Endophilin Promotes a Late Step in Endocytosis at Glial Invaginations in Drosophila Photoreceptor Terminals

Ruth Fabian-Fine, Patrik Verstreken, P. Robin Hiesinger, Jane Anne Horne, Rita Kostyleva, Yi Zhou, Hugo J. Bellen, Ian A. Meinertzhagen

Research output: Contribution to journalArticle

72 Citations (Scopus)

Abstract

Retrieval of synaptic vesicles from the membrane of neurons is crucial to maintain normal rates of neurotransmitter release. Photoreceptor terminals of the fly's eye release neurotransmitter in a tonic manner. They therefore rely heavily on vesicle regeneration. Null mutations in endophilin (endo) block clathrin-mediated endocytosis at the Drosophila neuromuscular junction, where previous analysis of hypomorphic mutations has suggested a function for Endophilin (Endo) before vesicle fission, during membrane bending. Here, at fly photoreceptor synapses, we show that Endo is localized to synaptic vesicles at sites of endocytosis that are glial invaginations called capitate projections, and that when the photoreceptor synapses lack Endo they are impaired in their ability to release neurotransmitter. Detailed ultrastructural analysis of endo null mutant photoreceptor synapses fails to reveal a defect at early stages of vesicle reformation but, instead, reveals an accumulation of clusters of electron-dense, apparently nonfunctional, late endocytotic vesicles. Using dynamin; endo double-mutant photoreceptors, we provide further evidence that ultimately the function of Endophilin is required late in endocytosis, allowing vesicles to progress through the synaptic vesicle cycle.

Original languageEnglish (US)
Pages (from-to)10732-10744
Number of pages13
JournalJournal of Neuroscience
Volume23
Issue number33
StatePublished - Nov 19 2003

Fingerprint

Synaptic Vesicles
Endocytosis
Neuroglia
Synapses
Drosophila
Neurotransmitter Agents
Diptera
Dynamins
Synaptic Membranes
Clathrin
Mutation
Neuromuscular Junction
Regeneration
Electrons
Neurons
Membranes

Keywords

  • Capitate projection
  • Clathrin
  • Endocytosis
  • Endophilin
  • Glia
  • Vesicle cycle

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Fabian-Fine, R., Verstreken, P., Hiesinger, P. R., Horne, J. A., Kostyleva, R., Zhou, Y., ... Meinertzhagen, I. A. (2003). Endophilin Promotes a Late Step in Endocytosis at Glial Invaginations in Drosophila Photoreceptor Terminals. Journal of Neuroscience, 23(33), 10732-10744.

Endophilin Promotes a Late Step in Endocytosis at Glial Invaginations in Drosophila Photoreceptor Terminals. / Fabian-Fine, Ruth; Verstreken, Patrik; Hiesinger, P. Robin; Horne, Jane Anne; Kostyleva, Rita; Zhou, Yi; Bellen, Hugo J.; Meinertzhagen, Ian A.

In: Journal of Neuroscience, Vol. 23, No. 33, 19.11.2003, p. 10732-10744.

Research output: Contribution to journalArticle

Fabian-Fine, R, Verstreken, P, Hiesinger, PR, Horne, JA, Kostyleva, R, Zhou, Y, Bellen, HJ & Meinertzhagen, IA 2003, 'Endophilin Promotes a Late Step in Endocytosis at Glial Invaginations in Drosophila Photoreceptor Terminals', Journal of Neuroscience, vol. 23, no. 33, pp. 10732-10744.
Fabian-Fine R, Verstreken P, Hiesinger PR, Horne JA, Kostyleva R, Zhou Y et al. Endophilin Promotes a Late Step in Endocytosis at Glial Invaginations in Drosophila Photoreceptor Terminals. Journal of Neuroscience. 2003 Nov 19;23(33):10732-10744.
Fabian-Fine, Ruth ; Verstreken, Patrik ; Hiesinger, P. Robin ; Horne, Jane Anne ; Kostyleva, Rita ; Zhou, Yi ; Bellen, Hugo J. ; Meinertzhagen, Ian A. / Endophilin Promotes a Late Step in Endocytosis at Glial Invaginations in Drosophila Photoreceptor Terminals. In: Journal of Neuroscience. 2003 ; Vol. 23, No. 33. pp. 10732-10744.
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