Mutations in human homologue of chicken talpid3 gene (KIAA0586) cause a hybrid ciliopathy with overlapping features of Jeune and Joubert syndromes

J Med Genet. 2015 Dec;52(12):830-9. doi: 10.1136/jmedgenet-2015-103316. Epub 2015 Sep 18.

Abstract

Background: In chicken, loss of TALPID3 results in non-functional cilia and short-rib polydactyly syndrome. This phenotype is caused by a frameshift mutation in the chicken ortholog of the human KIAA0586 gene, which encodes a novel coiled-coil domain protein essential for primary ciliogenesis, suggesting that KIAA0586 can be associated with ciliopathy in human beings.

Methods: In our patients with ciliopathy (http://www.clinicaltrials.gov: NCT00068224), we have collected extensive clinical and neuroimaging data from affected individuals, and performed whole exome sequencing on DNA from affected individuals and their parents. We analysed gene expression on fibroblast cell line, and determined the effect of gene mutation on ciliogenesis in cells derived from patients.

Results: We identified biallelic mutations in the human TALPID3 ortholog, KIAA0586, in six children with findings of overlapping Jeune and Joubert syndromes. Fibroblasts cultured from one of the patients with Jeune-Joubert syndrome exhibited more severe cilia defects than fibroblasts from patients with only Joubert syndrome; this difference was reflected in KIAA0586 RNA expression levels. Rescue of the cilia defect with full-length wild type KIAA0586 indicated a causal link between cilia formation and KIAA0586 function.

Conclusions: Our results show that biallelic deleterious mutations in KIAA0586 lead to Joubert syndrome with or without Jeune asphyxiating thoracic dystrophy. Furthermore, our results confirm that KIAA0586/TALPID3 is essential in cilia formation in human beings, expand the KIAA0586 phenotype to include features of Jeune syndrome and provide a pathogenetic connection between Joubert and Jeune syndromes, based on aberrant ciliogenesis.

Keywords: Clinical genetics; Developmental; ciliopathy; small thorax; whole exome sequencing.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Abnormalities, Multiple / genetics*
  • Animals
  • Base Sequence
  • Cell Cycle Proteins / genetics*
  • Cell Cycle Proteins / metabolism
  • Cells, Cultured
  • Cerebellum / abnormalities*
  • Chickens / genetics
  • Child
  • Child, Preschool
  • Cilia / pathology
  • DNA Mutational Analysis
  • Ellis-Van Creveld Syndrome / genetics*
  • Eye Abnormalities / genetics*
  • Female
  • Fibroblasts / pathology
  • Frameshift Mutation
  • Gene Expression
  • Humans
  • Kidney Diseases, Cystic / genetics*
  • Male
  • Pedigree
  • Primary Cell Culture
  • Retina / abnormalities*

Substances

  • Cell Cycle Proteins
  • KIAA0586 protein, human

Supplementary concepts

  • Agenesis of Cerebellar Vermis
  • Jeune syndrome

Associated data

  • ClinicalTrials.gov/NCT00068224