Rapid active zone remodeling consolidates presynaptic potentiation
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Rapid active zone remodeling consolidates presynaptic potentiation. / Böhme, Mathias A; McCarthy, Anthony W; Grasskamp, Andreas T; Beuschel, Christine B; Goel, Pragya; Jusyte, Meida; Laber, Desiree; Huang, Sheng; Rey, Ulises; Petzoldt, Astrid G; Lehmann, Martin; Göttfert, Fabian; Haghighi, Pejmun; Hell, Stefan W; Owald, David; Dickman, Dion; Sigrist, Stephan J; Walter, Alexander M.
In: Nature Communications, Vol. 10, No. 1, 1085, 2019.Research output: Contribution to journal › Journal article › Research › peer-review
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TY - JOUR
T1 - Rapid active zone remodeling consolidates presynaptic potentiation
AU - Böhme, Mathias A
AU - McCarthy, Anthony W
AU - Grasskamp, Andreas T
AU - Beuschel, Christine B
AU - Goel, Pragya
AU - Jusyte, Meida
AU - Laber, Desiree
AU - Huang, Sheng
AU - Rey, Ulises
AU - Petzoldt, Astrid G
AU - Lehmann, Martin
AU - Göttfert, Fabian
AU - Haghighi, Pejmun
AU - Hell, Stefan W
AU - Owald, David
AU - Dickman, Dion
AU - Sigrist, Stephan J
AU - Walter, Alexander M
PY - 2019
Y1 - 2019
N2 - Neuronal communication across synapses relies on neurotransmitter release from presynaptic active zones (AZs) followed by postsynaptic transmitter detection. Synaptic plasticity homeostatically maintains functionality during perturbations and enables memory formation. Postsynaptic plasticity targets neurotransmitter receptors, but presynaptic mechanisms regulating the neurotransmitter release apparatus remain largely enigmatic. By studying Drosophila neuromuscular junctions (NMJs) we show that AZs consist of nano-modular release sites and identify a molecular sequence that adds modules within minutes of inducing homeostatic plasticity. This requires cognate transport machinery and specific AZ-scaffolding proteins. Structural remodeling is not required for immediate potentiation of neurotransmitter release, but necessary to sustain potentiation over longer timescales. Finally, mutations in Unc13 disrupting homeostatic plasticity at the NMJ also impair short-term memory when central neurons are targeted, suggesting that both plasticity mechanisms utilize Unc13. Together, while immediate synaptic potentiation capitalizes on available material, it triggers the coincident incorporation of modular release sites to consolidate synaptic potentiation.
AB - Neuronal communication across synapses relies on neurotransmitter release from presynaptic active zones (AZs) followed by postsynaptic transmitter detection. Synaptic plasticity homeostatically maintains functionality during perturbations and enables memory formation. Postsynaptic plasticity targets neurotransmitter receptors, but presynaptic mechanisms regulating the neurotransmitter release apparatus remain largely enigmatic. By studying Drosophila neuromuscular junctions (NMJs) we show that AZs consist of nano-modular release sites and identify a molecular sequence that adds modules within minutes of inducing homeostatic plasticity. This requires cognate transport machinery and specific AZ-scaffolding proteins. Structural remodeling is not required for immediate potentiation of neurotransmitter release, but necessary to sustain potentiation over longer timescales. Finally, mutations in Unc13 disrupting homeostatic plasticity at the NMJ also impair short-term memory when central neurons are targeted, suggesting that both plasticity mechanisms utilize Unc13. Together, while immediate synaptic potentiation capitalizes on available material, it triggers the coincident incorporation of modular release sites to consolidate synaptic potentiation.
KW - Animals
KW - Animals, Genetically Modified
KW - Behavior, Animal
KW - Drosophila Proteins/genetics
KW - Drosophila melanogaster/physiology
KW - Female
KW - Long-Term Potentiation/physiology
KW - Male
KW - Membrane Proteins/genetics
KW - Memory, Short-Term/physiology
KW - Models, Animal
KW - Mushroom Bodies/cytology
KW - Nerve Tissue Proteins/genetics
KW - Neuromuscular Junction/metabolism
KW - Neurotransmitter Agents/metabolism
KW - Patch-Clamp Techniques
KW - Presynaptic Terminals/metabolism
KW - Synaptic Transmission/physiology
KW - Synaptic Vesicles/metabolism
U2 - 10.1038/s41467-019-08977-6
DO - 10.1038/s41467-019-08977-6
M3 - Journal article
C2 - 30842428
VL - 10
JO - Nature Communications
JF - Nature Communications
SN - 2041-1723
IS - 1
M1 - 1085
ER -
ID: 334033906