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@ARTICLE{Riemenschneider:259006,
author = {Riemenschneider, Henrick and Simonetti, Francesca and
Sheth, Udit and Katona, Eszter and Roth, Stefan and Hutten,
Saskia and Farny, Daniel and Michaelsen, Meike and Nuscher,
Brigitte and Schmidt, Michael K and Flatley, Andrew and
Schepers, Aloys and Gruijs da Silva, Lara A and Zhou, Qihui
and Klopstock, Thomas and Liesz, Arthur and Arzberger,
Thomas and Herms, Jochen and Feederle, Regina and Gendron,
Tania F and Dormann, Dorothee and Edbauer, Dieter},
title = {{T}argeting the glycine-rich domain of {TDP}-43 with
antibodies prevents its aggregation in vitro and reduces
neurofilament levels in vivo.},
journal = {Acta Neuropathologica Communications},
volume = {11},
number = {1},
issn = {2051-5960},
address = {London},
publisher = {Biomed Central},
reportid = {DZNE-2023-00715},
pages = {112},
year = {2023},
abstract = {Cytoplasmic aggregation and concomitant nuclear clearance
of the RNA-binding protein TDP-43 are found in ~ $90\%$ of
cases of amyotrophic lateral sclerosis and ~ $45\%$ of
patients living with frontotemporal lobar degeneration, but
no disease-modifying therapy is available. Antibody therapy
targeting other aggregating proteins associated with
neurodegenerative disorders has shown beneficial effects in
animal models and clinical trials. The most effective
epitopes for safe antibody therapy targeting TDP-43 are
unknown. Here, we identified safe and effective epitopes in
TDP-43 for active and potential future passive
immunotherapy. We prescreened 15 peptide antigens covering
all regions of TDP-43 to identify the most immunogenic
epitopes and to raise novel monoclonal antibodies in
wild-type mice. Most peptides induced a considerable
antibody response and no antigen triggered obvious side
effects. Thus, we immunized mice with rapidly progressing
TDP-43 proteinopathy ('rNLS8' model) with the nine most
immunogenic peptides in five pools prior to TDP-43ΔNLS
transgene induction. Strikingly, combined administration of
two N-terminal peptides induced genetic background-specific
sudden lethality in several mice and was therefore
discontinued. Despite a strong antibody response, no TDP-43
peptide prevented the rapid body weight loss or reduced
phospho-TDP-43 levels as well as the profound astrogliosis
and microgliosis in rNLS8 mice. However, immunization with a
C-terminal peptide containing the disease-associated
phospho-serines 409/410 significantly lowered serum
neurofilament light chain levels, indicative of reduced
neuroaxonal damage. Transcriptomic profiling showed a
pronounced neuroinflammatory signature (IL-1β, TNF-α,
NfκB) in rNLS8 mice and suggested modest benefits of
immunization targeting the glycine-rich region. Several
novel monoclonal antibodies targeting the glycine-rich
domain potently reduced phase separation and aggregation of
TDP-43 in vitro and prevented cellular uptake of preformed
aggregates. Our unbiased screen suggests that targeting the
RRM2 domain and the C-terminal region of TDP-43 by active or
passive immunization may be beneficial in TDP-43
proteinopathies by inhibiting cardinal processes of disease
progression.},
keywords = {Animals / Mice / Antibodies, Monoclonal / Epitopes /
Immunization / Intermediate Filaments / NF-kappa B /
Antibodies, Monoclonal (NLM Chemicals) / Aggregation (Other)
/ Amyotrophic lateral sclerosis (Other) / Frontotemporal
dementia (Other) / Immunotherapy (Other) / Neurodegeneration
(Other) / Phase separation (Other) / TDP-43 (Other) /
Epitopes (NLM Chemicals) / NF-kappa B (NLM Chemicals) /
TDP-43 protein, mouse (NLM Chemicals)},
cin = {AG Edbauer / AG Zhou / Neuropathology / Brainbank / AG
Herms / AG Feederle / Clinical Dementia Research München ;
AG Levin},
ddc = {610},
cid = {I:(DE-2719)1110004 / I:(DE-2719)5000080 /
I:(DE-2719)1140013 / I:(DE-2719)1110001 / I:(DE-2719)1140004
/ I:(DE-2719)1111016},
pnm = {352 - Disease Mechanisms (POF4-352) / 353 - Clinical and
Health Care Research (POF4-353)},
pid = {G:(DE-HGF)POF4-352 / G:(DE-HGF)POF4-353},
typ = {PUB:(DE-HGF)16},
pmc = {pmc:PMC10334564},
pubmed = {pmid:37434215},
doi = {10.1186/s40478-023-01592-z},
url = {https://pub.dzne.de/record/259006},
}