Human IFT52 mutations uncover a novel role for the protein in microtubule dynamics and centrosome cohesion

Hum Mol Genet. 2019 Aug 15;28(16):2720-2737. doi: 10.1093/hmg/ddz091.

Abstract

Mutations in genes encoding components of the intraflagellar transport (IFT) complexes have previously been associated with a spectrum of diseases collectively termed ciliopathies. Ciliopathies relate to defects in the formation or function of the cilium, a sensory or motile organelle present on the surface of most cell types. IFT52 is a key component of the IFT-B complex and ensures the interaction of the two subcomplexes, IFT-B1 and IFT-B2. Here, we report novel IFT52 biallelic mutations in cases with a short-rib thoracic dysplasia (SRTD) or a congenital anomaly of kidney and urinary tract (CAKUT). Combining in vitro and in vivo studies in zebrafish, we showed that SRTD-associated missense mutation impairs IFT-B complex assembly and IFT-B2 ciliary localization, resulting in decreased cilia length. In comparison, CAKUT-associated missense mutation has a mild pathogenicity, thus explaining the lack of skeletal defects in CAKUT case. In parallel, we demonstrated that the previously reported homozygous nonsense IFT52 mutation associated with Sensenbrenner syndrome [Girisha et al. (2016) A homozygous nonsense variant in IFT52 is associated with a human skeletal ciliopathy. Clin. Genet., 90, 536-539] leads to exon skipping and results in a partially functional protein. Finally, our work uncovered a novel role for IFT52 in microtubule network regulation. We showed that IFT52 interacts and partially co-localized with centrin at the distal end of centrioles where it is involved in its recruitment and/or maintenance. Alteration of this function likely contributes to centriole splitting observed in Ift52-/- cells. Altogether, our findings allow a better comprehensive genotype-phenotype correlation among IFT52-related cases and revealed a novel, extra-ciliary role for IFT52, i.e. disruption may contribute to pathophysiological mechanisms.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Animals, Genetically Modified
  • Carrier Proteins / chemistry
  • Carrier Proteins / genetics*
  • Carrier Proteins / metabolism
  • Centrosome / metabolism*
  • Child
  • Child, Preschool
  • Cilia / metabolism
  • Consanguinity
  • DNA Mutational Analysis
  • Exome Sequencing
  • Female
  • Genetic Association Studies*
  • Genetic Predisposition to Disease*
  • Genotype
  • Homozygote
  • Humans
  • Infant
  • Intracellular Signaling Peptides and Proteins
  • Male
  • Microtubules / metabolism*
  • Mutation*
  • Pedigree
  • Phenotype
  • Protein Binding
  • Protein Interaction Domains and Motifs / genetics
  • Trimethoprim, Sulfamethoxazole Drug Combination / metabolism
  • Zebrafish

Substances

  • Carrier Proteins
  • IFT52 protein, human
  • Intracellular Signaling Peptides and Proteins
  • Trimethoprim, Sulfamethoxazole Drug Combination