeat array in 4q35. We have characterized the double homeobox 4 (DUX4) gene in D4Z4 and its mRNA transcribed from the distal D4Z4 unit to a polyadenylation signal in the flanking pLAM region. It encodes a transcription factor expressed in FSHD but not healthy muscle cells which initiates a gene deregulation cascade causing differentiation defects, muscle atrophy and oxidative stress. PITX1 was the first identified DUX4 target and encodes a transcription factor involved in muscle atrophy. DUX4 was found expressed in only 1/1000 FSHD myoblasts. We have now shown it was induced upon differentiation and detected in about 1/200 myotube nuclei. The DUX4 and PITX1 proteins presented staining gradients in consecutive myonuclei which suggested a diffusion as known for other muscle nuclear proteins. Both protein half-lifes were regulated by the ubiquitin-proteasome pathway. In addition, we could immunodetect the DUX4 protein in FSHD muscle extracts. As a model, we propose the DUX4 gene is stochastically activated in a small number of FSHD myonuclei. The resulting mRNAs are translated in the cytoplasm around an activated nucleus and the DUX4 proteins diffuse to adjacent nuclei where they activate target genes such as PITX1. The PITX1 protein can further diffuse to additional myonuclei and expand the transcriptional deregulation cascade initiated by DUX4. Together the diffusion and the deregulation cascade would explain how a rare protein could cause the muscle defects observed in FSHD.

Publication types

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

MeSH terms

  • Animals
  • Cell Differentiation
  • Cell Nucleus / genetics
  • Cell Nucleus / metabolism
  • Cell Nucleus / pathology
  • Cytoplasm / genetics
  • Cytoplasm / metabolism
  • Gene Expression Regulation
  • Half-Life
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism*
  • Humans
  • Mice
  • Muscle Fibers, Skeletal / metabolism*
  • Muscle Fibers, Skeletal / pathology
  • Muscle Proteins / genetics
  • Muscle Proteins / metabolism*
  • Muscular Dystrophy, Facioscapulohumeral / genetics
  • Muscular Dystrophy, Facioscapulohumeral / metabolism*
  • Muscular Dystrophy, Facioscapulohumeral / pathology
  • Myoblasts, Skeletal / metabolism*
  • Myoblasts, Skeletal / pathology
  • Paired Box Transcription Factors / genetics
  • Paired Box Transcription Factors / metabolism*
  • Primary Cell Culture
  • Proteasome Endopeptidase Complex / metabolism
  • Protein Binding
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism*
  • Signal Transduction

Substances

  • DUX4L1 protein, human
  • Homeodomain Proteins
  • Muscle Proteins
  • Paired Box Transcription Factors
  • RNA, Messenger
  • homeobox protein PITX1
  • Proteasome Endopeptidase Complex