Plasma-derived extracellular vesicles released after endurance exercise exert cardioprotective activity through the activation of antioxidant pathways

Veronica Lisi; Giorgia Senesi; Nadia Bertola; Matteo Pecoraro; Sara Bolis; Alice Gualerzi; Silvia Picciolini; Andrea Raimondi; Cristina Fantini; Elisa Moretti; Attilio Parisi; Paolo Sgrò; Luigi Di Luigi; Roger Geiger; Silvia Ravera; Giuseppe Vassalli; Daniela Caporossi; Carolina Balbi

Redox Biology (Jul 2023)

Plasma-derived extracellular vesicles released after endurance exercise exert cardioprotective activity through the activation of antioxidant pathways

Veronica Lisi,
Giorgia Senesi,
Nadia Bertola,
Matteo Pecoraro,
Sara Bolis,
Alice Gualerzi,
Silvia Picciolini,
Andrea Raimondi,
Cristina Fantini,
Elisa Moretti,
Attilio Parisi,
Paolo Sgrò,
Luigi Di Luigi,
Roger Geiger,
Silvia Ravera,
Giuseppe Vassalli,
Daniela Caporossi,
Carolina Balbi

Affiliations

Veronica Lisi: Unit of Biology and Genetics of Movement, Department of Movement, Human and Health Sciences, University of Rome Foro Italico, Piazza Lauro de Bosis 15, 00135, Rome, Italy
Giorgia Senesi: Cellular and Molecular Cardiology, Istituto Cardiocentro Ticino, Laboratories for Translational Research, Ente Ospedaliero Cantonale, Bellinzona, Switzerland; Faculty of Biomedical Sciences, Università della Svizzera Italiana, Lugano, Switzerland
Nadia Bertola: Department of Experimental Medicine, University of Genoa, 16132, Genova, Italy
Matteo Pecoraro: Institute for Research in Biomedicine, Università della Svizzera italiana, Bellinzona, Switzerland
Sara Bolis: Cardiovascular Theranostics, Istituto Cardiocentro Ticino, Laboratories for Translational Research, Ente Ospedaliero Cantonale, Bellinzona, Switzerland
Alice Gualerzi: Laboratory of Nanomedicine and Clinical Biophotonics (LABION), IRCCS Fondazione Don Carlo Gnocchi, Milan, Italy
Silvia Picciolini: Laboratory of Nanomedicine and Clinical Biophotonics (LABION), IRCCS Fondazione Don Carlo Gnocchi, Milan, Italy
Andrea Raimondi: Institute for Research in Biomedicine, Università della Svizzera italiana, Bellinzona, Switzerland; Centro Imaging Sperimentale, IRCCS Istituto Scientifico San Raffaele, Via Olgettina 52, 20132, Milan, Italy
Cristina Fantini: Unit of Biology and Genetics of Movement, Department of Movement, Human and Health Sciences, University of Rome Foro Italico, Piazza Lauro de Bosis 15, 00135, Rome, Italy
Elisa Moretti: Laboratory of Physical Exercise and Sport Science, Department of Exercise, Human and Health Sciences, University of Rome Foro Italico, Piazza Lauro de Bosis 15, 00135, Rome, Italy
Attilio Parisi: Laboratory of Physical Exercise and Sport Science, Department of Exercise, Human and Health Sciences, University of Rome Foro Italico, Piazza Lauro de Bosis 15, 00135, Rome, Italy
Paolo Sgrò: Laboratory of Physical Exercise and Sport Science, Department of Exercise, Human and Health Sciences, University of Rome Foro Italico, Piazza Lauro de Bosis 15, 00135, Rome, Italy
Luigi Di Luigi: Endocrinology Unit, Department of Movement, Human and Health Sciences, University of Rome Foro Italico, Piazza Lauro de Bosis 15, 00135, Rome, Italy
Roger Geiger: Institute for Research in Biomedicine, Università della Svizzera italiana, Bellinzona, Switzerland
Silvia Ravera: Department of Experimental Medicine, University of Genoa, 16132, Genova, Italy
Giuseppe Vassalli: Cellular and Molecular Cardiology, Istituto Cardiocentro Ticino, Laboratories for Translational Research, Ente Ospedaliero Cantonale, Bellinzona, Switzerland; Faculty of Biomedical Sciences, Università della Svizzera Italiana, Lugano, Switzerland; Center for Molecular Cardiology, Zurich, Switzerland
Daniela Caporossi: Unit of Biology and Genetics of Movement, Department of Movement, Human and Health Sciences, University of Rome Foro Italico, Piazza Lauro de Bosis 15, 00135, Rome, Italy
Carolina Balbi: Cellular and Molecular Cardiology, Istituto Cardiocentro Ticino, Laboratories for Translational Research, Ente Ospedaliero Cantonale, Bellinzona, Switzerland; Center for Molecular Cardiology, Zurich, Switzerland; Corresponding author. Cellular and Molecular Cardiology, Istituto Cardiocentro Ticino, Laboratories for Translational Research, Ente Ospedaliero Cantonale, Bellinzona, Switzerland.

Journal volume & issue: Vol. 63
p. 102737

Abstract

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Cardiovascular diseases (CVD) can cause various conditions, including an increase in reactive oxygen species (ROS) levels that can decrease nitric oxide (NO) availability and promote vasoconstriction, leading to arterial hypertension. Physical exercise (PE) has been found to be protective against CVD by helping to maintain redox homeostasis through a decrease in ROS levels, achieved by increased expression of antioxidant enzymes (AOEs) and modulation of heat shock proteins (HSPs). Extracellular vesicles (EVs) circulating in the body are a major source of regulatory signals, including proteins and nucleic acids. Interestingly, the cardioprotective role of EVs released after PE has not been fully described.The aim of this study was to investigate the role of circulating EVs, obtained through Size Exclusion Chromatography (SEC) of plasma samples from healthy young males (age: 26.95 ± 3.07; estimated maximum oxygen consumption rate (VO2max): 51.22 ± 4.85 (mL/kg/min)) at basal level (Pre_EVs) and immediately after a single bout of endurance exercise (30’ treadmill, 70% heart rate (HR) -Post_EVs). Gene ontology (GO) analysis of proteomic data from isolated EVs, revealed enrichment in proteins endowed with catalytic activity in Post_EVs, compare to Pre_EVs, with MAP2K1 being the most significantly upregulated protein. Enzymatic assays on EVs derived from Pre and Post samples showed increment in Glutathione Reductase (GR) and Catalase (CAT) activity in Post_EVs. At functional level, Post_EVs, but not Pre_EVs, enhanced the activity of antioxidant enzymes (AOEs) and reduced oxidative damage accumulation in treated human iPS-derived cardiomyocytes (hCM) at basal level and under stress conditions (Hydrogen Peroxide (H2O2) treatment), resulting in a global cardioprotective effect.In conclusion, our data demonstrated, for the first time, that a single 30-min endurance exercise is able to alter the cargo of circulating EVs, resulting in cardioprotective effect through antioxidant activity.

Published in Redox Biology

ISSN: 2213-2317 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Medicine: Medicine (General); Science: Biology (General)
Website: http://www.journals.elsevier.com/redox-biology/

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