The Function of Kupffer Cell for The Ischemia Reperfusion Injury after Liver’s Transplantation_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

MA Yuanyuan , LI Jiyu

Department of General Surgery, Xinhua Hospital, Shanghai 200092, China;

Corresponding author：

Keywords：

Kupffer cells; Ischemia reperfusion injury; Liver transplantation

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Objective 　To summarize the function of Kupffer cell for the ischemia reperfusion injury after liver’s transplatation.
Methods 　The literatures which about the function of Kupffer cell for the ischemia reperfusion injury after liver’s transplatation were reviewed.
Results 　Kupffer cells are the resident macrophages of the liver, which can be activated to generate a range of inflammatory mediators, including cytokines, reactive oxygen intermediates, chemokines, and other factors to startup the ischemia reperfusion injury （IRI）, and to cause the liver graft dysfunction. On the other hand, Kupffer cells can protect the ischemia reperfusion injury by release NO and HO-1. The CO, which is the byproduct of heme degradation by the heme oxygenases （HO-1），has the same function for IRI.
Conclusions 　The Kupffer cells have bidirectional function for the ischemia reperfusion injury of liver’s transpatation. Thus, how to decrease the harmful factors and up-regulate the beneficial substances by Kupffer cells will be the key points in preventing IRI after liver transplantation in future.

Citation： MA Yuanyuan,LI Jiyu,.. The Function of Kupffer Cell for The Ischemia Reperfusion Injury after Liver’s Transplantation. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2012, 19(3): 341-345. doi: Copy

1.	Lloyd CM， Phillips AR， Cooper GJ， et al. Three-colour fluorescence immunohistochemistry reveals the diversity of cells staining for macrophage markers in murine spleen and liver [J]. J Immunol Methods， 2008， 334(1-2)： 70-81.
2.	Nemeth E， Baird AW， O’Farrelly C. Microanatomy of the liver immune system [J]. Semin Immunopathol， 2009， 31(3)： 333-343.
3.	Tiegs G， Lohse AW. Immune tolerance：what is unique about the liver[J]. J Autoimmun， 2010， 34(1)：1-6.
4.	Kolios G， Valatas V， Kouroumalis E， et al. Role of Kupffer cells in the pathogenesis of liver disease [J]. World J Gastroenterol，2006， 12(46)： 7413–7420.
5.	Kono H， Fujii H， Amemiya H， et al. Role of Kupffer cells in lung injury in rats administered endotoxin 1 [J]. J Surg Res，2005， 129(2)： 176–189.
6.	Kono H， Fujii H， Asakawa M， et al. Functional heterogeneity of the Kupffer cell population is involved in the mechanism of gadolinium chloride in rats administered endotoxin [J]. J Surg Res，2002， 106(1)： 179-187.
7.	Beattie L， Svensson M， Bune A， et al. Leishmania donovaniinduced expression of signal regulatory protein alpha on Kupffer cells enhances hepatic invariant NKT-cell activation [J]. Eur J Immunol， 2010， 40(1)： 117-123.
8.	You Q， Cheng L， Kedl RM， et al. Mechanism of T cell tolerance induction by murine hepatic Kupffer cells [J]. Hepatology，2008， 48(3)： 978-990.
9.	Crispe IN. The liver as a lymphoid organ [J]. Annu Rev Inununol，2009， 27： 147-163.
10.	Liang J， Yamaguchi Y， Matsumura F， et al. Calcium-channel blocker attenuates Kupffer cell production of cytokine-induced neutrophil chemoattractant following ischemia-reperfusion in rat liver [J]. Dig Dis Sci， 2000， 45(1)： 201-209.
11.	Casillas-Ramírez A， Mosbah IB， Franco-Gou R， et al. Ischemiareperfusion syndrome associated with liver transplantation： an update [J]. Gastroenterol Hepatol， 2006， 29(5)： 306-313.
12.	Jahnke C， Mehrabi A， Golling M， et al. Evaluation of microperfusion disturbances in the transplanted liver after Kupffer cell destruction using GdCl3： an experimental porcine study [J].Transplant Proc， 2006， 38(5)： 1588-1595.
13.	Tanaka Y， Chen C， Maher JM， et al. Kupffer cell-mediated downregulation of hepatic transporter expression in rat hepatic ischemia-reperfusion [J]. Transplantation， 2006， 82(2)： 258-266.
14.	Ellett JD， Atkinson C， Evans ZP， et al. Toll-like receptor 4 knockout mice are protected from endothelial overactivation in the absence of Kupffer cells after total hepatic ischemia/reperfusion [J]. Liver Transpl， 2011， 17(9)： 1089-1098.
15.	Jiang N， Zhang ZM， Liu L， et al. Effects of Ca2 ＋ Channel blockers on store-operated Ca2＋ channel currents of Kupffer cells after hepatic ischemia/reperfusion injury in rats [J]. World J Gastroenterol，2006， 12(29)： 4694-4698.
16.	Serracino-Inglott F， Habib N， Mathie RT. Hepatic ischemiareperfusion injury [J]. Am J Surg， 2001， 181(2)： 160-166.
17.	Mosher B， Dean R， Harkema J， et al. Inhibition of Kupffer cells reduced CXC chemokine production and liver injury [J]. J Surg Res， 2001， 99(2)： 201-210.
18.	Zhu H， Guo YZ， Zhang J， et al. Donor denervation and elimination of Kupffer cells affect expression of P-selectin and ICAM-1 in liver graft [J]. Hepatobiliary Pancreat Dis Int， 2007， 6(4)： 379-382.
19.	Andrukhiv A， Costa AD， West IC， et al. Opening mito K(ATP) increases superoxide generation from complex Ⅰ of the electron transport chain [J]. Am J Physiol Heart Circ Physiol， 2006，291(5)： H2067-H2074.
20.	Jaeschke H. Role of reactive oxygen species in hepatic ischemiareperfusion injury and preconditioning [J]. J Invest Surg， 2003，16(3)： 127-140.
21.	Urakami H， Abe Y， Grisham MB. Role of reactive metabolites of oxygen and nitrogen in partial liver transplantation： lessons learned from reduced-size liver ischaemia and reperfusion injury [J]. Clin Exp Pharmacol Physiol， 2007， 34(9)： 912-919.
22.	Schwabe RF， Brenner DA. TNF-alpha-induced liver injury： role of IKK， JNK and ROS pathways [J]. Am J Physiol Gastrointest Liver Physiol， 2006， 290(4)： G583-G589.
23.	Abu-Amara M， Yang SY， Tapuria N， et al. Liver Ischemia/ Reperfusion Injury： Processes in inflammatory Networks —— A Review [J]. Liver Transpl， 2010， 16(9)：1016-1032.
24.	Zhang M， Xu S， Han Y， et al. Apoptotic cells attenuate fulminant hepatitis by priming Kupffer cells to produce interleukin-10 through membrane-bound TGF-β [J]. Hepatology， 2011， 53(1)：306-316.
25.	Ellett JD， Atkinson C， Evans ZP， et al. Murine Kupffer cells are protective in total hepatic ischemia/reperfusion injury with bowel congestion through IL-10 [J]. J Immunol， 2010， 184(10)： 5849-5858.
26.	Jessup JM， Laguinge L， Lin S， et al. Carcinoembryonic antigen induction of IL-10 and IL-6 inhibits hepatic ischemic/reperfusion injury to colorectal carcinoma cells [J]. Int J Cancer， 2004，111(3)： 332-337.
27.	Hsu CM， Wang JS， Liu CH， et al. Kupffer cells protect liver from ischemia/reperfusion injury by an inducible nritirc oxide synthase-dependent mechanisam [J]. Shock， 2002， 17(4)：280–285.
28.	宿华威，孙世波，孙铁为，等. 血红素氧合酶-1 在临床肝移植中肝脏保护作用的研究 [J]. 中华肝胆外科杂志， 2010， 16 (7)： 504-507．.
29.	Ananta P， Eiz-Vesper B， Blasczyk R， et al. Signaling to heme oxygenase-1 and its anti-in?ammatory therapeutic potential [J].Biochemical Pharmacology， 2010， 80(12)： 1895-1903.
30.	Louvet A， Teixeira-Clerc F， Chobert MN， et al. Cannabinoid CB2 receptors protect against alcoholic liver disease by regulating Kupffer cell polarization in mice [J]. Hepatology， 2011， 54(4)：1217-1226.
31.	Wang CF， Wang ZY， Li JY. Dual protective role of HO-1 in transplanted liver grafts： a review of experimental and clinical studies [J]. World J Gastroenterol， 2011， 17(26)： 3101-3108.
32.	Babu AN， Damle SS， Moore EE， et al. Hemoglobin-based oxygen carrier induces hepatic heme oxygenase 1 expression in Kupffer cells [J]. Surgery， 2007， 142(2)： 289-294.
33.	Zeng Z， Huang HF， Chen MQ， et al. Heme oxygenase-1 protects donor livers from ischemia/reperfusion injury： the role of Kupffer cells [J]. World J Gastroenterol， 2010， 16(10)： 1285-1292.
34.	Tsuchihashi S， Livhits M， Zhai Y， et al. Basal rather than induced heme oxygenase-1 levels are crucial in the antioxidant cytoprotection [J]. J Immunol， 2006， 177(7)： 4749-4757.
35.	Devey L， Ferenbach D， Mohr E， et al. Tissue-resident macrophages protect the liver from ischemia reperfusion injury via a heme oxygenase-1-dependent mechanism [J]. Mol Ther， 2009，17(1)： 65-72.
36.	Redaelli CA， Tian YH， Schaffner T， et al. Extended preservation of rat liver graft by induction of heme oxygenase-1 [J]. Hepatology，2002， 35(5)： 1082-1092.
37.	Tomiyama K， Ikeda A， Ueki S， et al. Inhibition of Kupffer cellmediated early proin?ammatory response with carbon monoxide in transplant-induced hepatic ischemia/reperfusion injury in rats [J].Hepatology， 2008， 48(5)： 1608-1620.

1. Lloyd CM， Phillips AR， Cooper GJ， et al. Three-colour fluorescence immunohistochemistry reveals the diversity of cells staining for macrophage markers in murine spleen and liver [J]. J Immunol Methods， 2008， 334(1-2)： 70-81.
2. Nemeth E， Baird AW， O’Farrelly C. Microanatomy of the liver immune system [J]. Semin Immunopathol， 2009， 31(3)： 333-343.
3. Tiegs G， Lohse AW. Immune tolerance：what is unique about the liver[J]. J Autoimmun， 2010， 34(1)：1-6.
4. Kolios G， Valatas V， Kouroumalis E， et al. Role of Kupffer cells in the pathogenesis of liver disease [J]. World J Gastroenterol，2006， 12(46)： 7413–7420.
5. Kono H， Fujii H， Amemiya H， et al. Role of Kupffer cells in lung injury in rats administered endotoxin 1 [J]. J Surg Res，2005， 129(2)： 176–189.
6. Kono H， Fujii H， Asakawa M， et al. Functional heterogeneity of the Kupffer cell population is involved in the mechanism of gadolinium chloride in rats administered endotoxin [J]. J Surg Res，2002， 106(1)： 179-187.
7. Beattie L， Svensson M， Bune A， et al. Leishmania donovaniinduced expression of signal regulatory protein alpha on Kupffer cells enhances hepatic invariant NKT-cell activation [J]. Eur J Immunol， 2010， 40(1)： 117-123.
8. You Q， Cheng L， Kedl RM， et al. Mechanism of T cell tolerance induction by murine hepatic Kupffer cells [J]. Hepatology，2008， 48(3)： 978-990.
9. Crispe IN. The liver as a lymphoid organ [J]. Annu Rev Inununol，2009， 27： 147-163.
10. Liang J， Yamaguchi Y， Matsumura F， et al. Calcium-channel blocker attenuates Kupffer cell production of cytokine-induced neutrophil chemoattractant following ischemia-reperfusion in rat liver [J]. Dig Dis Sci， 2000， 45(1)： 201-209.
11. Casillas-Ramírez A， Mosbah IB， Franco-Gou R， et al. Ischemiareperfusion syndrome associated with liver transplantation： an update [J]. Gastroenterol Hepatol， 2006， 29(5)： 306-313.
12. Jahnke C， Mehrabi A， Golling M， et al. Evaluation of microperfusion disturbances in the transplanted liver after Kupffer cell destruction using GdCl3： an experimental porcine study [J].Transplant Proc， 2006， 38(5)： 1588-1595.
13. Tanaka Y， Chen C， Maher JM， et al. Kupffer cell-mediated downregulation of hepatic transporter expression in rat hepatic ischemia-reperfusion [J]. Transplantation， 2006， 82(2)： 258-266.
14. Ellett JD， Atkinson C， Evans ZP， et al. Toll-like receptor 4 knockout mice are protected from endothelial overactivation in the absence of Kupffer cells after total hepatic ischemia/reperfusion [J]. Liver Transpl， 2011， 17(9)： 1089-1098.
15. Jiang N， Zhang ZM， Liu L， et al. Effects of Ca2 ＋ Channel blockers on store-operated Ca2＋ channel currents of Kupffer cells after hepatic ischemia/reperfusion injury in rats [J]. World J Gastroenterol，2006， 12(29)： 4694-4698.
16. Serracino-Inglott F， Habib N， Mathie RT. Hepatic ischemiareperfusion injury [J]. Am J Surg， 2001， 181(2)： 160-166.
17. Mosher B， Dean R， Harkema J， et al. Inhibition of Kupffer cells reduced CXC chemokine production and liver injury [J]. J Surg Res， 2001， 99(2)： 201-210.
18. Zhu H， Guo YZ， Zhang J， et al. Donor denervation and elimination of Kupffer cells affect expression of P-selectin and ICAM-1 in liver graft [J]. Hepatobiliary Pancreat Dis Int， 2007， 6(4)： 379-382.
19. Andrukhiv A， Costa AD， West IC， et al. Opening mito K(ATP) increases superoxide generation from complex Ⅰ of the electron transport chain [J]. Am J Physiol Heart Circ Physiol， 2006，291(5)： H2067-H2074.
20. Jaeschke H. Role of reactive oxygen species in hepatic ischemiareperfusion injury and preconditioning [J]. J Invest Surg， 2003，16(3)： 127-140.
21. Urakami H， Abe Y， Grisham MB. Role of reactive metabolites of oxygen and nitrogen in partial liver transplantation： lessons learned from reduced-size liver ischaemia and reperfusion injury [J]. Clin Exp Pharmacol Physiol， 2007， 34(9)： 912-919.
22. Schwabe RF， Brenner DA. TNF-alpha-induced liver injury： role of IKK， JNK and ROS pathways [J]. Am J Physiol Gastrointest Liver Physiol， 2006， 290(4)： G583-G589.
23. Abu-Amara M， Yang SY， Tapuria N， et al. Liver Ischemia/ Reperfusion Injury： Processes in inflammatory Networks —— A Review [J]. Liver Transpl， 2010， 16(9)：1016-1032.
24. Zhang M， Xu S， Han Y， et al. Apoptotic cells attenuate fulminant hepatitis by priming Kupffer cells to produce interleukin-10 through membrane-bound TGF-β [J]. Hepatology， 2011， 53(1)：306-316.
25. Ellett JD， Atkinson C， Evans ZP， et al. Murine Kupffer cells are protective in total hepatic ischemia/reperfusion injury with bowel congestion through IL-10 [J]. J Immunol， 2010， 184(10)： 5849-5858.
26. Jessup JM， Laguinge L， Lin S， et al. Carcinoembryonic antigen induction of IL-10 and IL-6 inhibits hepatic ischemic/reperfusion injury to colorectal carcinoma cells [J]. Int J Cancer， 2004，111(3)： 332-337.
27. Hsu CM， Wang JS， Liu CH， et al. Kupffer cells protect liver from ischemia/reperfusion injury by an inducible nritirc oxide synthase-dependent mechanisam [J]. Shock， 2002， 17(4)：280–285.
28. 宿华威，孙世波，孙铁为，等. 血红素氧合酶-1 在临床肝移植中肝脏保护作用的研究 [J]. 中华肝胆外科杂志， 2010， 16 (7)： 504-507．.
29. Ananta P， Eiz-Vesper B， Blasczyk R， et al. Signaling to heme oxygenase-1 and its anti-in?ammatory therapeutic potential [J].Biochemical Pharmacology， 2010， 80(12)： 1895-1903.
30. Louvet A， Teixeira-Clerc F， Chobert MN， et al. Cannabinoid CB2 receptors protect against alcoholic liver disease by regulating Kupffer cell polarization in mice [J]. Hepatology， 2011， 54(4)：1217-1226.
31. Wang CF， Wang ZY， Li JY. Dual protective role of HO-1 in transplanted liver grafts： a review of experimental and clinical studies [J]. World J Gastroenterol， 2011， 17(26)： 3101-3108.
32. Babu AN， Damle SS， Moore EE， et al. Hemoglobin-based oxygen carrier induces hepatic heme oxygenase 1 expression in Kupffer cells [J]. Surgery， 2007， 142(2)： 289-294.
33. Zeng Z， Huang HF， Chen MQ， et al. Heme oxygenase-1 protects donor livers from ischemia/reperfusion injury： the role of Kupffer cells [J]. World J Gastroenterol， 2010， 16(10)： 1285-1292.
34. Tsuchihashi S， Livhits M， Zhai Y， et al. Basal rather than induced heme oxygenase-1 levels are crucial in the antioxidant cytoprotection [J]. J Immunol， 2006， 177(7)： 4749-4757.
35. Devey L， Ferenbach D， Mohr E， et al. Tissue-resident macrophages protect the liver from ischemia reperfusion injury via a heme oxygenase-1-dependent mechanism [J]. Mol Ther， 2009，17(1)： 65-72.
36. Redaelli CA， Tian YH， Schaffner T， et al. Extended preservation of rat liver graft by induction of heme oxygenase-1 [J]. Hepatology，2002， 35(5)： 1082-1092.
37. Tomiyama K， Ikeda A， Ueki S， et al. Inhibition of Kupffer cellmediated early proin?ammatory response with carbon monoxide in transplant-induced hepatic ischemia/reperfusion injury in rats [J].Hepatology， 2008， 48(5)： 1608-1620.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

The Function of Kupffer Cell for The Ischemia Reperfusion Injury after Liver’s Transplantation

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