SPATA7 maintains a novel photoreceptor-specific zone in the distal connecting cilium

J Cell Biol. 2018 Aug 6;217(8):2851-2865. doi: 10.1083/jcb.201712117. Epub 2018 Jun 13.

Abstract

Photoreceptor-specific ciliopathies often affect a structure that is considered functionally homologous to the ciliary transition zone (TZ) called the connecting cilium (CC). However, it is unclear how mutations in certain ciliary genes disrupt the photoreceptor CC without impacting the primary cilia systemically. By applying stochastic optical reconstruction microscopy technology in different genetic models, we show that the CC can be partitioned into two regions: the proximal CC (PCC), which is homologous to the TZ of primary cilia, and the distal CC (DCC), a photoreceptor-specific extension of the ciliary TZ. This specialized distal zone of the CC in photoreceptors is maintained by SPATA7, which interacts with other photoreceptor-specific ciliary proteins such as RPGR and RPGRIP1. The absence of Spata7 results in the mislocalization of DCC proteins without affecting the PCC protein complexes. This collapse results in destabilization of the axonemal microtubules, which consequently results in photoreceptor degeneration. These data provide a novel mechanism to explain how genetic disruption of ubiquitously present ciliary proteins exerts tissue-specific ciliopathy phenotypes.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / analysis
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Antigens, Neoplasm
  • Carrier Proteins / analysis
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cell Cycle Proteins
  • Cytoskeletal Proteins
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • DNA-Binding Proteins / physiology*
  • Eye Proteins / analysis
  • Eye Proteins / genetics
  • Eye Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Nuclear Proteins / metabolism
  • Nuclear Proteins / physiology
  • Photoreceptor Connecting Cilium / metabolism*
  • Photoreceptor Connecting Cilium / ultrastructure
  • Protein Transport / genetics

Substances

  • Adaptor Proteins, Signal Transducing
  • Antigens, Neoplasm
  • Carrier Proteins
  • Cell Cycle Proteins
  • Cep290 protein, mouse
  • Cytoskeletal Proteins
  • DNA-Binding Proteins
  • Eye Proteins
  • Ftm protein, mouse
  • Nuclear Proteins
  • RPGR protein, mouse
  • SPATA7 protein, mouse