PUBLICATION

Dysfunction of the ciliary ARMC9/TOGARAM1 protein module causes Joubert syndrome

Authors
Latour, B.L., Van De Weghe, J.C., Rusterholz, T.D., Letteboer, S.J., Gomez, A., Shaheen, R., Gesemann, M., Karamzade, A., Asadollahi, M., Barroso-Gil, M., Chitre, M., Grout, M.E., van Reeuwijk, J., van Beersum, S.E., Miller, C.V., Dempsey, J.C., Morsy, H., Bamshad, M.J., Nickerson, D.A., Neuhauss, S.C., Boldt, K., Ueffing, M., Keramatipour, M., Sayer, J.A., Alkuraya, F.S., Bachmann-Gagescu, R., Roepman, R., Doherty, D.
ID
ZDB-PUB-200527-4
Date
2020
Source
The Journal of Clinical Investigation   130(8): 4423-4439 (Journal)
Registered Authors
Bachmann-Gagescu, Ruxandra, Gesemann, Matthias, Neuhauss, Stephan, Rusterholz, Tamara, Sayer, John A.
Keywords
Genetic diseases, Genetics, Proteomics
MeSH Terms
  • Abnormalities, Multiple*/genetics
  • Abnormalities, Multiple*/metabolism
  • Acetylation
  • Animals
  • Armadillo Domain Proteins*/genetics
  • Armadillo Domain Proteins*/metabolism
  • CRISPR-Cas Systems
  • Cerebellum/abnormalities*
  • Cerebellum/metabolism
  • Cilia*/genetics
  • Cilia*/metabolism
  • Disease Models, Animal
  • Eye Abnormalities*/genetics
  • Eye Abnormalities*/metabolism
  • Humans
  • Kidney Diseases, Cystic*/genetics
  • Kidney Diseases, Cystic*/metabolism
  • Peptides/genetics
  • Peptides/metabolism
  • Retina/abnormalities*
  • Retina/metabolism
  • Zebrafish*/genetics
  • Zebrafish*/metabolism
  • Zebrafish Proteins*/genetics
  • Zebrafish Proteins*/metabolism
PubMed
32453716 Full text @ Journal of Clin. Invest.
Abstract
Joubert syndrome (JBTS) is a recessive neurodevelopmental ciliopathy, characterized by a pathognomonic hindbrain malformation. All known JBTS-genes encode proteins involved in the structure or function of primary cilia, ubiquitous antenna-like organelles essential for cellular signal transduction. Here, we use the recently identified JBTS-associated protein ARMC9 in tandem-affinity purification and yeast two-hybrid screens to identify a novel ciliary module whose dysfunction underlies JBTS. In addition to known JBTS-associated proteins CEP104 and CSPP1, we identify CCDC66 and TOGARAM1 as ARMC9 interaction partners. We show that TOGARAM1 variants cause JBTS and disrupt TOGARAM1 interaction with ARMC9. Using a combination of protein interaction analyses and characterization of patient-derived fibroblasts, CRISPR/Cas9-engineered zebrafish and hTERT-RPE1 cells, we demonstrate that dysfunction of ARMC9 or TOGARAM1 results in short cilia with decreased axonemal acetylation and polyglutamylation, but relatively intact transition zone function. Aberrant cold- and serum-induced ciliary loss in both ARMC9 and TOGARAM1 patient cell lines suggests a role for this new JBTS-associated protein module in ciliary stability.
Genes / Markers
Figures
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Expression
Phenotype
Mutations / Transgenics
Human Disease / Model
Sequence Targeting Reagents
Fish
Antibodies
Orthology
Engineered Foreign Genes
Mapping