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Presynaptic spinophilin tunes neurexin signalling to control active zone architecture and function

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  • Karzan Muhammad

    (Freie Universität Berlin, Institute for Biology/Genetics
    NeuroCure, Charité
    Present address: Max Planck Institute for Brain Research, Neocortical Circuits Lab, Max-von-Laue-Str. 4, 60438 Frankfurt, Germany)

  • Suneel Reddy-Alla

    (Freie Universität Berlin, Institute for Biology/Genetics
    NeuroCure, Charité)

  • Jan H Driller

    (Freie Universität Berlin, Institut für Chemie und Biochemie /Strukturbiochmie)

  • Dietmar Schreiner

    (Biozentrum, University of Basel)

  • Ulises Rey

    (NeuroCure, Charité)

  • Mathias A. Böhme

    (NeuroCure, Charité)

  • Christina Hollmann

    (NeuroCure, Charité)

  • Niraja Ramesh

    (Freie Universität Berlin, Institute for Biology/Genetics)

  • Harald Depner

    (Freie Universität Berlin, Institute for Biology/Genetics
    NeuroCure, Charité)

  • Janine Lützkendorf

    (NeuroCure, Charité)

  • Tanja Matkovic

    (Freie Universität Berlin, Institute for Biology/Genetics
    NeuroCure, Charité)

  • Torsten Götz

    (Freie Universität Berlin, Institute for Biology/Genetics
    NeuroCure, Charité)

  • Dominique D. Bergeron

    (NeuroCure, Charité)

  • Jan Schmoranzer

    (Freie Universität Berlin, Institut für Chemie und Biochemie /Strukturbiochmie
    Leibniz Institut für Molekulare Pharmakologie)

  • Fabian Goettfert

    (Max Planck Institute for Biophysical Chemistry)

  • Mathew Holt

    (VIB Center for the Biology of Disease)

  • Markus C. Wahl

    (Freie Universität Berlin, Institut für Chemie und Biochemie /Strukturbiochmie)

  • Stefan W. Hell

    (Max Planck Institute for Biophysical Chemistry)

  • Peter Scheiffele

    (Biozentrum, University of Basel)

  • Alexander M. Walter

    (NeuroCure, Charité
    Leibniz Institut für Molekulare Pharmakologie)

  • Bernhard Loll

    (Freie Universität Berlin, Institut für Chemie und Biochemie /Strukturbiochmie)

  • Stephan J. Sigrist

    (Freie Universität Berlin, Institute for Biology/Genetics
    NeuroCure, Charité)

Abstract

Assembly and maturation of synapses at the Drosophila neuromuscular junction (NMJ) depend on trans-synaptic neurexin/neuroligin signalling, which is promoted by the scaffolding protein Syd-1 binding to neurexin. Here we report that the scaffold protein spinophilin binds to the C-terminal portion of neurexin and is needed to limit neurexin/neuroligin signalling by acting antagonistic to Syd-1. Loss of presynaptic spinophilin results in the formation of excess, but atypically small active zones. Neuroligin-1/neurexin-1/Syd-1 levels are increased at spinophilin mutant NMJs, and removal of single copies of the neurexin-1, Syd-1 or neuroligin-1 genes suppresses the spinophilin-active zone phenotype. Evoked transmission is strongly reduced at spinophilin terminals, owing to a severely reduced release probability at individual active zones. We conclude that presynaptic spinophilin fine-tunes neurexin/neuroligin signalling to control active zone number and functionality, thereby optimizing them for action potential-induced exocytosis.

Suggested Citation

  • Karzan Muhammad & Suneel Reddy-Alla & Jan H Driller & Dietmar Schreiner & Ulises Rey & Mathias A. Böhme & Christina Hollmann & Niraja Ramesh & Harald Depner & Janine Lützkendorf & Tanja Matkovic & Tor, 2015. "Presynaptic spinophilin tunes neurexin signalling to control active zone architecture and function," Nature Communications, Nature, vol. 6(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms9362
    DOI: 10.1038/ncomms9362
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    Cited by:

    1. Rosario Vicidomini & Saumitra Dey Choudhury & Tae Hee Han & Tho Huu Nguyen & Peter Nguyen & Felipe Opazo & Mihaela Serpe, 2024. "Versatile nanobody-based approach to image, track and reconstitute functional Neurexin-1 in vivo," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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