Negative regulation of the novel norpA(P24) suppressor, diehard4, in the endo-lysosomal trafficking underlies photoreceptor cell degeneration

PLoS Genet. 2013 Jun;9(6):e1003559. doi: 10.1371/journal.pgen.1003559. Epub 2013 Jun 6.

Abstract

Rhodopsin has been used as a prototype system to investigate G protein-coupled receptor (GPCR) internalization and endocytic sorting mechanisms. Failure of rhodopsin recycling upon light activation results in various degenerative retinal diseases. Accumulation of internalized rhodopsin in late endosomes and the impairment of its lysosomal degradation are associated with unregulated cell death that occurs in dystrophies. However, the molecular basis of rhodopsin accumulation remains elusive. We found that the novel norpA(P24) suppressor, diehard4, is responsible for the inability of endo-lysosomal rhodopsin trafficking and retinal degeneration in Drosophila models of retinal dystrophies. We found that diehard4 encodes Osiris 21. Loss of its function suppresses retinal degeneration in norpA(P24), rdgC(306), and trp(1), but not in rdgB(2), suggesting a common cause of photoreceptor death. In addition, the loss of Osiris 21 function shifts the membrane balance between late endosomes and lysosomes as evidenced by smaller late endosomes and the proliferation of lysosomal compartments, thus facilitating the degradation of endocytosed rhodopsin. Our results demonstrate the existence of negative regulation in vesicular traffic between endosomes and lysosomes. We anticipate that the identification of additional components and an in-depth description of this specific molecular machinery will aid in therapeutic interventions of various retinal dystrophies and GPCR-related human diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Disease Models, Animal
  • Drosophila Proteins / antagonists & inhibitors
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster
  • Endocytosis / genetics*
  • Endosomes / genetics
  • Endosomes / metabolism
  • Humans
  • Lysosomes / genetics
  • Lysosomes / metabolism
  • Membrane Proteins / genetics*
  • Phospholipase C beta / antagonists & inhibitors
  • Phospholipase C beta / genetics*
  • Phospholipase C beta / metabolism
  • Photoreceptor Cells, Invertebrate / metabolism
  • Photoreceptor Cells, Invertebrate / pathology
  • Retinal Dystrophies / genetics*
  • Retinal Dystrophies / metabolism
  • Retinal Dystrophies / pathology
  • Rhodopsin / genetics*
  • Rhodopsin / metabolism
  • Vesicular Transport Proteins / genetics
  • Vesicular Transport Proteins / metabolism

Substances

  • Drosophila Proteins
  • Membrane Proteins
  • Osi21 protein, Drosophila
  • Vesicular Transport Proteins
  • Rhodopsin
  • NorpA protein, Drosophila
  • Phospholipase C beta

Grants and funding

This research was partly supported by the Basic Science Research Program (2011-0026739) through the National Research Foundation of Korea (NRF), funded by the Ministry of Education, Science and Technology, the Republic of Korea. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.