Biallelic Mutations in LRRC56, Encoding a Protein Associated with Intraflagellar Transport, Cause Mucociliary Clearance and Laterality Defects

Am J Hum Genet. 2018 Nov 1;103(5):727-739. doi: 10.1016/j.ajhg.2018.10.003.

Abstract

Primary defects in motile cilia result in dysfunction of the apparatus responsible for generating fluid flows. Defects in these mechanisms underlie disorders characterized by poor mucus clearance, resulting in susceptibility to chronic recurrent respiratory infections, often associated with infertility; laterality defects occur in about 50% of such individuals. Here we report biallelic variants in LRRC56 (known as oda8 in Chlamydomonas) identified in three unrelated families. The phenotype comprises laterality defects and chronic pulmonary infections. High-speed video microscopy of cultured epithelial cells from an affected individual showed severely dyskinetic cilia but no obvious ultra-structural abnormalities on routine transmission electron microscopy (TEM). Further investigation revealed that LRRC56 interacts with the intraflagellar transport (IFT) protein IFT88. The link with IFT was interrogated in Trypanosoma brucei. In this protist, LRRC56 is recruited to the cilium during axoneme construction, where it co-localizes with IFT trains and is required for the addition of dynein arms to the distal end of the flagellum. In T. brucei carrying LRRC56-null mutations, or a variant resulting in the p.Leu259Pro substitution corresponding to the p.Leu140Pro variant seen in one of the affected families, we observed abnormal ciliary beat patterns and an absence of outer dynein arms restricted to the distal portion of the axoneme. Together, our findings confirm that deleterious variants in LRRC56 result in a human disease and suggest that this protein has a likely role in dynein transport during cilia assembly that is evolutionarily important for cilia motility.

Keywords: cilia; ciliopathies; dynein arms; flagella; intraflagellar transport; left-right asymmetry; leucine-rich repeat protein; trypanosome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Alleles
  • Axoneme / genetics
  • Biological Transport / genetics*
  • Cell Line
  • Chlamydomonas / genetics
  • Cilia / genetics
  • Dyneins / genetics
  • Epithelial Cells / pathology
  • Female
  • Flagella / genetics*
  • HEK293 Cells
  • Humans
  • Infant
  • Male
  • Mucociliary Clearance / genetics*
  • Mutation / genetics*
  • Phenotype
  • Proteins / genetics*
  • Trypanosoma brucei brucei / genetics

Substances

  • Proteins
  • Dyneins