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Extramitochondrial energy production in platelets
Author(s) -
Ravera Silvia,
Signorello Maria Grazia,
Bartolucci Martina,
Ferrando Sara,
Manni Lucia,
Caicci Federico,
Calzia Daniela,
Panfoli Isabella,
Morelli Alessandro,
Leoncini Giuliana
Publication year - 2018
Publication title -
biology of the cell
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.543
H-Index - 85
eISSN - 1768-322X
pISSN - 0248-4900
DOI - 10.1111/boc.201700025
Subject(s) - biochemistry , mitochondrion , biology , oxidative phosphorylation , atp synthase , bioenergetics , platelet , chemiosmosis , adenosine diphosphate , cellular respiration , translocase , metabolism , electron transport chain , adenine nucleotide , glycolysis , enzyme , nucleotide , platelet aggregation , chromosomal translocation , gene , immunology
Background Information Energy demand in human platelets is very high, to carry out their functions. As for most human cells, the aerobic metabolism represents the primary energy source in platelets, even though mitochondria are negligibly represented. Following the hypothesis that other structures could be involved in chemical energy production, in this work, we have investigated the functional expression of an extramitochondrial aerobic metabolism in platelets. Results Oximetric and luminometric analyses showed that platelets consume large amounts of oxygen and produce ATP in the presence of common respiring substrates, such as pyruvate + malate or succinate, although morphological electron microscopy analysis showed that these contain few mitochondria. However, evaluation of the anaerobic glycolytic metabolism showed that only 13% of consumed glucose was converted to lactate. Interestingly, the highest OXPHOS activity was observed in the presence of NADH, not a readily permeant respiring substrate for mitochondria. Also, oxygen consumption and ATP synthesis fuelled by NADH were not affected by atractyloside, an inhibitor of the adenine nucleotide translocase, suggesting that these processes may not be ascribed to mitochondria. Functional data were confirmed by immunofluorescence microscopy and Western blot analyses, showing a consistent expression of the β subunit of F 1 F o ‐ATP synthase and COXII, a subunit of Complex IV, but a low signal of translocase of the inner mitochondrial membrane (a protein not involved in OXPHOS metabolism). Interestingly, the NADH‐stimulated oxygen consumption and ATP synthesis increased in the presence of the physiological platelets agonists, thrombin or collagen. Conclusions Data suggest that in platelets, aerobic energy production is mainly driven by an extramitochondrial OXPHOS machinery, originated inside the megakaryocyte, and that this metabolism plays a pivotal role in platelet activation. Significance This work represents a further example of the existence of an extramitochondrial aerobic metabolism, which can contribute to the cellular energy balance.