Unraveling mitochondrial pyruvate dysfunction to mitigate hyperlactatemia and lethality in sepsis

Summary: Sepsis, killing 11 million people yearly, is associated with increased production of lactate—a metabolite mechanistically linked to mortality—complicating glucose administration in sepsis. To understand the mechanism behind hyperlactatemia, we applied the cecal ligation and puncture (CLP) m...

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Main Authors: Louise Nuyttens, Marah Heyerick, Geike Heremans, Elise Moens, Maxime Roes, Céline Van Dender, Liesbet De Bus, Johan Decruyenaere, Jan Dewaele, Jolien Vandewalle, Claude Libert
Format: Article
Language:English
Published: Elsevier 2025-08-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124725008034
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author Louise Nuyttens
Marah Heyerick
Geike Heremans
Elise Moens
Maxime Roes
Céline Van Dender
Liesbet De Bus
Johan Decruyenaere
Jan Dewaele
Jolien Vandewalle
Claude Libert
author_facet Louise Nuyttens
Marah Heyerick
Geike Heremans
Elise Moens
Maxime Roes
Céline Van Dender
Liesbet De Bus
Johan Decruyenaere
Jan Dewaele
Jolien Vandewalle
Claude Libert
author_sort Louise Nuyttens
collection DOAJ
description Summary: Sepsis, killing 11 million people yearly, is associated with increased production of lactate—a metabolite mechanistically linked to mortality—complicating glucose administration in sepsis. To understand the mechanism behind hyperlactatemia, we applied the cecal ligation and puncture (CLP) model and studied all pyruvate processing routes in liver mitochondria during acute sepsis. Our data suggest that mitochondrial pyruvate-driven respiration is nearly nonexistent in sepsis, not due to insufficient pyruvate uptake or carboxylation, but due to a dysfunctional pyruvate dehydrogenase complex (PDC). Septic mitochondria compensate via glutamate-mediated tricarboxylic acid (TCA) anaplerosis, simultaneously converting some pyruvate into alanine via enhanced mitochondrial glutamic pyruvate transaminase (GPT2) activity. PDC dysfunction is not caused by PDC inactivation per se but by a shortage of its cofactor, thiamine pyrophosphate (TPP). TPP supplementation restores pyruvate oxidation and protects mice from sepsis. TPP also allows safe glucose administration in mice, leading to a robust TPP-plus-glucose therapy.
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institution Kabale University
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language English
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record_format Article
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spelling doaj-art-68cb2c673ae84a14ae0143b88ecfb6052025-08-20T03:31:20ZengElsevierCell Reports2211-12472025-08-0144811603210.1016/j.celrep.2025.116032Unraveling mitochondrial pyruvate dysfunction to mitigate hyperlactatemia and lethality in sepsisLouise Nuyttens0Marah Heyerick1Geike Heremans2Elise Moens3Maxime Roes4Céline Van Dender5Liesbet De Bus6Johan Decruyenaere7Jan Dewaele8Jolien Vandewalle9Claude Libert10Center for Inflammation Research, Vlaams Instituut voor Biotechnologie (VIB), Ghent, Belgium; Department of Biomedical Molecular Biology, Ghent University, Ghent, BelgiumCenter for Inflammation Research, Vlaams Instituut voor Biotechnologie (VIB), Ghent, Belgium; Department of Biomedical Molecular Biology, Ghent University, Ghent, BelgiumTranslational Nuclear Receptor Research, Department of Biomolecular Medicine, VIB Center for Medical Biotechnology, VIB, Ghent, Belgium; Hepatology Research Unit, Department of Internal Medicine and Pediatrics, Ghent University, Ghent, Belgium; Liver Research Center Ghent, Ghent University Hospital, Ghent, BelgiumCenter for Inflammation Research, Vlaams Instituut voor Biotechnologie (VIB), Ghent, Belgium; Department of Biomedical Molecular Biology, Ghent University, Ghent, BelgiumCenter for Inflammation Research, Vlaams Instituut voor Biotechnologie (VIB), Ghent, Belgium; Department of Biomedical Molecular Biology, Ghent University, Ghent, BelgiumCenter for Inflammation Research, Vlaams Instituut voor Biotechnologie (VIB), Ghent, Belgium; Department of Biomedical Molecular Biology, Ghent University, Ghent, BelgiumDepartment of Intensive Care Medicine, Ghent University Hospital, Ghent, BelgiumDepartment of Intensive Care Medicine, Ghent University Hospital, Ghent, BelgiumDepartment of Intensive Care Medicine, Ghent University Hospital, Ghent, BelgiumCenter for Inflammation Research, Vlaams Instituut voor Biotechnologie (VIB), Ghent, Belgium; Department of Biomedical Molecular Biology, Ghent University, Ghent, BelgiumCenter for Inflammation Research, Vlaams Instituut voor Biotechnologie (VIB), Ghent, Belgium; Department of Biomedical Molecular Biology, Ghent University, Ghent, Belgium; Corresponding authorSummary: Sepsis, killing 11 million people yearly, is associated with increased production of lactate—a metabolite mechanistically linked to mortality—complicating glucose administration in sepsis. To understand the mechanism behind hyperlactatemia, we applied the cecal ligation and puncture (CLP) model and studied all pyruvate processing routes in liver mitochondria during acute sepsis. Our data suggest that mitochondrial pyruvate-driven respiration is nearly nonexistent in sepsis, not due to insufficient pyruvate uptake or carboxylation, but due to a dysfunctional pyruvate dehydrogenase complex (PDC). Septic mitochondria compensate via glutamate-mediated tricarboxylic acid (TCA) anaplerosis, simultaneously converting some pyruvate into alanine via enhanced mitochondrial glutamic pyruvate transaminase (GPT2) activity. PDC dysfunction is not caused by PDC inactivation per se but by a shortage of its cofactor, thiamine pyrophosphate (TPP). TPP supplementation restores pyruvate oxidation and protects mice from sepsis. TPP also allows safe glucose administration in mice, leading to a robust TPP-plus-glucose therapy.http://www.sciencedirect.com/science/article/pii/S2211124725008034CP: MetabolismCP: Microbiology
spellingShingle Louise Nuyttens
Marah Heyerick
Geike Heremans
Elise Moens
Maxime Roes
Céline Van Dender
Liesbet De Bus
Johan Decruyenaere
Jan Dewaele
Jolien Vandewalle
Claude Libert
Unraveling mitochondrial pyruvate dysfunction to mitigate hyperlactatemia and lethality in sepsis
Cell Reports
CP: Metabolism
CP: Microbiology
title Unraveling mitochondrial pyruvate dysfunction to mitigate hyperlactatemia and lethality in sepsis
title_full Unraveling mitochondrial pyruvate dysfunction to mitigate hyperlactatemia and lethality in sepsis
title_fullStr Unraveling mitochondrial pyruvate dysfunction to mitigate hyperlactatemia and lethality in sepsis
title_full_unstemmed Unraveling mitochondrial pyruvate dysfunction to mitigate hyperlactatemia and lethality in sepsis
title_short Unraveling mitochondrial pyruvate dysfunction to mitigate hyperlactatemia and lethality in sepsis
title_sort unraveling mitochondrial pyruvate dysfunction to mitigate hyperlactatemia and lethality in sepsis
topic CP: Metabolism
CP: Microbiology
url http://www.sciencedirect.com/science/article/pii/S2211124725008034
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