The nucleoside-diphosphate kinase NME3 associates with nephronophthisis proteins and is required for ciliary function during renal development

J Biol Chem. 2018 Sep 28;293(39):15243-15255. doi: 10.1074/jbc.RA117.000847. Epub 2018 Aug 15.

Abstract

Nephronophthisis (NPH) is an autosomal recessive renal disease leading to kidney failure in children and young adults. The protein products of the corresponding genes (NPHPs) are localized in primary cilia or their appendages. Only about 70% of affected individuals have a mutation in one of 100 renal ciliopathy genes, and no unifying pathogenic mechanism has been identified. Recently, some NPHPs, including NIMA-related kinase 8 (NEK8) and centrosomal protein 164 (CEP164), have been found to act in the DNA-damage response pathway and to contribute to genome stability. Here, we show that NME/NM23 nucleoside-diphosphate kinase 3 (NME3) that has recently been found to facilitate DNA-repair mechanisms binds to several NPHPs, including NEK8, CEP164, and ankyrin repeat and sterile α motif domain-containing 6 (ANKS6). Depletion of nme3 in zebrafish and Xenopus resulted in typical ciliopathy-associated phenotypes, such as renal malformations and left-right asymmetry defects. We further found that endogenous NME3 localizes to the basal body and that it associates also with centrosomal proteins, such as NEK6, which regulates cell cycle arrest after DNA damage. The ciliopathy-typical manifestations of NME3 depletion in two vertebrate in vivo models, the biochemical association of NME3 with validated NPHPs, and its localization to the basal body reveal a role for NME3 in ciliary function. We conclude that mutations in the NME3 gene may aggravate the ciliopathy phenotypes observed in humans.

Keywords: DNA damage response; Xenopus; ciliopathies; kidney; nephronophthisis; nucleoside/nucleotide metabolism; primary cilium; zebrafish.

Publication types

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

MeSH terms

  • Animals
  • Cell Cycle Checkpoints / genetics
  • Cilia / genetics
  • Cilia / pathology
  • Ciliopathies / genetics*
  • Ciliopathies / physiopathology
  • DNA Damage / genetics
  • DNA Repair / genetics
  • Disease Models, Animal
  • Humans
  • Kidney / pathology
  • Kidney Diseases, Cystic / congenital*
  • Kidney Diseases, Cystic / genetics
  • Kidney Diseases, Cystic / pathology
  • Microtubule Proteins / genetics
  • NIMA-Related Kinases / genetics
  • NM23 Nucleoside Diphosphate Kinases / genetics*
  • Nuclear Proteins / genetics
  • Renal Insufficiency / genetics*
  • Renal Insufficiency / pathology
  • Xenopus / genetics
  • Zebrafish / genetics

Substances

  • ANKS6 protein, human
  • CEP164 protein, human
  • Microtubule Proteins
  • NM23 Nucleoside Diphosphate Kinases
  • Nuclear Proteins
  • NEK6 protein, human
  • NEK8 protein, human
  • NIMA-Related Kinases
  • NME3 protein, human

Supplementary concepts

  • Nephronophthisis, familial juvenile