Succinate accumulation drives ischaemia-reperfusion injury during organ transplantation.


Journal

Nature metabolism
ISSN: 2522-5812
Titre abrégé: Nat Metab
Pays: Germany
ID NLM: 101736592

Informations de publication

Date de publication:
30 09 2019
Historique:
entrez: 13 5 2020
pubmed: 13 5 2020
medline: 13 5 2020
Statut: ppublish

Résumé

During heart transplantation, storage in cold preservation solution is thought to protect the organ by slowing metabolism; by providing osmotic support; and by minimising ischaemia-reperfusion (IR) injury upon transplantation into the recipient

Identifiants

pubmed: 32395697
doi: 10.1038/s42255-019-0115-y
pmc: PMC7212038
mid: EMS84126
pii: 10.1038/s42255-019-0115-y
doi:

Substances chimiques

Succinic Acid AB6MNQ6J6L

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Pagination

966-974

Subventions

Organisme : Wellcome Trust
ID : 110158
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_00015/3
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_U105674181
Pays : United Kingdom
Organisme : Department of Health
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_12022/6
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_U105663142
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_EX_MR/M015769/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 110159
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 110158/Z/15/Z
Pays : United Kingdom

Déclaration de conflit d'intérêts

Competing interests The authors declare competing interests. MPM, TK AND RCH have submitted a patent application on the use of dimethyl malonate to prevent ischaemia reperfusion injury.

Références

Jahania, M. S., Sanchez, J. A., Narayan, P., Lasley, R. D. & Mentzer, R. M. Jr. Heart preservation for transplantation: principles and strategies. Ann. Thorac. Surg. 68, 1983–1987 (1999).
doi: 10.1016/S0003-4975(99)01028-0
Southard, J. H. & Belzer, F. O. Organ preservation. Annu. Rev. Med. 46, 235–247 (1995).
doi: 10.1146/annurev.med.46.1.235
Chouchani, E. T. et al. A unifying mechanism for mitochondrial superoxide production during ischemia-reperfusion injury. Cell Metab. 23, 254–263 (2016).
doi: 10.1016/j.cmet.2015.12.009
Chouchani, E. T. et al. Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS. Nature 515, 431–435 (2014).
doi: 10.1038/nature13909
Pagani, F. D. Use of heart donors following circulatory death: a viable addition to the heart donor pool. J. Am. Coll. Cardiol. 73, 1460–1462 (2019).
doi: 10.1016/j.jacc.2018.12.068
Johnson, R. J., Bradbury, L. L., Martin, K. & Neuberger, J. Organ donation and transplantation in the UK-the last decade: a report from the UK national transplant registry. Transplantation 97, S1–S27 (2014).
doi: 10.1097/01.TP.0000438215.16737.68
Chew, H. C. et al. Outcomes of donation after circulatory death heart transplantation in australia. J. Am. Coll. Cardiol. 73, 1447–1459 (2019).
doi: 10.1016/j.jacc.2018.12.067
Dhital, K. K. et al. Adult heart transplantation with distant procurement and ex-vivo preservation of donor hearts after circulatory death: a case series. Lancet 385, 2585–2591 (2015).
doi: 10.1016/S0140-6736(15)60038-1
Nasralla, D. et al. A randomized trial of normothermic preservation in liver transplantation. Nature 557, 50–56 (2018).
doi: 10.1038/s41586-018-0047-9
Coffey, J. C. et al. The influence of functional warm ischemia time on DCD liver transplant recipients’ outcomes. Clin. Transplant. 31, e13068 (2017).
doi: 10.1111/ctr.13068
Blok, J. J. et al. Longterm results of liver transplantation from donation after circulatory death. Liver Transplant. 22, 1107–1114 (2016).
doi: 10.1002/lt.24449
Eltzschig, H. K. & Eckle, T. Ischemia and reperfusion—from mechanism to translation. Nat. Med. 17, 1391–1401 (2011).
doi: 10.1038/nm.2507
Liu, F. & Kang, S. M. Heterotopic heart transplantation in mice. J. Vis. Exp. 6, 238 (2007).
Niimi, M. The technique for heterotopic cardiac transplantation in mice: experience of 3000 operations by one surgeon. J. Heart Lung Transplant. 20, 1123–1128 (2001).
doi: 10.1016/S1053-2498(01)00309-6
Zhang, Q. et al. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464, 104–107 (2010).
doi: 10.1038/nature08780
Nakahira, K. et al. Circulating mitochondrial DNA in patients in the ICU as a marker of mortality: derivation and validation. PLoS Med. 10, e1001577 (2013).
doi: 10.1371/journal.pmed.1001577
Ehinger, J. K. et al. Cell-permeable succinate prodrugs bypass mitochondrial complex I deficiency. Nat. Commun. 7, 12317 (2016).
doi: 10.1038/ncomms12317
Valls-Lacalle, L. et al. Selective inhibition of succinate dehydrogenase in reperfused myocardium with intracoronary malonate reduces infarct size. Sci. Rep. 8, 2442 (2018).
doi: 10.1038/s41598-018-20866-4
Valls-Lacalle, L. et al. Succinate dehydrogenase inhibition with malonate during reperfusion reduces infarct size by preventing mitochondrial permeability transition. Cardiovasc. Res. 109, 374–384 (2016).
doi: 10.1093/cvr/cvv279
Bundgaard, A. et al. Metabolic adaptations during extreme anoxia in the turtle heart and their implications for ischemia-reperfusion injury. Sci. Rep. 9, 2850 (2019).
doi: 10.1038/s41598-019-39836-5
Zhang, J. et al. Accumulation of succinate in cardiac ischemia primarily occurs via canonical krebs cycle activity. Cell Rep. 23, 2617–2628 (2018).
doi: 10.1016/j.celrep.2018.04.104
Dare, A. J. et al. The mitochondria-targeted anti-oxidant MitoQ decreases ischemia-reperfusion injury in a murine syngeneic heart transplant model. J. Heart Lung Transplant. 34, 1471–1480 (2015).
doi: 10.1016/j.healun.2015.05.007
Mackay, G. M., Zheng, L., van den Broek, N. J. & Gottlieb, E. Analysis of cell metabolism using LC-MS and isotope tracers. Meth. Enzymol. 561, 171–196 (2015).
doi: 10.1016/bs.mie.2015.05.016
Strehler, B. L. in Methods in Enzymatic Analysis (ed. Bergmeyer, U.) 2112–2126 (Academic Press, 1974).
Passonneau, J. V. & Lauderdale, V. R. A comparison of three methods of glycogen measurement in tissues. Anal. Biochem. 60, 405–412 (1974).
doi: 10.1016/0003-2697(74)90248-6
Santos, J. H., Meyer, J. N., Mandavilli, B. S. & Van Houten, B. Quantitative PCR-based measurement of nuclear and mitochondrial DNA damage and repair in mammalian cells. Methods Mol. Biol. 314, 183–199 (2006).
doi: 10.1385/1-59259-973-7:183
Ritchie, M. E. et al. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nuc. Acids Res. 43, e47 (2015).
doi: 10.1093/nar/gkv007

Auteurs

Jack L Martin (JL)

Department of Surgery and Cambridge NIHR Biomedical Research Centre, Biomedical Campus, University of Cambridge, Cambridge, UK.

Ana S H Costa (ASH)

MRC Cancer Unit, University of Cambridge, Hutchison/MRC Research Centre, Cambridge, UK.

Anja V Gruszczyk (AV)

Department of Surgery and Cambridge NIHR Biomedical Research Centre, Biomedical Campus, University of Cambridge, Cambridge, UK.
MRC Mitochondrial Biology Unit, University of Cambridge, Cambridge, UK.

Timothy E Beach (TE)

Department of Surgery and Cambridge NIHR Biomedical Research Centre, Biomedical Campus, University of Cambridge, Cambridge, UK.

Fay M Allen (FM)

MRC Mitochondrial Biology Unit, University of Cambridge, Cambridge, UK.

Hiran A Prag (HA)

MRC Mitochondrial Biology Unit, University of Cambridge, Cambridge, UK.

Elizabeth C Hinchy (EC)

MRC Mitochondrial Biology Unit, University of Cambridge, Cambridge, UK.

Krishnaa Mahbubani (K)

Department of Surgery and Cambridge NIHR Biomedical Research Centre, Biomedical Campus, University of Cambridge, Cambridge, UK.

Mazin Hamed (M)

Department of Surgery and Cambridge NIHR Biomedical Research Centre, Biomedical Campus, University of Cambridge, Cambridge, UK.

Laura Tronci (L)

MRC Cancer Unit, University of Cambridge, Hutchison/MRC Research Centre, Cambridge, UK.

Efterpi Nikitopoulou (E)

MRC Cancer Unit, University of Cambridge, Hutchison/MRC Research Centre, Cambridge, UK.

Andrew M James (AM)

MRC Mitochondrial Biology Unit, University of Cambridge, Cambridge, UK.

Thomas Krieg (T)

Department of Medicine, University of Cambridge, Cambridge, UK.

Alan J Robinson (AJ)

MRC Mitochondrial Biology Unit, University of Cambridge, Cambridge, UK.

Margaret M Huang (MM)

Department of Surgery and Cambridge NIHR Biomedical Research Centre, Biomedical Campus, University of Cambridge, Cambridge, UK.
MRC Mitochondrial Biology Unit, University of Cambridge, Cambridge, UK.

Stuart T Caldwell (ST)

School of Chemistry, University of Glasgow, Glasgow, UK.

Angela Logan (A)

MRC Mitochondrial Biology Unit, University of Cambridge, Cambridge, UK.

Laura Pala (L)

School of Chemistry, University of Glasgow, Glasgow, UK.

Richard C Hartley (RC)

School of Chemistry, University of Glasgow, Glasgow, UK.

Christian Frezza (C)

MRC Cancer Unit, University of Cambridge, Hutchison/MRC Research Centre, Cambridge, UK.

Kourosh Saeb-Parsy (K)

Department of Surgery and Cambridge NIHR Biomedical Research Centre, Biomedical Campus, University of Cambridge, Cambridge, UK.

Michael P Murphy (MP)

MRC Mitochondrial Biology Unit, University of Cambridge, Cambridge, UK. mpm@mrc-mbu.cam.ac.uk.
Department of Medicine, University of Cambridge, Cambridge, UK. mpm@mrc-mbu.cam.ac.uk.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH