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Supported by type I interferon (IFN) signalling, cardiomyocytes counteract infection by various effector processes, with the IFN-stimulated gene of 15\u2005kDa (ISG15) system being intensively regulated and protein modification with ISG15 protecting mice Coxsackievirus B3 (CVB3) infection. The underlying molecular aspects how the ISG15 system affects the functional properties of respective protein substrates in the heart are unknown.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods and results<\/jats:title>\n                    <jats:p>Based on the protective properties due to protein ISGylation, we set out a study investigating CVB3-infected mice in depth and found cardiac atrophy with lower cardiac output in ISG15\u2212\/\u2212 mice. By mass spectrometry, we identified the protein targets of the ISG15 conjugation machinery in heart tissue and explored how ISGylation affects their function. The cardiac ISGylome showed a strong enrichment of ISGylation substrates within glycolytic metabolic processes. Two control enzymes of the glycolytic pathway, hexokinase 2 (HK2) and phosphofructokinase muscle form (PFK1), were identified as bona fide ISGylation targets during infection. In an integrative approach complemented with enzymatic functional testing and structural modelling, we demonstrate that protein ISGylation obstructs the activity of HK2 and PFK1. Seahorse-based investigation of glycolysis in cardiomyocytes revealed that, by conjugating proteins, the ISG15 system prevents the infection-\/IFN-induced up-regulation of glycolysis. We complemented our analysis with proteomics-based advanced computational modelling of cardiac energy metabolism. Our calculations revealed an ISG15-dependent preservation of the metabolic capacity in cardiac tissue during CVB3 infection. Functional profiling of mitochondrial respiration in cardiomyocytes and mouse heart tissue by Seahorse technology showed an enhanced oxidative activity in cells with a competent ISG15 system.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusion<\/jats:title>\n                    <jats:p>Our study demonstrates that ISG15 controls critical nodes in cardiac metabolism. ISG15 reduces the glucose demand, supports higher ATP production capacity in the heart, despite nutrient shortage in infection, and counteracts cardiac atrophy and dysfunction.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1093\/cvr\/cvae026","type":"journal-article","created":{"date-parts":[[2024,2,3]],"date-time":"2024-02-03T20:53:35Z","timestamp":1706993615000},"page":"644-657","source":"Crossref","is-referenced-by-count":31,"title":["ISG15 blocks cardiac glycolysis and ensures sufficient mitochondrial energy production during Coxsackievirus B3 infection"],"prefix":"10.1093","volume":"120","author":[{"given":"Clara","family":"Bredow","sequence":"first","affiliation":[{"name":"Charit\u00e9 - Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, Institute of Biochemistry , Charit\u00e9platz 1, 10117 Berlin , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fabien","family":"Thery","sequence":"additional","affiliation":[{"name":"Department of Biomolecular Medicine, Ghent University , Ghent , Belgium"},{"name":"VIB-UGent Center for Medical Biotechnology , Ghent , Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eva Katrin","family":"Wirth","sequence":"additional","affiliation":[{"name":"Deutsches Zentrum f\u00fcr Herz-Kreislauf-Forschung, partner site Berlin , Berlin , Germany"},{"name":"Charit\u00e9 - Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin , Department of Endocrinology, Diabetes and Nutrition, Berlin , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah","family":"Ochs","sequence":"additional","affiliation":[{"name":"Charit\u00e9 - Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, Institute of Biochemistry , Charit\u00e9platz 1, 10117 Berlin , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meike","family":"Kespohl","sequence":"additional","affiliation":[{"name":"Charit\u00e9 - Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, Institute of Biochemistry , Charit\u00e9platz 1, 10117 Berlin , Germany"},{"name":"Deutsches Zentrum f\u00fcr Herz-Kreislauf-Forschung, partner site Berlin , Berlin , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gunnar","family":"Kleinau","sequence":"additional","affiliation":[{"name":"Charit\u00e9 - Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, Institute of Medical Physics and Biophysics, Group Protein X-ray Crystallography and Signal Transduction , Charit\u00e9platz 1, Berlin , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicolas","family":"Kelm","sequence":"additional","affiliation":[{"name":"Charit\u00e9 - Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, Institute of Biochemistry , Charit\u00e9platz 1, 10117 Berlin , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Niclas","family":"Gimber","sequence":"additional","affiliation":[{"name":"Charit\u00e9 - Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, Advanced Medical Bioimaging Core Facility , Berlin , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jan","family":"Schmoranzer","sequence":"additional","affiliation":[{"name":"Charit\u00e9 - Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, Advanced Medical 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Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, Core Facility\u2014High-Throughput Mass Spectrometry , Berlin , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arnd","family":"Heuser","sequence":"additional","affiliation":[{"name":"Max-Delbrueck-Center (MDC) for Molecular Medicine , Animal Phenotyping Platform, Berlin , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Klaus-Peter","family":"Knobeloch","sequence":"additional","affiliation":[{"name":"University of Freiburg, Institute of Neuropathology , Freiburg , Germany"},{"name":"CIBSS - Centre for Integrative Biological Signalling Studies, University of Freiburg , Freiburg , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patrick","family":"Scheerer","sequence":"additional","affiliation":[{"name":"Deutsches Zentrum f\u00fcr Herz-Kreislauf-Forschung, partner site Berlin , Berlin , Germany"},{"name":"Charit\u00e9 - Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, Institute of Medical Physics and Biophysics, Group Protein X-ray Crystallography and Signal Transduction , Charit\u00e9platz 1, Berlin , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jennifer","family":"Kirwan","sequence":"additional","affiliation":[{"name":"Berlin Institute of Health at Charit\u00e9 Universit\u00e4tsmedizin , Metabolomics, Charit\u00e9platz 1 Berlin 10117 , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ulrike","family":"Br\u00fcning","sequence":"additional","affiliation":[{"name":"Berlin Institute of Health at Charit\u00e9 Universit\u00e4tsmedizin , Metabolomics, Charit\u00e9platz 1 Berlin 10117 , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5594-9940","authenticated-orcid":false,"given":"Nikolaus","family":"Berndt","sequence":"additional","affiliation":[{"name":"German Institute of Human Nutrition Potsdam-Rehbruecke (DIfE), Department of Molecular Toxicology , Nuthetal , Germany"},{"name":"Deutsches Herzzentrum der Charit\u00e9 (DHZC), Institute of Computer-assisted Cardiovascular Medicine , Berlin , Germany"},{"name":"Charit\u00e9 - Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin , Berlin , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francis","family":"Impens","sequence":"additional","affiliation":[{"name":"Department of Biomolecular Medicine, Ghent University , Ghent , Belgium"},{"name":"VIB-UGent Center for Medical Biotechnology , Ghent , Belgium"},{"name":"VIB Proteomics Core , Ghent , 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