Molecular responses to ischemia and reperfusion in the liver

Archives of Toxicology

Volumn 89, Issue 5, 2015, Pages 651-657

  Quesnelle, Kelly M ^a   Bystrom, Phillip V ^a   Toledo Pereyra, Luis H ^a  

^a WESTERN MICHIGAN UNIVERSITY HOMER STRYKER MD SCHOOL OF MEDICINE   (United States)

Author keywords

Ischemia; Liver; Molecular response; Reperfusion; ROS; Sterile immune response

Indexed keywords

REACTIVE OXYGEN METABOLITE;

ADVERSE EFFECTS; HUMAN; ISCHEMIA; KUPFFER CELL; LIVER; LIVER TRANSPLANTATION; METABOLISM; NECROSIS; PATHOLOGY; PHYSIOLOGY; REPERFUSION INJURY; VASCULARIZATION;

HUMANS; ISCHEMIA; KUPFFER CELLS; LIVER; LIVER TRANSPLANTATION; NECROSIS; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY;

EID: 84939945977     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-014-1437-x     Document Type: Review

References (50)

1. Callapina M, Zhou J, Schmid T et al (2005) NO restores HIF-1alpha hydroxylation during hypoxia: role of reactive oxygen species. Free Radic Biol Med 39:925–936. doi:10.1016/j.freeradbiomed.2005.05.009
2. Camara AKS, Aldakkak M, Heisner JS et al (2007) ROS scavenging before 27 degrees C ischemia protects hearts and reduces mitochondrial ROS, Ca2+ overload, and changes in redox state. Am J Physiol Cell Physiol 292:C2021–C2031. doi:10.1152/ajpcell.00231.2006
3. Chandel NS, Trzyna WC, McClintock DS, Schumacker PT (2000) Role of oxidants in NF-kappa B activation and TNF-alpha gene transcription induced by hypoxia and endotoxin. J Immunol 165:1013–1021
4. Chang WJ, Toledo-Pereyra LH (2011) The role of HMGB1 and HSP72 in ischemia and reperfusion injury. J Surg Res 166:219–221. doi:10.1016/j.jss.2010.05.013
5. Chang WJ, Chehab M, Kink S, Toledo-Pereyra LH (2010) Intracellular calcium signaling pathways during liver ischemia and reperfusion. J Invest Surg 23:228–238. doi:10.3109/08941939.2010.496036
6. Datta G, Fuller BJ, Davidson BR (2013) Molecular mechanisms of liver ischemia reperfusion injury: insights from transgenic knockout models. World J Gastroenterol 19:1683–1698. doi:10.3748/wjg.v19.i11.1683
7. Du C, Fang M, Li Y et al (2000) Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102:33–42
8. Evankovich J, Cho SW, Zhang R et al (2010) High mobility group box 1 release from hepatocytes during ischemia and reperfusion injury is mediated by decreased histone deacetylase activity. J Biol Chem 285:39888–39897. doi:10.1074/jbc.M110.128348
9. Franchello A, Gilbo N, David E et al (2009) Ischemic preconditioning (IP) of the liver as a safe and protective technique against ischemia/reperfusion injury (IRI). Am J Transplant 9:1629–1639. doi:10.1111/j.1600-6143.2009.02680.x
10. Görlach A, Berchner-Pfannschmidt U, Wotzlaw C et al (2003) Reactive oxygen species modulate HIF-1 mediated PAI-1 expression: involvement of the GTPase Rac1. Thromb Haemost 89:926–935. doi:10.1267/THRO03050926
11. Grisham MB, Hernandez LA, Granger DN (1986) Xanthine oxidase and neutrophil infiltration in intestinal ischemia. Am J Physiol 251:G567–G574
12. Guzy RD, Schumacker PT (2006) Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia. Exp Physiol 91:807–819. doi:10.1113/expphysiol.2006.033506
13. Hanschen M, Zahler S, Krombach F, Khandoga A (2008) Reciprocal activation between CD4+ T cells and Kupffer cells during hepatic ischemia-reperfusion. Transplantation 86:710–718. doi:10.1097/TP.0b013e3181821aa7
14. Hu C-J, Wang L-Y, Chodosh LA et al (2003) Differential roles of hypoxia-inducible factor 1alpha (HIF-1α) and HIF-2α in hypoxic gene regulation. Mol Cell Biol 23:9361–9374
15. Imamura H, Sutto F, Brault A, Huet PM (1995) Role of Kupffer cells in cold ischemia/reperfusion injury of rat liver. Gastroenterology 109:189–197
16. Jaeschke H, Farhood A (1991) Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver. Am J Physiol 260:G355–G362
17. Jaeschke H, Lemasters JJ (2003) Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury. Gastroenterology 125:1246–1257. doi:10.1016/S0016-5085(03)01209-5
18. Jaeschke H, Woolbright BL (2012) Current strategies to minimize hepatic ischemia-reperfusion injury by targeting reactive oxygen species. Transplant Rev (Orlando) 26:103–114. doi:10.1016/j.trre.2011.10.006
19. Jaeschke H, Smith CV, Mitchell JR (1988) Hypoxic damage generates reactive oxygen species in isolated perfused rat liver. Biochem Biophys Res Commun 150:568–574
20. Kim JS, He L, Qian T, Lemasters JJ (2003) Role of the mitochondrial permeability transition in apoptotic and necrotic death after ischemia/reperfusion injury to hepatocytes. Curr Mol Med 3:527–535
21. Klinman JP (2007) How do enzymes activate oxygen without inactivating themselves? Acc Chem Res 40:325–333. doi:10.1021/ar6000507
22. Kussmaul L, Hirst J (2006) The mechanism of superoxide production by NADH: ubiquinone oxidoreductase (complex I) from bovine heart mitochondria. Proc Natl Acad Sci USA 103:7607–7612. doi:10.1073/pnas.0510977103
23. Lambert AJ, Brand MD (2004) Superoxide production by NADH: ubiquinone oxidoreductase (complex I) depends on the pH gradient across the mitochondrial inner membrane. Biochem J 382:511–517. doi:10.1042/BJ20040485
24. Lemasters JJ, DiGuiseppi J, Nieminen AL, Herman B (1987) Blebbing, free Ca2+ and mitochondrial membrane potential preceding cell death in hepatocytes. Nature 325:78–81. doi:10.1038/325078a0
25. Loschen G, Azzi A, Richter C, Flohé L (1974) Superoxide radicals as precursors of mitochondrial hydrogen peroxide. FEBS Lett 42:68–72
26. Latanich CA, Toledo-Pereyra LH (2009) Searching for NF-kappaB-based treatments of ischemia reperfusion injury. J Invest Surg 22:301–315
27. McCord JM (1985) Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med 312:159–163. doi:10.1056/NEJM198501173120305
28. Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417:1–13. doi:10.1042/BJ20081386
29. Nace GW, Huang H, Klune JR et al (2013) Cellular-specific role of toll-like receptor 4 in hepatic ischemia-reperfusion injury in mice. Hepatology 58:374–387. doi:10.1002/hep.26346
30. Patel RP, Lang JD, Smith AB, Crawford JH (2014) Redox therapeutics in hepatic ischemia reperfusion injury. World J Hepatol 6:1–8. doi:10.4254/wjh.v6.i1.1
31. Perry BC, Soltys D, Toledo AH, Toledo-Pereyra LH (2011) Tumor necrosis factor-α in liver ischemia/reperfusion injury. J Invest Surg 24:178–188. doi:10.3109/08941939.2011.568594
32. Prime TA, Blaikie FH, Evans C et al (2009) A mitochondria-targeted S-nitrosothiol modulates respiration, nitrosates thiols, and protects against ischemia-reperfusion injury. Proc Natl Acad Sci USA 106:10764–10769. doi:10.1073/pnas.0903250106
33. +] levels during short-term 17 °C ischemia in intact hearts. Cardiovasc Res 61:580–590. doi:10.1016/j.cardiores.2003.09.016
34. Romson JL, Hook BG, Kunkel SL et al (1983) Reduction of the extent of ischemic myocardial injury by neutrophil depletion in the dog. Circulation 67:1016–1023
35. Sanjuán-Pla A, Cervera AM, Apostolova N et al (2005) A targeted antioxidant reveals the importance of mitochondrial reactive oxygen species in the hypoxic signaling of HIF-1alpha. FEBS Lett 579:2669–2674. doi:10.1016/j.febslet.2005.03.088
36. Semenza GL (2004) O2-regulated gene expression: transcriptional control of cardiorespiratory physiology by HIF-1. J Appl Physiol 96:1173–1177; discussion 1170-2. doi:10.1152/japplphysiol.00770.2003
37. Shen X, Wang Y, Gao F et al (2009) CD4 T cells promote tissue inflammation via CD40 signaling without de novo activation in a murine model of liver ischemia/reperfusion injury. Hepatology 50:1537–1546. doi:10.1002/hep.23153
38. Steffan NM, Bren GD, Frantz B et al (1995) Regulation of IkB alpha phosphorylation by PKC- and Ca(2+)-dependent signal transduction pathways. J Immunol 155:4685–4691
39. Tacchini L, Fusar Poli D, Bernelli-Zazzera A, Cairo G (2002) Transferrin receptor gene expression and transferrin-bound iron uptake are increased during postischemic rat liver reperfusion. Hepatology 36:103–111. doi:10.1053/jhep.2002.33997
40. Taniai H, Hines IN, Bharwani S et al (2004) Susceptibility of murine periportal hepatocytes to hypoxia-reoxygenation: role for NO and Kupffer cell-derived oxidants. Hepatology 39:1544–1552. doi:10.1002/hep.20217
41. Thomas EL, Grisham MB, Jefferson MM (1983) Myeloperoxidase-dependent effect of amines on functions of isolated neutrophils. J Clin Invest 72:441–454
42. Tsung A, Sahai R, Tanaka H et al (2005) The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 201:1135–1143. doi:10.1084/jem.20042614
43. Tsung A, Klune JR, Zhang X et al (2007) HMGB1 release induced by liver ischemia involves Toll-like receptor 4 dependent reactive oxygen species production and calcium-mediated signaling. J Exp Med 204:2913–2923. doi:10.1084/jem.20070247
44. Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552:335–344. doi:10.1113/jphysiol.2003.049478
45. Van Golen RF, van Gulik TM, Heger M (2012) The sterile immune response during hepatic ischemia/reperfusion. Cytokine Growth Factor Rev 23:69–84. doi:10.1016/j.cytogfr.2012.04.006
46. Verhagen AM, Ekert PG, Pakusch M et al (2000) Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102:43–53
47. Wang H, Bloom O, Zhang M et al (1999) HMG-1 as a late mediator of endotoxin lethality in mice. Science 285:248–251
48. Yang Q, Liu Y, Shi Y et al (2013) The role of intracellular high-mobility group box 1 in the early activation of Kupffer cells and the development of Con A-induced acute liver failure. Immunobiology 218:1284–1292. doi:10.1016/j.imbio.2013.04.011
49. Zhang X, Lemasters JJ (2013) Translocation of iron from lysosomes to mitochondria during ischemia predisposes to injury after reperfusion in rat hepatocytes. Free Radic Biol Med 63:243–253. doi:10.1016/j.freeradbiomed.2013.05.004
50. Zimmerman JJ, Zuk SM, Millard JR (1989) In vitro modulation of human neutrophil superoxide anion generation by various calcium channel antagonists used in ischemia-reperfusion resuscitation. Biochem Pharmacol 38:3601–3610