C9ORF72 repeat expansion causes vulnerability of motor neurons to Ca2+-permeable AMPA receptor-mediated excitotoxicity

Bhuvaneish T. Selvaraj, Matthew R. Livesey, Chen Zhao, Jenna M. Gregory, Owain T. James, Elaine M. Cleary, Amit K. Chouhan, Angus B. Gane, Emma M. Perkins, Owen Dando, Simon G. Lillico, Youn Bok Lee, Agnes L. Nishimura, Urjana Poreci, Sai Thankamony, Meryll Pray, Navneet A. Vasistha, Dario Magnani, Shyamanga Borooah, Karen BurrDavid Story, Alexander McCampbell, Christopher E. Shaw, Peter C. Kind, Timothy J. Aitman, C. Bruce A. Whitelaw, Ian Wilmut, Colin Smith, Gareth B. Miles, Giles E. Hardingham, David J.A. Wyllie, Siddharthan Chandran*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

120 Citations (Scopus)

Abstract

Mutations in C9ORF72 are the most common cause of familial amyotrophic lateral sclerosis (ALS). Here, through a combination of RNA-Seq and electrophysiological studies on induced pluripotent stem cell (iPSC)-derived motor neurons (MNs), we show that increased expression of GluA1 AMPA receptor (AMPAR) subunit occurs in MNs with C9ORF72 mutations that leads to increased Ca2+-permeable AMPAR expression and results in enhanced selective MN vulnerability to excitotoxicity. These deficits are not found in iPSC-derived cortical neurons and are abolished by CRISPR/Cas9-mediated correction of the C9ORF72 repeat expansion in MNs. We also demonstrate that MN-specific dysregulation of AMPAR expression is also present in C9ORF72 patient post-mortem material. We therefore present multiple lines of evidence for the specific upregulation of GluA1 subunits in human mutant C9ORF72 MNs that could lead to a potential pathogenic excitotoxic mechanism in ALS.

Original languageEnglish
Article number347
JournalNature Communications
Volume9
Issue number1
DOIs
Publication statusPublished - 1 Dec 2018

Bibliographical note

Funding Information:
Funded by The Wellcome Trust (Grant 092742/Z/10/Z), MNDA (Miles/Oct14/878-792), MRC, Euan MacDonald Centre, UK DRI, DBT-India, ISSF (WT/UoE), Royal Society of Edinburgh (CRF), and Biogen/UoE Joint Discovery Research Collaboration. RNA-Seq raw reads were generated by Edinburgh Genomics, The University of Edinburgh. Edinburgh Genomics is partly supported through core grants from NERC (R8/H10/56), MRC (MR/K001744/1), and BBSRC (BB/J004243/1).

Publisher Copyright:
© 2018 The Author(s).

Fingerprint

Dive into the research topics of 'C9ORF72 repeat expansion causes vulnerability of motor neurons to Ca2+-permeable AMPA receptor-mediated excitotoxicity'. Together they form a unique fingerprint.

Cite this