Rapid active zone remodeling consolidates presynaptic potentiation

Research output: Contribution to journalJournal articleResearchpeer-review

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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 journalJournal articleResearchpeer-review

Harvard

Böhme, MA, McCarthy, AW, Grasskamp, AT, Beuschel, CB, Goel, P, Jusyte, M, Laber, D, Huang, S, Rey, U, Petzoldt, AG, Lehmann, M, Göttfert, F, Haghighi, P, Hell, SW, Owald, D, Dickman, D, Sigrist, SJ & Walter, AM 2019, 'Rapid active zone remodeling consolidates presynaptic potentiation', Nature Communications, vol. 10, no. 1, 1085. https://doi.org/10.1038/s41467-019-08977-6

APA

Böhme, M. A., McCarthy, A. W., Grasskamp, A. T., Beuschel, C. B., Goel, P., Jusyte, M., Laber, D., Huang, S., Rey, U., Petzoldt, A. G., Lehmann, M., Göttfert, F., Haghighi, P., Hell, S. W., Owald, D., Dickman, D., Sigrist, S. J., & Walter, A. M. (2019). Rapid active zone remodeling consolidates presynaptic potentiation. Nature Communications, 10(1), [1085]. https://doi.org/10.1038/s41467-019-08977-6

Vancouver

Böhme MA, McCarthy AW, Grasskamp AT, Beuschel CB, Goel P, Jusyte M et al. Rapid active zone remodeling consolidates presynaptic potentiation. Nature Communications. 2019;10(1). 1085. https://doi.org/10.1038/s41467-019-08977-6

Author

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. / Rapid active zone remodeling consolidates presynaptic potentiation. In: Nature Communications. 2019 ; Vol. 10, No. 1.

Bibtex

@article{4a049262bb834b78a714b369c90fb19c,
title = "Rapid active zone remodeling consolidates presynaptic potentiation",
abstract = "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.",
keywords = "Animals, Animals, Genetically Modified, Behavior, Animal, Drosophila Proteins/genetics, Drosophila melanogaster/physiology, Female, Long-Term Potentiation/physiology, Male, Membrane Proteins/genetics, Memory, Short-Term/physiology, Models, Animal, Mushroom Bodies/cytology, Nerve Tissue Proteins/genetics, Neuromuscular Junction/metabolism, Neurotransmitter Agents/metabolism, Patch-Clamp Techniques, Presynaptic Terminals/metabolism, Synaptic Transmission/physiology, Synaptic Vesicles/metabolism",
author = "B{\"o}hme, {Mathias A} and McCarthy, {Anthony W} and Grasskamp, {Andreas T} and Beuschel, {Christine B} and Pragya Goel and Meida Jusyte and Desiree Laber and Sheng Huang and Ulises Rey and Petzoldt, {Astrid G} and Martin Lehmann and Fabian G{\"o}ttfert and Pejmun Haghighi and Hell, {Stefan W} and David Owald and Dion Dickman and Sigrist, {Stephan J} and Walter, {Alexander M}",
year = "2019",
doi = "10.1038/s41467-019-08977-6",
language = "English",
volume = "10",
journal = "Nature Communications",
issn = "2041-1723",
publisher = "nature publishing group",
number = "1",

}

RIS

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