A laminopathic mutation disrupting lamin filament assembly causes disease-like phenotypes in Caenorhabditis elegans

Mol Biol Cell. 2011 Aug 1;22(15):2716-28. doi: 10.1091/mbc.E11-01-0064. Epub 2011 Jun 8.

Abstract

Mutations in the human LMNA gene underlie many laminopathic diseases, including Emery-Dreifuss muscular dystrophy (EDMD); however, a mechanistic link between the effect of mutations on lamin filament assembly and disease phenotypes has not been established. We studied the ΔK46 Caenorhabditis elegans lamin mutant, corresponding to EDMD-linked ΔK32 in human lamins A and C. Cryo-electron tomography of lamin ΔK46 filaments in vitro revealed alterations in the lateral assembly of dimeric head-to-tail polymers, which causes abnormal organization of tetrameric protofilaments. Green fluorescent protein (GFP):ΔK46 lamin expressed in C. elegans was found in nuclear aggregates in postembryonic stages along with LEM-2. GFP:ΔK46 also caused mislocalization of emerin away from the nuclear periphery, consistent with a decreased ability of purified emerin to associate with lamin ΔK46 filaments in vitro. GFP:ΔK46 animals had motility defects and muscle structure abnormalities. These results show that changes in lamin filament structure can translate into disease-like phenotypes via altering the localization of nuclear lamina proteins, and suggest a model for how the ΔK32 lamin mutation may cause EDMD in humans.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Caenorhabditis elegans / genetics*
  • Caenorhabditis elegans / metabolism
  • Cloning, Molecular
  • Cryoelectron Microscopy
  • Cytoskeleton / genetics*
  • Cytoskeleton / metabolism
  • Disease Models, Animal
  • Escherichia coli
  • Genetic Association Studies
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Humans
  • Lamin Type A / genetics*
  • Lamin Type A / metabolism
  • Membrane Proteins / metabolism*
  • Molecular Sequence Data
  • Movement
  • Muscles / physiopathology
  • Muscular Dystrophy, Emery-Dreifuss / genetics*
  • Muscular Dystrophy, Emery-Dreifuss / metabolism
  • Mutation
  • Nuclear Lamina / genetics*
  • Nuclear Lamina / metabolism
  • Nuclear Proteins / metabolism*
  • Phenotype
  • Plasmids
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism*
  • Transformation, Bacterial

Substances

  • Lamin Type A
  • Membrane Proteins
  • Nuclear Proteins
  • Recombinant Proteins
  • emerin
  • Green Fluorescent Proteins