PUBLICATION

NINL and DZANK1 Co-function in Vesicle Transport and Are Essential for Photoreceptor Development in Zebrafish

Authors
Dona, M., Bachmann-Gagescu, R., Texier, Y., Toedt, G., Hetterschijt, L., Tonnaer, E.L., Peters, T.A., van Beersum, S.E., Bergboer, J.G., Horn, N., de Vrieze, E., Slijkerman, R.W., van Reeuwijk, J., Flik, G., Keunen, J.E., Ueffing, M., Gibson, T.J., Roepman, R., Boldt, K., Kremer, H., van Wijk, E.
ID
ZDB-PUB-151021-4
Date
2015
Source
PLoS Genetics   11: e1005574 (Journal)
Registered Authors
Bachmann-Gagescu, Ruxandra, de Vrieze, Erik, Dona, Margo, Flik, Gert, Hetterschijt, Lisette, Kremer, Hannie, Slijkerman, Ralph, van Wijk, Erwin
Keywords
Larvae, Dyneins, Photoreceptors, Zebrafish, Motor proteins, Cilia, Vesicles, Retina
MeSH Terms
  • Animals
  • Biological Transport/genetics
  • Carrier Proteins/genetics*
  • Cilia/genetics
  • Dyneins/genetics*
  • HEK293 Cells
  • Humans
  • Larva/genetics*
  • Larva/growth & development
  • Microtubule-Associated Proteins/genetics*
  • Neurogenesis/genetics
  • Nuclear Proteins/genetics*
  • Photoreceptor Cells, Vertebrate*
  • Proteomics
  • Retina/growth & development*
  • Signal Transduction
  • Zebrafish/genetics
  • Zebrafish/growth & development
  • Zebrafish Proteins/genetics*
PubMed
26485514 Full text @ PLoS Genet.
Abstract
Ciliopathies are Mendelian disorders caused by dysfunction of cilia, ubiquitous organelles involved in fluid propulsion (motile cilia) or signal transduction (primary cilia). Retinal dystrophy is a common phenotypic characteristic of ciliopathies since photoreceptor outer segments are specialized primary cilia. These ciliary structures heavily rely on intracellular minus-end directed transport of cargo, mediated at least in part by the cytoplasmic dynein 1 motor complex, for their formation, maintenance and function. Ninein-like protein (NINL) is known to associate with this motor complex and is an important interaction partner of the ciliopathy-associated proteins lebercilin, USH2A and CC2D2A. Here, we scrutinize the function of NINL with combined proteomic and zebrafish in vivo approaches. We identify Double Zinc Ribbon and Ankyrin Repeat domains 1 (DZANK1) as a novel interaction partner of NINL and show that loss of Ninl, Dzank1 or both synergistically leads to dysmorphic photoreceptor outer segments, accumulation of trans-Golgi-derived vesicles and mislocalization of Rhodopsin and Ush2a in zebrafish. In addition, retrograde melanosome transport is severely impaired in zebrafish lacking Ninl or Dzank1. We further demonstrate that NINL and DZANK1 are essential for intracellular dynein-based transport by associating with complementary subunits of the cytoplasmic dynein 1 motor complex, thus shedding light on the structure and stoichiometry of this important motor complex. Altogether, our results support a model in which the NINL-DZANK1 protein module is involved in the proper assembly and folding of the cytoplasmic dynein 1 motor complex in photoreceptor cells, a process essential for outer segment formation and function.
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Human Disease / Model
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