Characterization of tetratricopeptide repeat-containing proteins critical for cilia formation and function

PLoS One. 2015 Apr 10;10(4):e0124378. doi: 10.1371/journal.pone.0124378. eCollection 2015.

Abstract

Cilia formation and function require a special set of trafficking machinery termed intraflagellar transport (IFT), consisting mainly of protein complexes IFT-A, IFT-B, BBSome, and microtubule-dependent molecular motors. Tetratricopeptide repeat-containing (TTC) proteins are widely involved in protein complex formation. Nine of them are known to serve as components of the IFT or BBSome complexes. How many TTC proteins are cilia-related and how they function, however, remain unclear. Here we show that twenty TTC genes were upregulated by at least 2-fold during the differentiation of cultured mouse tracheal epithelial cells (MTECs) into multiciliated cells. Our systematic screen in zebrafish identified four novel TTC genes, ttc4, -9c, -36, and -39c, that are critical for cilia formation and motility. Accordingly, their zebrafish morphants displayed typical ciliopathy-related phenotypes, including curved body, abnormal otolith, hydrocephalus, and defective left-right patterning. The morphants of ttc4 and ttc25, a known cilia-related gene, additionally showed pronephric cyst formation. Immunoprecipitation indicated associations of TTC4, -9c, -25, -36, and -39c with components or entire complexes of IFT-A, IFT-B, or BBSome, implying their participations in IFT or IFT-related activities. Our results provide a global view for the relationship between TTC proteins and cilia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carrier Proteins / chemistry
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Cell Differentiation
  • Cells, Cultured
  • Cilia / genetics
  • Cilia / metabolism*
  • Epithelial Cells / cytology
  • Epithelial Cells / metabolism
  • Humans
  • Mice
  • Multiprotein Complexes / chemistry
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / metabolism
  • Oligonucleotide Array Sequence Analysis
  • Phenotype
  • Trachea / cytology
  • Trachea / metabolism
  • Up-Regulation
  • Zebrafish / embryology
  • Zebrafish / genetics
  • Zebrafish / metabolism
  • Zebrafish Proteins / chemistry
  • Zebrafish Proteins / genetics
  • Zebrafish Proteins / metabolism

Substances

  • Carrier Proteins
  • Multiprotein Complexes
  • Zebrafish Proteins

Grants and funding

This work was supported by Chinese Academy of Sciences (XDA01010107), National Basic Research Program of China (2012CB945003), National Natural Science Foundation of China (31330045, 31271427 and 31471323), and Shanghai Municipal Science and Technology Commission (12JC1409900). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.