FGFR1-mediated protocadherin-15 loading mediates cargo specificity during intraflagellar transport in inner ear hair-cell kinocilia

Proc Natl Acad Sci U S A. 2018 Aug 14;115(33):8388-8393. doi: 10.1073/pnas.1719861115. Epub 2018 Jul 30.

Abstract

The mechanosensory hair cells of the inner ear are required for hearing and balance and have a distinctive apical structure, the hair bundle, that converts mechanical stimuli into electrical signals. This structure comprises a single cilium, the kinocilium, lying adjacent to an ensemble of actin-based projections known as stereocilia. Hair bundle polarity depends on kinociliary protocadherin-15 (Pcdh15) localization. Protocadherin-15 is found only in hair-cell kinocilia, and is not localized to the primary cilia of adjacent supporting cells. Thus, Pcdh15 must be specifically targeted and trafficked into the hair-cell kinocilium. Here we show that kinocilial Pcdh15 trafficking relies on cell type-specific coupling to the generic intraflagellar transport (IFT) transport mechanism. We uncover a role for fibroblast growth factor receptor 1 (FGFR1) in loading Pcdh15 onto kinociliary transport particles in hair cells. We find that on activation, FGFR1 binds and phosphorylates Pcdh15. Moreover, we find a previously uncharacterized role for clathrin in coupling this kinocilia-specific cargo with the anterograde IFT-B complex through the adaptor, DAB2. Our results identify a modified ciliary transport pathway used for Pcdh15 transport into the cilium of the inner ear hair cell and coordinated by FGFR1 activity.

Keywords: ciliogenesis; fibroblast growth factor; inner ear; protein trafficking; signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Adaptor Proteins, Vesicular Transport / physiology
  • Animals
  • Apoptosis Regulatory Proteins
  • Cadherin Related Proteins
  • Cadherins / physiology*
  • Chick Embryo
  • Clathrin / physiology
  • Flagella / metabolism*
  • Hair Cells, Auditory, Inner / metabolism*
  • Mice
  • Phosphorylation
  • Protein Precursors / physiology*
  • Protein Transport
  • Receptor, Fibroblast Growth Factor, Type 1 / analysis
  • Receptor, Fibroblast Growth Factor, Type 1 / physiology*

Substances

  • Adaptor Proteins, Signal Transducing
  • Adaptor Proteins, Vesicular Transport
  • Apoptosis Regulatory Proteins
  • CDHR15 protein, mouse
  • Cadherin Related Proteins
  • Cadherins
  • Clathrin
  • Dab2 protein, mouse
  • Protein Precursors
  • Fgfr1 protein, mouse
  • Receptor, Fibroblast Growth Factor, Type 1