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@ARTICLE{Nieborak:259129,
author = {Nieborak, Anna and Lukauskas, Saulius and Capellades, Jordi
and Heyn, Patricia and Santos, Gabriela Silva and Motzler,
Karsten and Zeigerer, Anja and Bester, Romina and Protzer,
Ulrike and Schelter, Florian and Wagner, Mirko and Carell,
Thomas and Hruscha, Alexander and Schmid, Bettina and Yanes,
Oscar and Schneider, Robert},
title = {{D}epletion of pyruvate kinase ({PK}) activity causes
glycolytic intermediate imbalances and reveals a
{PK}-{TXNIP} regulatory axis.},
journal = {Molecular metabolism},
volume = {74},
issn = {2212-8778},
address = {Oxford [u.a.]},
publisher = {Elsevier},
reportid = {DZNE-2023-00725},
pages = {101748},
year = {2023},
abstract = {Cancer cells convert more glucose into lactate than healthy
cells, what contributes to their growth advantage. Pyruvate
kinase (PK) is a key rate limiting enzyme in this process,
what makes it a promising potential therapeutic target.
However, currently it is still unclear what consequences the
inhibition of PK has on cellular processes. Here, we
systematically investigate the consequences of PK depletion
for gene expression, histone modifications and
metabolism.Epigenetic, transcriptional and metabolic targets
were analysed in different cellular and animal models with
stable knockdown or knockout of PK.Depleting PK activity
reduces the glycolytic flux and causes accumulation of
glucose-6-phosphate (G6P). Such metabolic perturbation
results in stimulation of the activity of a heterodimeric
pair of transcription factors MondoA and MLX but not in a
major reprogramming of the global H3K9ac and H3K4me3 histone
modification landscape. The MondoA:MLX heterodimer
upregulates expression of thioredoxin-interacting protein
(TXNIP) - a tumour suppressor with multifaceted anticancer
activity. This effect of TXNIP upregulation extends beyond
immortalised cancer cell lines and is applicable to multiple
cellular and animal models.Our work shows that actions of
often pro-tumorigenic PK and anti-tumorigenic TXNIP are
tightly linked via a glycolytic intermediate. We suggest
that PK depletion stimulates the activity of MondoA:MLX
transcription factor heterodimers and subsequently,
increases cellular TXNIP levels. TXNIP-mediated inhibition
of thioredoxin (TXN) can reduce the ability of cells to
scavenge reactive oxygen species (ROS) leading to the
oxidative damage of cellular structures including DNA. These
findings highlight an important regulatory axis affecting
tumour suppression mechanisms and provide an attractive
opportunity for combination cancer therapies targeting
glycolytic activity and ROS-generating pathways.},
keywords = {Animals / Pyruvate Kinase: genetics / Reactive Oxygen
Species / Basic Helix-Loop-Helix Leucine Zipper
Transcription Factors: metabolism / Neoplasms: genetics /
Neoplasms: metabolism / Thioredoxins: chemistry /
Thioredoxins: metabolism / Arrestins (Other) / Cancer
(Other) / Glycolysis (Other) / Metabolic flux (Other) /
Pyruvate kinase (Other) / ROS (Other) /
Thioredoxin-interacting protein (Other) / Pyruvate Kinase
(NLM Chemicals) / Reactive Oxygen Species (NLM Chemicals) /
Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
(NLM Chemicals) / Thioredoxins (NLM Chemicals)},
cin = {AG Schmid},
ddc = {610},
cid = {I:(DE-2719)1140002},
pnm = {352 - Disease Mechanisms (POF4-352)},
pid = {G:(DE-HGF)POF4-352},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:37290673},
pmc = {pmc:PMC10336528},
doi = {10.1016/j.molmet.2023.101748},
url = {https://pub.dzne.de/record/259129},
}