Journal of Yeungnam Medical Science

Yeungnam University College of Medicine, Yeungnam University Institute Medical Science (영남대 의대 학술지 편집위원회)
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Hepatic ischemia-reperfusion injury with respect to oxidative stress and inflammatory response: a narrative review

  • Eun Kyung Choi (Department of Anesthesiology and Pain Medicine, Yeungnam University College of Medicine) ;
  • Dong Gun Lim (Department of Anesthesiology and Pain Medicine, School of Medicine, Kyungpook National University)
  • Received : 2022.01.06
  • Accepted : 2022.02.17
  • Published : 2023.04.30
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Abstract

Hepatic ischemia-reperfusion injury is a major complication of liver transplantation, trauma, and shock. This pathological condition can lead to graft dysfunction and rejection in the field of liver transplantation and clinical hepatic dysfunction with increased mortality. Although the pathological mechanisms of hepatic ischemia-reperfusion injury are very complex, and several intermediators and cells are involved in this phenomenon, oxidative stress and inflammatory responses are the key processes that aggravate hepatic injury. This review summarizes the current understanding of oxidative stress and inflammatory responses and, in that respect, addresses the therapeutic approaches to attenuate hepatic ischemia-reperfusion injury.

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References

  1. Mendes-Braz M, Elias-Miro M, Jimenez-Castro MB, Casillas-Ramirez A, Ramalho FS, Peralta C. The current state of knowledge of hepatic ischemia-reperfusion injury based on its study in experimental models. J Biomed Biotechnol 2012;2012:298657.
  2. Kalogeris T, Baines CP, Krenz M, Korthuis RJ. Cell biology of ischemia/reperfusion injury. Int Rev Cell Mol Biol 2012;298:229-317. https://doi.org/10.1016/B978-0-12-394309-5.00006-7
  3. Heijnen BH, Elkhaloufi Y, Straatsburg IH, Van Gulik TM. Influence of acidosis and hypoxia on liver ischemia and reperfusion injury in an in vivo rat model. J Appl Physiol (1985) 2002;93:319-23. https://doi.org/10.1152/japplphysiol.01112.2001
  4. Li J, Li RJ, Lv GY, Liu HQ. The mechanisms and strategies to protect from hepatic ischemia-reperfusion injury. Eur Rev Med Pharmacol Sci 2015;19:2036-47.
  5. Gnaiger E, Kuznetsov AV, Rieger G, Amberger A, Fuchs A, Stadlmann S, et al. Mitochondrial defects by intracellular calcium overload versus endothelial cold ischemia/reperfusion injury. Transpl Int 2000;13(Suppl 1):S555-7. https://doi.org/10.1007/s001470050401
  6. Camara AK, Bienengraeber M, Stowe DF. Mitochondrial approaches to protect against cardiac ischemia and reperfusion injury. Front Physiol 2011;2:13.
  7. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 2004;287:C817-33. https://doi.org/10.1152/ajpcell.00139.2004
  8. Qian T, Nieminen AL, Herman B, Lemasters JJ. Mitochondrial permeability transition in pH-dependent reperfusion injury to rat hepatocytes. Am J Physiol 1997;273:C1783-92. https://doi.org/10.1152/ajpcell.1997.273.6.C1783
  9. Stowe DF, Camara AK. Mitochondrial reactive oxygen species production in excitable cells: modulators of mitochondrial and cell function. Antioxid Redox Signal 2009;11:1373-414. https://doi.org/10.1089/ars.2008.2331
  10. Kim JS, He L, Qian T, Lemasters JJ. Role of the mitochondrial permeability transition in apoptotic and necrotic death after ischemia/reperfusion injury to hepatocytes. Curr Mol Med 2003;3:527-35. https://doi.org/10.2174/1566524033479564
  11. Nohl H, Gille L, Kozlov A, Staniek K. Are mitochondria a spontaneous and permanent source of reactive oxygen species? Redox Rep 2003;8:135-41. https://doi.org/10.1179/135100003225001502
  12. Ischiropoulos H, Zhu L, Beckman JS. Peroxynitrite formation from macrophage-derived nitric oxide. Arch Biochem Biophys 1992;298:446-51. https://doi.org/10.1016/0003-9861(92)90433-W
  13. Sutton HC, Winterbourn CC. On the participation of higher oxidation states of iron and copper in Fenton reactions. Free Radic Biol Med 1989;6:53-60. https://doi.org/10.1016/0891-5849(89)90160-3
  14. Fan C, Zwacka RM, Engelhardt JF. Therapeutic approaches for ischemia/reperfusion injury in the liver. J Mol Med (Berl) 1999;77:577-92. https://doi.org/10.1007/s001099900029
  15. Nieminen AL, Byrne AM, Herman B, Lemasters JJ. Mitochondrial permeability transition in hepatocytes induced by t-BuOOH: NAD(P)H and reactive oxygen species. Am J Physiol 1997;272(4 Pt 1):C1286-94. https://doi.org/10.1152/ajpcell.1997.272.4.C1286
  16. Bryan NS, Grisham MB. Methods to detect nitric oxide and its metabolites in biological samples. Free Radic Biol Med 2007;43:645-57. https://doi.org/10.1016/j.freeradbiomed.2007.04.026
  17. Mitrogianni Z, Barbouti A, Galaris D, Siamopoulos KC. Tyrosine nitration in plasma proteins from patients undergoing hemodialysis. Am J Kidney Dis 2004;44:286-92. https://doi.org/10.1053/j.ajkd.2004.04.034
  18. Fondevila C, Shen XD, Tsuchihashi S, Uchida Y, Freitas MC, Ke B, et al. The membrane attack complex (C5b-9) in liver cold ischemia and reperfusion injury. Liver Transpl 2008;14:1133-41. https://doi.org/10.1002/lt.21496
  19. Chiang N, Gronert K, Clish CB, O'Brien JA, Freeman MW, Serhan CN. Leukotriene B4 receptor transgenic mice reveal novel protective roles for lipoxins and aspirin-triggered lipoxins in reperfusion. J Clin Invest 1999;104:309-16. https://doi.org/10.1172/JCI7016
  20. Inderbitzin D, Beldi G, Avital I, Vinci G, Candinas D. Local and remote ischemia-reperfusion injury is mitigated in mice overexpressing human C1 inhibitor. Eur Surg Res 2004;36:142-7. https://doi.org/10.1159/000077255
  21. Peralta C, Fernandez L, Panes J, Prats N, Sans M, Pique JM, et al. 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 2001;33:100-13. https://doi.org/10.1053/jhep.2001.20529
  22. Rajesh M, Pan H, Mukhopadhyay P, Batkai S, Osei-Hyiaman D, Hasko G, et al. Cannabinoid-2 receptor agonist HU-308 protects against hepatic ischemia/reperfusion injury by attenuating oxidative stress, inflammatory response, and apoptosis. J Leukoc Biol 2007;82:1382-9. https://doi.org/10.1189/jlb.0307180
  23. Doulias PT, Barbouti A, Galaris D, Ischiropoulos H. SIN-1-induced DNA damage in isolated human peripheral blood lymphocytes as assessed by single cell gel electrophoresis (comet assay). Free Radic Biol Med 2001;30:679-85. https://doi.org/10.1016/S0891-5849(00)00511-6
  24. Hon WM, Lee KH, Khoo HE. Nitric oxide in liver diseases: friend, foe, or just passerby? Ann N Y Acad Sci 2002;962:275-95. https://doi.org/10.1111/j.1749-6632.2002.tb04074.x
  25. Szabo C. Multiple pathways of peroxynitrite cytotoxicity. Toxicol Lett 2003;140-1:105-12. https://doi.org/10.1016/S0378-4274(02)00507-6
  26. Montalvo-Jave EE, Escalante-Tattersfield T, Ortega-Salgado JA, Pina E, Geller DA. Factors in the pathophysiology of the liver ischemia-reperfusion injury. J Surg Res 2008;147:153-9. https://doi.org/10.1016/j.jss.2007.06.015
  27. Haddad JJ. Antioxidant and prooxidant mechanisms in the regulation of redox(y)-sensitive transcription factors. Cell Signal 2002;14:879-97. https://doi.org/10.1016/S0898-6568(02)00053-0
  28. Gutteridge JM. Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clin Chem 1995;41(12 Pt 2):1819-28. https://doi.org/10.1093/clinchem/41.12.1819
  29. Kang SW, Chae HZ, Seo MS, Kim K, Baines IC, Rhee SG. Mammalian peroxiredoxin isoforms can reduce hydrogen peroxide generated in response to growth factors and tumor necrosis factor-alpha. J Biol Chem 1998;273:6297-302. https://doi.org/10.1074/jbc.273.11.6297
  30. Phillips L, Toledo AH, Lopez-Neblina F, Anaya-Prado R, Toledo-Pereyra LH. Nitric oxide mechanism of protection in ischemia and reperfusion injury. J Invest Surg 2009;22:46-55. https://doi.org/10.1080/08941930802709470
  31. Caban A, Oczkowicz G, Abdel-Samad O, Cierpka L. Influence of Kupffer cells on the early phase of liver reperfusion. Transplant Proc 2002;34:694-7. https://doi.org/10.1016/S0041-1345(01)02891-3
  32. Jaeschke H, Farhood A. Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver. Am J Physiol 1991;260(3 Pt 1):G355-62. https://doi.org/10.1152/ajpgi.1991.260.3.G355
  33. Jaeschke H. Reactive oxygen and mechanisms of inflammatory liver injury. J Gastroenterol Hepatol 2000;15:718-24. https://doi.org/10.1046/j.1440-1746.2000.02207.x
  34. Hanschen M, Zahler S, Krombach F, Khandoga A. Reciprocal activation between CD4+ T cells and Kupffer cells during hepatic ischemia-reperfusion. Transplantation 2008;86:710-8. https://doi.org/10.1097/TP.0b013e3181821aa7
  35. Caldwell CC, Tschoep J, Lentsch AB. Lymphocyte function during hepatic ischemia/reperfusion injury. J Leukoc Biol 2007;82:457-64. https://doi.org/10.1189/jlb.0107062
  36. van Golen RF, van Gulik TM, Heger M. The sterile immune response during hepatic ischemia/reperfusion. Cytokine Growth Factor Rev 2012;23:69-84. https://doi.org/10.1016/j.cytogfr.2012.04.006
  37. Collard CD, Lekowski R, Jordan JE, Agah A, Stahl GL. Complement activation following oxidative stress. Mol Immunol 1999;36:941-8. https://doi.org/10.1016/S0161-5890(99)00116-9
  38. Colletti LM, Remick DG, Burtch GD, Kunkel SL, Strieter RM, Campbell DA Jr. Role of tumor necrosis factor-alpha in the pathophysiologic alterations after hepatic ischemia/reperfusion injury in the rat. J Clin Invest 1990;85:1936-43. https://doi.org/10.1172/JCI114656
  39. Schwabe RF, Brenner DA. Mechanisms of Liver Injury. I. TNF-alpha-induced liver injury: role of IKK, JNK, and ROS pathways. Am J Physiol Gastrointest Liver Physiol 2006;290:G583-9. https://doi.org/10.1152/ajpgi.00422.2005
  40. Kato A, Gabay C, Okaya T, Lentsch AB. Specific role of interleukin-1 in hepatic neutrophil recruitment after ischemia/reperfusion. Am J Pathol 2002;161:1797-803. https://doi.org/10.1016/S0002-9440(10)64456-2
  41. Husted TL, Blanchard J, Schuster R, Shen H, Lentsch AB. Potential role for IL-23 in hepatic ischemia/reperfusion injury. Inflamm Res 2006;55:177-8. https://doi.org/10.1007/s00011-006-0073-1
  42. Mukhopadhyay P, Horvath B, Zsengeller Z, Batkai S, Cao Z, Kechrid M, et al. Mitochondrial reactive oxygen species generation triggers inflammatory response and tissue injury associated with hepatic ischemia-reperfusion: therapeutic potential of mitochondrially targeted antioxidants. Free Radic Biol Med 2012;53:1123-38. https://doi.org/10.1016/j.freeradbiomed.2012.05.036
  43. Kono H, Rock KL. How dying cells alert the immune system to danger. Nat Rev Immunol 2008;8:279-89. https://doi.org/10.1038/nri2215
  44. Romson JL, Hook BG, Kunkel SL, Abrams GD, Schork MA, Lucchesi BR. Reduction of the extent of ischemic myocardial injury by neutrophil depletion in the dog. Circulation 1983;67:1016-23. https://doi.org/10.1161/01.CIR.67.5.1016
  45. Tsung A, Sahai R, Tanaka H, Nakao A, Fink MP, Lotze MT, et al. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 2005;201:1135-43. https://doi.org/10.1084/jem.20042614
  46. Zhai Y, Shen XD, O'Connell R, Gao F, Lassman C, Busuttil RW, et al. Cutting edge: TLR4 activation mediates liver ischemia/reperfusion inflammatory response via IFN regulatory factor 3-dependent MyD88-independent pathway. J Immunol 2004;173:7115-9. https://doi.org/10.4049/jimmunol.173.12.7115
  47. Karwinski W, Soreide O. Allopurinol improves scavenging ability of the liver after ischemia/reperfusion injury. Liver 1997;17:139-43. https://doi.org/10.1111/j.1600-0676.1997.tb00796.x
  48. Liu PG, He SQ, Zhang YH, Wu J. Protective effects of apocynin and allopurinol on ischemia/reperfusion-induced liver injury in mice. World J Gastroenterol 2008;14:2832-7. https://doi.org/10.3748/wjg.14.2832
  49. Abe T, Unno M, Takeuchi H, Kakita T, Katayose Y, Rikiyama T, et al. A new free radical scavenger, edaravone, ameliorates oxidative liver damage due to ischemia-reperfusion in vitro and in vivo. J Gastrointest Surg 2004;8:604-15. https://doi.org/10.1016/j.gassur.2004.02.011
  50. He L, Lemasters JJ. Regulated and unregulated mitochondrial permeability transition pores: a new paradigm of pore structure and function? FEBS Lett 2002;512:1-7. https://doi.org/10.1016/S0014-5793(01)03314-2
  51. Bilzer M, Lauterburg BH. Effects of hypochlorous acid and chloramines on vascular resistance, cell integrity, and biliary glutathione disulfide in the perfused rat liver: modulation by glutathione. J Hepatol 1991;13:84-9. https://doi.org/10.1016/0168-8278(91)90868-C
  52. Atalla SL, Toledo-Pereyra LH, MacKenzie GH, Cederna JP. Influence of oxygen-derived free radical scavengers on ischemic livers. Transplantation 1985;40:584-90. https://doi.org/10.1097/00007890-198512000-00002
  53. Nordstrom G, Saljo A, Hasselgren PO. Studies on the possible role of oxygen-derived free radicals for impairment of protein and energy metabolism in liver ischemia. Circ Shock 1988;26:115-26.
  54. Marubayashi S, Dohi K, Yamada K, Kawasaki T. Changes in the levels of endogenous coenzyme Q homologs, alpha-tocopherol, and glutathione in rat liver after hepatic ischemia and reperfusion, and the effect of pretreatment with coenzyme Q10. Biochim Biophys Acta 1984;797:1-9. https://doi.org/10.1016/0304-4165(84)90375-1
  55. Betteridge DJ. What is oxidative stress? Metabolism 2000;49(2 Suppl 1):3-8. https://doi.org/10.1016/S0026-0495(00)80077-3
  56. Layton ME, Wood JG, Yan ZY, Forster J. Ischemia/reperfusion alters uric acid and ascorbic acid levels in liver. J Surg Res 1996;64:1-5. https://doi.org/10.1006/jsre.1996.0297
  57. Birlouez-Aragon I, Tessier FJ. Antioxidant vitamins and degenerative pathologies. A review of vitamin C. J Nutr Health Aging 2003;7:103-9.
  58. Traber MG. Determinants of plasma vitamin E concentrations. Free Radic Biol Med 1994;16:229-39. https://doi.org/10.1016/0891-5849(94)90148-1
  59. Vertuani S, Angusti A, Manfredini S. The antioxidants and pro-antioxidants network: an overview. Curr Pharm Des 2004;10:1677-94. https://doi.org/10.2174/1381612043384655
  60. Mallick IH, Yang W, Winslet MC, Seifalian AM. Ischemia-reperfusion injury of the intestine and protective strategies against injury. Dig Dis Sci 2004;49:1359-77. https://doi.org/10.1023/B:DDAS.0000042232.98927.91
  61. Carini R, Albano E. Recent insights on the mechanisms of liver preconditioning. Gastroenterology 2003;125:1480-91. https://doi.org/10.1016/j.gastro.2003.05.005
  62. Anttila V, Haapanen H, Yannopoulos F, Herajarvi J, Anttila T, Juvonen T. Review of remote ischemic preconditioning: from laboratory studies to clinical trials. Scand Cardiovasc J 2016;50:355-61. https://doi.org/10.1080/14017431.2016.1233351
  63. Ocuin LM, Zeng S, Cavnar MJ, Sorenson EC, Bamboat ZM, Greer JB, et al. Nilotinib protects the murine liver from ischemia/reperfusion injury. J Hepatol 2012;57:766-73. https://doi.org/10.1016/j.jhep.2012.05.012
  64. Prime TA, Blaikie FH, Evans C, Nadtochiy SM, James AM, Dahm CC, et al. A mitochondria-targeted S-nitrosothiol modulates respiration, nitrosates thiols, and protects against ischemia-reperfusion injury. Proc Natl Acad Sci U S A 2009;106:10764-9. https://doi.org/10.1073/pnas.0903250106
  65. Shiratori Y, Kiriyama H, Fukushi Y, Nagura T, Takada H, Hai K, et al. Modulation of ischemia-reperfusion-induced hepatic injury by Kupffer cells. Dig Dis Sci 1994;39:1265-72. https://doi.org/10.1007/BF02093792
  66. Panes J, Perry M, Granger DN. Leukocyte-endothelial cell adhesion: avenues for therapeutic intervention. Br J Pharmacol 1999;126:537-50. https://doi.org/10.1038/sj.bjp.0702328
  67. Caldwell-Kenkel JC, Currin RT, Tanaka Y, Thurman RG, Lemasters JJ. Kupffer cell activation and endothelial cell damage after storage of rat livers: effects of reperfusion. Hepatology 1991;13:83-95.
  68. Oliveira TH, Marques PE, Proost P, Teixeira MM. Neutrophils: a cornerstone of liver ischemia and reperfusion injury. Lab Invest 2018;98:51-62. https://doi.org/10.1038/labinvest.2017.90
  69. Yang YL, Li JP, Xu XP, Dou KF, Yue SQ, Li KZ. Protective effects of tumor necrosis factor alpha antibody and ulinastatin on liver ischemic reperfusion in rats. World J Gastroenterol 2004;10:3161-4. https://doi.org/10.3748/wjg.v10.i21.3161
  70. Jaeschke H, Farhood A, Bautista AP, Spolarics Z, Spitzer JJ. Complement activates Kupffer cells and neutrophils during reperfusion after hepatic ischemia. Am J Physiol 1993;264(4 Pt 1):G801-9. https://doi.org/10.1152/ajpgi.1993.264.4.G801