Enhanced induction of heme oxygenase-1 suppresses thrombus formation and affects the protein C system in sepsis

Translational Research

Volumn 159, Issue 2, 2012, Pages 99-109

  Fei, Dongsheng ^a,b,c   Meng, Xianglin ^a,b,c   Zhao, Mingran ^a,b,c   Kang, Kai ^a,b,c   Tan, Gang ^a,b,c   Pan, Shangha ^a,b,c   Luo, Yunpeng ^a,b,c   Liu, Wen ^a,b,c   Nan, Chuanchuan ^a,b,c   Jiang, Hongchi ^a,b,c   Krissansen, Geoffrey W ^a,b,c   Zhao, Mingyan ^a,b,c   Sun, Xueying ^a,b,c  

^a THE FIRST AFFILIATED HOSPITAL OF HARBIN MEDICAL UNIVERSITY   (China)

^b The Maternal and Child Health Hospital of Harbin City   (China)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATED PROTEIN C; CARBON MONOXIDE; HEME OXYGENASE 1; HEMIN; INTERLEUKIN 6; PROTEIN C; PROTOPORPHYRIN ZINC; THROMBOMODULIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LOCALIZATION; KIDNEY; LIVER; LUNG; MALE; MOUSE; NONHUMAN; PARTIAL THROMBOPLASTIN TIME; PRIORITY JOURNAL; PROTHROMBIN TIME; SEPSIS; THROMBOGENESIS; THROMBOSIS; TISSUE DISTRIBUTION;

EID: 84862959949     PISSN: 19315244     EISSN: 18781810     Source Type: Journal    
DOI: 10.1016/j.trsl.2011.10.009     Document Type: Article

References (45)

1. J.L. Vincent, Y. Sakr, and C.L. Sprung Sepsis in European intensive care units: results of the SOAP study Crit Care Med 34 2006 344 353 (Pubitemid 43145611)
2. C. Ince The microcirculation is the motor of sepsis Crit Care 9 2005 S13 S19 (Pubitemid 41498527)
3. T. Van der Poll, M. Levi, and C.E. Hack Elimination of interleukin 6 attenuates coagulation activation in experimental endotoxemia in chimpanzees J Exp Med 179 1994 1253 1259 (Pubitemid 24091784)
4. S.J. Van Deventer, H.R. Buller, and J.W. ten Cate Experimental endotoxemia in humans: analysis of cytokine release and coagulation, fibrinolytic, and complement pathways Blood 76 1990 2520 2526
5. H. Weiler Regulation of inflammation by the protein C system Crit Care Med 38 2010 S18 S25
6. S.N. Faust, M. Levin, and O.B. Harrison Dysfunction of endothelial protein C activation in severe meningococcal sepsis N Engl J Med 345 2001 408 416 (Pubitemid 32747604)
7. W.A. Dittman, and P.W. Majerus Structure and function of thrombomodulin: a natural anticoagulant Blood 75 1990 329 336 (Pubitemid 20035260)
8. C.J. Fisher Jr., and S.B. Yan Protein C levels as a prognostic indicator of outcome in sepsis and related diseases Crit Care Med 28 2000 S49 S56
9. D.E. Joyce, L. Gelbert, and A. Ciaccia Gene expression profile of antithrombotic protein c defines new mechanisms modulating inflammation and apoptosis J Biol Chem 276 2001 11199 11203 (Pubitemid 38089304)
10. T. Huynh, N. Nguyen, and S. Keller Reducing leukocyte trafficking preserves hepatic function after sepsis J Trauma 69 2010 360 367
11. N. Sennoun, F. Meziani, and O. Dessebe Activated protein C improves lipopolysaccharide-induced cardiovascular dysfunction by decreasing tissular inflammation and oxidative stress Crit Care Med 37 2009 246 255
12. S.A. Keller, C.C. Moore, S.L. Evans, I.H. McKillop, and T. Huynh Activated protein C alters inflammation and protects renal function in sepsis J Surg Res 168 2011 e103 e109
13. M.D. Maines, G.M. Trakshel, and R.K. Kutty Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible J Biol Chem 261 1986 411 419 (Pubitemid 16103962)
14. P. Yao, L. Hao, and N. Nussler The protective role of HO-1 and its generated products (CO, bilirubin and Fe) in ethanol-induced human hepatocyte damage Am J Physiol Gastrointest Liver Physiol 296 2009 G1318 G1323
15. L.E. Otterbein, F.H. Bach, and J. Alam Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway Nat Med 6 2000 422 428 (Pubitemid 30208159)
16. A. Yachie, Y. Niida, and T. Wada Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency J Clin Invest 103 1999 129 135 (Pubitemid 29031171)
17. T.Y. Tsui, Y.T. Siu, and H.J. Schlitt Heme oxygenase-1-derived carbon monoxide stimulates adenosine triphosphate generation in human hepatocyte Biochem Biophys Res Commun 336 2005 898 902 (Pubitemid 41338353)
18. B. Ke, R. Buelow, and X.D. Shen Heme oxygenase 1 gene transfer prevents CD95/Fas ligand-mediated apoptosis and improves liver allograft survival via carbon monoxide signaling pathway Hum Gene Ther 13 2002 1189 1199 (Pubitemid 34746699)
19. Y.T. Lin, Y.H. Chen, and Y.H. Yang Heme oxygenase-1 suppresses the infiltration of neutrophils in rat liver during sepsis through inactivation of p38 MAPK Shock 34 2010 615 621
20. J.B. Yu, F. Zhou, and S.L. Yao Effect of heme oxygenase-1 on the kidney during septic shock in rats Transl Res 153 2009 283 287
21. S. Takaki, N. Takeyama, and Y. Kajita Beneficial effects of the heme oxygenase-1/carbon monoxide system in patients with severe sepsis/septic shock Intensive Care Med 36 2010 42 48
22. S.W. Chung, X. Liu, A.A. Macias, R.M. Baron, and M.A. Perrella Heme oxygenase-1-derived carbon monoxide enhances the host defense response to microbial sepsis in mice J Clin Invest 118 2008 239 247
23. N. Lindenblatt, R. Bordel, W. Schareck, M.D. Menger, and B. Vollmar Vascular heme oxygenase-1 induction suppresses microvascular thrombus formation in vivo Arterioscler Thromb Vasc Biol 24 2004 601 606 (Pubitemid 38326159)
24. D.G. Johns, D. Zelent, and Z. Ao Heme-oxygenase induction inhibits arteriolar thrombosis in vivo: effect of the non-substrate inducer cobalt protoporphyrin Eur J Pharmacol 606 2009 109 114
25. N. Desbuards, G.Y. Rochefort, and D. Schlecht Heme oxygenase-1 inducer hemin prevents vascular thrombosis Thromb Haemost 98 2007 614 620 (Pubitemid 47412887)
26. M.J. Tracz, J.P. Juncos, and J.P. Grande Induction of heme oxygenase-1 is a beneficial response in a murine model of venous thrombosis Am J Pathol 173 2008 1882 1890
27. A.L. True, M. Olive, and M. Boehm Heme oxygenase-1 deficiency accelerates formation of arterial thrombosis through oxidative damage to the endothelium, which is rescued by inhaled carbon monoxide Circ Res 101 2007 893 901 (Pubitemid 350287176)
28. N. Lindenblatt, R. Bordel, and W. Schareck Vascular heme oxygenase-1 induction suppresses microvascular thrombus formation in vivo Arterioscler Thromb Vasc Biol 24 2004 601 606 (Pubitemid 38326159)
29. M. Amon, M.D. Menger, and B. Vollmar Heme oxygenase and nitric oxide synthase mediate cooling-associated protection against TNF-α-induced microcirculatory dysfunction and apoptotic cell death FASEB J 17 2003 175 185 (Pubitemid 36164387)
30. B. Sun, Z. Sun, Q. Jin, and X. Chen CO-releasing molecules (CORM-2)-liberated CO attenuates leukocytes infiltration in the renal tissue of thermally injured mice Int J Biol Sci 4 2008 176 183 (Pubitemid 351876995)
31. H.L. Yang, X.C. Jiang, and X.Y. Zhang Thrombocytopenia in the experimental leptospirosis of guinea pig is not related to disseminated intravascular coagulation BMC Infect Dis 6 2006 19
32. K. Kang, M. Zhao, and H. Jiang The role of hydrogen sulfide in hepatic ischemia reperfusion-induced injury in rats Liver Transpl 15 2009 1306 1314
33. K. Hirai, T. Sasahira, H. Ohmori, K. Fujii, and H. Kuniyasu Inhibition of heme oxygenase-1 by zinc protoporphyrin IX reduces tumor growth of LL/2 lung cancer in C57BL mice Int J Cancer 120 2007 500 505 (Pubitemid 44969019)
34. E.H. Carchman, J. Rao, P.A. Loughran, M.R. Rosengart, and B.S. Zuckerbraun Heme oxygenase-1-mediated autophagy protects against hepatocyte cell death and hepatic injury from infection/sepsis in mice Hepatology 53 2011 2053 2062
35. T.S. Lee, and L.Y. Chau Heme oxygenase-1 mediates the anti-inflammatory effect of IL-10 in mice Nat Med 8 2002 240 246
36. Y. Drechsler, A. Dolganiuc, and O. Norkina Heme oxygenase-1 mediates the anti-inflammatory effects of acute alcohol on IL-10 induction involving p38 mapk activation in monocytes J Immunol 177 2006 2592 2600 (Pubitemid 44201018)
37. P. Mandal, P.H. Park, M.R. McMullen, B.T. Pratt, and L.E. Nagy The anti-inflammatory effects of adiponectin are mediated via a heme oxygenase-1-dependent pathway in rat Kupffer cells Hepatology 51 2010 1420 1429
38. K. Kambas, M.M. Markiewski, and I.A. Pneumatikos C5a and TNF-alpha up-regulate the expression of tissue factor in intraalveolar neutrophils of patients with the acute respiratory distress syndrome J. Immunol 180 2008 7368 7375
39. B. Szotowski, S. Antoniak, W. Poller, H.P. Schultheiss, and U. Rauch Procoagulant soluble tissue factor is released from endothelial cells in response to inflammatory cytokines Circ Res 96 2005 1233 1239 (Pubitemid 40962100)
40. T. Van der Poll, J.D. Boer, and M. Levi The effect of inflammation on coagulation and vice versa Curr Opin Infect Dis 24 2011 273 278
41. S. Danese, S. Vetrano, and L. Zhang The protein C pathway in tissue inflammation and injury: pathogenic role and therapeutic implications Blood 115 2010 1121 1130
42. F.B. Taylor Jr., A. Chang, and C.T. Esmon Protein C prevents the coagulopathic and lethal effects of Escherichia coli infusion in the baboon J Clin Invest 79 1987 918 925 (Pubitemid 17050920)
43. J. Petäjä Inflammation and coagulation. An overview Thromb Res 127 2011 S34 S37
44. S. Takano, S. Kimura, S. Ohdama, and N. Aoki Plasma thrombomodulin in health and diseases Blood 76 1990 2024 2029
45. T. Iba, Y. Yagi, A. Kidokoro, M. Fukunaga, and T. Fukunaga Increased plasma levels of soluble thrombomodulin in patients with sepsis and organ failure Surg Today 25 1995 585 590