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@ARTICLE{Deshpande:304091,
author = {A. Deshpande and L. Weirauch and T. K. Baral and M. Steier
and A. Borlepawar and M. Kumari and L. S. Kilian and K.
Richter$^*$ and E. Hammer and D. Frank and C. Schmidt and N.
Frey and A. Y. Rangrez},
title = {{E}levated levels of {L}etm1 drives mitochondrial
dysfunction and cardiomyocyte stress-mediated apoptosis in
cultured cardiomyocytes.},
journal = {Cell communication and signaling},
volume = {23},
number = {1},
issn = {1478-811X},
address = {London},
publisher = {Biomed Central},
reportid = {DKFZ-2025-01759},
pages = {378},
year = {2025},
abstract = {Cardiac ischemia, a predominant cause of heart failure, is
marked by profound mitochondrial dysfunction, dysregulated
ion homeostasis, and maladaptive cellular remodeling, all of
which compromise cardiac performance. The mitochondrial
inner membrane protein Leucine zipper-EF-hand containing
Transmembrane Protein 1 (Letm1), implicated in
Wolf-Hirschhorn Syndrome, is essential for mitochondrial
function. Although genetic alterations in Letm1 are linked
to cardiomyopathies, its specific contributions to cardiac
pathophysiology, particularly in the context of ischemic
heart disease, remain poorly defined. This study aims to
elucidate the role of Letm1 in ischemic cardiac pathology
and its mechanistic impact on cardiomyocyte function.Letm1
expression was assessed in human and murine models of heart
failure due to ischemic cardiomyopathy (ICM) and cardiac
hypertrophy. Letm1 was overexpressed in neonatal rat
ventricular cardiomyocytes, adult mouse cardiomyocytes, and
human induced pluripotent stem cell (iPSC)-derived
cardiomyocytes to study mitochondrial function (Seahorse
assays), structural and molecular remodeling (fluorescence
microscopy, transmission electron microscopy (TEM), qPCR,
immunoblotting), transcriptomic/proteomic profiles, calcium
handling and electrophysiology (patch-clamp), autophagic
flux (Bafilomycin A1, LC3-RFP-GFP), and cell survival.Letm1
was markedly upregulated in ICM in both human and murine
hearts, but unchanged in hypertrophic heart failure.
Overexpression of Letm1 in cardiomyocytes resulted in
profound mitochondrial dysfunction, including downregulation
of oxidative phosphorylation (OXPHOS) genes, impaired
membrane potential, reduced ATP output, increased proton
leak, and elevated ROS levels. A metabolic shift toward
glycolysis was observed, accompanied by reduced fatty acid
oxidation. Electron microscopy revealed mitochondrial
fragmentation, mitophagic vesicles, and sarcomeric disarray.
Transcriptomic and proteomic analyses highlighted
dysregulation of genes linked to mitochondrial organization,
ion transport, and autophagy. Electrophysiologically, Letm1
reduced L-type Ca2+ current density and significantly
shortened action potential duration, leading to impaired
contractility. Letm1 overexpression activated upstream
autophagy regulators (AMPK, ULK1) and enhanced LC3-II and
p62 accumulation, but autophagic flux was impaired, as
confirmed by LC3-RFP-GFP reporter and exacerbated by
Bafilomycin A1 treatment. This dysregulated autophagy was
coupled with mitochondrial stress, increased apoptosis
(cleaved caspases), and reduced cardiomyocyte viability.This
study indicates that Letm1 upregulation drives mitochondrial
dysfunction, electrophysiology alterations, and activation
of autophagy and apoptosis, culminating in cardiomyocyte
injury in ischemic cardiomyopathy. By disrupting OXPHOS,
calcium handling, and cell survival pathways, Letm1
contributes to ischemic remodeling and cardiac dysfunction.
Targeting Letm1 presents a promising therapeutic strategy to
alleviate ischemic damage and preserve cardiac function.},
keywords = {Myocytes, Cardiac: metabolism / Myocytes, Cardiac:
pathology / Animals / Humans / Apoptosis / Mice / Rats /
Mitochondria: metabolism / Mitochondria: pathology / Cells,
Cultured / Membrane Proteins: metabolism / Membrane
Proteins: genetics / Autophagy / Calcium-Binding Proteins:
metabolism / Calcium-Binding Proteins: genetics / Induced
Pluripotent Stem Cells: metabolism / Male / Arrhythmias
(Other) / Cardiomyocytes (Other) / Hypertrophy (Other) /
Letm1 (Other) / Mitochondrial metabolism (Other) / LETM1
protein, human (NLM Chemicals) / Membrane Proteins (NLM
Chemicals) / Calcium-Binding Proteins (NLM Chemicals)},
cin = {W230},
ddc = {570},
cid = {I:(DE-He78)W230-20160331},
pnm = {319H - Addenda (POF4-319H)},
pid = {G:(DE-HGF)POF4-319H},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:40849623},
doi = {10.1186/s12964-025-02378-7},
url = {https://inrepo02.dkfz.de/record/304091},
}