Ischemia-Reperfusion Injury in Aged Livers - The Energy Metabolism, Inflammatory Response, and Autophagy

Transplantation

Volumn 102, Issue 3, 2018, Pages 368-377

  Kan, Chunyi ^a,b   Ungelenk, Luisa ^a   Lupp, Amelie ^a   Dirsch, Olaf ^c   Dahmen, Uta ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b Wuhan Central Hospital   (China)

^c KLINIKUM CHEMNITZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; FREE RADICAL;

AGING; APOPTOSIS; AUTOPHAGY; CELL AGING; CELL PROTECTION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY METABOLISM; GRAFT RECIPIENT; HEPATITIS; HUMAN; IMMUNE RESPONSE; LIVER GRAFT; LIVER INJURY; LIVER ISCHEMIA; LIVER METABOLISM; LIVER MITOCHONDRION; METABOLIC DISORDER; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; ANIMAL; INFLAMMATION; LIVER; VASCULARIZATION;

AGING; ANIMALS; AUTOPHAGY; ENERGY METABOLISM; HUMANS; INFLAMMATION; LIVER; REPERFUSION INJURY;

EID: 85042859818     PISSN: 00411337     EISSN: None     Source Type: Journal    
DOI: 10.1097/TP.0000000000001999     Document Type: Review

References (104)

1. Jadlowiec CC, Taner T. Liver transplantation: current status and challenges. World J Gastroenterol. 2016;22:4438-4445.
2. Bertuzzo VR, CesconM,Odaldi F, et al. Actual risk of using very aged donors for unselected liver transplant candidates: a European single-center experience in the MELD era. Ann Surg. 2017;265:388-396.
3. Busquets J, Xiol X, Figueras J, et al. The impact of donor age on liver transplantation: influence of donor age on early liver function and on subsequent patient and graft survival. Transplantation. 2001;71:1765-1771.
4. Markmann JF, Markmann JW, Markmann DA, et al. Preoperative factors associated with outcome and their impact on resource use in 1148 consecutive primary liver transplants. Transplantation. 2001; 72:1113-1122.
5. Johnson SR, Alexopoulos S, CurryM, et al. Primary nonfunction (PNF) in the MELD era: an SRTR database analysis. Am J Transplant. 2007;7: 1003-1009.
6. Clavien PA, Selzner M, Rüdiger HA, et al. A prospective randomized study in 100 consecutive patients undergoing major liver resection with versus without ischemic preconditioning. Ann Surg. 2003;238: 843-850.
7. Lake JR, Shorr JS, Steffen BJ, et al. Differential effects of donor age in liver transplant recipients infected with hepatitis B, hepatitis C and without viral hepatitis. Am J Transplant. 2005;5:549-557.
8. Lai Q, Melandro F, Levi Sandri G, et al. Use of elderly donors for liver transplantation: has the limit been reached. J Gastrointestin Liver Dis. 2011;20:383-387.
9. Nardo B, Masetti M, Urbani L, et al. Liver transplantation from donors aged 80 years and over: pushing the limit. Am J Transplant. 2004;4: 1139-1147.
10. Cescon M, Grazi GL, Cucchetti A, et al. Improving the outcome of liver transplantation with very old donors with updated selection and management criteria. Liver Transpl. 2008;14:672-679.
11. Ravaioli M, Grazi GL, Cescon M, et al. Liver transplantations with donors aged 60 years and above: the low liver damage strategy. Transpl Int. 2009;22:423-433.
12. Dasari BVM, Schlegel A, Mergental H, et al. The use of old donors in liver transplantation. Best Pract Res Clin Gastroenterol. 2017;31:211-217.
13. Jimenez-Romero C, Caso Maestro O, Cambra Molero F, et al. Using old liver grafts for liver transplantation: where are the limits? World J Gastroenterol. 2014;20:10691-10702.
14. Le Couteur DG, Rivory LP, Pond SM. The effects of aging and nutritional state on hypoxia-reoxygenation injury in the perfused rat liver. Transplantation. 1994;58:531-536.
15. Zhai Y, Petrowsky H, Hong JC, et al. Ischaemia-reperfusion injury in liver transplantation-from bench to bedside. Nat Rev Gastroenterol Hepatol. 2013;10:79-89.
16. Lim WH, Clayton P, Wong G, et al. Outcomes of kidney transplantation from older living donors. Transplantation. 2013;95:106-113.
17. Massie AB, Leanza J, Fahmy LM, et al. A risk index for living donor kidney transplantation. Am J Transplant. 2016;16:2077-2084.
18. Jaeschke H, Farhood A, Smith CW. Neutrophils contribute to ischemia/reperfusion injury in rat liver in vivo. FASEB J. 1990;4:3355-3359.
19. Jaeschke H, Farhood A. Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver. Am J Physiol. 1991; 260:G355-G362.
20. Jaeschke H. Reactive oxygen and ischemia/reperfusion injury of the liver. Chem Biol Interact. 1991;79:115-136.
21. Jaeschke H, Smith CW. Mechanisms of neutrophil-induced parenchymal cell injury. J Leukoc Biol. 1997;61:647-653.
22. Jaeschke H. Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am J Physiol Gastrointest Liver Physiol. 2003; 284:G15-G26.
23. Fondevila C, Busuttil RW, Kupiec-Weglinski JW. Hepatic ischemia/reperfusion injury - a fresh look. Exp Mol Pathol. 2003;74:86-93.
24. Serracino-Inglott F, Habib NA, Mathie RT. Hepatic ischemia-reperfusion injury. Am J Surg. 2001;181:160-166.
25. Rautou PE, Mansouri A, Lebrec D, et al. Autophagy in liver diseases. J Hepatol. 2010;53:1123-1134.
26. Lemasters JJ, Nieminen AL, Qian T, et al. The mitochondrial permeability transition in cell death: a commonmechanismin necrosis, apoptosis and autophagy. Biochim Biophys Acta. 1998;1366:177-196.
27. Kim JS, He L, Qian T, et al. Role of the mitochondrial permeability transition in apoptotic and necrotic death after ischemia/reperfusion injury to hepatocytes. Curr Mol Med. 2003;3:527-535.
28. Schinzel AC, Takeuchi O, Huang Z, et al. Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc Natl Acad Sci U S A. 2005;102: 12005-12010.
29. Morin D, Pires F, Plin C, et al. Role of the permeability transition pore in cytochrome C release from mitochondria during ischemia-reperfusion in rat liver. Biochem Pharmacol. 2004;68:2065-2073.
30. Teoh NC, Farrell GC. Hepatic ischemia reperfusion injury: pathogenic mechanisms and basis for hepatoprotection. J Gastroenterol Hepatol. 2003;18:891-902.
31. Lemasters JJ, Theruvath TP, Zhong Z, et al. Mitochondrial calcium and the permeability transition in cell death. Biochim Biophys Acta. 2009; 1787:1395-1401.
32. Wang C, Youle RJ. The role of mitochondria in apoptosis. Annu Rev Genet. 2009;43:95-118.
33. Tsung A, Sahai R, Tanaka H, et al. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med. 2005; 201:1135-1143.
34. Liu A, Dirsch O, Fang H, et al. HMGB1 in ischemic and non-ischemic liver after selective warm ischemia/reperfusion in rat. Histochem Cell Biol. 2011;135:443-452.
35. Zhang T, Wei W, Dirsch O, et al. Identification of proteins interacting with cytoplasmic high-mobility group box 1 during the hepatocellular response to ischemia reperfusion injury. Int J Mol Sci. 2017;18:167.
36. Lentsch AB, Kato A, Yoshidome H, et al. Inflammatory mechanisms and therapeutic strategies for warm hepatic ischemia/reperfusion injury. Hepatology. 2000;32:169-173.
37. Jaeschke H, Lemasters JJ. Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury. Gastroenterology. 2003;125:1246-1257.
38. King LA, ToledoAH,Rivera-Chavez FA, et al. Role of p38 and JNK in liver ischemia and reperfusion. J Hepatobiliary Pancreat Surg. 2009;16:763-770.
39. Abu-Amara M, Yang SY, Tapuria N, et al. Liver ischemia/reperfusion injury: processes in inflammatory networks - a review. Liver Transpl. 2010;16:1016-1032.
40. Eltzschig HK, Eckle T. Ischemia and reperfusion-from mechanism to translation. Nat Med. 2011;17:1391-1401.
41. Liu A, Fang H, Dahmen U, et al. Chronic lithium treatment protects against liver ischemia/reperfusion injury in rats. Liver Transpl. 2013;19: 762-772.
42. Cursio R, Colosetti P, Gugenheim J. Autophagy and liver ischemiareperfusion injury. Biomed Res Int. 2015;2015:417590.
43. Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays formonitoring autophagy (3rd edition). Autophagy. 2016;12:1-222.
44. Liang XH, Jackson S, Seaman M, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 1999;402:672-676.
45. Ravikumar B, Vacher C, Berger Z, et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet. 2004;36: 585-595.
46. Wang K, Klionsky DJ. Mitochondria removal by autophagy. Autophagy. 2011;7:297-300.
47. Woodhouse KW, Wynne HA. Age-related changes in liver size and hepatic blood flow. The influence on drug metabolism in the elderly. Clin Pharmacokinet. 1988;15:287-294.
48. Jansen PL. Liver disease in the elderly. Best Pract Res ClinGastroenterol. 2002;16:149-158.
49. Hoare M, Das T, Alexander G. Ageing, telomeres, senescence, and liver injury. J Hepatol. 2010;53:950-961.
50. Poynard T, Bedossa P, Opolon P. Natural history of liver fibrosis progression in patients with chronic hepatitis C. The OBSVIRC, METAVIR, CLINIVIR, and DOSVIRC groups. Lancet. 1997;349:825-832.
51. Poynard T, Zoulim F, Ratziu V, et al. Longitudinal assessment of histology surrogate markers (FibroTest-ActiTest) during lamivudine therapy in patients with chronic hepatitis B infection. Am J Gastroenterol. 2005;100: 1970-1980.
52. Goudie BM, Burt AD, Macfarlane GJ, et al. Risk factors and prognosis in primary biliary cirrhosis. Am J Gastroenterol. 1989;84:713-716.
53. Forrest E, Evans C, Stewart S, et al. Analysis of factors predictive ofmortality in alcoholic hepatitis and derivation and validation of the Glasgow alcoholic hepatitis score. Gut. 2005;54:1174-1179.
54. Floreani A, Niro G, Rosa Rizzotto E, et al. Type I autoimmune hepatitis: clinical course and outcome in an Italian multicentre study. Aliment Pharmacol Ther. 2006;24:1051-1057.
55. Ratziu V, Giral P, Charlotte F, et al. Liver fibrosis in overweight patients. Gastroenterology. 2000;118:1117-1123.
56. Okaya T, Blanchard J, Schuster R, et al. Age-dependent responses to hepatic ischemia/reperfusion injury. Shock. 2005;24:421-427.
57. Park Y, Hirose R, Coatney JL, et al. Ischemia-reperfusion injury is more severe in older versus young rat livers. J Surg Res. 2007;137:96-102.
58. Selzner M, Selzner N, JochumW, et al. Increased ischemic injury in old mouse liver: an ATP-dependent mechanism. Liver Transpl. 2007;13: 382-390.
59. Selzner M, Selzner N, Chen L, et al. Exaggerated up-regulation of tumor necrosis factor alpha-dependent apoptosis in the older mouse liver following reperfusion injury: targeting liver protective strategies to patient age. Liver Transpl. 2009;15:1594-1604.
60. Schiesser M, Wittert A, Nieuwenhuijs VB, et al. Intermittent ischemia but not ischemic preconditioning is effective in restoring bile flow after ischemia reperfusion injury in the livers of aged rats. J Surg Res. 2009;152: 61-68.
61. Huber N, Sakai N, Eismann T, et al. Age-related decrease in proteasome expression contributes to defective nuclear factor-kappaB activation during hepatic ischemia/reperfusion. Hepatology. 2009;49:1718-1728.
62. Wang JH, Ahn IS, Fischer TD, et al. Autophagy suppresses agedependent ischemia and reperfusion injury in livers of mice. Gastroenterology. 2011;141:2188-2199. e2186.
63. Kireev RA, Cuesta S, Ibarrola C, et al. Age-related differences in hepatic ischemia/reperfusion: gene activation, liver injury, and protective effect of melatonin. J Surg Res. 2012;178:922-934.
64. Trocha M, Merwid-Ląd A, Chlebda-Sieragowska E, et al. Age-related changes in ADMA-DDAH-NO pathway in rat liver subjected to partial ischemia followed by global reperfusion. Exp Gerontol. 2014;50:45-51.
65. Liu ZY, Wang W, Jin B, et al. Protection against ischemia-reperfusion injury in aged liver donor by the induction of exogenous human telomerase reverse transcriptase gene. Transplant Proc, 2014;46:1567-1572.
66. Huang X, Gao Y, Qin J, et al. The role ofmiR-34a in the hepatoprotective effect of hydrogen sulfide on ischemia/reperfusion injury in young and old rats. PLoS One. 2014;9:e113305.
67. Limani P, Linecker M, Oberkofler CE, et al. Remote ischemic preconditioning: a novel strategy in rescuing older livers from ischemiareperfusion injury in a rodent model. Ann Surg. 2016;264:797-803.
68. Altman P, Katz D. Biological handbooks III, inbred and genetically defined strains of laboratory animals (part I: mouse and rat). Washington, DC: Federation of American Societies for Experimental Biology; 1979.
69. Harman D. Aging: a theory based on free radical and radiation chemistry. J Gerontol. 1956;11:298-300.
70. Lesnefsky EJ, Gudz TI, Migita CT, et al. Ischemic injury to mitochondrial electron transport in the aging heart: damage to the iron-sulfur protein subunit of electron transport complex III. Arch Biochem Biophys. 2001; 385:117-128.
71. Cadenas E, Davies KJ. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med. 2000;29:222-230.
72. Navarro A, Boveris A. Themitochondrial energy transduction system and the aging process. Am J Physiol Cell Physiol. 2007;292:C670-C686.
73. Harris NR, Langlois KW. Age-dependent responses of the mesenteric vasculature to ischemia-reperfusion. Am J Physiol. 1998;274: H1509-H1515.
74. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74: 1124-1136.
75. Marecki H, Bozorgzadeh A, Porte RJ, et al. Liver ex situ machine perfusion preservation: a reviewof themethodology and results of large animal studies and clinical trials. Liver Transpl. 2017;23:679-695.
76. Banan B, Xiao Z,Watson R, et al. Novel strategy to decrease reperfusion injuries and improve function of cold-preserved livers using normothermic ex vivo liver perfusion machine. Liver Transpl. 2016;22: 333-343.
77. Bruinsma BG, Avruch JH,Weeder PD, et al. Functional human liver preservation and recovery bymeans of subnormothermicmachine perfusion. J Vis Exp. 2015.
78. Schlegel A, de Rougemont O, Graf R, et al. Protective mechanisms of end-ischemic cold machine perfusion in DCD liver grafts. J Hepatol. 2013:58:278-286.
79. Minor T, Efferz P, Fox M, et al. Controlled oxygenated rewarming of cold stored liver grafts by thermally graduated machine perfusion prior to reperfusion. Am J Transplant. 2013;13:1450-1460.
80. Mergental H, PereraMT, Laing RW, et al. Transplantation of declined liver allografts following normothermic ex-situ evaluation. Am J Transplant. 2016;16:3235-3245.
81. op den Dries S, Karimian N, Sutton ME, et al. Ex vivo normothermic machine perfusion and viability testing of discarded human donor livers. Am J Transplant. 2013;13:1327-1335.
82. GoldaracenaN,Barbas AS, SelznerM. Normothermic and subnormothermic ex-vivo liver perfusion in liver transplantation. Curr Opin Organ Transplant. 2016;21:315-321.
83. Dutkowski P, de Rougemont O, Clavien PA. Machine perfusion for 'marginal' liver grafts. Am J Transplant. 2008;8:917-924.
84. Pezzati D, Ghinolfi D, Balzano E, et al. Salvage of an octogenarian liver graft using normothermic perfusion: a case report. Transplant Proc. 2017;49:726-728.
85. Harris NR, Rumbaut RE. Age-related responses of the microcirculation to ischemia-reperfusion and inflammation. Pathophysiology. 2001;8:1-10.
86. Majmundar AJ,WongWJ, SimonMC. Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell. 2010;40:294-309.
87. Kuboki S, Schuster R, Blanchard J, et al. Role of heat shock protein 70 in hepatic ischemia-reperfusion injury in mice. Am J Physiol Gastrointest Liver Physiol. 2007;292:G1141-G1149.
88. Li C, Browder W, Kao RL. Early activation of transcription factor NF-kappaB during ischemia in perfused rat heart. Am J Physiol. 1999; 276:H543-H552.
89. Stoppe C, Rex S, Goetzenich A, et al. Interaction of MIF family proteins in myocardial ischemia/reperfusion damage and their influence on clinical outcome of cardiac surgery patients. Antioxid Redox Signal. 2015;23:865-879.
90. Matsutani T, Kang S-C, Miyashita M, et al. Liver cytokine production and ICAM-1 expression following bone fracture, tissue trauma, and hemorrhage in middle-aged mice. Am J Physiol Gastrointest Liver Physiol. 2007;292:G268-G274.
91. Nichols TC. NF-kappaB and reperfusion injury. Drug News Perspect. 2004;17:99-104.
92. Toledo-Pereyra LH, Toledo AH, Walsh J, et al. Molecular signaling pathways in ischemia/reperfusion. Exp Clin Transplant. 2004;2:174-177.
93. Lee VG, Johnson ML, Baust J, et al. The roles of iNOS in liver ischemiareperfusion injury. Shock. 2001;16:355-360.
94. Crespo E, Macías M, Pozo D, et al. Melatonin inhibits expression of the inducible NO synthase II in liver and lung and prevents endotoxemia in lipopolysaccharide-induced multiple organ dysfunction syndrome in rats. FASEB J. 1999;13:1537-1546.
95. Wu CC, Chiao CW, Hsiao G, et al. Melatonin prevents endotoxininduced circulatory failure in rats. J Pineal Res. 2001;30:147-156.
96. Rubinsztein DC, Mariño G, Kroemer G. Autophagy and aging. Cell. 2011;146:682-695.
97. Martinez-Lopez N, Athonvarangkul D, Singh R. Autophagy and aging. Adv Exp Med Biol. 2015;847:73-87.
98. Matsui Y, Takagi H, Qu X, et al. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ Res. 2007;100:914-922.
99. Moors TE, Hoozemans JJ, Ingrassia A, et al. Therapeutic potential of autophagy-enhancing agents in Parkinson's disease. Mol Neurodegener. 2017;12:11.
100. Kan C, Liu A, Fang H, et al. Induction of autophagy reduces ischemia/reperfusion injury in steatotic rat livers. J Surg Res. 2017;216:207-218.
101. Decuypere JP, Ceulemans LJ, Agostinis P, et al. Autophagy and the kidney: implications for ischemia-reperfusion injury and therapy. Am J Kidney Dis. 2015;66:699-709.
102. MalekM, Nematbakhsh M. Renal ischemia/reperfusion injury; from pathophysiology to treatment. J Renal Inj Prev. 2015;4:20-27.
103. Frank A, BonneyM, Bonney S, et al. Myocardial ischemia reperfusion injury: from basic science to clinical bedside. Semin Cardiothorac Vasc Anesth. 2012;16:123-132.
104. Ma S, Wang Y, Chen Y, et al. The role of the autophagy in myocardial ischemia/reperfusion injury. Biochim Biophys Acta. 2015;1852:271-276.