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@ARTICLE{deCalbiac:272348,
author = {de Calbiac, Hortense and Renault, Solène and Haouy,
Grégoire and Jung, Vincent and Roger, Kevin and Zhou, Qihui
and Campanari, Maria-Letizia and Chentout, Loïc and Demy,
Doris Lou and Marian, Anca and Goudin, Nicolas and Edbauer,
Dieter and Guerrera, Chiara and Ciura, Sorana and Kabashi,
Edor},
title = {{P}oly-{GP} accumulation due to {C}9orf72 loss of function
induces motor neuron apoptosis through autophagy and
mitophagy defects.},
journal = {Autophagy},
volume = {20},
number = {10},
issn = {1554-8627},
address = {Abingdon, Oxon},
publisher = {Taylor $\&$ Francis},
reportid = {DZNE-2024-01165},
pages = {2164 - 2185},
year = {2024},
abstract = {The GGGGCC hexanucleotide repeat expansion (HRE) of the
C9orf72 gene is the most frequent cause of amyotrophic
lateral sclerosis (ALS), a devastative neurodegenerative
disease characterized by motor neuron degeneration. C9orf72
HRE is associated with lowered levels of C9orf72 expression
and its translation results in the production of
dipeptide-repeats (DPRs). To recapitulate C9orf72-related
ALS disease in vivo, we developed a zebrafish model where we
expressed glycine-proline (GP) DPR in a c9orf72 knockdown
context. We report that C9orf72 gain- and loss-of-function
properties act synergistically to induce motor neuron
degeneration and paralysis with poly(GP) accumulating
preferentially within motor neurons along with Sqstm1/p62
aggregation indicating macroautophagy/autophagy deficits.
Poly(GP) levels were shown to accumulate upon c9orf72
downregulation and were comparable to levels assessed in
autopsy samples of patients carrying C9orf72 HRE. Chemical
boosting of autophagy using rapamycin or apilimod, is able
to rescue motor deficits. Proteomics analysis of
zebrafish-purified motor neurons unravels mitochondria
dysfunction confirmed through a comparative analysis of
previously published C9orf72 iPSC-derived motor neurons.
Consistently, 3D-reconstructions of motor neuron demonstrate
that poly(GP) aggregates colocalize to mitochondria, thus
inducing their elongation and swelling and the failure of
their processing by mitophagy, with mitophagy activation
through urolithin A preventing locomotor deficits. Finally,
we report apoptotic-related increased amounts of cleaved
Casp3 (caspase 3, apoptosis-related cysteine peptidase) and
rescue of motor neuron degeneration by constitutive
inhibition of Casp9 or treatment with decylubiquinone. Here
we provide evidence of key pathogenic steps in C9ALS-FTD
that can be targeted through pharmacological avenues, thus
raising new therapeutic perspectives for ALS patients.},
keywords = {Motor Neurons: metabolism / Motor Neurons: pathology /
Animals / C9orf72 Protein: genetics / C9orf72 Protein:
metabolism / Zebrafish / Mitophagy: genetics / Apoptosis:
genetics / Humans / Autophagy: genetics / Autophagy:
physiology / Amyotrophic Lateral Sclerosis: metabolism /
Amyotrophic Lateral Sclerosis: pathology / Amyotrophic
Lateral Sclerosis: genetics / Dipeptides: pharmacology /
Dipeptides: metabolism / Loss of Function Mutation: genetics
/ Mitochondria: metabolism / Disease Models, Animal /
Amyotrophic lateral sclerosis (Other) / apoptosis (Other) /
mitochondria (Other) / motor neuron (Other) /
neurodegeneration (Other) / poly-GP (Other) / C9orf72
Protein (NLM Chemicals) / Dipeptides (NLM Chemicals)},
cin = {AG Zhou / AG Edbauer},
ddc = {570},
cid = {I:(DE-2719)5000080 / I:(DE-2719)1110004},
pnm = {352 - Disease Mechanisms (POF4-352)},
pid = {G:(DE-HGF)POF4-352},
typ = {PUB:(DE-HGF)16},
pmc = {pmc:PMC11423671},
pubmed = {pmid:39316747},
doi = {10.1080/15548627.2024.2358736},
url = {https://pub.dzne.de/record/272348},
}