A theory of centriole duplication based on self-organized spatial pattern formation

J Cell Biol. 2019 Nov 4;218(11):3537-3547. doi: 10.1083/jcb.201904156. Epub 2019 Aug 26.

Abstract

In each cell cycle, centrioles are duplicated to produce a single copy of each preexisting centriole. At the onset of centriole duplication, the master regulator Polo-like kinase 4 (Plk4) undergoes a dynamic change in its spatial pattern around the preexisting centriole, forming a single duplication site. However, the significance and mechanisms of this pattern transition remain unknown. Using super-resolution imaging, we found that centriolar Plk4 exhibits periodic discrete patterns resembling pearl necklaces, frequently with single prominent foci. Mathematical modeling and simulations incorporating the self-organization properties of Plk4 successfully generated the experimentally observed patterns. We therefore propose that the self-patterning of Plk4 is crucial for the regulation of centriole duplication. These results, defining the mechanisms of self-organized regulation, provide a fundamental principle for understanding centriole duplication.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Centrioles / metabolism*
  • HCT116 Cells
  • Humans
  • Protein Serine-Threonine Kinases / metabolism*

Substances

  • PLK4 protein, human
  • Protein Serine-Threonine Kinases