ZMYND10 functions in a chaperone relay during axonemal dynein assembly

Elife. 2018 Jun 19:7:e34389. doi: 10.7554/eLife.34389.

Abstract

Molecular chaperones promote the folding and macromolecular assembly of a diverse set of 'client' proteins. How ubiquitous chaperone machineries direct their activities towards specific sets of substrates is unclear. Through the use of mouse genetics, imaging and quantitative proteomics we uncover that ZMYND10 is a novel co-chaperone that confers specificity for the FKBP8-HSP90 chaperone complex towards axonemal dynein clients required for cilia motility. Loss of ZMYND10 perturbs the chaperoning of axonemal dynein heavy chains, triggering broader degradation of dynein motor subunits. We show that pharmacological inhibition of FKBP8 phenocopies dynein motor instability associated with the loss of ZMYND10 in airway cells and that human disease-causing variants of ZMYND10 disrupt its ability to act as an FKBP8-HSP90 co-chaperone. Our study indicates that primary ciliary dyskinesia (PCD), caused by mutations in dynein assembly factors disrupting cytoplasmic pre-assembly of axonemal dynein motors, should be considered a cell-type specific protein-misfolding disease.

Keywords: D. melanogaster; cell biology; chaperone; cilia; developmental biology; dynein; human; human disease; macromolecular assembly; mouse; proteastasis; regenerative medicine; stem cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Axoneme / metabolism*
  • Axoneme / ultrastructure
  • Base Sequence
  • Brain / cytology
  • Brain / metabolism
  • Cell Line
  • Cilia / metabolism*
  • Cilia / ultrastructure
  • Cytoskeletal Proteins
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • Dyneins / chemistry*
  • Dyneins / genetics
  • Dyneins / metabolism
  • Epithelial Cells / cytology
  • Epithelial Cells / metabolism
  • Gene Expression Regulation
  • HEK293 Cells
  • HSP90 Heat-Shock Proteins / genetics*
  • HSP90 Heat-Shock Proteins / metabolism
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Molecular Chaperones / genetics*
  • Molecular Chaperones / metabolism
  • Primary Cell Culture
  • Tacrolimus Binding Proteins / genetics*
  • Tacrolimus Binding Proteins / metabolism
  • Trachea / cytology
  • Trachea / metabolism

Substances

  • Cytoskeletal Proteins
  • DNA-Binding Proteins
  • Fkbp8 protein, mouse
  • HSP90 Heat-Shock Proteins
  • Molecular Chaperones
  • ZMYND10 protein, mouse
  • Dyneins
  • Tacrolimus Binding Proteins