FGL2/Fibroleukin mediates hepatic reperfusion injury by induction of sinusoidal endothelial cell and hepatocyte apoptosis in mice

Journal of Hepatology

Volumn 56, Issue 1, 2012, Pages 153-159

  Selzner, Nazia ^a   Liu, Hao ^a   Boehnert, Markus U ^a   Adeyi, Oyedele A ^a   Shalev, Itay ^a   Bartczak, Agata M ^a   Xue Zhong, Max ^a   Manuel, Justin ^a   Rotstein, Ori D ^b   McGilvray, Ian D ^a   Grant, David R ^a   Phillips, Melville J ^a   Levy, Gary A ^a   Selzner, Markus ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

Apoptosis; Fc RIIB; FGL2; Reperfusion injury

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CASPASE 3; FC RECEPTOR IIB; FIBRINOGEN; FIBRINOGEN LIKE PROTEIN 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME RELEASE; GENE DELETION; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; LIVER INJURY; LIVER ISCHEMIA; LIVER SINUSOID; MALE; MOUSE; NICK END LABELING; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RECEPTOR BINDING; REPERFUSION INJURY; SURVIVAL; WILD TYPE;

ANIMALS; APOPTOSIS; ENDOTHELIAL CELLS; FIBRINOGEN; HEPATOCYTES; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, IGG; REPERFUSION INJURY;

EID: 83555163882     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2011.05.033     Document Type: Article

References (43)

1. S. Natori, M. Selzner, K. Valentino, L. Fritz, A. Srinivasan, and P.-A. Clavien Apoptosis of sinusoidal endothelial cells occurs during liver preservation injury by a caspase-dependent mechanism Transplantation 68 1999 89 96 (Pubitemid 29352837)
2. V. Kohli, M. Selzner, J. Madden, R. Bentley, and P. Clavien Endothelial cell and hepatocyte deaths occur by apoptosis after ischemia-reperfusion injury in the rat liver Transplantation 67 1999 1099 1105 (Pubitemid 29205570)
3. J. Caldwell-Kenkel, R. Currin, Y. Tanaka, R. Thurman, and J. Lemasters Reperfusion injury to endothelial cells following cold ischemic storage of rat livers Hepatology 10 1989 292 299 (Pubitemid 19214952)
4. T. Ikeda, K. Yanaga, K. Kishikawa, S. Kakizoe, M. Shimada, and K. Sugimachi Ischemic injury in liver transplantation: difference in injury sites between warm and cold ischemia in rats Hepatology 16 1992 454 461
5. P.A. Clavien, P.R. Harvey, and S.M. Strasberg Preservation and reperfusion injuries in liver allografts. An overview and synthesis of current studies Transplantation 53 1992 957 978
6. K. Vajdova, S. Heinrich, Y. Tian, R. Graf, and P.A. Clavien Ischemic preconditioning and intermittent clamping improve murine hepatic microcirculation and Kupffer cell function after ischemic injury Liver Transpl 10 2004 520 528 (Pubitemid 38443591)
7. J. Panes, and D.N. Granger Leukocyte-endothelial cell interactions: molecular mechanisms and implications in gastrointestinal disease Gastroenterology 114 1998 1066 1090 (Pubitemid 28217575)
8. J.J. Lemasters, and R.G. Thurman Reperfusion injury after liver preservation for transplantation Annu Rev Pharmacol Toxicol 37 1997 327 338 (Pubitemid 27238879)
9. S. Natori, H. Higuchi, P. Contreras, and G.J. Gores The caspase inhibitor IDN-6556 prevents caspase activation and apoptosis in sinusoidal endothelial cells during liver preservation injury Liver Transpl 9 2003 278 284 (Pubitemid 36322330)
10. X. Liu, and T.H. Piela-Smith Fibrin(ogen)-induced expression of ICAM-1 and chemokines in human synovial fibroblasts J Immunol 165 2000 5255 5261
11. R.G. Sitrin, P.M. Pan, S. Srikanth, and R.F. Todd 3rd Fibrinogen activates NF-kappa B transcription factors in mononuclear phagocytes J Immunol 161 1998 1462 1470 (Pubitemid 28380578)
12. A. Ghanekar, M. Mendicino, H. Liu, W. He, M. Liu, and R. Zhong Endothelial induction of fgl2 contributes to thrombosis during acute vascular xenograft rejection J Immunol 172 2004 5693 5701 (Pubitemid 38542073)
13. M. Liu, M. Mendicino, Q. Ning, A. Ghanekar, W. He, and I. McGilvray Cytokine-induced hepatic apoptosis is dependent on FGL2/fibroleukin: the role of Sp1/Sp3 and STAT1/PU.1 composite cis elements J Immunol 176 2006 7028 7038 (Pubitemid 43787884)
14. S. Marazzi, S. Blum, R. Hartmann, D. Gundersen, M. Schreyer, and S. Argraves Characterization of human fibroleukin, a fibrinogen-like protein secreted by T lymphocytes J Immunol 161 1998 138 147 (Pubitemid 28285516)
15. J.W. Ding, Q. Ning, M.F. Liu, A. Lai, J. Leibowitz, and K.M. Peltekian Fulminant hepatic failure in murine hepatitis virus strain 3 infection: tissue-specific expression of a novel fgl2 prothrombinase Journal of Virology 71 1997 9223 9230 [erratum appears in J Virol 1998 Apr;72(4):3504] (Pubitemid 27492364)
16. D.F. Rychlik, E.K. Chien, D. Wolff, S. Phillippe, and M. Phillippe Cloning and tissue expression of the tissue prothrombinase Fgl-2 in the Sprague-Dawley rat J Soc Gynecol Investig 10 2003 67 73 (Pubitemid 36184761)
17. O. Le Moine, H. Louis, A. Demols, F. Desalle, F. Demoor, and E. Quertinmont Cold liver ischemia-reperfusion injury critically depends on liver T cells and is improved by donor pretreatment with interleukin 10 in mice Hepatology 31 2000 1266 1274 (Pubitemid 30351288)
18. C.M. Lappas, Y.J. Day, M.A. Marshall, V.H. Engelhard, and J. Linden Adenosine A2A receptor activation reduces hepatic ischemia reperfusion injury by inhibiting CD1d-dependent NKT cell activation J Exp Med 203 2006 2639 2648 (Pubitemid 44833340)
19. H. Liu, I. Shalev, J. Manuel, W. He, E. Leung, and J. Crookshank The FGL2-FcgammaRIIB pathway: a novel mechanism leading to immunosuppression Eur J Immunol 38 2008 3114 3126
20. Y. Xu, A.J. Szalai, T. Zhou, K.R. Zinn, T.R. Chaudhuri, and X. Li Fc gamma Rs modulate cytotoxicity of anti-Fas antibodies: implications for agonistic antibody-based therapeutics J Immunol 171 2003 562 568 (Pubitemid 36871362)
21. S.A. Mousavi, M. Sporstol, C. Fladeby, R. Kjeken, N. Barois, and T. Berg Receptor-mediated endocytosis of immune complexes in rat liver sinusoidal endothelial cells is mediated by FcgammaRIIb2 Hepatology 46 2007 871 884 (Pubitemid 47436133)
22. P.A. Marsden, Q. Ning, L.S. Fung, X. Luo, Y. Chen, and M. Mendicino The Fgl2/fibroleukin prothrombinase contributes to immunologically mediated thrombosis in experimental and human viral hepatitis J Clin Invest 112 2003 58 66 (Pubitemid 38056376)
23. M. Mendicino, M. Liu, A. Ghanekar, W. He, C. Koscik, and I. Shalev Targeted deletion of Fgl-2/fibroleukin in the donor modulates immunologic response and acute vascular rejection in cardiac xenografts Circulation 112 2005 248 256 (Pubitemid 40982308)
24. S.S. Yadav, W. Gao, R.C. Harland, and P.A. Clavien A new and simple technique of total hepatic ischemia in the mouse Transplantation 65 1998 1433 1436 (Pubitemid 28285240)
25. N. Selzner, M. Selzner, W. Jochum, B. Amann-Vesti, R. Graf, and P.A. Clavien Mouse livers with macrosteatosis are more susceptible to normothermic ischemic injury than those with microsteatosis Journal of hepatology 44 2006 694 701
26. M. Selzner, H. Rudiger, N. Malekkiani, D. Thomas, D. Sindram, and P. Clavien Transgenic mice overexpressing Bcl-2 are resistent to hepatic ischemia and reperfusion J Hepatol 36 2002 218 225 (Pubitemid 34146428)
27. J.H. Wijsman, R.R. Jonker, R. Keijzer, C.J. van de Velde, C.J. Cornelisse, and J.H. van Dierendonck A new method to detect apoptosis in paraffin sections: in situ end-labeling of fragmented DNA J Histochem Cytochem 41 1993 7 12 (Pubitemid 23014194)
28. I. Shalev, K.M. Wong, K. Foerster, Y. Zhu, C. Chan, and A. Maknojia The novel CD4+CD25+ regulatory T cell effector molecule fibrinogen-like protein 2 contributes to the outcome of murine fulminant viral hepatitis Hepatology 49 2009 387 397
29. V. Kohli, J.F. Madden, R.C. Bentley, and P.A. Clavien Calpain mediates ischemic injury of the liver through modulation of apoptosis and necrosis Gastroenterology 116 1999 168 178 (Pubitemid 29013506)
30. C.A. McQueen, and G.M. Williams The hepatocyte primary culture/DNA repair test using hepatocytes from several species Cell Biol Toxicol 3 1987 209 218 (Pubitemid 17126184)
31. M. Liu, J.L. Leibowitz, D.A. Clark, M. Mendicino, Q. Ning, and J.W. Ding Gene transcription of fgl2 in endothelial cells is controlled by Ets-1 and Oct-1 and requires the presence of both Sp1 and Sp3 Eur J Biochem 270 2003 2274 2286 (Pubitemid 36605577)
32. W. Gao, R.C. Bentley, J.F. Madden, and P.A. Clavien Apoptosis of sinusoidal endothelial cells is a critical mechanism of prevention injury in rat liver transplantation Hepatology 27 1998 1652 1660 (Pubitemid 28264691)
33. D. Sindram, R.J. Porte, M.R. Hoffman, R.C. Bentley, and P.A. Clavien Platelets induce sinusoidal endothelial cell apoptosis upon reperfusion of the cold ischemic rat liver Gastroenterology 118 2000 183 191 (Pubitemid 30020386)
34. D. Sindram, R. Prote, M. Hoffmann, R. Bentley, and P. Clavien Synergism between platelets and leukocytes in inducing endothelial cell apoptosis in the cold ischemic rat liver: a Kupffer-mediated injury FASEB J 15 2001 1230 1232
35. D. Samarasinghe, M. Tapner, and G. Farrell Role of oxidative stress in hypoxia-reoxygenation injury to cultured rat hepatic sinusoidal endothelial cells Hepatology 31 2000 160 165 (Pubitemid 30033702)
36. D.A. Samarasinghe, and G.C. Farrell The central role of sinusoidal endothelial cells in hepatic hypoxia-reoxygenation injury in the rat Hepatology 24 1996 1230 1237 (Pubitemid 26365931)
37. K. Zeilinger, B. Tonnelier, A. Tschesche, W. Nehls, G. Spatkowski, and R. Schindler Effect of energy substrates on the preservation outcome of hepatocytes and sinusoidal endothelial cells in an experimental hypoxia/reoxygenation model Transpl Proc 29 1997 403 405 (Pubitemid 27123461)
38. R.N. Pearse, T. Kawabe, S. Bolland, R. Guinamard, T. Kurosaki, and J.V. Ravetch SHIP recruitment attenuates Fc gamma RIIB-induced B cell apoptosis Immunity 10 1999 753 760 (Pubitemid 29302928)
39. H. Rudiger, and P. Clavien Tumor necrosis factor-alpha, but not Fas, mediates hepatocellular apoptosis in the murine ischemic liver Gastroenterology 122 2002 202 210 (Pubitemid 34049208)
40. D. Sindram, H.A. Rudiger, A.G. Upadhya, S.M. Strasberg, and P.A. Clavien Ischemic preconditioning protects against cold ischemic injury through an oxidative stress dependent mechanism J Hepatol 36 2002 78 84 (Pubitemid 34234020)
41. H. Jaeschke Kupffer cell-induced oxidant stress during hepatic ischemia-reperfusion: does the controversy continue? Hepatology 30 1999 1527 1528
42. H. Jaeschke, and A. Farhood Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver in vivo Am J Physiol 260 1991 G355 G362
43. S.K. Ramaiah, and H. Jaeschke Role of neutrophils in the pathogenesis of acute inflammatory liver injury Toxicol Pathol 35 2007 757 766 (Pubitemid 47613608)