Loss-of-function mutations in LRRC6, a gene essential for proper axonemal assembly of inner and outer dynein arms, cause primary ciliary dyskinesia

Am J Hum Genet. 2012 Nov 2;91(5):958-64. doi: 10.1016/j.ajhg.2012.10.003.

Abstract

Primary ciliary dyskinesia (PCD) is a group of autosomal-recessive disorders resulting from cilia and sperm-flagella defects, which lead to respiratory infections and male infertility. Most implicated genes encode structural proteins that participate in the composition of axonemal components, such as dynein arms (DAs), that are essential for ciliary and flagellar movements; they explain the pathology in fewer than half of the affected individuals. We undertook this study to further understand the pathogenesis of PCD due to the absence of both DAs. We identified, via homozygosity mapping, an early frameshift in LRRC6, a gene that encodes a leucine-rich-repeat (LRR)-containing protein. Subsequent analyses of this gene mainly expressed in testis and respiratory cells identified biallelic mutations in several independent individuals. The situs inversus observed in two of them supports a key role for LRRC6 in embryonic nodal cilia. Study of native LRRC6 in airway epithelial cells revealed that it localizes to the cytoplasm and within cilia, whereas it is absent from cells with loss-of-function mutations, in which DA protein markers are also missing. These results are consistent with the transmission-electron-microscopy data showing the absence of both DAs in cilia or flagella from individuals with LRRC6 mutations. In spite of structural and functional similarities between LRRC6 and DNAAF1, another LRR-containing protein involved in the same PCD phenotype, the two proteins are not redundant. The evolutionarily conserved LRRC6, therefore, emerges as an additional player in DA assembly, a process that is essential for proper axoneme building and that appears to be much more complex than was previously thought.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Amino Acid Sequence
  • Axonemal Dyneins / genetics*
  • Axonemal Dyneins / metabolism
  • Cilia / genetics
  • Cilia / pathology
  • Consanguinity
  • Consensus Sequence
  • Cytoskeletal Proteins
  • Female
  • Fertility / genetics
  • Gene Order
  • Humans
  • Kartagener Syndrome / genetics*
  • Kartagener Syndrome / metabolism
  • Male
  • Molecular Sequence Data
  • Mutation*
  • Phenotype
  • Protein Transport
  • Proteins / chemistry
  • Proteins / genetics*
  • Proteins / metabolism
  • Sequence Alignment
  • Sperm Tail / metabolism
  • Sperm Tail / pathology

Substances

  • Cytoskeletal Proteins
  • LRRC6 protein, human
  • Proteins
  • Axonemal Dyneins