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@ARTICLE{Szibor:151065,
author = {Szibor, Marten and Gizatullina, Zemfira and Gainutdinov,
Timur and Endres, Thomas and Debska-Vielhaber, Grazyna and
Kunz, Matthias and Karavasili, Niki and Hallmann, Kerstin
and Schreiber, Frank and Bamberger, Alexandra and Schwarzer,
Michael and Doenst, Torsten and Heinze, Hans-Jochen and
Lessmann, Volkmar and Vielhaber, Stefan and Kunz, Wolfram S.
and Gellerich, Frank N.},
title = {{C}ytosolic, but not matrix, calcium is essential for
adjustment of mitochondrial pyruvate supply},
journal = {The journal of biological chemistry},
volume = {295},
number = {14},
issn = {0021-9258},
address = {Bethesda, MD.},
publisher = {American Soc. for Biochemistry and Molecular Biology8772},
reportid = {DZNE-2020-01050},
pages = {4383-4397},
year = {2020},
abstract = {Mitochondrial oxidative phosphorylation (OXPHOS) and
cellular workload are tightly balanced by the key cellular
regulator, calcium (Ca2+). Current models assume that
cytosolic Ca2+ regulates workload and that mitochondrial
Ca2+ uptake precedes activation of matrix dehydrogenases,
thereby matching OXPHOS substrate supply to ATP demand.
Surprisingly, knockout (KO) of the mitochondrial Ca2+
uniporter (MCU) in mice results in only minimal phenotypic
changes and does not alter OXPHOS. This implies that
adaptive activation of mitochondrial dehydrogenases by
intramitochondrial Ca2+ cannot be the exclusive mechanism
for OXPHOS control. We hypothesized that cytosolic Ca2+, but
not mitochondrial matrix Ca2+, may adapt OXPHOS to workload
by adjusting the rate of pyruvate supply from the cytosol to
the mitochondria. Here, we studied the role of
malate-aspartate shuttle (MAS)-dependent substrate supply in
OXPHOS responses to changing Ca2+ concentrations in isolated
brain and heart mitochondria, synaptosomes, fibroblasts, and
thymocytes from WT and MCU KO mice and the isolated working
rat heart. Our results indicate that extramitochondrial Ca2+
controls up to $85\%$ of maximal pyruvate-driven OXPHOS
rates, mediated by the activity of the complete MAS, and
that intramitochondrial Ca2+ accounts for the remaining
$15\%.$ Of note, the complete MAS, as applied here, included
besides its classical NADH oxidation reaction the generation
of cytosolic pyruvate. Part of this largely neglected
mechanism has previously been described as the
“mitochondrial gas pedal.” Its implementation into
OXPHOS control models integrates seemingly contradictory
results and warrants a critical reappraisal of metabolic
control mechanisms in health and disease.},
keywords = {Animals / Aspartic Acid: metabolism / Brain: metabolism /
Calcium: metabolism / Calcium Channels: deficiency / Calcium
Channels: genetics / Cytosol: metabolism / Glutamic Acid:
chemistry / Glutamic Acid: metabolism / Heart: physiology /
Malates: chemistry / Malates: metabolism / Membrane
Potential, Mitochondrial / Mice / Mice, Inbred C57BL / Mice,
Knockout / Mitochondria: metabolism / Myocardium: metabolism
/ Oxidative Phosphorylation / Pyruvic Acid: metabolism /
Rats / Substrate Specificity / Synaptosomes: metabolism},
cin = {Magdeburg Pre 2020 / U Clinical Researchers - Magdeburg},
ddc = {610},
cid = {I:(DE-2719)6000015 / I:(DE-2719)7000000},
pnm = {344 - Clinical and Health Care Research (POF3-344)},
pid = {G:(DE-HGF)POF3-344},
typ = {PUB:(DE-HGF)16},
pmc = {pmc:PMC7135991},
pubmed = {pmid:32094224},
doi = {10.1074/jbc.RA119.011902},
url = {https://pub.dzne.de/record/151065},
}