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@ARTICLE{Willem:138158,
author = {Willem, Michael and Tahirovic, Sabina and Busche, Marc
Aurel and Ovsepian, Saak V and Chafai, Magda and Kootar,
Scherazad and Hornburg, Daniel and Evans, Lewis D B and
Moore, Steven and Daria, Anna and Hampel, Heike and Müller,
Veronika and Giudici, Camilla and Nuscher, Brigitte and
Wenninger-Weinzierl, Andrea and Kremmer, Elisabeth and
Heneka, Michael T and Thal, Dietmar R and Giedraitis,
Vilmantas and Lannfelt, Lars and Müller, Ulrike and
Livesey, Frederick J and Meissner, Felix and Herms, Jochen
and Konnerth, Arthur and Marie, Hélène and Haass,
Christian},
title = {η-{S}ecretase processing of {APP} inhibits neuronal
activity in the hippocampus.},
journal = {Nature},
volume = {526},
number = {7573},
issn = {0028-0836},
address = {London [u.a.]},
publisher = {Nature Publ. Group65848},
reportid = {DZNE-2020-04480},
pages = {443-447},
year = {2015},
abstract = {Alzheimer disease (AD) is characterized by the accumulation
of amyloid plaques, which are predominantly composed of
amyloid-β peptide. Two principal physiological pathways
either prevent or promote amyloid-β generation from its
precursor, β-amyloid precursor protein (APP), in a
competitive manner. Although APP processing has been studied
in great detail, unknown proteolytic events seem to hinder
stoichiometric analyses of APP metabolism in vivo. Here we
describe a new physiological APP processing pathway, which
generates proteolytic fragments capable of inhibiting
neuronal activity within the hippocampus. We identify higher
molecular mass carboxy-terminal fragments (CTFs) of APP,
termed CTF-η, in addition to the long-known CTF-α and
CTF-β fragments generated by the α- and β-secretases
ADAM10 (a disintegrin and metalloproteinase 10) and BACE1
(β-site APP cleaving enzyme 1), respectively. CTF-η
generation is mediated in part by membrane-bound matrix
metalloproteinases such as MT5-MMP, referred to as
η-secretase activity. η-Secretase cleavage occurs
primarily at amino acids 504-505 of APP695, releasing a
truncated ectodomain. After shedding of this ectodomain,
CTF-η is further processed by ADAM10 and BACE1 to release
long and short Aη peptides (termed Aη-α and Aη-β). CTFs
produced by η-secretase are enriched in dystrophic neurites
in an AD mouse model and in human AD brains. Genetic and
pharmacological inhibition of BACE1 activity results in
robust accumulation of CTF-η and Aη-α. In mice treated
with a potent BACE1 inhibitor, hippocampal long-term
potentiation was reduced. Notably, when recombinant or
synthetic Aη-α was applied on hippocampal slices ex vivo,
long-term potentiation was lowered. Furthermore, in vivo
single-cell two-photon calcium imaging showed that
hippocampal neuronal activity was attenuated by Aη-α.
These findings not only demonstrate a major functionally
relevant APP processing pathway, but may also indicate
potential translational relevance for therapeutic strategies
targeting APP processing.},
keywords = {ADAM Proteins: metabolism / ADAM10 Protein / Alzheimer
Disease: enzymology / Alzheimer Disease: metabolism /
Amyloid Precursor Protein Secretases: antagonists $\&$
inhibitors / Amyloid Precursor Protein Secretases:
cerebrospinal fluid / Amyloid Precursor Protein Secretases:
deficiency / Amyloid Precursor Protein Secretases: genetics
/ Amyloid Precursor Protein Secretases: metabolism / Amyloid
beta-Protein Precursor: cerebrospinal fluid / Amyloid
beta-Protein Precursor: chemistry / Amyloid beta-Protein
Precursor: genetics / Amyloid beta-Protein Precursor:
metabolism / Animals / Aspartic Acid Endopeptidases:
antagonists $\&$ inhibitors / Aspartic Acid Endopeptidases:
deficiency / Aspartic Acid Endopeptidases: genetics /
Aspartic Acid Endopeptidases: metabolism / Calcium Signaling
/ Disease Models, Animal / Female / Hippocampus: cytology /
Hippocampus: enzymology / Hippocampus: physiology / Humans /
In Vitro Techniques / Long-Term Potentiation / Male / Matrix
Metalloproteinases, Membrane-Associated: deficiency / Matrix
Metalloproteinases, Membrane-Associated: metabolism /
Membrane Proteins: metabolism / Mice / Molecular Weight /
Neurites: enzymology / Neurites: metabolism / Neurons:
enzymology / Neurons: physiology / Peptide Fragments:
chemistry / Peptide Fragments: metabolism / Plaque, Amyloid
/ Protein Processing, Post-Translational / Proteolysis /
Single-Cell Analysis / APP protein, human (NLM Chemicals) /
Amyloid beta-Protein Precursor (NLM Chemicals) / Membrane
Proteins (NLM Chemicals) / Peptide Fragments (NLM Chemicals)
/ Amyloid Precursor Protein Secretases (NLM Chemicals) /
Aspartic Acid Endopeptidases (NLM Chemicals) / BACE1
protein, human (NLM Chemicals) / Bace1 protein, mouse (NLM
Chemicals) / ADAM Proteins (NLM Chemicals) / Matrix
Metalloproteinases, Membrane-Associated (NLM Chemicals) /
Mmp24 protein, mouse (NLM Chemicals) / ADAM10 Protein (NLM
Chemicals) / ADAM10 protein, human (NLM Chemicals)},
cin = {AG Tahirovic / AG Herms / AG Haass old / Ext HZM / AG
Heneka2},
ddc = {500},
cid = {I:(DE-2719)1140003 / I:(DE-2719)1110001 /
I:(DE-2719)1110007 / I:(DE-2719)5000050 /
I:(DE-2719)1011303},
pnm = {342 - Disease Mechanisms and Model Systems (POF3-342) / 344
- Clinical and Health Care Research (POF3-344)},
pid = {G:(DE-HGF)POF3-342 / G:(DE-HGF)POF3-344},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:26322584},
pmc = {pmc:PMC6570618},
doi = {10.1038/nature14864},
url = {https://pub.dzne.de/record/138158},
}