PUBLICATION

A CEP104-CSPP1 Complex Is Required for Formation of Primary Cilia Competent in Hedgehog Signaling

Authors
Frikstad, K.M., Molinari, E., Thoresen, M., Ramsbottom, S.A., Hughes, F., Letteboer, S.J.F., Gilani, S., Schink, K.O., Stokke, T., Geimer, S., Pedersen, L.B., Giles, R.H., Akhmanova, A., Roepman, R., Sayer, J.A., Patzke, S.
ID
ZDB-PUB-190815-7
Date
2019
Source
Cell Reports   28: 1907-1922.e6 (Journal)
Registered Authors
Sayer, John A.
Keywords
CEP104, CSPP1, Hedgehog signaling, Joubert syndrome, MT plus end, centriolar satellites, ciliopathies, primary cilium
MeSH Terms
  • Animals
  • Cell Cycle Proteins/genetics
  • Cell Cycle Proteins/metabolism*
  • Cells, Cultured
  • Cilia/physiology*
  • Ciliopathies/metabolism
  • Ciliopathies/pathology*
  • Hedgehog Proteins/genetics
  • Hedgehog Proteins/metabolism*
  • Humans
  • Microtubule-Associated Proteins/genetics
  • Microtubule-Associated Proteins/metabolism*
  • Mutation
  • Retinal Pigment Epithelium/cytology
  • Retinal Pigment Epithelium/metabolism*
  • Signal Transduction
  • Zebrafish/genetics
  • Zebrafish/growth & development
  • Zebrafish/metabolism
  • Zebrafish Proteins/genetics
  • Zebrafish Proteins/metabolism*
PubMed
31412255 Full text @ Cell Rep.
Abstract
CEP104 is an evolutionarily conserved centrosomal and ciliary tip protein. CEP104 loss-of-function mutations are reported in patients with Joubert syndrome, but their function in the etiology of ciliopathies is poorly understood. Here, we show that cep104 silencing in zebrafish causes cilia-related manifestations: shortened cilia in Kupffer's vesicle, heart laterality, and cranial nerve development defects. We show that another Joubert syndrome-associated cilia tip protein, CSPP1, interacts with CEP104 at microtubules for the regulation of axoneme length. We demonstrate in human telomerase reverse transcriptase-immortalized retinal pigmented epithelium (hTERT-RPE1) cells that ciliary translocation of Smoothened in response to Hedgehog pathway stimulation is both CEP104 and CSPP1 dependent. However, CEP104 is not required for the ciliary recruitment of CSPP1, indicating that an intra-ciliary CEP104-CSPP1 complex controls axoneme length and Hedgehog signaling competence. Our in vivo and in vitro analyses of CEP104 define its interaction with CSPP1 as a requirement for the formation of Hedgehog signaling-competent cilia, defects that underlie Joubert syndrome.
Genes / Markers
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Mutations / Transgenics
Human Disease / Model
Sequence Targeting Reagents
Fish
Antibodies
Orthology
Engineered Foreign Genes
Mapping