DMA-tudor interaction modules control the specificity of in vivo condensates

Cell. 2021 Jul 8;184(14):3612-3625.e17. doi: 10.1016/j.cell.2021.05.008. Epub 2021 Jun 10.

Abstract

Biomolecular condensation is a widespread mechanism of cellular compartmentalization. Because the "survival of motor neuron protein" (SMN) is implicated in the formation of three different membraneless organelles (MLOs), we hypothesized that SMN promotes condensation. Unexpectedly, we found that SMN's globular tudor domain was sufficient for dimerization-induced condensation in vivo, whereas its two intrinsically disordered regions (IDRs) were not. Binding to dimethylarginine (DMA) modified protein ligands was required for condensate formation by the tudor domains in SMN and at least seven other fly and human proteins. Remarkably, asymmetric versus symmetric DMA determined whether two distinct nuclear MLOs-gems and Cajal bodies-were separate or "docked" to one another. This substructure depended on the presence of either asymmetric or symmetric DMA as visualized with sub-diffraction microscopy. Thus, DMA-tudor interaction modules-combinations of tudor domains bound to their DMA ligand(s)-represent versatile yet specific regulators of MLO assembly, composition, and morphology.

Keywords: Cajal body; DMA; MLO; biomolecular condensation; dimethylarginine; membraneless organelle; nuclear gem; post-translational modification; tudor domains.

Publication types

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

MeSH terms

  • Animals
  • Arginine / analogs & derivatives*
  • Arginine / metabolism
  • Biomolecular Condensates / metabolism*
  • Cell Nucleus / metabolism
  • Coiled Bodies / metabolism
  • Drosophila melanogaster / metabolism
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Ligands
  • Methylation
  • Mice
  • Models, Biological
  • NIH 3T3 Cells
  • Protein Binding
  • Protein Domains
  • Protein Multimerization
  • Ribonucleoproteins, Small Nuclear / metabolism
  • SMN Complex Proteins / chemistry*
  • SMN Complex Proteins / metabolism*

Substances

  • Ligands
  • Ribonucleoproteins, Small Nuclear
  • SMN Complex Proteins
  • dimethylarginine
  • Arginine