Skip to search boxSkip to navigationSkip to main content

G-quadruplex-binding small molecules ameliorate C9orf72 FTD/ALS pathology in vitro and in vivo

  • Roberto Simone
    ,
  • Rubika Balendra
    ,
  • Thomas G. Moens
    ,
  • Elisavet Preza
    ,
  • Katherine M. Wilson
    ,
  • Amanda Heslegrave
*Corresponding author for this work
  • University College London
    ,
  • Escuela Superior Politécnica del Litoral
    ,
  • MRC Prion Unit
    ,
  • University of Turin
    ,
  • Georgia State University
    ,
  • University of Gothenburg
Scholary Output:
Contribution to journal
Article
Peer-review

Open access

Abstract

Intronic GGGGCC repeat expansions in C9orf72 are the most common known cause of frontotemporal dementia (FTD) and amyotrophic lateral sclerosis (ALS), which are characterised by degeneration of cortical and motor neurons, respectively. Repeat expansions have been proposed to cause disease by both the repeat RNA forming foci that sequester RNA-binding proteins and through toxic dipeptide repeat proteins generated by repeat-associated non-ATG translation. GGGGCC repeat RNA folds into a G-quadruplex secondary structure, and we investigated whether targeting this structure is a potential therapeutic strategy. We performed a screen that identified three structurally related small molecules that specifically stabilise GGGGCC repeat G-quadruplex RNA. We investigated their effect in C9orf72 patient iPSC-derived motor and cortical neurons and show that they significantly reduce RNA foci burden and the levels of dipeptide repeat proteins. Furthermore, they also reduce dipeptide repeat proteins and improve survival in vivo, in GGGGCC repeat-expressing Drosophila. Therefore, small molecules that target GGGGCC repeat G-quadruplexes can ameliorate the two key pathologies associated with C9orf72 FTD/ALS. These data provide proof of principle that targeting GGGGCC repeat G-quadruplexes has therapeutic potential.

Publication Information

Output type

Scholary Output:
Contribution to journal
Article
Peer-review

Original language

English (US)

Pages from-to (Number of pages)

Pages 22-31 (10 pages)

Journal (Volume, Issue Number)

EMBO Molecular Medicine (Volume 10, Issue 1)

Publication milestones

  • Published - 01/2018

Publication status

Published - 01/2018

ISSN

1757-4676

Publication IDs

  • Scopus: 85040286038
  • PubMed: 29113975

Publication metrics

Metrics

Scopus
citations
SciVal
FWCI
8.16
SciVal
Author count
33
SciVal
citations
90
SciVal
Paper percentile
99
SciVal
Top percentile
1
Fractional count
1
Fractional count
0.03
Fractional count
32
Fractional count
0.97
Fractional count
1
Fractional count
1

PlumX, opens in new tab

Citation count
215
Mentions
2
Captures
269

Funding Details

We thank Professor Chris Shaw for providing C9orf72 iPSC line 3 and Lucy Minkley for technical assistance. This work was funded by the Thierry Latran Foundation (AMI, PF, GP), ERC (AMI, H2020-ERC-2014-CoG-648716), MRC (PF, MR/M008606/1), Brain Research Trust (TGM), Alzheimer’s Research UK (SW, AMI, ARUK-PPG2012B-13), Leonard Wolfson Foundation (AJH), NIH (GM111749 to W. D. W. and D. W. B), and Clinical Research in ALS and Related Disorders for Therapeutic Development (CReATe), which is funded through a collaboration between NCATS and National Institute of Neurological Disorders and Stroke. RB is a Leonard Wolfson Clinical Research Training Fellow and funded by a Wellcome Trust Research Training Fellowship (107196/Z/14/Z). HZ is a Wallenberg Academy Fellow. SW and EP are supported by the NIHR Queen Square Dementia Biomedical Research Unit. RP is a Wellcome Trust Intermediate Clinical Fellow (101149/Z/13/A). Some of this work was undertaken at UCLH/UCL who received a proportion of funding from the Department of Health’s NIHR Biomedical Research Centres funding scheme. We thank Professor Chris Shaw for providing C9orf72 iPSC line 3 and Lucy Minkley for technical assistance. This work was funded by the Thierry Latran Foundation (AMI, PF, GP), ERC (AMI, H2020-ERC-2014-CoG-648716), MRC (PF, MR/M008606/1), Brain Research Trust (TGM), Alzheimer's Research UK (SW, AMI, ARUK-PPG2012B-13), Leonard Wolfson Foundation (AJH), NIH (GM111749 to W. D. W. and D. W. B), and Clinical Research in ALS and Related Disorders for Therapeutic Development (CReATe), which is funded through a collaboration between NCATS and National Institute of Neurological Disorders and Stroke. RB is a Leonard Wolfson Clinical Research Training Fellow and funded by a Wellcome Trust Research Training Fellowship (107196/Z/14/Z). HZ is a Wallenberg Academy Fellow. SW and EP are supported by the NIHR Queen Square Dementia Biomedical Research Unit. RP is a Wellcome Trust Intermediate Clinical Fellow (101149/Z/13/A). Some of this work was undertaken at UCLH/UCL who received a proportion of funding from the Department of Health's NIHR Biomedical Research Centres funding scheme.
FundersFunding numbers
Leonard Wolfson Foundation
-
AJH
-
BRT
-
NIHR Queen Square Dementia Biomedical Research Unit
-
NINDS
-
NIH
-
H2020
-
Department of Health’s NIHR Biomedical Research Centres
-
TGM
-
NCATS
-
Fondation Thierry Latran
-
UKRI
-
EC
617198
AMI
H2020-ERC-2014-CoG-648716
NIGMS
R01GM111749
WT
107196/Z/14/Z, 101149/Z/13/A, 107196
ARUK
ARUK-PPG2012B-13
MRC
MR/M008606/1
ERC
648716