Pre-Ischemic Hypothermic Oxygenated Perfusion Alleviates Protective Molecular Markers of Ischemia-Reperfusion Injury in Rat Liver

Macedo, 2010, Role of ischemic preconditioning in liver transplant: a review of literature, Exp Clin Transplant, 8, 1 Jassem, 2006, Ischemic preconditioning of cadaver donor livers protects allografts following transplantation, Transplantation, 81, 169, 10.1097/01.tp.0000188640.05459.37 Klein, 2003, Protective effects of superoxide dismutase against ischemia-reperfusion injury: development and application of a transgenic animal model, Plast Reconstr Surg, 111, 251, 10.1097/01.PRS.0000034938.58120.12 Matsui, 2005, Inhibition of NF-kappaB activation during ischemia reduces hepatic ischemia/reperfusion injury in rats, J Toxicol Sci, 30, 103, 10.2131/jts.30.103 Peng, 1995, Protection by pentoxifylline against normothermic liver ischemia/reperfusion in rats, Transplantation, 59, 1537, 10.1097/00007890-199506000-00006 Southard, 1990, New solution for organ preservation, 145 Karangwa, 2016, Machine Perfusion of donor livers for transplantation: a proposal for standardized nomenclature and reporting guidelines, Am J Transplant, 16, 2932, 10.1111/ajt.13843 Dutkowski, 2015, Challenges to liver transplantation and strategies to improve outcomes, Gastroenterology, 148, 307, 10.1053/j.gastro.2014.08.045 Graham, 2014, Resuscitation” of marginal liver allografts for transplantation with machine perfusion technology, J Hepatol, 61, 418, 10.1016/j.jhep.2014.04.019 op den Dries, 2013, Ex vivo normothermic machine perfusion and viability testing of discarded human donor livers: normothermic perfusion of human livers, Am J Transplant, 13, 1327, 10.1111/ajt.12187 Schlegel, 2015, Hypothermic oxygenated liver perfusion: basic mechanisms and clinical application, Curr Transpl Rep, 2, 52, 10.1007/s40472-014-0046-1 Kron, 2018, Hypothermic oxygenated perfusion (HOPE) for fatty liver grafts in rats and humans, J Hepatol, 68, 82, 10.1016/j.jhep.2017.08.028 Berendsen, 2012, A simplified subnormothermic machine perfusion system restores ischemically damaged liver grafts in a rat model of orthotopic liver transplantation, Transplant Res, 1, 6, 10.1186/2047-1440-1-6 Nepal, 2013, Activation of autophagy by globular adiponectin attenuates ethanol-induced apoptosis in HepG2 cells: involvement of AMPK/FoxO3A axis, Biochim Biophys Acta, 1833, 2111, 10.1016/j.bbamcr.2013.05.013 Wilson, 2015, CXC chemokine receptor-4 signaling limits hepatocyte proliferation after hepatic ischemia-reperfusion in mice, Am J Physiol Gastrointest Liver Physiol, 308, G702, 10.1152/ajpgi.00257.2014 Hines, 2011, Divergent roles of superoxide and nitric oxide in liver ischemia and reperfusion injury, J Clin Biochem Nutr, 48, 50, 10.3164/jcbn.11-016FR Shang, 2016, Downregulation of glutathione biosynthesis contributes to oxidative stress and liver dysfunction in acute kidney injury, Oxid Med Cell Longev, 2016, 10.1155/2016/9707292 Lim, 2009, Glutathione peroxidase deficiency exacerbates ischemia-reperfusion injury in male but not female myocardium: insights into antioxidant compensatory mechanisms, Am J Physiol Heart Circ Physiol, 297, H2144, 10.1152/ajpheart.00673.2009 Panisello-Roselló, 2018, Aldehyde dehydrogenase 2 (ALDH2) in rat fatty liver cold ischemia injury, IJMS, 19, 2479, 10.3390/ijms19092479 Seelan, 1996, Cytochrome c oxidase subunit VIIa liver isoform. Characterization and identification of promoter elements in the bovine gene, J Biol Chem, 271, 2112, 10.1074/jbc.271.4.2112 Carter, 1994, Cooperative binding of GA-binding protein transcription factors to duplicated transcription initiation region repeats of the cytochrome c oxidase subunit IV gene, J Biol Chem, 269, 4381, 10.1016/S0021-9258(17)41791-1 Virbasius, 1993, Identity of GABP with NRF-2, a multisubunit activator of cytochrome oxidase expression, reveals a cellular role for an ETS domain activator of viral promoters, Genes Dev, 7, 380, 10.1101/gad.7.3.380 Rosmarin, 2004, GA-binding protein transcription factor: a review of GABP as an integrator of intracellular signaling and protein–protein interactions, Blood Cells Mol Dis, 32, 143, 10.1016/j.bcmd.2003.09.005 Guo, 2015, Systematic review with meta-analysis: HIF-1α attenuates liver ischemia–reperfusion injury, Transplant Rev (Orlando), 29, 127, 10.1016/j.trre.2015.05.001 Yu, 2012, IGF-1 induces hypoxia-inducible factor 1α-mediated GLUT3 expression through PI3K/Akt/mTOR dependent pathways in PC12 cells, Brain Res, 1430, 18, 10.1016/j.brainres.2011.10.046 Kula-Alwar, 2019, Targeting Succinate Metabolism in Ischemia/Reperfusion Injury, Circulation, 140, 1968, 10.1161/CIRCULATIONAHA.119.042791 Chappell, 2010, Glycocalyx protection reduces leukocyte adhesion after ischemia/reperfusion, Shock, 34, 133, 10.1097/SHK.0b013e3181cdc363 Schiefer, 2013, Syndecan-1 as marker of ischemia and reperfusion in patients undergoing liver transplantation. A pilot study: 12AP5-11, Eur J Anaesthesiol, 30, 196, 10.1097/00003643-201306001-00613 Masola, 2018, Inhibition of heparanase protects against chronic kidney dysfunction following ischemia/reperfusion injury, Oncotarget, 9, 36185, 10.18632/oncotarget.26324 Ghimire, 2017, Nitric oxide: what's new to NO?, Am J Physiol Cell Physiol, 312, C254, 10.1152/ajpcell.00315.2016 Guan, 2014, Mechanisms of hepatic ischemia-reperfusion injury and protective effects of nitric oxide, WJGS, 6, 122, 10.4240/wjgs.v6.i7.122 Moncada, 1991, Nitric oxide: physiology, pathophysiology, and pharmacology, Pharmacol Rev, 43, 109 Lopez, 2018, Glycocalyx preservation and NO production in fatty livers-the protective role of high molecular polyethylene glycol in cold ischemia injury, Int J Mol Sci, 19, 2375, 10.3390/ijms19082375 Yan, 2013, The protective roles of autophagy in ischemic preconditioning, Acta Pharmacol Sin, 34, 636, 10.1038/aps.2013.18 Chen, 2016, Dihydromyricetin protects against liver ischemia/reperfusion induced apoptosis via activation of FOXO3a-mediated autophagy, Oncotarget, 7, 76508, 10.18632/oncotarget.12894 Tikhanovich, 2013, Forkhead box class O transcription factors in liver function and disease: FOXO and the liver, J Gastroenterol Hepatol, 28, 125, 10.1111/jgh.12021 Nakamura, 2018, Heme oxygenase-1 regulates sirtuin-1-autophagy pathway in liver transplantation: From mouse to human, Am J Transplant, 18, 1110, 10.1111/ajt.14586 Kim, 2015, Carbon monoxide protects against hepatic ischemia/reperfusion injury by modulating the miR-34a/SIRT1 pathway, Biochim Biophys Acta, 1852, 1550, 10.1016/j.bbadis.2015.04.017 Nakamura, 2017, Sirtuin 1 attenuates inflammation and hepatocellular damage in liver transplant ischemia/reperfusion: from mouse to human: Nakamura et al, Liver Transpl, 23, 1282, 10.1002/lt.24821 Janani, 2015, PPAR gamma gene–a review, Diabetes Metab Syndr, 9, 46, 10.1016/j.dsx.2014.09.015 Jiang, 1998, PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines, Nature, 391, 82, 10.1038/34184 von Knethen, 2003, PPARgamma–an important regulator of monocyte/macrophage function, Arch Immunol Ther Exp (Warsz), 51, 219 Kuboki, 2008, Peroxisome proliferator-activated receptor-gamma protects against hepatic ischemia/reperfusion injury in mice, Hepatology, 47, 215, 10.1002/hep.21963 Marion-Letellier, 2016, Fatty acids, eicosanoids and PPAR gamma, Eur J Pharmacol, 785, 44, 10.1016/j.ejphar.2015.11.004 Gressner, 2002, Roles of TGF-beta in hepatic fibrosis, Front Biosci, 7, d793, 10.2741/gressner Zhao, 2017, Down-regulation of nuclear HMGB1 reduces ischemia-induced HMGB1 translocation and release and protects against liver ischemia-reperfusion injury, Sci Rep, 7, 46272, 10.1038/srep46272 Evankovich, 2010, Toll-like receptors in hepatic ischemia/reperfusion and transplantation, Gastroenterol Res Pract, 2010, 10.1155/2010/537263 Perry, 2011, Tumor necrosis factor-α in liver ischemia/reperfusion injury, J Invest Surg, 24, 178, 10.3109/08941939.2011.568594 Jiménez-Castro, 2019, Inflammasome-mediated inflammation in liver ischemia-reperfusion injury, Cells, 8, 1131, 10.3390/cells8101131 Rmilah, 2019, Understanding the marvels behind liver regeneration, Wiley Interdiscip Rev Dev Biol, 8, e340, 10.1002/wdev.340 Lentsch, 1999, Requirement for interleukin-12 in the pathogenesis of warm hepatic ischemia/reperfusion injury in mice, Hepatology, 30, 1448, 10.1002/hep.510300615 Langdale, 1999, Effects of immunomodulation with interferon-gamma on hepatic ischemia-reperfusion injury, Shock, 11, 356, 10.1097/00024382-199905000-00009 Shiratori, 1998, Hepatocyte nitric oxide production is induced by Kupffer cells, Dig Dis Sci, 43, 1737, 10.1023/A:1018879502520 Carlos, 1994, Leukocyte-endothelial adhesion molecules, Blood, 84, 2068, 10.1182/blood.V84.7.2068.2068 Hu, 2016, Inhibiting matrix metalloproteinase 3 ameliorates neuronal loss in the ganglion cell layer of rats in retinal ischemia/reperfusion, Neurochem Res, 41, 1107, 10.1007/s11064-015-1800-1 Yano, 2001, Increased matrix metalloproteinase 9 activity and mRNA expression in lung ischemia-reperfusion injury, J Heart Lung Transplant, 20, 679, 10.1016/S1053-2498(01)00250-9 Martynova, 2003, [Regulation of caspase activity in apoptosis], Bioorg Khim, 29, 518 Kamada, 1980, Orthotopic rat liver transplantation after long-term preservation by continuous perfusion with fluorocarbon emulsion, Transplantation, 30, 43, 10.1097/00007890-198007000-00009 Bessems, 2006, Machine perfusion preservation of the pig liver using a new preservation solution, polysol, Transplant Proc, 38, 1238, 10.1016/j.transproceed.2006.02.063 Dutkowski, 1998, Rat liver preservation by hypothermic oscillating liver perfusion compared to simple cold storage, Cryobiology, 36, 61, 10.1006/cryo.1997.2066 Manekeller, 2007, Liver integrity after warm ischemia in situ and brief preservation ex vivo: the value of aerobic post-conditioning, Cryobiology, 55, 249, 10.1016/j.cryobiol.2007.08.005 Mochida, 2008, Oxidative stress in hepatocytes and stimulatory state of Kupffer cells after reperfusion differ between warm and cold ischemia in rats, Liver, 14, 234, 10.1111/j.1600-0676.1994.tb00081.x Schön, 1998, Cold ischemia affects sinusoidal endothelial cells while warm ischemia affects hepatocytes in liver transplantation, Transplantation Proceedings, 30, 2318, 10.1016/S0041-1345(98)00638-1 Solaini, 2010, Hypoxia and mitochondrial oxidative metabolism, Biochim Biophys Acta, 1797, 1171, 10.1016/j.bbabio.2010.02.011 Farber, 1994, Mechanisms of cell injury by activated oxygen species, Environ Health Perspect, 102, 17, 10.1289/ehp.94102s1017 Theruvath, 2007, Minocycline and N-methyl-4-isoleucine cyclosporin (NIM811) mitigate storage/reperfusion injury after rat liver transplantation through suppression of the mitochondrial permeability transition, Hepatology, 47, 236, 10.1002/hep.21912 Waldmeier, 2002, Inhibition of the mitochondrial permeability transition by the nonimmunosuppressive cyclosporin derivative NIM811, Mol Pharmacol, 62, 22, 10.1124/mol.62.1.22 Kim, 2003, Role of the mitochondrial permeability transition in apoptotic and necrotic death after ischemia/reperfusion injury to hepatocytes, Curr Mol Med, 3, 527, 10.2174/1566524033479564 Kim, 2003, Mitochondrial permeability transition: a common pathway to necrosis and apoptosis, Biochem Biophys Res Commun, 304, 463, 10.1016/S0006-291X(03)00618-1 Yabe, 2001, Prevention of neutrophil-mediated hepatic ischemia/reperfusion injury by superoxide dismutase and catalase derivatives, J Pharmacol Exp Ther, 298, 894 Chouchani, 2014, Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS, Nature, 515, 431, 10.1038/nature13909 Chipuk, 2008, How do BCL-2 proteins induce mitochondrial outer membrane permeabilization?, Trends Cell Biol, 18, 157, 10.1016/j.tcb.2008.01.007 Marzo, 1998, Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis, Science, 281, 2027, 10.1126/science.281.5385.2027 Kornblau, 1999, Apoptosis regulating proteins as targets of therapy for haematological malignancies, Expert Opin Investig Drugs, 8, 2027, 10.1517/13543784.8.12.2027 Marquez, 2012, Bcl-2:Beclin 1 complex: multiple, mechanisms regulating autophagy/apoptosis toggle switch, Am J Cancer Res, 2, 214 Redaelli, 2002, Extended preservation of rat liver graft by induction of heme oxygenase-1, Hepatology, 35, 1082, 10.1053/jhep.2002.33067 Karin, 2000, Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity, Annu Rev Immunol, 18, 621, 10.1146/annurev.immunol.18.1.621 Peralta, 2001, Preconditioning protects against systemic disorders associated with hepatic ischemia-reperfusion through blockade of tumor necrosis factor-induced P-selectin up-regulation in the rat, Hepatology, 33, 100, 10.1053/jhep.2001.20529 Chen, 2003, Role of nitric oxide in liver injury, Curr Mol Med, 3, 519, 10.2174/1566524033479582 Fridman, 2003, Control of apoptosis by p53, Oncogene, 22, 9030, 10.1038/sj.onc.1207116 Koumenis, 2001, Regulation of p53 by hypoxia: dissociation of transcriptional repression and apoptosis from p53-dependent transactivation, Mol Cell Biol, 21, 1297, 10.1128/MCB.21.4.1297-1310.2001 Kang, 2011, HMGB1 as an autophagy sensor in oxidative stress, Autophagy, 7, 904, 10.4161/auto.7.8.15704 Colletti, 1990, Role of tumor necrosis factor-alpha in the pathophysiologic alterations after hepatic ischemia/reperfusion injury in the rat, J Clin Invest, 85, 1936, 10.1172/JCI114656 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 Cursio, 2015, Autophagy and liver ischemia-reperfusion injury, Biomed Res Int, 2015, 10.1155/2015/417590