Health position paper and redox perspectives on reactive oxygen species as signals and targets of cardioprotection

The present review summarizes the beneficial and detrimental roles of reactive oxygen species in myocardial ischemia/reperfusion injury and cardioprotection. In the first part, the continued need for cardioprotection beyond that by rapid reperfusion of acute myocardial infarction is emphasized. Then...

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Published inRedox biology Vol. 67; p. 102894
Main Authors Heusch, Gerd, Andreadou, Ioanna, Bell, Robert, Bertero, Edoardo, Botker, Hans-Erik, Davidson, Sean M., Downey, James, Eaton, Philip, Ferdinandy, Peter, Gersh, Bernard J., Giacca, Mauro, Hausenloy, Derek J., Ibanez, Borja, Krieg, Thomas, Maack, Christoph, Schulz, Rainer, Sellke, Frank, Shah, Ajay M., Thiele, Holger, Yellon, Derek M., Di Lisa, Fabio
Format Journal Article
LanguageEnglish
Published Netherlands Elsevier B.V 01.11.2023
Elsevier
Subjects
Cardioprotection
Humans
Infarct size
Ischemic conditioning
Mitochondrion
Myocardial infarction
Myocardial Infarction - metabolism
Myocardial ischemia
Myocardial Reperfusion Injury - metabolism
Myocardial Reperfusion Injury - prevention & control
Myocardium - metabolism
Oxidation-Reduction
Reactive Oxygen Species - metabolism
Reperfusion
Review
Mitochondrion
Myocardial infarction
Cardioprotection
Reperfusion
Ischemic conditioning
Infarct size
Myocardial ischemia
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Abstract The present review summarizes the beneficial and detrimental roles of reactive oxygen species in myocardial ischemia/reperfusion injury and cardioprotection. In the first part, the continued need for cardioprotection beyond that by rapid reperfusion of acute myocardial infarction is emphasized. Then, pathomechanisms of myocardial ischemia/reperfusion to the myocardium and the coronary circulation and the different modes of cell death in myocardial infarction are characterized. Different mechanical and pharmacological interventions to protect the ischemic/reperfused myocardium in elective percutaneous coronary interventions and coronary artery bypass grafting, in acute myocardial infarction and in cardiotoxicity from cancer therapy are detailed. The second part keeps the focus on ROS providing a comprehensive overview of molecular and cellular mechanisms involved in ischemia/reperfusion injury. Starting from mitochondria as the main sources and targets of ROS in ischemic/reperfused myocardium, a complex network of cellular and extracellular processes is discussed, including relationships with Ca2+ homeostasis, thiol group redox balance, hydrogen sulfide modulation, cross-talk with NAPDH oxidases, exosomes, cytokines and growth factors. While mechanistic insights are needed to improve our current therapeutic approaches, advancements in knowledge of ROS-mediated processes indicate that detrimental facets of oxidative stress are opposed by ROS requirement for physiological and protective reactions. This inevitable contrast is likely to underlie unsuccessful clinical trials and limits the development of novel cardioprotective interventions simply based upon ROS removal. [Display omitted] •Ischemic heart disease is the most frequent cause of death worldwide.•Ischemia/reperfusion is the substrate of ischemic heart disease.•Cardioprotection reduces infarct size and coronary microvascular obstruction.•ROS are signals of cardioprotection and executors of injury.•Translation of cardioprotection to clinical benefits has been difficult so far.•The role of ROS in cardioprotection remains ambivalent.
AbstractList The present review summarizes the beneficial and detrimental roles of reactive oxygen species in myocardial ischemia/reperfusion injury and cardioprotection. In the first part, the continued need for cardioprotection beyond that by rapid reperfusion of acute myocardial infarction is emphasized. Then, pathomechanisms of myocardial ischemia/reperfusion to the myocardium and the coronary circulation and the different modes of cell death in myocardial infarction are characterized. Different mechanical and pharmacological interventions to protect the ischemic/reperfused myocardium in elective percutaneous coronary interventions and coronary artery bypass grafting, in acute myocardial infarction and in cardiotoxicity from cancer therapy are detailed. The second part keeps the focus on ROS providing a comprehensive overview of molecular and cellular mechanisms involved in ischemia/reperfusion injury. Starting from mitochondria as the main sources and targets of ROS in ischemic/reperfused myocardium, a complex network of cellular and extracellular processes is discussed, including relationships with Ca homeostasis, thiol group redox balance, hydrogen sulfide modulation, cross-talk with NAPDH oxidases, exosomes, cytokines and growth factors. While mechanistic insights are needed to improve our current therapeutic approaches, advancements in knowledge of ROS-mediated processes indicate that detrimental facets of oxidative stress are opposed by ROS requirement for physiological and protective reactions. This inevitable contrast is likely to underlie unsuccessful clinical trials and limits the development of novel cardioprotective interventions simply based upon ROS removal.
The present review summarizes the beneficial and detrimental roles of reactive oxygen species in myocardial ischemia/reperfusion injury and cardioprotection. In the first part, the continued need for cardioprotection beyond that by rapid reperfusion of acute myocardial infarction is emphasized. Then, pathomechanisms of myocardial ischemia/reperfusion to the myocardium and the coronary circulation and the different modes of cell death in myocardial infarction are characterized. Different mechanical and pharmacological interventions to protect the ischemic/reperfused myocardium in elective percutaneous coronary interventions and coronary artery bypass grafting, in acute myocardial infarction and in cardiotoxicity from cancer therapy are detailed. The second part keeps the focus on ROS providing a comprehensive overview of molecular and cellular mechanisms involved in ischemia/reperfusion injury. Starting from mitochondria as the main sources and targets of ROS in ischemic/reperfused myocardium, a complex network of cellular and extracellular processes is discussed, including relationships with Ca2+ homeostasis, thiol group redox balance, hydrogen sulfide modulation, cross-talk with NAPDH oxidases, exosomes, cytokines and growth factors. While mechanistic insights are needed to improve our current therapeutic approaches, advancements in knowledge of ROS-mediated processes indicate that detrimental facets of oxidative stress are opposed by ROS requirement for physiological and protective reactions. This inevitable contrast is likely to underlie unsuccessful clinical trials and limits the development of novel cardioprotective interventions simply based upon ROS removal.
The present review summarizes the beneficial and detrimental roles of reactive oxygen species in myocardial ischemia/reperfusion injury and cardioprotection. In the first part, the continued need for cardioprotection beyond that by rapid reperfusion of acute myocardial infarction is emphasized. Then, pathomechanisms of myocardial ischemia/reperfusion to the myocardium and the coronary circulation and the different modes of cell death in myocardial infarction are characterized. Different mechanical and pharmacological interventions to protect the ischemic/reperfused myocardium in elective percutaneous coronary interventions and coronary artery bypass grafting, in acute myocardial infarction and in cardiotoxicity from cancer therapy are detailed. The second part keeps the focus on ROS providing a comprehensive overview of molecular and cellular mechanisms involved in ischemia/reperfusion injury. Starting from mitochondria as the main sources and targets of ROS in ischemic/reperfused myocardium, a complex network of cellular and extracellular processes is discussed, including relationships with Ca2+ homeostasis, thiol group redox balance, hydrogen sulfide modulation, cross-talk with NAPDH oxidases, exosomes, cytokines and growth factors. While mechanistic insights are needed to improve our current therapeutic approaches, advancements in knowledge of ROS-mediated processes indicate that detrimental facets of oxidative stress are opposed by ROS requirement for physiological and protective reactions. This inevitable contrast is likely to underlie unsuccessful clinical trials and limits the development of novel cardioprotective interventions simply based upon ROS removal.The present review summarizes the beneficial and detrimental roles of reactive oxygen species in myocardial ischemia/reperfusion injury and cardioprotection. In the first part, the continued need for cardioprotection beyond that by rapid reperfusion of acute myocardial infarction is emphasized. Then, pathomechanisms of myocardial ischemia/reperfusion to the myocardium and the coronary circulation and the different modes of cell death in myocardial infarction are characterized. Different mechanical and pharmacological interventions to protect the ischemic/reperfused myocardium in elective percutaneous coronary interventions and coronary artery bypass grafting, in acute myocardial infarction and in cardiotoxicity from cancer therapy are detailed. The second part keeps the focus on ROS providing a comprehensive overview of molecular and cellular mechanisms involved in ischemia/reperfusion injury. Starting from mitochondria as the main sources and targets of ROS in ischemic/reperfused myocardium, a complex network of cellular and extracellular processes is discussed, including relationships with Ca2+ homeostasis, thiol group redox balance, hydrogen sulfide modulation, cross-talk with NAPDH oxidases, exosomes, cytokines and growth factors. While mechanistic insights are needed to improve our current therapeutic approaches, advancements in knowledge of ROS-mediated processes indicate that detrimental facets of oxidative stress are opposed by ROS requirement for physiological and protective reactions. This inevitable contrast is likely to underlie unsuccessful clinical trials and limits the development of novel cardioprotective interventions simply based upon ROS removal.
The present review summarizes the beneficial and detrimental roles of reactive oxygen species in myocardial ischemia/reperfusion injury and cardioprotection. In the first part, the continued need for cardioprotection beyond that by rapid reperfusion of acute myocardial infarction is emphasized. Then, pathomechanisms of myocardial ischemia/reperfusion to the myocardium and the coronary circulation and the different modes of cell death in myocardial infarction are characterized. Different mechanical and pharmacological interventions to protect the ischemic/reperfused myocardium in elective percutaneous coronary interventions and coronary artery bypass grafting, in acute myocardial infarction and in cardiotoxicity from cancer therapy are detailed. The second part keeps the focus on ROS providing a comprehensive overview of molecular and cellular mechanisms involved in ischemia/reperfusion injury. Starting from mitochondria as the main sources and targets of ROS in ischemic/reperfused myocardium, a complex network of cellular and extracellular processes is discussed, including relationships with Ca 2+ homeostasis, thiol group redox balance, hydrogen sulfide modulation, cross-talk with NAPDH oxidases, exosomes, cytokines and growth factors. While mechanistic insights are needed to improve our current therapeutic approaches, advancements in knowledge of ROS-mediated processes indicate that detrimental facets of oxidative stress are opposed by ROS requirement for physiological and protective reactions. This inevitable contrast is likely to underlie unsuccessful clinical trials and limits the development of novel cardioprotective interventions simply based upon ROS removal. Image 1 • Ischemic heart disease is the most frequent cause of death worldwide. • Ischemia/reperfusion is the substrate of ischemic heart disease. • Cardioprotection reduces infarct size and coronary microvascular obstruction. • ROS are signals of cardioprotection and executors of injury. • Translation of cardioprotection to clinical benefits has been difficult so far. • The role of ROS in cardioprotection remains ambivalent.
The present review summarizes the beneficial and detrimental roles of reactive oxygen species in myocardial ischemia/reperfusion injury and cardioprotection. In the first part, the continued need for cardioprotection beyond that by rapid reperfusion of acute myocardial infarction is emphasized. Then, pathomechanisms of myocardial ischemia/reperfusion to the myocardium and the coronary circulation and the different modes of cell death in myocardial infarction are characterized. Different mechanical and pharmacological interventions to protect the ischemic/reperfused myocardium in elective percutaneous coronary interventions and coronary artery bypass grafting, in acute myocardial infarction and in cardiotoxicity from cancer therapy are detailed. The second part keeps the focus on ROS providing a comprehensive overview of molecular and cellular mechanisms involved in ischemia/reperfusion injury. Starting from mitochondria as the main sources and targets of ROS in ischemic/reperfused myocardium, a complex network of cellular and extracellular processes is discussed, including relationships with Ca2+ homeostasis, thiol group redox balance, hydrogen sulfide modulation, cross-talk with NAPDH oxidases, exosomes, cytokines and growth factors. While mechanistic insights are needed to improve our current therapeutic approaches, advancements in knowledge of ROS-mediated processes indicate that detrimental facets of oxidative stress are opposed by ROS requirement for physiological and protective reactions. This inevitable contrast is likely to underlie unsuccessful clinical trials and limits the development of novel cardioprotective interventions simply based upon ROS removal. [Display omitted] •Ischemic heart disease is the most frequent cause of death worldwide.•Ischemia/reperfusion is the substrate of ischemic heart disease.•Cardioprotection reduces infarct size and coronary microvascular obstruction.•ROS are signals of cardioprotection and executors of injury.•Translation of cardioprotection to clinical benefits has been difficult so far.•The role of ROS in cardioprotection remains ambivalent.
ArticleNumber 102894
Author Bertero, Edoardo
Shah, Ajay M.
Sellke, Frank
Eaton, Philip
Ibanez, Borja
Giacca, Mauro
Yellon, Derek M.
Bell, Robert
Hausenloy, Derek J.
Ferdinandy, Peter
Schulz, Rainer
Heusch, Gerd
Botker, Hans-Erik
Krieg, Thomas
Davidson, Sean M.
Thiele, Holger
Di Lisa, Fabio
Downey, James
Maack, Christoph
Andreadou, Ioanna
Gersh, Bernard J.
Author_xml – sequence: 1
  givenname: Gerd
  orcidid: 0000-0001-7078-4160
  surname: Heusch
  fullname: Heusch, Gerd
  email: gerd.heusch@uk-essen.de
  organization: Institute for Pathophysiology, West German Heart and Vascular Center, University of Duisburg-Essen, Essen, Germany
– sequence: 2
  givenname: Ioanna
  surname: Andreadou
  fullname: Andreadou, Ioanna
  organization: Laboratory of Pharmacology, Faculty of Pharmacy, National and Kapodistrian University of Athens, Athens, Greece
– sequence: 3
  givenname: Robert
  surname: Bell
  fullname: Bell, Robert
  organization: The Hatter Cardiovascular Institute, University College London, London, United Kingdom
– sequence: 4
  givenname: Edoardo
  surname: Bertero
  fullname: Bertero, Edoardo
  organization: Chair of Cardiovascular Disease, Department of Internal Medicine and Specialties, University of Genova, Genova, Italy
– sequence: 5
  givenname: Hans-Erik
  surname: Botker
  fullname: Botker, Hans-Erik
  organization: Department of Cardiology, Institute for Clinical Medicine, Aarhus University, Aarhus N, Denmark
– sequence: 6
  givenname: Sean M.
  surname: Davidson
  fullname: Davidson, Sean M.
  organization: The Hatter Cardiovascular Institute, University College London, London, United Kingdom
– sequence: 7
  givenname: James
  surname: Downey
  fullname: Downey, James
  organization: Department of Physiology, University of South Alabama, Mobile, AL, USA
– sequence: 8
  givenname: Philip
  surname: Eaton
  fullname: Eaton, Philip
  organization: William Harvey Research Institute, Queen Mary University of London, Heart Centre, Charterhouse Square, London, United Kingdom
– sequence: 9
  givenname: Peter
  surname: Ferdinandy
  fullname: Ferdinandy, Peter
  organization: Department of Pharmacology and Pharmacotherapy, Semmelweis University, Budapest, Hungary
– sequence: 10
  givenname: Bernard J.
  surname: Gersh
  fullname: Gersh, Bernard J.
  organization: Department of Cardiovascular Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN, USA
– sequence: 11
  givenname: Mauro
  surname: Giacca
  fullname: Giacca, Mauro
  organization: School of Cardiovascular and Metabolic Medicine & Sciences, King's College, London, United Kingdom
– sequence: 12
  givenname: Derek J.
  surname: Hausenloy
  fullname: Hausenloy, Derek J.
  organization: The Hatter Cardiovascular Institute, University College London, London, United Kingdom
– sequence: 13
  givenname: Borja
  surname: Ibanez
  fullname: Ibanez, Borja
  organization: Centro Nacional de Investigaciones Cardiovasculares (CNIC), IIS-Fundación Jiménez Díaz University Hospital, and CIBERCV, Madrid, Spain
– sequence: 14
  givenname: Thomas
  surname: Krieg
  fullname: Krieg, Thomas
  organization: Department of Medicine, University of Cambridge, Cambridge, United Kingdom
– sequence: 15
  givenname: Christoph
  surname: Maack
  fullname: Maack, Christoph
  organization: Department of Translational Research, Comprehensive Heart Failure Center, University Clinic Würzburg, Würzburg, Germany
– sequence: 16
  givenname: Rainer
  surname: Schulz
  fullname: Schulz, Rainer
  organization: Institute for Physiology, Justus-Liebig -Universität, Giessen, Germany
– sequence: 17
  givenname: Frank
  surname: Sellke
  fullname: Sellke, Frank
  organization: Division of Cardiothoracic Surgery, Alpert Medical School of Brown University and Rhode Island Hospital, Providence, RI, USA
– sequence: 18
  givenname: Ajay M.
  surname: Shah
  fullname: Shah, Ajay M.
  organization: King's College London British Heart Foundation Centre of Excellence, London, United Kingdom
– sequence: 19
  givenname: Holger
  surname: Thiele
  fullname: Thiele, Holger
  organization: Heart Center Leipzig at University of Leipzig and Leipzig Heart Science, Leipzig, Germany
– sequence: 20
  givenname: Derek M.
  surname: Yellon
  fullname: Yellon, Derek M.
  organization: The Hatter Cardiovascular Institute, University College London, London, United Kingdom
– sequence: 21
  givenname: Fabio
  surname: Di Lisa
  fullname: Di Lisa, Fabio
  email: fabio.dilisa@gmail.com
  organization: Dipartimento di Scienze Biomediche, Università degli studi di Padova, Padova, Italy
BackLink https://www.ncbi.nlm.nih.gov/pubmed/37839355$$D View this record in MEDLINE/PubMed
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Keywords Mitochondrion
Myocardial infarction
Cardioprotection
Reperfusion
Ischemic conditioning
Infarct size
Myocardial ischemia
Language English
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Snippet The present review summarizes the beneficial and detrimental roles of reactive oxygen species in myocardial ischemia/reperfusion injury and cardioprotection....
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SubjectTerms Cardioprotection
Humans
Infarct size
Ischemic conditioning
Mitochondrion
Myocardial infarction
Myocardial Infarction - metabolism
Myocardial ischemia
Myocardial Reperfusion Injury - metabolism
Myocardial Reperfusion Injury - prevention & control
Myocardium - metabolism
Oxidation-Reduction
Reactive Oxygen Species - metabolism
Reperfusion
Review
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Title Health position paper and redox perspectives on reactive oxygen species as signals and targets of cardioprotection
URI https://dx.doi.org/10.1016/j.redox.2023.102894
https://www.ncbi.nlm.nih.gov/pubmed/37839355
https://www.proquest.com/docview/2878020397
https://pubmed.ncbi.nlm.nih.gov/PMC10590874
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Volume 67
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