HO-1-STAT3 axis in mouse liver ischemia/reperfusion injury: Regulation of TLR4 innate responses through PI3K/PTEN signaling

Journal of Hepatology

Volumn 56, Issue 2, 2012, Pages 359-366

  Ke, Bibo ^a   Shen, Xiu Da ^a   Ji, Haofeng ^a   Kamo, Naoko ^a   Gao, Feng ^a   Freitas, Maria Cecilia S ^a   Busuttil, Ronald W ^a   Kupiec Weglinski, Jerzy W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Heme oxygenase 1; Innate immunity; Liver ischemia reperfusion injury; STAT3; Transplantation

Indexed keywords

ADENOVIRUS VECTOR; HEME OXYGENASE 1; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; SMALL INTERFERING RNA; STAT3 PROTEIN; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; C57BL 6 MOUSE; CELL PROTECTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INDUCTION; GENE SILENCING; GENE TRANSFER; IN VITRO STUDY; INFLAMMATION; INNATE IMMUNITY; LIVER CELL DAMAGE; LIVER ISCHEMIA; MALE; MOUSE; NONHUMAN; PARTIAL WARM ISCHEMIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; SIGNAL TRANSDUCTION;

ANIMALS; BASE SEQUENCE; DISEASE MODELS, ANIMAL; HEME OXYGENASE-1; HUMANS; IMMUNITY, INNATE; LIVER; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MODELS, IMMUNOLOGICAL; NF-KAPPA B; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; REPERFUSION INJURY; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TOLL-LIKE RECEPTOR 4;

EID: 84855958437     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2011.05.023     Document Type: Article

References (42)

1. C. Fondevila, R.W. Busuttil, and J.W. Kupiec-Weglinski Hepatic ischemia/reperfusion injury - a fresh look Exp Mol Pathol 74 2003 86 93 (Pubitemid 36438656)
2. H. Jaeschke, A.P. Bautista, Z. Spolarics, and J.J. Spitzer Superoxide generation by Kupffer cells and priming of neutrophils during reperfusion after hepatic ischemia Free Radic Res Commun 15 1991 277 284
3. 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)
4. D.A. Samarasinghe, M. Tapner, and G.C. Farrell Role of oxidative stress in hypoxia-reoxygenation injury to cultured rat hepatic sinusoidal endothelial cells Hepatology 31 2000 160 165 (Pubitemid 30033702)
5. L.M. Colletti, D.G. Remick, G.D. Burtch, S.L. Kunkel, R.M. Strieter, and D.A. Campbell Jr. Role of tumor necrosis factor-alpha in the pathophysiologic alterations after hepatic ischemia/reperfusion injury in the rat J Clin Invest 85 1990 1936 1943 (Pubitemid 20192970)
6. R.M. Zwacka, Y. Zhang, J. Halldorson, H. Schlossberg, L. Dudus, and J.F. Engelhardt CD4(+) T-lymphocytes mediate ischemia/reperfusion-induced inflammatory responses in mouse liver J Clin Invest 100 1997 279 289 (Pubitemid 27349074)
7. X.D. Shen, B. Ke, Y. Zhai, F. Amersi, F. Gao, and D.M. Anselmo CD154-CD40 T-cell costimulation pathway is required in the mechanism of hepatic ischemia/reperfusion injury, and its blockade facilitates and depends on heme oxygenase-1 mediated cytoprotection Transplantation 74 2002 315 319
8. L.E. Otterbein, M.P. Soares, K. Yamashita, and F.H. Bach Heme oxygenase-1: unleashing the protective properties of heme Trends Immunol 24 2003 449 455 (Pubitemid 36928103)
9. F. Amersi, R. Buelow, H. Kato, B. Ke, A.J. Coito, and X.D. Shen Upregulation of heme oxygenase-1 protects genetically fat Zucker rat livers from ischemia/reperfusion injury J Clin Invest 104 1999 1631 1639 (Pubitemid 30002375)
10. M. Katori, R.W. Busuttil, and J.W. Kupiec-Weglinski Heme oxygenase 1 system in organ transplantation Transplantation 74 2002 905 912 (Pubitemid 35191234)
11. B. Ke, X.D. Shen, F. Gao, H. Ji, B. Qiao, and Y. Zhai Adoptive transfer of ex vivo HO-1 modified bone marrow-derived macrophages prevents liver ischemia and reperfusion injury Mol Ther 18 2010 1019 1025
12. A. Yachie, Y. Niida, T. Wada, N. Igarashi, H. Kaneda, and T. Toma Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency J Clin Invest 103 1999 129 135 (Pubitemid 29031171)
13. M.P. Soares, Y. Lin, J. Anrather, E. Csizmadia, K. Takigami, and K. Sato Expression of heme oxygenase-1 can determine cardiac xenograft survival Nat Med 4 1998 1073 1077 (Pubitemid 28417343)
14. Y. Zhai, X.D. Shen, R. O'Connell, F. Gao, C.R. Lassman, and R.W. Busuttil Cutting edge: TLR4 activation mediates liver ischemia/reperfusion inflammatory response via IFN regulatory factor 3-dependent MyD88-independent pathway J Immunol 173 2004 7115 7119 (Pubitemid 39628144)
15. X.D. Shen, B. Ke, Y. Zhai, F. Gao, R.W. Busuttil, and G. Cheng Toll-like receptor and heme oxygenase-1 signaling in hepatic ischemia/reperfusion injury Am J Transplant 5 2005 1793 1800 (Pubitemid 41039851)
16. X. Zhang, P. Shan, S. Qureshi, R. Homer, R. Medzhitov, and P.W. Noble Cutting edge: TLR4 deficiency confers susceptibility to lethal oxidant lung injury J Immunol 175 2005 4834 4838 (Pubitemid 41456364)
17. X. Zhang, P. Shan, G. Jiang, S.S. Zhang, L.E. Otterbein, and X.Y. Fu Endothelial STAT3 is essential for the protective effects of HO-1 in oxidant-induced lung injury FASEB J 20 2006 2156 2158
18. J.E. Darnell Jr. STATs and gene regulation Science 277 1997 1630 1635 (Pubitemid 27446219)
19. T. Welte, S.S. Zhang, T. Wang, Z. Zhang, D.G. Hesslein, and Z. Yin STAT3 deletion during hematopoiesis causes Crohn's disease-like pathogenesis and lethality: a critical role of STAT3 in innate immunity Proc Natl Acad Sci USA 100 2003 1879 1884 (Pubitemid 36254542)
20. J. Li, C. Yen, D. Liaw, K. Podsypanina, S. Bose, and S.I. Wang PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer Science 275 1997 1943 1947 (Pubitemid 27148818)
21. D. Liaw, D.J. Marsh, J. Li, P.L. Dahia, S.I. Wang, and Z. Zheng Germline mutations of the PTEN gene in Cowden disease, an inherited breast and thyroid cancer syndrome Nat Genet 16 1997 64 67 (Pubitemid 27198157)
22. D.J. Marsh, P.L. Dahia, Z. Zheng, D. Liaw, R. Parsons, and R.J. Gorlin Germline mutations in PTEN are present in Bannayan-Zonana syndrome Nat Genet 16 1997 333 334
23. G. Schabbauer, M. Tencati, B. Pedersen, R. Pawlinski, and N. Mackman PI3K-Akt pathway suppresses coagulation and inflammation in endotoxemic mice Arterioscler Thromb Vasc Biol 24 2004 1963 1969 (Pubitemid 39350320)
24. Z. Cai, and G.L. Semenza PTEN activity is modulated during ischemia and reperfusion: involvement in the induction and decay of preconditioning Circ Res 97 2005 1351 1359
25. N. Omori, G. Jin, F. Li, W.R. Zhang, S.J. Wang, and Y. Hamakawa Enhanced phosphorylation of PTEN in rat brain after transient middle cerebral artery occlusion Brain Res 954 2002 317 322 (Pubitemid 35284673)
26. J.H. Lee, K.Y. Kim, Y.K. Lee, S.Y. Park, C.D. Kim, and W.S. Lee Cilostazol prevents focal cerebral ischemic injury by enhancing casein kinase 2 phosphorylation and suppression of phosphatase and tensin homolog deleted from chromosome 10 phosphorylation in rats J Pharmacol Exp Ther 308 2004 896 903 (Pubitemid 38263963)
27. A.P. Curnock, M.K. Logan, and S.G. Ward Chemokine signalling: pivoting around multiple phosphoinositide 3-kinases Immunology 105 2002 125 136 (Pubitemid 34146678)
28. L. Arbibe, J.P. Mira, N. Teusch, L. Kline, M. Guha, and N. Mackman Toll-like receptor 2-mediated NF-kappa B activation requires a Rac1-dependent pathway Nat Immunol 1 2000 533 540
29. M. Ojaniemi, V. Glumoff, K. Harju, M. Liljeroos, K. Vuori, and M. Hallman Phosphatidylinositol 3-kinase is involved in Toll-like receptor 4-mediated cytokine expression in mouse macrophages Eur J Immunol 33 2003 597 605 (Pubitemid 36367663)
30. S.H. Rhee, H. Kim, M.P. Moyer, and C. Pothoulakis Role of MyD88 in phosphatidylinositol 3-kinase activation by flagellin/toll-like receptor 5 engagement in colonic epithelial cells J Biol Chem 281 2006 18560 18568 (Pubitemid 44035515)
31. B. Ke, X.D. Shen, F. Gao, B. Qiao, H. Ji, and R.W. Busuttil Small interfering RNA targeting heme oxygenase-1 (HO-1) reinforces liver apoptosis induced by ischemia-reperfusion injury in mice: HO-1 is necessary for cytoprotection Hum Gene Ther 20 2009 1133 1142
32. S. Suzuki, L.H. Toledo-Pereyra, F.J. Rodriguez, and D. Cejalvo Neutrophil infiltration as an important factor in liver ischemia and reperfusion injury. Modulating effects of FK506 and cyclosporine Transplantation 55 1993 1265 1272 (Pubitemid 23183235)
33. F. Meng, R. Henson, H. Wehbe-Janek, K. Ghoshal, S.T. Jacob, and T. Patel MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer Gastroenterology 133 2007 647 658 (Pubitemid 47187346)
34. A. Suzuki, J.L. de la Pompa, V. Stambolic, A.J. Elia, T. Sasaki, and I. del Barco High cancer susceptibility and embryonic lethality associated with mutation of the PTEN tumor suppressor gene in mice Curr Biol 8 1998 1169 1178 (Pubitemid 28494715)
35. T. Fukao, and S. Koyasu PI3K and negative regulation of TLR signaling Trends Immunol 24 2003 358 363 (Pubitemid 36830961)
36. H. Kato, F. Amersi, R. Buelow, J. Melinek, A.J. Coito, and B. Ke Heme oxygenase-1 overexpression protects rat livers from ischemia/reperfusion injury with extended cold preservation Am J Transplant 1 2001 121 128 (Pubitemid 33674151)
37. P.J. Lee, S.L. Camhi, B.Y. Chin, J. Alam, and A.M. Choi AP-1 and STAT mediate hyperoxia-induced gene transcription of heme oxygenase-1 Am J Physiol Lung Cell Mol Physiol 279 2000 L175 L182
38. Y. Uchida, M.C. Freitas, D. Zhao, R.W. Busuttil, and J.W. Kupiec-Weglinski The inhibition of neutrophil elastase ameliorates mouse liver damage due to ischemia and reperfusion Liver Transpl 15 2009 939 947
39. V. Stambolic, A. Suzuki, J.L. de la Pompa, G.M. Brothers, C. Mirtsos, and T. Sasaki Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN Cell 95 1998 29 39 (Pubitemid 28458022)
40. J.P. Luyendyk, G.A. Schabbauer, M. Tencati, T. Holscher, R. Pawlinski, and N. Mackman Genetic analysis of the role of the PI3K-Akt pathway in lipopolysaccharide-induced cytokine and tissue factor gene expression in monocytes/macrophages J Immunol 180 2008 4218 4226
41. Y. Uchida, B. Ke, M.C. Freitas, H. Yagita, H. Akiba, and R.W. Busuttil T-cell immunoglobulin mucin-3 determines severity of liver ischemia/reperfusion injury in mice in a TLR4-dependent manner Gastroenterology 139 2010 2195 2206
42. S.R. Datta, H. Dudek, X. Tao, S. Masters, H. Fu, and Y. Gotoh Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery Cell 91 1997 231 241 (Pubitemid 27456390)