Mitochondria in the Cold (original) (raw)
Abstract
Development of hibernation strategies for cold preservation of human organs represents a far-reaching goal in transplantation surgery. Short cold storage times of <6 h tolerated by the human heart remain a major clinical problem. Mitochondrial cold storagereperfusion injury is becoming recognized as a limiting factor in preservation of organs from non-hibernating mammals. Damaged mitochondria lead to cellular injury by reduction of ATP supply, oxidative stress, disturbance of ion balance, cytochrome c release and induction of apoptosis and necrosis. Profiles of mitochondrial injuries differed after (1) cold preservation of isolated rat heart mitochondria, (2) cold preservation of the rat heart, and (3) after transplantation and rewarming/reperfusion. Importantly, a specific defect of complex I of the electron transport chain, uncoupling of oxidative phosphorylation and the pronounced release of cytochromec from mitochondria were absent after cold storage but developed during reperfusion, in proportion to the loss of heart function. Cold preservation of isolated heart mitochondria could be significantly prolonged by a mitochondrial preservation solution containing antioxidants, mitochondrial substrates, ATP, histidine, and oncotic agents. Successful cold storage of heart mitochondria demonstrates a large scope for improvement of heart preservation solutions. In this context, comparison of intracellular conditions and cold ischemia-reperfusion injury in hibernating and non-hibernating mammals may provide a rationale for improvement of clinical organ hibernation strategies.
Preview
Unable to display preview. Download preview PDF.
Similar content being viewed by others
References
- Bolling SF, Su T-P, Childs KF, Ning X-H, Horton N, Kilgore K, Oeltgen PR (1997) The use of hibernation induction triggers for cardiac transplant preservation. Transplantation 63: 326–329
Article PubMed CAS Google Scholar - Brustovetsky NN, Amerkhanov ZG, Popova Eyu, Konstantinov AA (1990) Reversible inhibition of electron transfer in the ubiquinol cytochrome c reductase segment of the mitochondrial respiratory chain in hibernating ground squirrels. FEBS Lett 263: 73–76
Article PubMed CAS Google Scholar - Brustovetsky NN, Egorova MV, Gnutov Dyu, Mokhova EN, Skulachev VP (1993) Cyclosporin A suppression of uncoupling in liver mitochondria of ground squirrel during arousal from hibernation. FEBS Lett 315: 233–236
Article PubMed CAS Google Scholar - Di Lisa F, Menabò R, Canton M, Petronilli V (1995) The role of mitochondria in the salvage and the injury of the ischemic myocardium. Biochim Biophys Acta 1366: 69–78
Google Scholar - Fedotcheva NJ, Sharyshev AA, Mironova GD, Kondrashova MN (1985) Inhibition of succinate oxidation and K+ transport in mitochondria during hibernation. Comp Biochem Physiol B 82: 191–195
PubMed CAS Google Scholar - Garlid KD, Paucek P, Yarov-Yarovoy V, Murray HN, Darbenzio RB, D’Alonzo AJ, Lodge NJ, Smith MA, Grover GJ (1997) Cardioprotective effect of diazoxide and its interaction with mitochondrial ATP-sensitive KC channels. Possible mechanism of cardioprotection. Circ Res 81: 1072–1082
Article PubMed CAS Google Scholar - Ghafourifar P, Klein SD, Schucht O, Schenk U, Pruschy M, Rocha S, Richter C (1999) Ceramide induces cytochrome c release from isolated mitochondria. Importance of mitochondrial redox state. J Biol Chem 274: 6080–6084
Article PubMed CAS Google Scholar - Gnaiger E, Lassnig B, Kuznetsov AV, Rieger G, Margreiter R (1998) Mitochondrial oxygen affinity, respiratory flux control and excess capacity of cytochrome c oxidase. J exp Biol 201: 1129–1139
PubMed CAS Google Scholar - Gnaiger E, Rieger G, Stadlmann S, Amberger A, Eberl T, Margreiter R (1999) Mitochondrial defect in endothelial cold ischemia/reperfusion injury. Transplant Proc 31: 994–995
Article PubMed CAS Google Scholar - Gnaiger E, Steinlechner-Maran R, Méndez G, Eberl T, Margreiter R (1995) Control of mitochondrial and cellular respiration by oxygen. J Bioenerg Biomembr 27: 583–596
Article PubMed CAS Google Scholar - Heldmaier G, Klingenspor M, Werneyer M, Lampi BJ, Brooks SP, Storey B (1999) Metabolic adjustments during daily torpor in the Djungarian hamster. Am J Physiol 276: E896-E906
PubMed CAS Google Scholar - Heldrnaier G, Ruf T(1992) Body temperature and metabolic rate during natural hypothermia in endotherms. J Comp Physiol B 162: 696–706
Article Google Scholar - Hochachka PW, Guppy M(1987) Metabolic arrest and the control of biological time. Harvard University Press, Cambridge, Mass.
Google Scholar - Kay L, Daneshrad Z, Saks VA, Rossi A (1997) Alteration in the control of mitochondrial respiration by outer mitochondrial membrane and creatine during heart preservation. Cardiovasc Res 34: 547–556
Article PubMed CAS Google Scholar - Ku K, Oku H, Alam MS, Saitoh Y, Nosaka S, Nakayama K (1997) Prolonged hypothermic cardiac storage with histidine-tryptophan-ketoglutarate solution. Transplantation 64: 971–975
Article PubMed CAS Google Scholar - Kuznetsov AV, Brandacher G, Steurer W, Margreiter R, Gnaiger E (1999) Estimation of mitochondrial damage in heart preservation. Transplant Proc 31: 992
Article PubMed CAS Google Scholar - Kuznetsov AV, Brandacher G, Steurer W, Margreiter R, Gnaiger E (2000) Isolated rat heart mitochondria and whole rat heart as models for mitochondrial cold ischemia-reperfusion injury. Transplant Proc 32 (in press)
Google Scholar - Lemasters JJ, Bond JM, Currin RT, Nieminen A-L, Caldwell-Kenkel JC, Harrison DC, Kaplan SH, Cascio WE, Thurman RG, Gores GJ, Herman B (1993) Reperfusion injury to heart and liver cells: Protection by acidosis during ischemia and a “pH paradox” after reperfusion. In: Hochachka PW, Lutz PL, Sick T, Rosenthal M, Van den Thillart G (eds.) Surviving hypoxia: Mechanisms of control and adaptation. CRC Press, Boca Raton Ann Arbor London Tokyo, pp 495–507
Google Scholar - Martin SL, Maniero GD, Carey C, Hand SC (1999) Reversible depression of oxygen consumption in isolated liver mitochondria during hibernation. Physiol Biochem Zool 72: 255–264
Article PubMed CAS Google Scholar - Menasché P, Pradier F, Grousset C, Peynet J, Mouas C, Bloch G, Piwnica A (1993) Improved recovery of heart transplants with a specific kit of preservation solutions. J Thorac Cardiovasc Surg 105: 353–363
PubMed Google Scholar - Opie LH (1997) The heart. Physiology, from cell to circulation. Lippincott-Raven, Philadelphia New York
Google Scholar - Parce JW, Spach PI, Cunningham CC (1980) Deterioration of rat liver mitochondria under conditions of metabolite deprivation. Biochem J 188: 817–822
PubMed CAS Google Scholar - Saks VA, Veksler VI, Kuznetsov AV, Kay L, Sikk P, Tiivel T, Tranqui L, Olivares J, Winkler K, Wiedemann F, Kunz WS (1998) Permeabilized cell and skinned fiber techniques in studies of mitochondrial function in vivo. Mol Cell Biochem 184: 81–100
Article PubMed CAS Google Scholar - Scholte HR, Yu Y, Ross JD, Oosterkamp II, Boonman AM, Busch HF (1997) Rapid isolation of muscle and heart mitochondria, the lability of oxidative phosphorylation and attempts to stabilize the process in vitro by taurine, carnitine and other compounds. Mol Cell Biochem 174: 61–66
Article PubMed CAS Google Scholar - Southard JH, Belzer FO (1995) Organ preservation. Annu Rev Med 46: 235–247
Article PubMed CAS Google Scholar - Steinlechner-Maran R, Eberl T, Kunc M, Schröcksnadel H, Margreiter R, Gnaiger E (1997) Respiratory defect as an early event in preservation/reoxygenation injury in endothelial cells. Transplantation 63: 136–142
Article PubMed CAS Google Scholar - Storey KB (1997) Metabolic regulation in mammalian hibernation: enzyme and protein adaptations. Comp Biochem Physiol A 118: 1115–1124
Article CAS Google Scholar - Sumeray MS, Yellon DM (1999) Ischemic preconditioning. In: Grace PA, Mathie RT (eds) Ischemia-reperfusion injury.Blackwell Science, Oxford, pp 328–343
Google Scholar - Tseng EE, Cameron DE (1999) Myocardial protection from ischemia-reperfusion injury in cardiac surgery. In: Grace PA, Mathie RT (eds) Ischemia-reperfusion injury.Blackwell Science, Oxford, pp 344–356
Google Scholar
Author information
Authors and Affiliations
- Department of Transplant Surgery, D. Swarovski Research Laboratory, University Hospital Innsbruck, A-6020, Innsbruck, Austria
Erich Gnaiger, Andrej V. Kuznetsov, Stefan Schneeberger, RÜdiger Seiler, Gerald Brandacher, Wolfgang Steurer & Raimund Margreiter
Authors
- Erich Gnaiger
You can also search for this author inPubMed Google Scholar - Andrej V. Kuznetsov
You can also search for this author inPubMed Google Scholar - Stefan Schneeberger
You can also search for this author inPubMed Google Scholar - RÜdiger Seiler
You can also search for this author inPubMed Google Scholar - Gerald Brandacher
You can also search for this author inPubMed Google Scholar - Wolfgang Steurer
You can also search for this author inPubMed Google Scholar - Raimund Margreiter
You can also search for this author inPubMed Google Scholar
Editor information
Editors and Affiliations
- Department of Biology, Philipps University, 35032, Marburg, Germany
Gerhard Heldmaier & Martin Klingenspor &
Rights and permissions
Copyright information
© 2000 Springer-Verlag Berlin Heidelberg
About this paper
Cite this paper
Gnaiger, E. et al. (2000). Mitochondria in the Cold. In: Heldmaier, G., Klingenspor, M. (eds) Life in the Cold. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-04162-8\_45
Download citation
- .RIS
- .ENW
- .BIB
- DOI: https://doi.org/10.1007/978-3-662-04162-8\_45
- Publisher Name: Springer, Berlin, Heidelberg
- Print ISBN: 978-3-642-08682-3
- Online ISBN: 978-3-662-04162-8
- eBook Packages: Springer Book Archive