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@ARTICLE{Jamet:271072,
author = {Jamet, Zoe and Mergaux, Camille and Meras, Morgane and
Bouchet, Delphine and Villega, Frédéric and Kreye, Jakob
and Prüss, Harald and Groc, Laurent},
title = {{NMDA} receptor autoantibodies primarily impair the
extrasynaptic compartment.},
journal = {Brain},
volume = {147},
number = {8},
issn = {0006-8950},
address = {Oxford},
publisher = {Oxford Univ. Press},
reportid = {DZNE-2024-00944},
pages = {2745 - 2760},
year = {2024},
abstract = {Autoantibodies directed against the N-methyl-D-aspartate
receptor (NMDAR-Ab) are pathogenic immunoglobulins detected
in patients suffering from NMDAR encephalitis. NMDAR-Ab
alter the receptor membrane trafficking, synaptic
transmission and neuronal network properties, leading to
neurological and psychiatric symptoms in patients. Patients
often have very little neuronal damage but rapid and massive
(treatment-responsive) brain dysfunctions related to an
unknown early mechanism of NMDAR-Ab. Our understanding of
this early molecular cascade remains surprisingly
fragmented. Here, we used a combination of single
molecule-based imaging of membrane proteins to unveil the
spatiotemporal action of NMDAR-Ab on live hippocampal
neurons. We first demonstrate that different clones of
NMDAR-Ab primarily affect extrasynaptic (and not synaptic)
NMDARs. In the first minutes, NMDAR-Ab increase
extrasynaptic NMDAR membrane dynamics, declustering its
surface interactome. NMDAR-Ab also rapidly reshuffle all
membrane proteins located in the extrasynaptic compartment.
Consistent with this alteration of multiple proteins,
effects of NMDAR-Ab were not mediated through the sole
interaction between the NMDAR and EphB2 receptor. In the
long term, NMDAR-Ab reduce the NMDAR synaptic pool by
slowing down receptor membrane dynamics in a
cross-linking-independent manner. Remarkably, exposing only
extrasynaptic NMDARs to NMDAR-Ab was sufficient to produce
their full-blown effect on synaptic receptors. Collectively,
we demonstrate that NMDAR-Ab initially impair extrasynaptic
proteins, then the synaptic ones. These data thus shed new
and unsuspected light on the mode of action of NMDAR-Ab and,
probably, our understanding of (extra)synaptopathies.},
keywords = {Receptors, N-Methyl-D-Aspartate: immunology / Receptors,
N-Methyl-D-Aspartate: metabolism / Autoantibodies:
immunology / Autoantibodies: pharmacology / Animals /
Hippocampus: metabolism / Neurons: metabolism / Rats /
Synapses: metabolism / Humans / Cells, Cultured / Receptor,
EphB2: metabolism / Mice / Anti-N-Methyl-D-Aspartate
Receptor Encephalitis: immunology / autoantibody (Other) /
encephalitis (Other) / extrasynaptic NMDA receptor (Other) /
interactome (Other) / membrane proteins (Other) / Receptors,
N-Methyl-D-Aspartate (NLM Chemicals) / Autoantibodies (NLM
Chemicals) / Receptor, EphB2 (NLM Chemicals)},
cin = {AG Prüß},
ddc = {610},
cid = {I:(DE-2719)1810003},
pnm = {353 - Clinical and Health Care Research (POF4-353)},
pid = {G:(DE-HGF)POF4-353},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:38758090},
pmc = {pmc:PMC11292910},
doi = {10.1093/brain/awae163},
url = {https://pub.dzne.de/record/271072},
}