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@ARTICLE{Hoffmann:140581,
author = {Hoffmann, Sheila and Orlando, Marta and Andrzejak, Ewa and
Bruns, Christine and Trimbuch, Thorsten and Rosenmund,
Christian and Garner, Craig C and Ackermann, Frauke},
title = {{L}ight-{A}ctivated {ROS} {P}roduction {I}nduces {S}ynaptic
{A}utophagy.},
journal = {The journal of neuroscience},
volume = {39},
number = {12},
issn = {0270-6474},
address = {Washington, DC},
publisher = {Soc.57413},
reportid = {DZNE-2020-06903},
pages = {2163-2183},
year = {2019},
abstract = {The regulated turnover of synaptic vesicle (SV) proteins is
thought to involve the ubiquitin-dependent tagging and
degradation through endo-lysosomal and autophagy pathways.
Yet, it remains unclear which of these pathways are used,
when they become activated, and whether SVs are cleared en
masse together with SV proteins or whether both are degraded
selectively. Equally puzzling is how quickly these systems
can be activated and whether they function in real-time to
support synaptic health. To address these questions, we have
developed an imaging-based system that simultaneously tags
presynaptic proteins while monitoring autophagy. Moreover,
by tagging SV proteins with a light-activated ROS generator,
Supernova, it was possible to temporally control the damage
to specific SV proteins and assess their consequence to
autophagy-mediated clearance mechanisms and synaptic
function. Our results show that, in mouse hippocampal
neurons of either sex, presynaptic autophagy can be induced
in as little as 5-10 min and eliminates primarily the
damaged protein rather than the SV en masse. Importantly, we
also find that autophagy is essential for synaptic function,
as light-activated damage to, for example, Synaptophysin
only compromises synaptic function when autophagy is
simultaneously blocked. These data support the concept that
presynaptic boutons have a robust highly regulated clearance
system to maintain not only synapse integrity, but also
synaptic function.SIGNIFICANCE STATEMENT The real-time
surveillance and clearance of synaptic proteins are thought
to be vital to the health, functionality, and integrity of
vertebrate synapses and are compromised in neurodegenerative
disorders, yet the fundamental mechanisms regulating these
systems remain enigmatic. Our analysis reveals that
presynaptic autophagy is a critical part of a real-time
clearance system at synapses capable of responding to local
damage of synaptic vesicle proteins within minutes and to be
critical for the ongoing functionality of these synapses.
These data indicate that synapse autophagy is not only
locally regulated but also crucial for the health and
functionality of vertebrate presynaptic boutons.},
keywords = {Animals / Autophagy: physiology / Female / HEK293 Cells /
HeLa Cells / Hippocampus: metabolism / Hippocampus:
ultrastructure / Humans / Male / Mice, Inbred C57BL /
Neurons: metabolism / Neurons: ultrastructure / Presynaptic
Terminals: metabolism / Presynaptic Terminals:
ultrastructure / Reactive Oxygen Species: metabolism /
Synaptic Vesicles: metabolism / Synaptic Vesicles:
ultrastructure},
cin = {AG Garner / AG Ackermann},
ddc = {610},
cid = {I:(DE-2719)1810001 / I:(DE-2719)1813004},
pnm = {341 - Molecular Signaling (POF3-341)},
pid = {G:(DE-HGF)POF3-341},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:30655355},
pmc = {pmc:PMC6433757},
doi = {10.1523/JNEUROSCI.1317-18.2019},
url = {https://pub.dzne.de/record/140581},
}