Mutations in PIH1D3 Cause X-Linked Primary Ciliary Dyskinesia with Outer and Inner Dynein Arm Defects

  • Am J Hum Genet. 2017 Jan 5;100(1):160-168. doi: 10.1016/j.ajhg.2016.11.019.
Tamara Paff  1 ,  Niki T Loges  2 ,  Isabella Aprea  2 ,  Kaman Wu  3 ,  Zeineb Bakey  3 ,  Eric G Haarman  4 ,  Johannes M A Daniels  5 ,  Erik A Sistermans  6 ,  Natalija Bogunovic  7 ,  Gerard W Dougherty  2 ,  Inga M Höben  2 ,  Jörg Große-Onnebrink  2 ,  Anja Matter  2 ,  Heike Olbrich  2 ,  Claudius Werner  2 ,  Gerard Pals  6 ,  Miriam Schmidts  8 ,  Heymut Omran  2 ,  Dimitra Micha  9
Affiliations
  • 1. Department of Pulmonary Diseases, VU University Medical Center, 1007 MB Amsterdam, the Netherlands; Department of Paediatric Pulmonology, VU University Medical Center, 1007 MB Amsterdam, the Netherlands; Department of Clinical Genetics, VU University Medical Center, 1007 MB Amsterdam, the Netherlands.
  • 2. Department of General Pediatrics, University Children's Hospital Muenster, 48149 Muenster, Germany.
  • 3. Department of Human Genetics, Radboud University Nijmegen Medical Centre, 6500 HB Nijmegen, the Netherlands.
  • 4. Department of Paediatric Pulmonology, VU University Medical Center, 1007 MB Amsterdam, the Netherlands.
  • 5. Department of Pulmonary Diseases, VU University Medical Center, 1007 MB Amsterdam, the Netherlands.
  • 6. Department of Clinical Genetics, VU University Medical Center, 1007 MB Amsterdam, the Netherlands.
  • 7. Department of Surgery and Physiology, Amsterdam Cardiovascular Sciences, VU University Medical Center, 1007 MB Amsterdam, the Netherlands.
  • 8. Department of Human Genetics, Radboud University Nijmegen Medical Centre, 6500 HB Nijmegen, the Netherlands; Pediatric Genetics Division, Center for Pediatrics and Adolescent Medicine, University Hospital Freiburg, 79110 Freiburg, Germany.
  • 9. Department of Clinical Genetics, VU University Medical Center, 1007 MB Amsterdam, the Netherlands. Electronic address: [email protected].
Abstract

Defects in motile cilia and sperm flagella cause primary ciliary dyskinesia (PCD), characterized by chronic airway disease, infertility, and left-right body axis disturbance. Here we report maternally inherited and de novo mutations in PIH1D3 in four men affected with PCD. PIH1D3 is located on the X chromosome and is involved in the preassembly of both outer (ODA) and inner (IDA) dynein arms of cilia and sperm flagella. Loss-of-function mutations in PIH1D3 lead to absent ODAs and reduced to absent IDAs, causing ciliary and flagellar immotility. Further, PIH1D3 interacts and co-precipitates with cytoplasmic ODA/IDA assembly factors DNAAF2 and DNAAF4. This result has clinical and genetic counseling implications for genetically unsolved male case subjects with a classic PCD phenotype that lack additional phenotypes such as intellectual disability or retinitis pigmentosa.