Basal body proteins regulate Notch signaling through endosomal trafficking

J Cell Sci. 2014 Jun 1;127(Pt 11):2407-19. doi: 10.1242/jcs.130344. Epub 2014 Mar 28.

Abstract

Proteins associated with primary cilia and basal bodies mediate numerous signaling pathways, but little is known about their role in Notch signaling. Here, we report that loss of the Bardet-Biedl syndrome proteins BBS1 or BBS4 produces increased Notch-directed transcription in a zebrafish reporter line and in human cell lines. Pathway overactivation is accompanied by reduced localization of Notch receptor at both the plasma membrane and the cilium. In Drosophila mutants, overactivation of Notch can result from receptor accumulation in endosomes, and recent studies implicate ciliary proteins in endosomal trafficking, suggesting a possible mechanism by which overactivation occurs in BBS mutants. Consistent with this, we observe genetic interaction of BBS1 and BBS4 with the endosomal sorting complexes required for transport (ESCRT) gene TSG101 and accumulation of receptor in late endosomes, reduced endosomal recycling and reduced receptor degradation in lysosomes. We observe similar defects with disruption of BBS3. Loss of another basal body protein, ALMS1, also enhances Notch activation and the accumulation of receptor in late endosomes, but does not disrupt recycling. These findings suggest a role for these proteins in the regulation of Notch through endosomal trafficking of the receptor.

Keywords: Alstrom Syndrome; Bardet-Biedl Syndrome; Basal body; Cilia; Endosomal sorting; Notch.

Publication types

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

MeSH terms

  • ADP-Ribosylation Factors / genetics
  • ADP-Ribosylation Factors / metabolism
  • Animals
  • Basal Bodies / physiology*
  • Cell Cycle Proteins
  • Cell Line
  • Cell Membrane / metabolism*
  • Cilia / physiology*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Drosophila
  • Endosomal Sorting Complexes Required for Transport / genetics
  • Endosomal Sorting Complexes Required for Transport / metabolism
  • Endosomes / metabolism*
  • Humans
  • Microtubule-Associated Proteins / genetics
  • Microtubule-Associated Proteins / metabolism*
  • Mutation / genetics
  • Protein Transport / genetics
  • Proteins / genetics
  • Proteins / metabolism*
  • Receptors, Notch / metabolism*
  • Signal Transduction / genetics
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Zebrafish

Substances

  • ALMS1 protein, human
  • BBS4 protein, human
  • Bbs1 protein, human
  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • Endosomal Sorting Complexes Required for Transport
  • Microtubule-Associated Proteins
  • Proteins
  • Receptors, Notch
  • Transcription Factors
  • Tsg101 protein
  • ARL6 protein, human
  • ADP-Ribosylation Factors