Centrosomal protein CP110 controls maturation of the mother centriole during cilia biogenesis

Development. 2016 May 1;143(9):1491-501. doi: 10.1242/dev.130120. Epub 2016 Mar 10.

Abstract

Defects in cilia centrosomal genes cause pleiotropic clinical phenotypes, collectively called ciliopathies. Cilia biogenesis is initiated by the interaction of positive and negative regulators. Centriolar coiled coil protein 110 (CP110) caps the distal end of the mother centriole and is known to act as a suppressor to control the timing of ciliogenesis. Here, we demonstrate that CP110 promotes cilia formation in vivo, in contrast to findings in cultured cells. Cp110(-/-) mice die shortly after birth owing to organogenesis defects as in ciliopathies. Shh signaling is impaired in null embryos and primary cilia are reduced in multiple tissues. We show that CP110 is required for anchoring of basal bodies to the membrane during cilia formation. CP110 loss resulted in an abnormal distribution of core components of subdistal appendages (SDAs) and of recycling endosomes, which may be associated with premature extension of axonemal microtubules. Our data implicate CP110 in SDA assembly and ciliary vesicle docking, two requisite early steps in cilia formation. We suggest that CP110 has unique context-dependent functions, acting as both a suppressor and a promoter of ciliogenesis.

Keywords: Ccp110; Centrosome; Ciliopathies; Membrane anchoring; Microtubule; Mouse; Organogenesis; Primary cilia.

Publication types

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

MeSH terms

  • Animals
  • Axoneme / metabolism
  • Basal Bodies / metabolism
  • Calmodulin-Binding Proteins / genetics
  • Calmodulin-Binding Proteins / metabolism*
  • Cell Line
  • Centrioles / physiology*
  • Centrosome / metabolism
  • Cilia / physiology*
  • Endosomes / metabolism
  • Hedgehog Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microtubules / metabolism
  • Organogenesis / genetics
  • Organogenesis / physiology*

Substances

  • Calmodulin-Binding Proteins
  • Cp110 protein, mouse
  • Hedgehog Proteins
  • Shh protein, mouse