Interaction between the Caenorhabditis elegans centriolar protein SAS-5 and microtubules facilitates organelle assembly

Mol Biol Cell. 2018 Mar 15;29(6):722-735. doi: 10.1091/mbc.E17-06-0412. Epub 2018 Jan 24.

Abstract

Centrioles are microtubule-based organelles that organize the microtubule network and seed the formation of cilia and flagella. New centrioles assemble through a stepwise process dependent notably on the centriolar protein SAS-5 in Caenorhabditis elegans SAS-5 and its functional homologues in other species form oligomers that bind the centriolar proteins SAS-6 and SAS-4, thereby forming an evolutionarily conserved structural core at the onset of organelle assembly. Here, we report a novel interaction of SAS-5 with microtubules. Microtubule binding requires SAS-5 oligomerization and a disordered protein segment that overlaps with the SAS-4 binding site. Combined in vitro and in vivo analysis of select mutants reveals that the SAS-5-microtubule interaction facilitates centriole assembly in C. elegans embryos. Our findings lead us to propose that the interdependence of SAS-5 oligomerization and microtubule binding reflects an avidity mechanism, which also strengthens SAS-5 associations with other centriole components and, thus, promotes organelle assembly.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / metabolism*
  • Cell Cycle Proteins / metabolism*
  • Centrioles / metabolism
  • Cilia / metabolism
  • Embryo, Nonmammalian / metabolism*
  • Flagella / metabolism
  • Microtubules / metabolism*
  • Organelle Biogenesis*

Substances

  • Caenorhabditis elegans Proteins
  • Cell Cycle Proteins
  • SAS-4 protein, C elegans
  • SAS-5 protein, C elegans
  • SAS-6 protein, C elegans