Nesprin interchain associations control nuclear size

Cell Mol Life Sci. 2012 Oct;69(20):3493-509. doi: 10.1007/s00018-012-1034-1. Epub 2012 Jun 1.

Abstract

Nesprins-1/-2/-3/-4 are nuclear envelope proteins, which connect nuclei to the cytoskeleton. The largest nesprin-1/-2 isoforms (termed giant) tether F-actin through their N-terminal actin binding domain (ABD). Nesprin-3, however, lacks an ABD and associates instead to plectin, which binds intermediate filaments. Nesprins are integrated into the outer nuclear membrane via their C-terminal KASH-domain. Here, we show that nesprin-1/-2 ABDs physically and functionally interact with nesprin-3. Thus, both ends of nesprin-1/-2 giant are integrated at the nuclear surface: via the C-terminal KASH-domain and the N-terminal ABD-nesprin-3 association. Interestingly, nesprin-2 ABD or KASH-domain overexpression leads to increased nuclear areas. Conversely, nesprin-2 mini (contains the ABD and KASH-domain but lacks the massive nesprin-2 giant rod segment) expression yields smaller nuclei. Nuclear shrinkage is further enhanced upon nesprin-3 co-expression or microfilament depolymerization. Our findings suggest that multivariate intermolecular nesprin interactions with the cytoskeleton form a lattice-like filamentous network covering the outer nuclear membrane, which determines nuclear size.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism*
  • Blotting, Western
  • Cell Nucleus / metabolism*
  • Cell Nucleus / ultrastructure
  • Cells, Cultured
  • Cytoskeletal Proteins
  • Fibroblasts / cytology
  • Fibroblasts / metabolism
  • Fluorescent Antibody Technique
  • Genes, Dominant
  • Humans
  • Immunoprecipitation
  • Keratinocytes / cytology
  • Keratinocytes / metabolism
  • Microfilament Proteins / antagonists & inhibitors
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism*
  • Nerve Tissue Proteins / antagonists & inhibitors
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Nuclear Envelope / metabolism*
  • Nuclear Proteins / antagonists & inhibitors
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Plasmids
  • Protein Structure, Tertiary
  • RNA, Small Interfering / genetics

Substances

  • Actins
  • Cytoskeletal Proteins
  • Microfilament Proteins
  • Nerve Tissue Proteins
  • Nuclear Proteins
  • RNA, Small Interfering
  • SYNE1 protein, human
  • SYNE2 protein, human
  • SYNE3 protein, human