Mitochondrial Calcium Uptake Regulates Cold Preservation-Induced Bax Translocation and Early Reperfusion Apoptosis

Porte, 1998, Long-term graft survival after liver transplantation in the UW era: late effects of cold ischemia and primary dysfunction. European Multicentre Study Group, Transpl Int, 11, S164, 10.1007/s001470050452 Serracino-Inglott, 2001, Hepatic ischemia-reperfusion injury, Am J Surg, 181, 160, 10.1016/S0002-9610(00)00573-0 Vollmar, 1994, Hepatic microcirculatory perfusion failure is a determinant of liver dysfunction in warm ischemia-reperfusion, Am J Pathol, 145, 1421 Colletti, 1996, The role of cytokine networks in the local liver injury following hepatic ischemia/reperfusion in the rat, Hepatology, 23, 506, 10.1002/hep.510230315 Shirasugi, 1997, Up-regulation of oxygen-derived free radicals by interleukin-1 in hepatic ischemia/reperfusion injury, Transplantation, 64, 1398, 10.1097/00007890-199711270-00004 Bernardi, 1999, Mitochondrial transport of cations: channels, exchangers, and permeability transition, Physiol Rev, 79, 1127, 10.1152/physrev.1999.79.4.1127 Orrenius, 2003, Regulation of cell death: the calcium-apoptosis link, Nat Rev Mol Cell Biol, 4, 552, 10.1038/nrm1150 Farber, 1990, The role of calcium in lethal cell injury, Chem Res Toxicol, 3, 503, 10.1021/tx00018a003 Eskes, 1998, Bax-induced cytochrome C release from mitochondria is independent of the permeability transition pore but highly dependent on Mg2+ ions, J Cell Biol, 143, 217, 10.1083/jcb.143.1.217 Farber, 1990, The role of calcium ions in toxic cell injury, Environ Health Perspect, 84, 107, 10.1289/ehp.9084107 Blankensteijn, 1991, Liver preservation: the past and the future, Hepatology, 13, 1235, 10.1002/hep.1840130633 Janicki, 2001, Interspecies differences in hepatic Ca (2+) -ATPase activity and the effect of cold preservation on porcine liver Ca (2+) -ATPase function, Liver Transpl, 7, 132, 10.1053/jlts.2001.21459 Amberger, 2001, A subpopulation of mitochondria prevents cytosolic calcium overload in endothelial cells after cold ischemia/reperfusion, Transplantation, 71, 1821, 10.1097/00007890-200106270-00019 Litsky, 1997, Regulation of the mitochondrial Ca2+ uniporter by external adenine nucleotides: the uniporter behaves like a gated channel which is regulated by nucleotides and divalent cations, Biochemistry, 36, 7071, 10.1021/bi970180y Bernardi, 1999, Mitochondria and cell death. Mechanistic aspects and methodological issues, Eur J Biochem, 264, 687, 10.1046/j.1432-1327.1999.00725.x Kroemer, 1998, The mitochondrial death/life regulator in apoptosis and necrosis, Annu Rev Physiol, 60, 619, 10.1146/annurev.physiol.60.1.619 Kim, 1998, Alteration in cellular calcium and mitochondrial functions in the rat liver during cold preservation, Transplantation, 65, 369, 10.1097/00007890-199802150-00012 Crompton, 1999, The mitochondrial permeability transition pore and its role in cell death, Biochem J, 341, 233, 10.1042/bj3410233 Kroemer, 2000, Mitochondrial control of cell death, Nat Med, 6, 513, 10.1038/74994 Brustovetsky, 1996, Mitochondrial ADP/ATP carrier can be reversibly converted into a large channel by Ca2+, Biochemistry, 35, 8483, 10.1021/bi960833v Lim, 2003, On the Release of cytochrome c from mitochondria during cell death signaling, J Clin Oncol, 9, 488 Desagher, 1999, Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis, J Cell Biol, 144, 891, 10.1083/jcb.144.5.891 Nutt, 2002, Bax-mediated Ca2+ mobilization promotes cytochrome c release during apoptosis, J Biol Chem, 277, 20301, 10.1074/jbc.M201604200 Nutt, 2002, Bax and Bak promote apoptosis by modulating endoplasmic reticular and mitochondrial Ca2+ stores, J Biol Chem, 277, 9219, 10.1074/jbc.M106817200 Liu, 1996, Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c, Cell, 86, 147, 10.1016/S0092-8674(00)80085-9 Lorenzo, 1999, Apoptosis inducing factor (AIF): a phylogenetically old, caspase- independent effector of cell death, Cell Death Differ, 6, 516, 10.1038/sj.cdd.4400527 Du, 2000, Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition, Cell, 102, 33, 10.1016/S0092-8674(00)00008-8 Luthra, 1977, The inhibition of calcium uptake and release by rat liver mitochondria by ruthenium red, FEBS Lett, 81, 142, 10.1016/0014-5793(77)80947-2 Puskin, 1976, Evidence for more than one Ca2+ transport mechanism in mitochondria, Biochemistry, 15, 3834, 10.1021/bi00662a029 Rossi, 1973, The effect of ruthenium red on the uptake and release of Ca 2+ by mitochondria, Biochem Biophys Res Commun, 50, 846, 10.1016/0006-291X(73)91322-3 Tapia, 1997, Ruthenium red as a tool to study calcium channels, neuronal death and the function of neural pathways, Neurochem Int, 30, 137, 10.1016/S0197-0186(96)00056-3 Belous, 2003, Altered ATP-dependent mitochondrial Ca (2+) uptake in cold ischemia is attenuated by ruthenium red, J Surg Res, 111, 284, 10.1016/S0022-4804(03)00092-1 Kim, 2001, Activator protein 1 activation following hypoosmotic stress in HepG2 cells is actin cytoskeleton dependent, J Surg Res, 100, 176, 10.1006/jsre.2001.6225 Enosawa, 2001, In vivo estimation of bioartificial liver with recombinant HepG2 cells using pigs with ischemic liver failure, Cell Transplant, 10, 429, 10.3727/000000001783986459 Afford, 1999, CD40 activation induces apoptosis in cultured human hepatocytes via induction of cell surface fas ligand expression and amplifies fas-mediated hepatocyte death during allograft rejection, J Exp Med, 189, 441, 10.1084/jem.189.2.441 Esumi, 2002, Hypoxia and nitric oxide treatment confer tolerance to glucose starvation in a 5′-AMP-activated protein kinase-dependent manner, J Biol Chem, 277, 32791, 10.1074/jbc.M112270200 Heiskanen, 1999, Mitochondrial depolarization accompanies cytochrome c release during apoptosis in PC6 cells, J Biol Chem, 274, 5654, 10.1074/jbc.274.9.5654 Brustovetsky, 2003, Two pathways for tBID-induced cytochrome c release from rat brain mitochondria: BAK- versus BAX-dependence, J Neurochem, 84, 196, 10.1046/j.1471-4159.2003.01545.x van Gurp, 2003, Mitochondrial intermembrane proteins in cell death, Biochem Biophys Res Commun, 304, 487, 10.1016/S0006-291X(03)00621-1 Gottlieb, 2002, Analyzing mitochondrial changes during apoptosis, Methods, 26, 341, 10.1016/S1046-2023(02)00040-3 Abrahamse, 2003, Induction of necrosis and DNA fragmentation during hypothermic preservation of hepatocytes in UW, HTK and Celsior solutions, Cell Transplant, 12, 59, 10.3727/000000003783985160 Salahudeen, 2003, Involvement of the mitochondrial pathway in cold storage and rewarming-associated apoptosis of human renal proximal tubular cells, Am J Transplant, 3, 273, 10.1034/j.1600-6143.2003.00042.x Miyamae, 1996, Attenuation of postischemic reperfusion injury is related to prevention of [Ca2+]m overload in rat hearts, Am J Physiol, 271, H2145 Figueredo, 1991, Postischaemic reperfusion injury in the isolated rat heart: effect of ruthenium red, Cardiovasc Res, 25, 337, 10.1093/cvr/25.4.337 Liu, 2002, Activation of mitochondrial ATP-dependent potassium channels protects neurons against ischemia-induced death by a mechanism involving suppression of Bax translocation and cytochrome c release, J Cereb Blood Flow Metab, 22, 431, 10.1097/00004647-200204000-00007 Wolter, 1997, Movement of Bax from the cytosol to mitochondria during apoptosis, J Cell Biol, 139, 1281, 10.1083/jcb.139.5.1281 Nguyen, 1998, Regulated targeting of BAX to mitochondria, J Cell Biol, 143, 207, 10.1083/jcb.143.1.207 Hajnoczky, 2003, Calcium Signaling and Apoptosis, Biochem Biophys Res Commun, 304, 445, 10.1016/S0006-291X(03)00616-8 Szakai, 1999, Apoptosis driven by IP (3) -linked mitochondrial calcium signals, EMBO J, 18, 6349, 10.1093/emboj/18.22.6349 Madesh, 2002, Rapid kinetics of tBid-induced cytochrome c and Smac/DIABLO release and mitochondrial depolarization, J Biol Chem, 277, 5651, 10.1074/jbc.M108171200 Demol, 2001, Endonuclease G. a mitochondrial protein released in apoptosis and involved in caspase-independent DNA degradation, Cell Death Differ, 8, 1136, 10.1038/sj.cdd.4400944 Li, 2001, Endonuclease G is an apoptotic DNase when released from mitochondria, Nature, 412, 95, 10.1038/35083620 Ravagnan, 2002, Apoptosis-inducing factor (AIF): a novel caspase-independent death effector released from mitochondria, Biochimie, 84, 215, 10.1016/S0300-9084(02)01374-3 Wang, 2003, Mitochondria-mediated caspase-independent apoptosis induced by cadmium in normal human lung cells, J Cell Biochem, 89, 335, 10.1002/jcb.10488 Ferrer, 2003, Caspase-dependent and caspase-independent signalling of apoptosis in the penumbra following middle cerebral artery occlusion in the adult rat, Neuropathol Appl Neurobiol, 29, 472, 10.1046/j.1365-2990.2003.00485.x Kim, 2003, Role of apoptosis-inducing factor in myocardial cell death by ischemia-reperfusion, Biochem Biophys Res Commun, 309, 619, 10.1016/j.bbrc.2003.08.045 Hallin, 2003, Involvement of apoptosis-inducing factor in neuronal death after hypoxia-ischemia in the neonatal rat brain, J Neurochem, 86, 306 Bellemare, 2002, Enhanced development of caspase-independent cortical cell death during cold storage in kidneys of non-heart-beating donors, Transplantation, 73, 1742, 10.1097/00007890-200206150-00009 Rauen, 2000, Hypothermia injury/cold-induced apoptosis – evidence of an increase in chelatable iron causing oxidative injury in spite of low O2-/H2O2 formation, FASEB J, 14, 1953, 10.1096/fj.00-0071com Vairetti, 2001, Cold-induced apoptosis in isolated rat hepatocytes. protective role of glutathione, Free Radic Biol Med, 31, 954, 10.1016/S0891-5849(01)00670-0 Rauen, 1999, Cold-induced apoptosis in cultured hepatocytes and liver endothelial cells: mediation by reactive oxygen species, FASEB J, 13, 155, 10.1096/fasebj.13.1.155