The role of succinate and ROS in reperfusion injury – A critical appraisal
We critically assess the proposal that succinate-fuelled reverse electron flow (REF) drives mitochondrial matrix superoxide production from Complex I early in reperfusion, thus acting as a key mediator of ischemia/reperfusion (IR) injury. Real-time surface fluorescence measurements of NAD(P)H and fl...
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| Published in | Journal of molecular and cellular cardiology Vol. 110; pp. 1 - 14 |
|---|---|
| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
Elsevier Ltd
01.09.2017
Academic Press |
| Subjects | |
| Online Access | Get full text |
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| Abstract | We critically assess the proposal that succinate-fuelled reverse electron flow (REF) drives mitochondrial matrix superoxide production from Complex I early in reperfusion, thus acting as a key mediator of ischemia/reperfusion (IR) injury. Real-time surface fluorescence measurements of NAD(P)H and flavoprotein redox state suggest that conditions are unfavourable for REF during early reperfusion. Furthermore, rapid loss of succinate accumulated during ischemia can be explained by its efflux rather than oxidation. Moreover, succinate accumulation during ischemia is not attenuated by ischemic preconditioning (IP) despite powerful cardioprotection. In addition, measurement of intracellular reactive oxygen species (ROS) during reperfusion using surface fluorescence and mitochondrial aconitase activity detected major increases in ROS only after mitochondrial permeability transition pore (mPTP) opening was first detected. We conclude that mPTP opening is probably triggered initially by factors other than ROS, including increased mitochondrial [Ca2+]. However, IP only attenuates [Ca2+] increases later in reperfusion, again after initial mPTP opening, implying that IP regulates mPTP opening through additional mechanisms. One such is mitochondria-bound hexokinase 2 (HK2) which dissociates from mitochondria during ischemia in control hearts but not those subject to IP. Indeed, there is a strong correlation between the extent of HK2 loss from mitochondria during ischemia and infarct size on subsequent reperfusion. Mechanisms linking HK2 dissociation to mPTP sensitisation remain to be fully established but several related processes have been implicated including VDAC1 oligomerisation, the stability of contact sites between the inner and outer membranes, cristae morphology, Bcl-2 family members and mitochondrial fission proteins such as Drp1.
[Display omitted]
•Mitochondrial ROS production during early reperfusion (RPF) occurs after mPTP opening.•Conditions do not favour ROS production by reverse electron flow during early RPF.•Ischemic preconditioning (IP) does not attenuate succinate accumulation in ischemia.•IP reduction of ROS and Ca2+ during RPF is secondary to attenuation of mPTP opening.•IP attenuates mPTP opening by mechanisms independent of ROS and Ca2+ such as HK2. |
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| AbstractList | We critically assess the proposal that succinate-fuelled reverse electron flow (REF) drives mitochondrial matrix superoxide production from Complex I early in reperfusion, thus acting as a key mediator of ischemia/reperfusion (IR) injury. Real-time surface fluorescence measurements of NAD(P)H and flavoprotein redox state suggest that conditions are unfavourable for REF during early reperfusion. Furthermore, rapid loss of succinate accumulated during ischemia can be explained by its efflux rather than oxidation. Moreover, succinate accumulation during ischemia is not attenuated by ischemic preconditioning (IP) despite powerful cardioprotection. In addition, measurement of intracellular reactive oxygen species (ROS) during reperfusion using surface fluorescence and mitochondrial aconitase activity detected major increases in ROS only after mitochondrial permeability transition pore (mPTP) opening was first detected. We conclude that mPTP opening is probably triggered initially by factors other than ROS, including increased mitochondrial [Ca2+]. However, IP only attenuates [Ca2+] increases later in reperfusion, again after initial mPTP opening, implying that IP regulates mPTP opening through additional mechanisms. One such is mitochondria-bound hexokinase 2 (HK2) which dissociates from mitochondria during ischemia in control hearts but not those subject to IP. Indeed, there is a strong correlation between the extent of HK2 loss from mitochondria during ischemia and infarct size on subsequent reperfusion. Mechanisms linking HK2 dissociation to mPTP sensitisation remain to be fully established but several related processes have been implicated including VDAC1 oligomerisation, the stability of contact sites between the inner and outer membranes, cristae morphology, Bcl-2 family members and mitochondrial fission proteins such as Drp1.We critically assess the proposal that succinate-fuelled reverse electron flow (REF) drives mitochondrial matrix superoxide production from Complex I early in reperfusion, thus acting as a key mediator of ischemia/reperfusion (IR) injury. Real-time surface fluorescence measurements of NAD(P)H and flavoprotein redox state suggest that conditions are unfavourable for REF during early reperfusion. Furthermore, rapid loss of succinate accumulated during ischemia can be explained by its efflux rather than oxidation. Moreover, succinate accumulation during ischemia is not attenuated by ischemic preconditioning (IP) despite powerful cardioprotection. In addition, measurement of intracellular reactive oxygen species (ROS) during reperfusion using surface fluorescence and mitochondrial aconitase activity detected major increases in ROS only after mitochondrial permeability transition pore (mPTP) opening was first detected. We conclude that mPTP opening is probably triggered initially by factors other than ROS, including increased mitochondrial [Ca2+]. However, IP only attenuates [Ca2+] increases later in reperfusion, again after initial mPTP opening, implying that IP regulates mPTP opening through additional mechanisms. One such is mitochondria-bound hexokinase 2 (HK2) which dissociates from mitochondria during ischemia in control hearts but not those subject to IP. Indeed, there is a strong correlation between the extent of HK2 loss from mitochondria during ischemia and infarct size on subsequent reperfusion. Mechanisms linking HK2 dissociation to mPTP sensitisation remain to be fully established but several related processes have been implicated including VDAC1 oligomerisation, the stability of contact sites between the inner and outer membranes, cristae morphology, Bcl-2 family members and mitochondrial fission proteins such as Drp1. We critically assess the proposal that succinate-fuelled reverse electron flow (REF) drives mitochondrial matrix superoxide production from Complex I early in reperfusion, thus acting as a key mediator of ischemia/reperfusion (IR) injury. Real-time surface fluorescence measurements of NAD(P)H and flavoprotein redox state suggest that conditions are unfavourable for REF during early reperfusion. Furthermore, rapid loss of succinate accumulated during ischemia can be explained by its efflux rather than oxidation. Moreover, succinate accumulation during ischemia is not attenuated by ischemic preconditioning (IP) despite powerful cardioprotection. In addition, measurement of intracellular reactive oxygen species (ROS) during reperfusion using surface fluorescence and mitochondrial aconitase activity detected major increases in ROS only after mitochondrial permeability transition pore (mPTP) opening was first detected. We conclude that mPTP opening is probably triggered initially by factors other than ROS, including increased mitochondrial [Ca2+]. However, IP only attenuates [Ca2+] increases later in reperfusion, again after initial mPTP opening, implying that IP regulates mPTP opening through additional mechanisms. One such is mitochondria-bound hexokinase 2 (HK2) which dissociates from mitochondria during ischemia in control hearts but not those subject to IP. Indeed, there is a strong correlation between the extent of HK2 loss from mitochondria during ischemia and infarct size on subsequent reperfusion. Mechanisms linking HK2 dissociation to mPTP sensitisation remain to be fully established but several related processes have been implicated including VDAC1 oligomerisation, the stability of contact sites between the inner and outer membranes, cristae morphology, Bcl-2 family members and mitochondrial fission proteins such as Drp1. [Display omitted] •Mitochondrial ROS production during early reperfusion (RPF) occurs after mPTP opening.•Conditions do not favour ROS production by reverse electron flow during early RPF.•Ischemic preconditioning (IP) does not attenuate succinate accumulation in ischemia.•IP reduction of ROS and Ca2+ during RPF is secondary to attenuation of mPTP opening.•IP attenuates mPTP opening by mechanisms independent of ROS and Ca2+ such as HK2. We critically assess the proposal that succinate-fuelled reverse electron flow (REF) drives mitochondrial matrix superoxide production from Complex I early in reperfusion, thus acting as a key mediator of ischemia/reperfusion (IR) injury. Real-time surface fluorescence measurements of NAD(P)H and flavoprotein redox state suggest that conditions are unfavourable for REF during early reperfusion. Furthermore, rapid loss of succinate accumulated during ischemia can be explained by its efflux rather than oxidation. Moreover, succinate accumulation during ischemia is not attenuated by ischemic preconditioning (IP) despite powerful cardioprotection. In addition, measurement of intracellular reactive oxygen species (ROS) during reperfusion using surface fluorescence and mitochondrial aconitase activity detected major increases in ROS only after mitochondrial permeability transition pore (mPTP) opening was first detected. We conclude that mPTP opening is probably triggered initially by factors other than ROS, including increased mitochondrial [Ca ]. However, IP only attenuates [Ca ] increases later in reperfusion, again after initial mPTP opening, implying that IP regulates mPTP opening through additional mechanisms. One such is mitochondria-bound hexokinase 2 (HK2) which dissociates from mitochondria during ischemia in control hearts but not those subject to IP. Indeed, there is a strong correlation between the extent of HK2 loss from mitochondria during ischemia and infarct size on subsequent reperfusion. Mechanisms linking HK2 dissociation to mPTP sensitisation remain to be fully established but several related processes have been implicated including VDAC1 oligomerisation, the stability of contact sites between the inner and outer membranes, cristae morphology, Bcl-2 family members and mitochondrial fission proteins such as Drp1. We critically assess the proposal that succinate-fuelled reverse electron flow (REF) drives mitochondrial matrix superoxide production from Complex I early in reperfusion, thus acting as a key mediator of ischemia/reperfusion (IR) injury. Real-time surface fluorescence measurements of NAD(P)H and flavoprotein redox state suggest that conditions are unfavourable for REF during early reperfusion. Furthermore, rapid loss of succinate accumulated during ischemia can be explained by its efflux rather than oxidation. Moreover, succinate accumulation during ischemia is not attenuated by ischemic preconditioning (IP) despite powerful cardioprotection. In addition, measurement of intracellular reactive oxygen species (ROS) during reperfusion using surface fluorescence and mitochondrial aconitase activity detected major increases in ROS only after mitochondrial permeability transition pore (mPTP) opening was first detected. We conclude that mPTP opening is probably triggered initially by factors other than ROS, including increased mitochondrial [Ca 2+ ]. However, IP only attenuates [Ca 2+ ] increases later in reperfusion, again after initial mPTP opening, implying that IP regulates mPTP opening through additional mechanisms. One such is mitochondria-bound hexokinase 2 (HK2) which dissociates from mitochondria during ischemia in control hearts but not those subject to IP. Indeed, there is a strong correlation between the extent of HK2 loss from mitochondria during ischemia and infarct size on subsequent reperfusion. Mechanisms linking HK2 dissociation to mPTP sensitisation remain to be fully established but several related processes have been implicated including VDAC1 oligomerisation, the stability of contact sites between the inner and outer membranes, cristae morphology, Bcl-2 family members and mitochondrial fission proteins such as Drp1. Image 1 • Mitochondrial ROS production during early reperfusion (RPF) occurs after mPTP opening. • Conditions do not favour ROS production by reverse electron flow during early RPF. • Ischemic preconditioning (IP) does not attenuate succinate accumulation in ischemia. • IP reduction of ROS and Ca 2+ during RPF is secondary to attenuation of mPTP opening. • IP attenuates mPTP opening by mechanisms independent of ROS and Ca 2+ such as HK2. |
| Author | Pasdois, Philippe Ovens, Matthew J. Andrienko, Tatyana N. Halestrap, Andrew P. Pereira, Gonçalo C. |
| AuthorAffiliation | School of Biochemistry and The Bristol Heart Institute, Medical Sciences Building, University of Bristol, Bristol BS8 1TD, UK |
| AuthorAffiliation_xml | – name: School of Biochemistry and The Bristol Heart Institute, Medical Sciences Building, University of Bristol, Bristol BS8 1TD, UK |
| Author_xml | – sequence: 1 givenname: Tatyana N. surname: Andrienko fullname: Andrienko, Tatyana N. – sequence: 2 givenname: Philippe surname: Pasdois fullname: Pasdois, Philippe – sequence: 3 givenname: Gonçalo C. surname: Pereira fullname: Pereira, Gonçalo C. – sequence: 4 givenname: Matthew J. surname: Ovens fullname: Ovens, Matthew J. – sequence: 5 givenname: Andrew P. orcidid: 0000-0001-5374-2778 surname: Halestrap fullname: Halestrap, Andrew P. email: A.Halestrap@bristol.ac.uk |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28689004$$D View this record in MEDLINE/PubMed |
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| Keywords | Bcl-2 DHE Heart Reactive oxygen species HK Ischemia/reperfusion injury Calcium BCECF ANT LS pmf Mdivi-1 mPTP 5-cH2DCFDA G-6-P Drp1 Mitochondria PO1 Permeability transition pore Bid PCr CrP Bad NCLX Succinate IP CK IMM PKCε IR SOD Bak OMM Hexokinase CsA GSK3β Bcl-xL REF MitoPY1 IF1 ROS Bax VDAC Cyp-D MCU |
| Language | English |
| License | This is an open access article under the CC BY license. Copyright © 2017 The Authors. Published by Elsevier Ltd.. All rights reserved. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 ObjectType-Review-3 content type line 23 Current address: IHU-LIRYC, Inserm U1045, Université de Bordeaux, 33600 Pessac, France. |
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| PublicationTitle | Journal of molecular and cellular cardiology |
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| Snippet | We critically assess the proposal that succinate-fuelled reverse electron flow (REF) drives mitochondrial matrix superoxide production from Complex I early in... |
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| SubjectTerms | Animals Calcium Electron Transport Complex I - metabolism Heart Hexokinase Humans Ischemia/reperfusion injury Mitochondria Mitochondria, Heart - metabolism Mitochondrial Membrane Transport Proteins - metabolism Mitochondrial Permeability Transition Pore Myocardial Reperfusion Injury - metabolism Permeability transition pore Reactive oxygen species Reactive Oxygen Species - metabolism Succinate Succinic Acid - metabolism |
| Title | The role of succinate and ROS in reperfusion injury – A critical appraisal |
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