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

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, Torsten Götz, Dominique D. Bergeron, Jan Schmoranzer, Fabian Goettfert, Mathew Holt, Markus C. Wahl, Stefan W. Hell, Peter Scheiffele, Alexander M. Walter, Bernhard Loll and Stephan J. Sigrist ()
Additional contact information
Karzan Muhammad: Freie Universität Berlin, Institute for Biology/Genetics
Suneel Reddy-Alla: Freie Universität Berlin, Institute for Biology/Genetics
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
Janine Lützkendorf: NeuroCure, Charité
Tanja Matkovic: Freie Universität Berlin, Institute for Biology/Genetics
Torsten Götz: Freie Universität Berlin, Institute for Biology/Genetics
Dominique D. Bergeron: NeuroCure, Charité
Jan Schmoranzer: Freie Universität Berlin, Institut für Chemie und Biochemie /Strukturbiochmie
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
Bernhard Loll: Freie Universität Berlin, Institut für Chemie und Biochemie /Strukturbiochmie
Stephan J. Sigrist: Freie Universität Berlin, Institute for Biology/Genetics

Nature Communications, 2015, vol. 6, issue 1, 1-15

Abstract: 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.

Date: 2015
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DOI: 10.1038/ncomms9362

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