Mechanical actions of dendritic-spine enlargement on presynaptic exocytosis

Hasan Ucar, Satoshi Watanabe, Jun Noguchi, Yuichi Morimoto, Yusuke Iino, Sho Yagishita, Noriko Takahashi and Haruo Kasai ()
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Hasan Ucar: The University of Tokyo
Satoshi Watanabe: The University of Tokyo
Jun Noguchi: The University of Tokyo
Yuichi Morimoto: The University of Tokyo
Yusuke Iino: The University of Tokyo
Sho Yagishita: The University of Tokyo
Noriko Takahashi: The University of Tokyo
Haruo Kasai: The University of Tokyo

Nature, 2021, vol. 600, issue 7890, 686-689

Abstract: Abstract Synaptic transmission involves cell-to-cell communication at the synaptic junction between two neurons, and chemical and electrical forms of this process have been extensively studied. In the brain, excitatory glutamatergic synapses are often made on dendritic spines that enlarge during learning1–5. As dendritic spines and the presynaptic terminals are tightly connected with the synaptic cleft6, the enlargement may have mechanical effects on presynaptic functions7. Here we show that fine and transient pushing of the presynaptic boutons with a glass pipette markedly promotes both the evoked release of glutamate and the assembly of SNARE (soluble N-ethylmaleimide-sensitive factor attachment protein receptor) proteins8–12—as measured by Förster resonance transfer (FRET) and fluorescence lifetime imaging—in rat slice culture preparations13. Both of these effects persisted for more than 20 minutes. The increased presynaptic FRET was independent of cytosolic calcium (Ca2+), but dependent on the assembly of SNARE proteins and actin polymerization in the boutons. Notably, a low hypertonic solution of sucrose (20 mM) had facilitatory effects on both the FRET and the evoked release without inducing spontaneous release, in striking contrast with a high hypertonic sucrose solution (300 mM), which induced exocytosis by itself14. Finally, spine enlargement induced by two-photon glutamate uncaging enhanced the evoked release and the FRET only when the spines pushed the boutons by their elongation. Thus, we have identified a mechanosensory and transduction mechanism15 in the presynaptic boutons, in which the evoked release of glutamate is enhanced for more than 20 min.

Date: 2021
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DOI: 10.1038/s41586-021-04125-7

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