Distribution of synaptic vesicle proteins in the mammalian retina identifies obligatory and facultative components of ribbon synapses

Eur J Neurosci. 1999 Apr;11(4):1335-48. doi: 10.1046/j.1460-9568.1999.00542.x.

Abstract

The mammalian retina contains two synaptic layers. The outer plexiform layer (OPL) is primarily composed of ribbon synapses while the inner plexiform layer (IPL) comprises largely conventional synapses. In presynaptic terminals of ribbon synapses, electron-dense projections called ribbons are present at the synaptic plasma membranes. Ribbons bind synaptic vesicles and guide them to the synaptic membrane for fusion. In this manner, ribbons are thought to accelerate the delivery of vesicles for continuous exocytosis. In recent years, a large number of synaptic proteins has been described but it is not known if these protein colocalize in the same types of synapses. In previous studies, several proteins essential for synaptic function were not detected in ribbon synapses, suggesting that the mechanism of synaptic vesicle exocytosis may be very different in ribbon and conventional synapses. Using confocal laser scanning microscopy, we have now systematically investigated the protein composition of ribbon synapses. Our results show that, of the 19 synaptic proteins investigated, all except synapsin and rabphilin are obligatorily present in ribbon synapses. For example, rab3 which was reported to be absent from ribbon synapses, was found in bovine, rat and mouse ribbon synapses using multiple independent antibodies. In addition, we found staining in these synapses for PSD-95 and NMDA receptors, which suggested a similar design for the postsynaptic component in ribbon and conventional synapses. Our data show that ribbon synapses are more conventional in composition than reported, that most synaptic proteins are colocalized to the same type of synapse, and that synapsin and rabphilin are likely to be dispensible for basic synaptic functions.

MeSH terms

  • Animals
  • Cattle
  • Endocytosis / physiology
  • Eye Proteins / analysis*
  • GTP-Binding Proteins / analysis
  • Immunohistochemistry
  • Membrane Proteins*
  • Mice
  • Nerve Tissue Proteins / analysis*
  • Presynaptic Terminals / chemistry*
  • Rats
  • Retina / chemistry*
  • Retinal Rod Photoreceptor Cells / chemistry
  • Retinal Rod Photoreceptor Cells / ultrastructure
  • Synapsins / analysis
  • Synaptic Membranes / chemistry*
  • Synaptic Vesicles / chemistry*
  • Synaptosomal-Associated Protein 25
  • rab3 GTP-Binding Proteins

Substances

  • Eye Proteins
  • Membrane Proteins
  • Nerve Tissue Proteins
  • Snap25 protein, mouse
  • Snap25 protein, rat
  • Synapsins
  • Synaptosomal-Associated Protein 25
  • GTP-Binding Proteins
  • rab3 GTP-Binding Proteins