---
APC_amount: 6248,82 EUR
DOAJ_listed: '1'
OA_place: publisher
OA_type: gold
_id: '18603'
abstract:
- lang: eng
text: It is widely believed that information storage in neuronal circuits involves
nanoscopic structural changes at synapses, resulting in the formation of synaptic
engrams. However, direct evidence for this hypothesis is lacking. To test this
conjecture, we combined chemical potentiation, functional analysis by paired pre-postsynaptic
recordings, and structural analysis by electron microscopy (EM) and freeze-fracture
replica labeling (FRL) at the rodent hippocampal mossy fiber synapse, a key synapse
in the trisynaptic circuit of the hippocampus. Biophysical analysis of synaptic
transmission revealed that forskolin-induced chemical potentiation increased the
readily releasable vesicle pool size and vesicular release probability by 146%
and 49%, respectively. Structural analysis of mossy fiber synapses by EM and FRL
demonstrated an increase in the number of vesicles close to the plasma membrane
and the number of clusters of the priming protein Munc13-1, indicating an increase
in the number of both docked and primed vesicles. Furthermore, FRL analysis revealed
a significant reduction of the distance between Munc13-1 and CaV2.1 Ca2+ channels,
suggesting reconfiguration of the channel-vesicle coupling nanotopography. Our
results indicate that presynaptic plasticity is associated with structural reorganization
of active zones. We propose that changes in potential nanoscopic organization
at synaptic vesicle release sites may be correlates of learning and memory at
a plastic central synapse.
acknowledged_ssus:
- _id: EM-Fac
- _id: PreCl
acknowledgement: "We thank Carolina Borges-Merjane, Jing-Jing Chen, Katharina Lichter,
and Samuel Young for critically reading the manuscript; the Electron Microscopy
Facility of ISTA, in particular Vanessa Zheden, for extensive support, advice, and
experimental assistance; the Preclinical Facility of ISTA, in particular Victoria
Wimmer and Michael Schunn, for experimental assistance; Florian Marr and Christina
Altmutter for technical support; Alois Schlögl for help with analysis; and Eleftheria
Kralli-Beller for manuscript editing. We also thank Cordelia Imig for providing
Munc13-1cKO-Munc13-2/3(−/−) mutant mice. Part of the work has been published in
O.K.’s thesis in partial fulfillment of the requirements for the degree of Doctor
of Philosophy.\r\nThis project received funding from the European Research Council
and European Union’s Horizon 2020 research and innovation programme (ERC 692692
to P.J.; https://cordis.europa.eu/project/id/692692/de) and from the Fond zur Förderung
der Wissenschaftlichen Forschung (Z312-B27 Wittgenstein award to P.J., https://www.fwf.ac.at/en/funding/portfolio/projects/fwf-wittgenstein-award;
W1205-B09 and P36232-B to P.J., https://www.fwf.ac.at/en/funding; I6166-B to R.S.;
https://www.fwf.ac.at/en/funding). The funders had no role in study design, data
collection and analysis, decision to publish, or preparation of the manuscript."
article_number: e3002879
article_processing_charge: Yes
article_type: original
author:
- first_name: Olena
full_name: Kim, Olena
id: 3F8ABDDA-F248-11E8-B48F-1D18A9856A87
last_name: Kim
orcid: 0000-0003-2344-1039
- first_name: Yuji
full_name: Okamoto, Yuji
id: 3337E116-F248-11E8-B48F-1D18A9856A87
last_name: Okamoto
orcid: 0000-0003-0408-6094
- first_name: Walter
full_name: Kaufmann, Walter
id: 3F99E422-F248-11E8-B48F-1D18A9856A87
last_name: Kaufmann
orcid: 0000-0001-9735-5315
- first_name: Nils
full_name: Brose, Nils
last_name: Brose
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
- first_name: Peter M
full_name: Jonas, Peter M
id: 353C1B58-F248-11E8-B48F-1D18A9856A87
last_name: Jonas
orcid: 0000-0001-5001-4804
citation:
ama: Kim O, Okamoto Y, Kaufmann W, Brose N, Shigemoto R, Jonas PM. Presynaptic cAMP-PKA-mediated
potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle
coupling at hippocampal mossy fiber boutons. PLoS Biology. 2024;22(11).
doi:10.1371/journal.pbio.3002879
apa: Kim, O., Okamoto, Y., Kaufmann, W., Brose, N., Shigemoto, R., & Jonas,
P. M. (2024). Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration
of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber
boutons. PLoS Biology. Public Library of Science. https://doi.org/10.1371/journal.pbio.3002879
chicago: Kim, Olena, Yuji Okamoto, Walter Kaufmann, Nils Brose, Ryuichi Shigemoto,
and Peter M Jonas. “Presynaptic CAMP-PKA-Mediated Potentiation Induces Reconfiguration
of Synaptic Vesicle Pools and Channel-Vesicle Coupling at Hippocampal Mossy Fiber
Boutons.” PLoS Biology. Public Library of Science, 2024. https://doi.org/10.1371/journal.pbio.3002879.
ieee: O. Kim, Y. Okamoto, W. Kaufmann, N. Brose, R. Shigemoto, and P. M. Jonas,
“Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic
vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons,”
PLoS Biology, vol. 22, no. 11. Public Library of Science, 2024.
ista: Kim O, Okamoto Y, Kaufmann W, Brose N, Shigemoto R, Jonas PM. 2024. Presynaptic
cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools
and channel-vesicle coupling at hippocampal mossy fiber boutons. PLoS Biology.
22(11), e3002879.
mla: Kim, Olena, et al. “Presynaptic CAMP-PKA-Mediated Potentiation Induces Reconfiguration
of Synaptic Vesicle Pools and Channel-Vesicle Coupling at Hippocampal Mossy Fiber
Boutons.” PLoS Biology, vol. 22, no. 11, e3002879, Public Library of Science,
2024, doi:10.1371/journal.pbio.3002879.
short: O. Kim, Y. Okamoto, W. Kaufmann, N. Brose, R. Shigemoto, P.M. Jonas, PLoS
Biology 22 (2024).
corr_author: '1'
date_created: 2024-12-01T23:01:54Z
date_published: 2024-11-18T00:00:00Z
date_updated: 2026-04-16T12:20:34Z
day: '18'
ddc:
- '570'
department:
- _id: PeJo
- _id: EM-Fac
- _id: RySh
doi: 10.1371/journal.pbio.3002879
ec_funded: 1
external_id:
isi:
- '001358568700003'
pmid:
- '39556620'
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creator: dernst
date_created: 2024-12-03T08:56:53Z
date_updated: 2024-12-03T08:56:53Z
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has_accepted_license: '1'
intvolume: ' 22'
isi: 1
issue: '11'
language:
- iso: eng
license: https://creativecommons.org/licenses/by/4.0/
month: '11'
oa: 1
oa_version: Published Version
pmid: 1
project:
- _id: 25B7EB9E-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '692692'
name: Biophysics and circuit function of a giant cortical glutamatergic synapse
- _id: 25C5A090-B435-11E9-9278-68D0E5697425
call_identifier: FWF
grant_number: Z00312
name: Synaptic communication in neuronal microcircuits
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grant_number: P36232
name: Mechanisms of GABA release in hippocampal circuits
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grant_number: I06166
name: Structural & functional basis of presynaptic plasticity
- _id: 25C3DBB6-B435-11E9-9278-68D0E5697425
call_identifier: FWF
grant_number: W01205
name: Zellkommunikation in Gesundheit und Krankheit
- _id: 3AC91DDA-15DF-11EA-824D-93A3E7B544D1
call_identifier: FWF
name: FWF Open Access Fund
publication: PLoS Biology
publication_identifier:
eissn:
- 1545-7885
issn:
- 1544-9173
publication_status: published
publisher: Public Library of Science
quality_controlled: '1'
related_material:
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relation: research_data
status: public
scopus_import: '1'
status: public
title: Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic
vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 317138e5-6ab7-11ef-aa6d-ffef3953e345
volume: 22
year: '2024'
...