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@ARTICLE{FerreiraRodrigues:266329,
author = {Ferreira Rodrigues, Sara and Anglada-Huguet, Marta and
Hochgräfe, Katja and Kaniyappan, Senthilvelrajan and
Wegmann, Susanne and Mandelkow, Eva Maria},
title = {{S}preading of {T}au {P}rotein {D}oes {N}ot {D}epend on
{A}ggregation {P}ropensity.},
journal = {Journal of molecular neuroscience},
volume = {73},
number = {9-10},
issn = {0895-8696},
address = {New York, NY},
publisher = {Springer},
reportid = {DZNE-2023-01118},
pages = {693 - 712},
year = {2023},
abstract = {The stereotypical progression of Tau pathology during
Alzheimer disease has been attributed to trans-neuronal
spreading of misfolded Tau proteins, followed by prion-like
templated aggregation of Tau. The nature of Tau and the
cellular mechanisms of Tau spreading are still under debate.
We hypothesized that Tau's propensity for aggregation would
correlate with its ability to spread across synapses and
propagate pathology. To study the progressive propagation of
Tau proteins in brain regions relevant for Alzheimer
disease, we used mice expressing near-physiological levels
of full-length human Tau protein carrying pro-aggregant
(TauΔK280, TauΔK) or anti-aggregant (TauΔK280-PP,
TauΔK-PP) mutations in the entorhinal cortex (EC). To
enhance Tau expression in the EC, we performed EC injections
of adeno-associated virus (AAV) particles encoding TauΔK or
TauΔK-PP. The brains of injected and non-injected EC/TauΔK
and EC/TauΔK-PP mice were studied by immunohistological and
biochemical techniques to detect Tau propagation to dentate
gyrus (DG) neurons and Tau-induced pathological changes.
Pro- and anti-aggregant mice had comparable low transgene
expression (~0.2 times endogenous mouse Tau). They
accumulated human Tau at similar rates and only in
expressing EC neurons, including their axonal projections of
the perforant path and presynaptic terminals in the
molecular layer of the DG. Pro-aggregant EC/TauΔK mice
showed misfolded Tau and synaptic protein alterations in EC
neurons, not observed in anti-aggregant EC/TauΔK-PP mice.
Additional AAV-mediated expression of TauΔK or TauΔK-PP in
EC/TauΔK or EC/TauΔK-PP mice, respectively, increased the
human Tau expression to ~0.65 times endogenous mouse Tau,
with comparable spreading of TauΔK and TauΔK-PP throughout
the EC. There was a low level of transcellular propagation
of Tau protein, without pathological phosphorylation or
misfolding, as judged by diagnostic antibodies.
Additionally, TauΔK but not TauΔK-PP expression induced
hippocampal astrogliosis. Low levels of pro- or
anti-aggregant full-length Tau show equivalent distributions
in EC neurons, independent of their aggregation propensity.
Increasing the expression via AAV induce local Tau
misfolding in the EC neurons, synaptotoxicity, and
astrogliosis and lead to a low level of detectable
trans-neuronal spreading of Tau. This depends on its
concentration in the EC, but, contrary to expectations, does
not depend on Tau's aggregation propensity/misfolding and
does not lead to templated misfolding in recipient neurons.},
keywords = {Mice / Animals / Humans / tau Proteins: genetics / tau
Proteins: metabolism / Alzheimer Disease: genetics /
Tauopathies: metabolism / Gliosis / Hippocampus: metabolism
/ Disease Models, Animal / Mice, Transgenic / Aggregation
propensity (Other) / Alzheimer disease (Other) /
Neuroinflammation (Other) / Tau pathology (Other) / Tau
spreading (Other) / tau Proteins (NLM Chemicals)},
cin = {AG Mandelkow 2 / AG Schneider / AG Wegmann},
ddc = {610},
cid = {I:(DE-2719)1013015 / I:(DE-2719)1011305 /
I:(DE-2719)1810006},
pnm = {352 - Disease Mechanisms (POF4-352)},
pid = {G:(DE-HGF)POF4-352},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:37606769},
pmc = {pmc:PMC10694122},
doi = {10.1007/s12031-023-02143-w},
url = {https://pub.dzne.de/record/266329},
}