Dissecting Torsin/cofactor function at the nuclear envelope: a genetic study

Mol Biol Cell. 2016 Dec 15;27(25):3964-3971. doi: 10.1091/mbc.E16-07-0511. Epub 2016 Oct 26.

Abstract

The human genome encodes four Torsin ATPases, the functions of which are poorly understood. In this study, we use CRISPR/Cas9 engineering to delete all four Torsin ATPases individually and in combination. Using nuclear envelope (NE) blebbing as a phenotypic measure, we establish a direct correlation between the number of inactivated Torsin alleles and the occurrence of omega-shaped herniations within the lumen of the NE. A similar, although not identical, redundancy is observed for LAP1 and LULL1, which serve as regulatory cofactors for a subset of Torsin ATPases. Unexpectedly, deletion of Tor2A in a TorA/B/3A-deficient background results in a stark increase of bleb formation, even though Tor2A does not respond to LAP1/LULL1 stimulation. The robustness of the observed phenotype in Torsin-deficient cells enables a structural analysis via electron microscopy tomography and a compositional analysis via immunogold labeling. Ubiquitin and nucleoporins were identified as distinctively localizing components of the omega-shaped bleb structure. These findings suggest a functional link between the Torsin/cofactor system and NE/nuclear pore complex biogenesis or homeostasis and establish a Torsin-deficient cell line as a valuable experimental platform with which to decipher Torsin function.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adenosine Triphosphatases / genetics
  • Adenosine Triphosphatases / metabolism
  • HeLa Cells
  • Humans
  • Intercellular Signaling Peptides and Proteins / genetics*
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Membrane Proteins / metabolism
  • Minor Histocompatibility Antigens / genetics
  • Minor Histocompatibility Antigens / metabolism
  • Molecular Chaperones / genetics*
  • Molecular Chaperones / metabolism
  • Nuclear Envelope / metabolism*
  • Nuclear Envelope / physiology
  • Nuclear Pore / metabolism
  • Nuclear Pore Complex Proteins / metabolism

Substances

  • Intercellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Minor Histocompatibility Antigens
  • Molecular Chaperones
  • Nuclear Pore Complex Proteins
  • TOR1A protein, human
  • TOR1B protein, human
  • TOR2A protein, human
  • Adenosine Triphosphatases
  • TOR3A protein, human