A multiple piccolino-RIBEYE interaction supports plate-shaped synaptic ribbons in retinal neurons

Tanja M. Müller, Kaspar Gierke, Anneka Joachimsthaler, Heinrich Sticht, Zsuzsanna Izsvák, F. Kent Hamra, Anna Fejtová, Frauke Ackermann, Craig C. Garner, Jan Kremers, Johann H. Brandstätter, Hanna Regus-Leidig

Research output: Contribution to journalArticle

4 Scopus citations

Abstract

Active zones at chemical synapses are highly specialized sites for the regulated release of neurotransmitters. Despite a high degree of active zone protein conservation in vertebrates, every type of chemical synapse expresses a given set of protein isoforms and splice variants adapted to the demands on neurotransmitter release. So far, we know little about how specific active zone proteins contribute to the structural and functional diversity of active zones. In this study, we explored the nanodomain organization of ribbon-type active zones by addressing the significance of Piccolino, the ribbon synapse-specific splice variant of Piccolo, for shaping the ribbon structure. We followed up on previous results, which indicated that rod photoreceptor synaptic ribbons lose their structural integrity in a knockdown of Piccolino. Here, we demonstrate an interaction between Piccolino and the major ribbon component RIBEYE that supports plate-shaped synaptic ribbons in retinal neurons. In a detailed ultrastructural analysis of three different types of retinal ribbon synapses in Piccolo/Piccolino-deficient male and female rats, we show that the absence of Piccolino destabilizes the superstructure of plate-shaped synaptic ribbons, although with variable manifestation in the cell types examined. Our analysis illustrates how the expression of a specific active zone protein splice variant (e.g., Piccolino) contributes to structural diversity of vertebrate active zones.

Original languageEnglish (US)
Pages (from-to)2606-2619
Number of pages14
JournalJournal of Neuroscience
Volume39
Issue number14
DOIs
StatePublished - Apr 3 2019

    Fingerprint

Keywords

  • Active zone
  • Photoreceptor
  • Piccolino
  • RIBEYE
  • Ribbon synapse

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Müller, T. M., Gierke, K., Joachimsthaler, A., Sticht, H., Izsvák, Z., Hamra, F. K., Fejtová, A., Ackermann, F., Garner, C. C., Kremers, J., Brandstätter, J. H., & Regus-Leidig, H. (2019). A multiple piccolino-RIBEYE interaction supports plate-shaped synaptic ribbons in retinal neurons. Journal of Neuroscience, 39(14), 2606-2619. https://doi.org/10.1523/JNEUROSCI.2038-18.2019