A human ciliopathy reveals essential functions for NEK10 in airway mucociliary clearance

Nat Med. 2020 Feb;26(2):244-251. doi: 10.1038/s41591-019-0730-x. Epub 2020 Jan 20.

Abstract

Mucociliary clearance, the physiological process by which mammalian conducting airways expel pathogens and unwanted surface materials from the respiratory tract, depends on the coordinated function of multiple specialized cell types, including basal stem cells, mucus-secreting goblet cells, motile ciliated cells, cystic fibrosis transmembrane conductance regulator (CFTR)-rich ionocytes, and immune cells1,2. Bronchiectasis, a syndrome of pathological airway dilation associated with impaired mucociliary clearance, may occur sporadically or as a consequence of Mendelian inheritance, for example in cystic fibrosis, primary ciliary dyskinesia (PCD), and select immunodeficiencies3. Previous studies have identified mutations that affect ciliary structure and nucleation in PCD4, but the regulation of mucociliary transport remains incompletely understood, and therapeutic targets for its modulation are lacking. Here we identify a bronchiectasis syndrome caused by mutations that inactivate NIMA-related kinase 10 (NEK10), a protein kinase with previously unknown in vivo functions in mammals. Genetically modified primary human airway cultures establish NEK10 as a ciliated-cell-specific kinase whose activity regulates the motile ciliary proteome to promote ciliary length and mucociliary transport but which is dispensable for normal ciliary number, radial structure, and beat frequency. Together, these data identify a novel and likely targetable signaling axis that controls motile ciliary function in humans and has potential implications for other respiratory disorders that are characterized by impaired mucociliary clearance.

Publication types

  • Case Reports
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Cell Separation
  • Child
  • Ciliopathies / immunology*
  • Ciliopathies / metabolism
  • Cystic Fibrosis Transmembrane Conductance Regulator / metabolism*
  • Epithelial Cells / metabolism
  • Exome
  • Female
  • Flow Cytometry
  • HEK293 Cells
  • Homozygote
  • Humans
  • Microscopy, Phase-Contrast
  • Microscopy, Video
  • Mucociliary Clearance*
  • Mutation
  • NIMA-Related Kinases / metabolism*
  • Phenotype
  • Proteome
  • Respiratory System
  • Tomography, X-Ray Computed
  • X-Ray Microtomography
  • Young Adult

Substances

  • CFTR protein, human
  • Proteome
  • Cystic Fibrosis Transmembrane Conductance Regulator
  • NIMA-Related Kinases
  • Nek10 protein, human