Balancing the length of the distal tip by septins is key for stability and signalling function of primary cilia

EMBO J. 2022 Jan 4;41(1):e108843. doi: 10.15252/embj.2021108843. Epub 2021 Nov 22.

Abstract

Primary cilia are antenna-like organelles required for signalling transduction. How cilia structure is mechanistically maintained at steady-state to promote signalling is largely unknown. Here, we define that mammalian primary cilia axonemes are formed by proximal segment (PS) and distal segment (DS) delineated by tubulin polyglutamylation-rich and -poor regions, respectively. The analysis of proximal/distal segmentation indicated that perturbations leading to cilia over-elongation influenced PS or DS length with a different impact on cilia behaviour. We identified septins as novel repressors of DS growth. We show that septins control the localisation of MKS3 and CEP290 required for a functional transition zone (TZ), and the cilia tip accumulation of the microtubule-capping kinesin KIF7, a cilia-growth inhibitor. Live-cell imaging and analysis of sonic-hedgehog (SHH) signalling activation established that DS over-extension increased cilia ectocytosis events and decreased SHH activation. Our data underlines the importance of understanding cilia segmentation for length control and cilia-dependent signalling.

Keywords: KIF7; cilia length/segmentation; septins; sonic hedgehog signalling; transition zone.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, Neoplasm / metabolism
  • Cell Cycle Proteins / metabolism
  • Cell Line
  • Cilia / metabolism*
  • Cytoskeletal Proteins / metabolism
  • Hedgehog Proteins / metabolism
  • Humans
  • Kinesins / metabolism
  • Membrane Proteins / metabolism
  • Mice
  • Microtubules / metabolism
  • Retinal Pigment Epithelium / cytology
  • Septins / metabolism*
  • Signal Transduction

Substances

  • Antigens, Neoplasm
  • Cell Cycle Proteins
  • Cep290 protein, human
  • Cytoskeletal Proteins
  • Hedgehog Proteins
  • KIF7 protein, human
  • Membrane Proteins
  • TMEM67 protein, human
  • Septins
  • Kinesins