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C9orf72 and RAB7L1 regulate vesicle trafficking in amyotrophic lateral sclerosis and frontotemporal dementia

C9orf72 and RAB7L1 regulate vesicle trafficking in amyotrophic lateral sclerosis and frontotemporal dementia
C9orf72 and RAB7L1 regulate vesicle trafficking in amyotrophic lateral sclerosis and frontotemporal dementia
A non-coding hexanucleotide repeat expansion in intron 1 of the C9orf72 gene is the most common cause of amyotrophic lateral sclerosis and frontotemporal dementia (C9ALS/FTD), however, the precise molecular mechanism by which the C9orf72 hexanucleotide repeat expansion directs C9ALS/FTD pathogenesis remains unclear. Here, we report a novel disease mechanism arising due to the interaction of C9ORF72 with the RAB7L1 GTPase to regulate vesicle trafficking. Endogenous interaction between C9ORF72 and RAB7L1 was confirmed in human SH-SY5Y neuroblastoma cells. The C9orf72 hexanucleotide repeat expansion led to haploinsufficiency resulting in severely defective intracellular and extracellular vesicle trafficking and a dysfunctional trans-Golgi network phenotype in patient-derived fibroblasts and induced pluripotent stem cell-derived motor neurons. Genetic ablation of RAB7L1or C9orf72 in SH-SY5Y cells recapitulated the findings in C9ALS/FTD fibroblasts and induced pluripotent stem cell neurons. When C9ORF72 was overexpressed or antisense oligonucleotides were targeted to the C9orf72 hexanucleotide repeat expansion to upregulate normal variant 1 transcript levels, the defective vesicle trafficking and dysfunctional trans-Golgi network phenotypes were reversed, suggesting that both loss- and gain-of-function mechanisms play a role in disease pathogenesis. In conclusion, we have identified a novel mechanism for C9ALS/FTD pathogenesis highlighting the molecular regulation of intracellular and extracellular vesicle trafficking as an important pathway in C9ALS/FTD pathogenesis.
0006-8950
887-897
Aoki, Yoshitsugu
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Manzano, Raquel
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Lee, Yi
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Dafinca, Ruxandra
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Aoki, Misako
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Douglas, Andrew
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Varela, Miguel A.
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Sathyaprakash, Chaitra
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Scaber, Jakub
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Barbagallo, Paola
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Vader, Pieter
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Mäger, Imre
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Ezzat, Kariem
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Turner, Martin R.
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Ito, Naoki
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Gasco, Samanta
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Ohbayashi, Norihiko
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El Andaloussi, Samir
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Takeda, Shin'ichi
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Fukuda, Mitsunori
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Talbot, Kevin
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Wood, Matthew J.A.
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Aoki, Yoshitsugu
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Manzano, Raquel
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Lee, Yi
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Dafinca, Ruxandra
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Aoki, Misako
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Douglas, Andrew
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Varela, Miguel A.
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Sathyaprakash, Chaitra
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Scaber, Jakub
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Barbagallo, Paola
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Vader, Pieter
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Mäger, Imre
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Ezzat, Kariem
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Turner, Martin R.
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Ito, Naoki
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Gasco, Samanta
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Ohbayashi, Norihiko
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El Andaloussi, Samir
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Takeda, Shin'ichi
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Fukuda, Mitsunori
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Talbot, Kevin
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Wood, Matthew J.A.
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Aoki, Yoshitsugu, Manzano, Raquel, Lee, Yi, Dafinca, Ruxandra, Aoki, Misako, Douglas, Andrew, Varela, Miguel A., Sathyaprakash, Chaitra, Scaber, Jakub, Barbagallo, Paola, Vader, Pieter, Mäger, Imre, Ezzat, Kariem, Turner, Martin R., Ito, Naoki, Gasco, Samanta, Ohbayashi, Norihiko, El Andaloussi, Samir, Takeda, Shin'ichi, Fukuda, Mitsunori, Talbot, Kevin and Wood, Matthew J.A. (2017) C9orf72 and RAB7L1 regulate vesicle trafficking in amyotrophic lateral sclerosis and frontotemporal dementia. Brain, 140 (4), 887-897. (doi:10.1093/brain/awx024).

Record type: Article

Abstract

A non-coding hexanucleotide repeat expansion in intron 1 of the C9orf72 gene is the most common cause of amyotrophic lateral sclerosis and frontotemporal dementia (C9ALS/FTD), however, the precise molecular mechanism by which the C9orf72 hexanucleotide repeat expansion directs C9ALS/FTD pathogenesis remains unclear. Here, we report a novel disease mechanism arising due to the interaction of C9ORF72 with the RAB7L1 GTPase to regulate vesicle trafficking. Endogenous interaction between C9ORF72 and RAB7L1 was confirmed in human SH-SY5Y neuroblastoma cells. The C9orf72 hexanucleotide repeat expansion led to haploinsufficiency resulting in severely defective intracellular and extracellular vesicle trafficking and a dysfunctional trans-Golgi network phenotype in patient-derived fibroblasts and induced pluripotent stem cell-derived motor neurons. Genetic ablation of RAB7L1or C9orf72 in SH-SY5Y cells recapitulated the findings in C9ALS/FTD fibroblasts and induced pluripotent stem cell neurons. When C9ORF72 was overexpressed or antisense oligonucleotides were targeted to the C9orf72 hexanucleotide repeat expansion to upregulate normal variant 1 transcript levels, the defective vesicle trafficking and dysfunctional trans-Golgi network phenotypes were reversed, suggesting that both loss- and gain-of-function mechanisms play a role in disease pathogenesis. In conclusion, we have identified a novel mechanism for C9ALS/FTD pathogenesis highlighting the molecular regulation of intracellular and extracellular vesicle trafficking as an important pathway in C9ALS/FTD pathogenesis.

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Aoki et al - Brain manuscript - for PURE - Accepted Manuscript
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Accepted/In Press date: 28 December 2016
e-pub ahead of print date: 23 February 2017
Published date: 1 April 2017

Identifiers

Local EPrints ID: 413125
URI: http://eprints.soton.ac.uk/id/eprint/413125
ISSN: 0006-8950
PURE UUID: 003d0d8b-5587-432d-a560-8352dfe0932e
ORCID for Andrew Douglas: ORCID iD orcid.org/0000-0001-5154-6714

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Date deposited: 15 Aug 2017 16:31
Last modified: 16 Mar 2024 05:10

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Contributors

Author: Yoshitsugu Aoki
Author: Raquel Manzano
Author: Yi Lee
Author: Ruxandra Dafinca
Author: Misako Aoki
Author: Andrew Douglas ORCID iD
Author: Miguel A. Varela
Author: Chaitra Sathyaprakash
Author: Jakub Scaber
Author: Paola Barbagallo
Author: Pieter Vader
Author: Imre Mäger
Author: Kariem Ezzat
Author: Martin R. Turner
Author: Naoki Ito
Author: Samanta Gasco
Author: Norihiko Ohbayashi
Author: Samir El Andaloussi
Author: Shin'ichi Takeda
Author: Mitsunori Fukuda
Author: Kevin Talbot
Author: Matthew J.A. Wood

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