Hypomorphic CEP290/NPHP6 mutations result in anosmia caused by the selective loss of G proteins in cilia of olfactory sensory neurons

Proc Natl Acad Sci U S A. 2007 Oct 2;104(40):15917-22. doi: 10.1073/pnas.0704140104. Epub 2007 Sep 26.

Abstract

Cilia regulate diverse functions such as motility, fluid balance, and sensory perception. The cilia of olfactory sensory neurons (OSNs) compartmentalize the signaling proteins necessary for odor detection; however, little is known regarding the mechanisms of protein sorting/entry into olfactory cilia. Nephrocystins are a family of ciliary proteins likely involved in cargo sorting during transport from the basal body to the ciliary axoneme. In humans, loss-of-function of the cilia-centrosomal protein CEP290/NPHP6 is associated with Joubert and Meckel syndromes, whereas hypomorphic mutations result in Leber congenital amaurosis (LCA), a form of early-onset retinal dystrophy. Here, we report that CEP290-LCA patients exhibit severely abnormal olfactory function. In a mouse model with hypomorphic mutations in CEP290 [retinal dystrophy-16 mice (rd16)], electro-olfactogram recordings revealed an anosmic phenotype analogous to that of CEP290-LCA patients. Despite the loss of olfactory function, cilia of OSNs remained intact in the rd16 mice. As in wild type, CEP290 localized to dendritic knobs of rd16 OSNs, where it was in complex with ciliary transport proteins and the olfactory G proteins G(olf) and Ggamma(13). Interestingly, we observed defective ciliary localization of G(olf) and Ggamma(13) but not of G protein-coupled odorant receptors or other components of the odorant signaling pathway in the rd16 OSNs. Our data implicate distinct mechanisms for ciliary transport of olfactory signaling proteins, with CEP290 being a key mediator involved in G protein trafficking. The assessment of olfactory function can, therefore, serve as a useful diagnostic tool for genetic screening of certain syndromic ciliary diseases.

Publication types

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

MeSH terms

  • Alternative Splicing
  • Animals
  • Antigens, Neoplasm / genetics*
  • Cell Cycle Proteins
  • Cytoskeletal Proteins
  • Disease Models, Animal
  • Female
  • GTP-Binding Proteins / deficiency*
  • Genetic Carrier Screening
  • Humans
  • Male
  • Mice
  • Mutation
  • Neoplasm Proteins / genetics*
  • Neurons, Afferent / pathology*
  • Nuclear Proteins / genetics*
  • Olfaction Disorders / genetics*
  • Olfactory Mucosa / pathology
  • Olfactory Mucosa / physiology
  • Olfactory Pathways / pathology*
  • Sequence Deletion
  • Smell / genetics
  • Smell / physiology

Substances

  • Antigens, Neoplasm
  • Cell Cycle Proteins
  • Cep290 protein, human
  • Cep290 protein, mouse
  • Cytoskeletal Proteins
  • Neoplasm Proteins
  • Nuclear Proteins
  • GTP-Binding Proteins