A ciliopathy complex builds distal appendages to initiate ciliogenesis

J Cell Biol. 2021 Sep 6;220(9):e202011133. doi: 10.1083/jcb.202011133. Epub 2021 Jul 9.

Abstract

Cells inherit two centrioles, the older of which is uniquely capable of generating a cilium. Using proteomics and superresolved imaging, we identify a module that we term DISCO (distal centriole complex). The DISCO components CEP90, MNR, and OFD1 underlie human ciliopathies. This complex localizes to both distal centrioles and centriolar satellites, proteinaceous granules surrounding centrioles. Cells and mice lacking CEP90 or MNR do not generate cilia, fail to assemble distal appendages, and do not transduce Hedgehog signals. Disrupting the satellite pools does not affect distal appendage assembly, indicating that it is the centriolar populations of MNR and CEP90 that are critical for ciliogenesis. CEP90 recruits the most proximal known distal appendage component, CEP83, to root distal appendage formation, an early step in ciliogenesis. In addition, MNR, but not CEP90, restricts centriolar length by recruiting OFD1. We conclude that DISCO acts at the distal centriole to support ciliogenesis by restraining centriole length and assembling distal appendages, defects in which cause human ciliopathies.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Cell Line
  • Centrioles / metabolism*
  • Centrioles / pathology
  • Centrioles / ultrastructure
  • Cilia / metabolism*
  • Cilia / pathology
  • Cilia / ultrastructure
  • Ciliopathies / genetics*
  • Ciliopathies / metabolism
  • Ciliopathies / pathology
  • Embryo, Mammalian
  • Epithelial Cells / cytology
  • Epithelial Cells / metabolism
  • Gene Expression Regulation
  • Genes, Reporter
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Humans
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microtubule-Associated Proteins / deficiency
  • Microtubule-Associated Proteins / genetics*
  • Microtubule-Associated Proteins / metabolism
  • Proteins / genetics*
  • Proteins / metabolism
  • Retinal Pigment Epithelium / cytology
  • Retinal Pigment Epithelium / metabolism
  • Signal Transduction

Substances

  • Bacterial Proteins
  • CEP83 protein, human
  • Luminescent Proteins
  • Microtubule-Associated Proteins
  • OFD1 protein, human
  • Proteins
  • yellow fluorescent protein, Bacteria
  • Green Fluorescent Proteins