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

Authors

  • Katharina Von Kriegstein,

    1. Abteilung Molekulare Neurobiologie, MPI für experimentelle Medizin, 37075 Göttingen, Germany
    Search for more papers by this author
  • Frank Schmitz,

    1. Abteilung Molekulare Neurobiologie, MPI für experimentelle Medizin, 37075 Göttingen, Germany
    2. Center for Basic Neuroscience, Department of Molecular Genetics, and Howard Hughes Medical Institute, The University of Texas South-Western Medical School, 5323 Harry Hines Blvd., Dallas TX 75235–9050, USA
    Search for more papers by this author
  • Egenhard Link,

    Search for more papers by this author
    • *

      Present address: Synaptic Systems GmbH, Rudolf-Wissell-Str. 28, 37079 Göttingen, Germany

  • Thomas C. Südhof

    1. Abteilung Molekulare Neurobiologie, MPI für experimentelle Medizin, 37075 Göttingen, Germany
    Search for more papers by this author

Professor Thomas C. Südhof, as above.
E-mail: TSudho@Mednet.SWMED.edu

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.

Ancillary