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@ARTICLE{Nihei:141597,
author = {Nihei, Yoshihiro and Mori, Kohji and Werner, Georg and
Arzberger, Thomas and Zhou, Qihui and Khosravi, Bahram and
Japtok, Julia and Hermann, Andreas and Sommacal, Andreas and
Weber, Markus and Degeneration, German Consortium for
Frontotemporal Lobar and Alliance, Bavarian Brain Banking
and Kamp, Frits and Nuscher, Brigitte and Edbauer, Dieter
and Haass, Christian},
title = {{P}oly-glycine-alanine exacerbates {C}9orf72 repeat
expansion-mediated {DNA} damage via sequestration of
phosphorylated {ATM} and loss of nuclear hn{RNPA}3.},
journal = {Acta neuropathologica},
volume = {139},
number = {1},
issn = {0001-6322},
address = {Heidelberg},
publisher = {Springer},
reportid = {DZNE-2020-07921},
pages = {99-118},
year = {2020},
abstract = {Repeat expansion in C9orf72 causes amyotrophic lateral
sclerosis and frontotemporal lobar degeneration. Expanded
sense and antisense repeat RNA transcripts in C9orf72 are
translated into five dipeptide-repeat proteins (DPRs) in an
AUG-independent manner. We previously identified the
heterogeneous ribonucleoprotein (hnRNP) A3 as an interactor
of the sense repeat RNA that reduces its translation into
DPRs. Furthermore, we found that hnRNPA3 is depleted from
the nucleus and partially mislocalized to cytoplasmic
poly-GA inclusions in C9orf72 patients, suggesting that
poly-GA sequesters hnRNPA3 within the cytoplasm. We now
demonstrate that hnRNPA3 also binds to the antisense repeat
RNA. Both DPR production and deposition from sense and
antisense RNA repeats are increased upon hnRNPA3 reduction.
All DPRs induced DNA double strand breaks (DSB), which was
further enhanced upon reduction of hnRNPA3.
Poly-glycine-arginine and poly-proline-arginine increased
foci formed by phosphorylated Ataxia Telangiectasia
Mutated (pATM), a major sensor of DSBs, whereas
poly-glycine-alanine (poly-GA) evoked a reduction of pATM
foci. In dentate gyri of C9orf72 patients, lower nuclear
hnRNPA3 levels were associated with increased DNA damage.
Moreover, enhanced poly-GA deposition correlated with
reduced pATM foci. Since cytoplasmic pATM deposits partially
colocalized with poly-GA deposits, these results suggest
that poly-GA, the most frequent DPR observed in C9orf72
patients, differentially causes DNA damage and that poly-GA
selectively sequesters pATM in the cytoplasm inhibiting its
recruitment to sites of DNA damage. Thus, mislocalization of
nuclear hnRNPA3 caused by poly-GA leads to increased poly-GA
production, which partially depletes pATM, and consequently
enhances DSB.},
keywords = {Aged / Amyotrophic Lateral Sclerosis: genetics /
Amyotrophic Lateral Sclerosis: metabolism / Ataxia
Telangiectasia Mutated Proteins: metabolism / C9orf72
Protein: genetics / DNA Damage: genetics / Dinucleotide
Repeats: physiology / Female / Frontotemporal Lobar
Degeneration: genetics / Frontotemporal Lobar Degeneration:
metabolism / Heterogeneous-Nuclear Ribonucleoprotein Group
A-B: metabolism / Humans / Male / Middle Aged /
Phosphorylation},
cin = {AG Haass old / Clinical Dementia Research München / AG
Edbauer / AG Teipel / AG Zhou},
ddc = {610},
cid = {I:(DE-2719)1110007 / I:(DE-2719)1111016 /
I:(DE-2719)1110004 / I:(DE-2719)1510100 /
I:(DE-2719)5000080},
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:31642962},
pmc = {pmc:PMC6942035},
doi = {10.1007/s00401-019-02082-0},
url = {https://pub.dzne.de/record/141597},
}