Emerin binding to Btf, a death-promoting transcriptional repressor, is disrupted by a missense mutation that causes Emery-Dreifuss muscular dystrophy

Eur J Biochem. 2004 Mar;271(5):1035-45. doi: 10.1111/j.1432-1033.2004.04007.x.

Abstract

Loss of functional emerin, a nuclear membrane protein, causes X-linked recessive Emery-Dreifuss muscular dystrophy. In a yeast two-hybrid screen, we found that emerin interacts with Btf, a death-promoting transcriptional repressor, which is expressed at high levels in skeletal muscle. Biochemical analysis showed that emerin binds Btf with an equilibrium affinity (KD) of 100 nm. Using a collection of 21 clustered alanine-substitution mutations in emerin, the residues required for binding to Btf mapped to two regions of emerin that flank its lamin-binding domain. Two disease-causing mutations in emerin, S54F and Delta95-99, disrupted binding to Btf. The Delta95-99 mutation was relatively uninformative, as this mutation also disrupts emerin binding to lamin A and a different transcription repressor named germ cell-less (GCL). In striking contrast, emerin mutant S54F, which binds normally to barrier-to-autointegration factor, lamin A and GCL, selectively disrupted emerin binding to Btf. We localized endogenous Btf in HeLa cells by indirect immunoflurorescence using affinity-purified antibodies against Btf. In nonapoptotic HeLa cells Btf was found in dot-like structures throughout the nuclear interior. However, within 3 h after treating cells with Fas antibody to induce apoptosis, the distribution of Btf changed, and Btf concentrated in a distinct zone near the nuclear envelope. These results suggest that Btf localization is regulated by apoptotic signals, and that loss of emerin binding to Btf may be relevant to muscle wasting in Emery-Dreifuss muscular dystrophy.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Apoptosis / physiology
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • HeLa Cells
  • Humans
  • Membrane Proteins / genetics*
  • Membrane Proteins / metabolism*
  • Muscular Dystrophy, Emery-Dreifuss / genetics*
  • Muscular Dystrophy, Emery-Dreifuss / metabolism*
  • Mutation, Missense*
  • Nuclear Envelope / metabolism
  • Nuclear Proteins
  • Protein Binding
  • Protein Structure, Tertiary
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism*
  • Thymopoietins / genetics*
  • Thymopoietins / metabolism*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism*
  • Two-Hybrid System Techniques

Substances

  • BCLAF1 protein, human
  • DNA-Binding Proteins
  • Membrane Proteins
  • Nuclear Proteins
  • Repressor Proteins
  • Thymopoietins
  • Transcription Factors
  • Tumor Suppressor Proteins
  • emerin