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@ARTICLE{Annamalai:282912,
author = {Annamalai, Karthika and Dilliker, Soniya and Buchholz, Eric
and Castro-Hernández, Ricardo and Panyam, Nikita and
Pommeranz, Alessa and Wiederhake, Pascal and Wery von
Limont, Nelly and Hempel, Nina and Ebner, Verena and
Swarnkar, Surabhi and Mohamed, Belal A and
Streckfuss-Bömeke, Katrin and Steffens, Sabine and Herzig,
Stephan and Ebert, Antje and Fischer, Andre and Toischer,
Karl},
title = {{D}eregulation of m6{A}-{RNA} methylation impairs adaptive
hypertrophic response and drives maladaptation via
m{TORC}1-{S}6{K}1-hyperactivation and autophagy impairment.},
journal = {Cell communication and signaling},
volume = {23},
number = {1},
issn = {1478-811X},
address = {London},
publisher = {Biomed Central},
reportid = {DZNE-2025-01373},
pages = {522},
year = {2025},
abstract = {Pressure overload first leads to compensated hypertrophy
and secondary to heart failure. m6A-RNA methylation is a
fast process for the adaptation of cell composition.
m6A-RNA-methylation is regulated by the demethylase, fat
mass and obesity-associated protein (FTO), and FTO protein
levels are diminished in heart failure.
Cardiomyocyte-specific FTO-transgenic/knockout-mice have
shown the relevance of FTO in pressure overload remodeling.
However, its functional downstream regulatory mechanisms are
still unclear. In this study, we discover the harmful
signaling pathways that are triggered by m6A imbalance and
FTO loss, which eventually lead to adverse cardiac
remodeling and heart failure.FTOcKO animals were generated
by crossing FTOfl/fl mice with [Formula: see text]-MHC Cre
mice using Cre-lox system. Control and the FTOcKO animals
groups were subjected to TAC (transverse aortic
constriction) surgery. Echocardiography was performed 1-week
post-TAC surgery. MeRIP (m6A RNA immunoprecipitation)
sequencing was performed from the heart tissues of mice
after one week TAC surgery. Additionally, the mechanistical
interrelation between the signaling pathways during FTO loss
and adverse cardiac remodeling were investigated in human
iPS-CMs (hiPS-CMs).One week post-TAC surgery, FTOcKO mice
showed impaired cardiac function (EF: CreC TAC $(45\%)$ vs.
FTOcKO TAC $(25\%),$ p < 0.0001) and increased LVID (CreC
TAC(3.9 mm) vs. FTOcKO TAC (4.8 mm), p < 0.0001), indicating
a lack of adaption to pressure overload. Knockdown of FTO in
hiPS-cardiomyocytes also reduced endothelin-induced
hypertrophic response. MeRIP-seq data of FTOcKO mice showed
that the differentially hypermethylated transcripts were
associated with cardiac apoptosis inhibition (CDK1, CFLAR),
mTORC1 signaling pathway (AKT1S1) and autophagy regulation
(TFEB). mTORC1 was identified as a central player of
dysregulation with hyperactivation of its canonical
substrates phospho-S6K1 (Thr 389) and phospho-S6
(ser235/236) ex-vivo (FTOcKO) and in-vitro
(FTO-KD-hiPS-CMs). Moreover, FTO-deficient cardiomyocytes
cause autophagic flux impairment and defective autophagy.
The effect of atrophy and induced apoptosis upon FTO-m6A
imbalance could be rescued by pharmacological inhibiton of
the mTORC1-S6K1 pathway.Downregulation of FTO leads to
mTORC1-S6K1 hyperactivation that shift the compensative
hypertrophic response to atrophy and apoptosis leading to
progressive heart failure. These findings might pave the way
for the development of novel therapeutic targets for the
early phases of heart failure treatments.The online version
contains supplementary material available at
10.1186/s12964-025-02509-0.},
keywords = {Apoptosis (Other) / Atrophy (Other) / Cardiac hypertrophy
(Other) / Mouse (Other) / N6-methyladenosine (Other) /
Pathological remodeling (Other)},
cin = {AG Fischer},
ddc = {570},
cid = {I:(DE-2719)1410002},
pnm = {352 - Disease Mechanisms (POF4-352)},
pid = {G:(DE-HGF)POF4-352},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:41327199},
pmc = {pmc:PMC12690826},
doi = {10.1186/s12964-025-02509-0},
url = {https://pub.dzne.de/record/282912},
}