Antiinflammatory and anticoagulant effects of transgenic expression of human thrombomodulin in mice

American Journal of Transplantation

Volumn 10, Issue 2, 2010, Pages 242-250

  Crikis, S ^a   Zhang, X M ^a   Dezfouli, S ^a   Dwyer, K M ^a   Murray Segal, L M ^a   Salvaris, E ^a   Selan, C ^a   Robson, S C ^b   Nandurkar, H H ^a   Cowan, P J ^a   D'Apice, A J F ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Acute; Clotting factors; Coagulation; Coagulation factors; Rejection; Thrombosis; Transgenic; Vascular; Xenotransplantation

Indexed keywords

COLLAGEN; CYCLOSPORIN; HIGH MOBILITY GROUP B1 PROTEIN; THROMBOMODULIN; ANTIINFLAMMATORY AGENT;

ACUTE VASCULAR REJECTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTICOAGULATION; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLEEDING; BLEEDING TIME; CARDIAC GRAFT REJECTION; CONTROLLED STUDY; EXPERIMENTAL MODEL; HEART GRAFT; INFLAMMATION; LUNG CONGESTION; LUNG EMBOLISM; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SURVIVAL RATE; TRANSGENIC MOUSE; VEIN THROMBOSIS; VEIN WALL; XENOGRAFT; ANIMAL; DISEASE MODEL; DRUG EFFECT; HUMAN; SWINE; TRANSGENE;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CYCLOSPORINE; DISEASE MODELS, ANIMAL; HUMANS; MICE; MICE, TRANSGENIC; RATS; SWINE; THROMBOMODULIN; TRANSGENES;

EID: 75149169244     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2009.02939.x     Document Type: Article

References (48)

1. Cowan PJ, Aminian A, Barlow H et al. Protective effects of recombinant human antithrombin III in pig-to-primate renal xenotransplantation. Am J Transplant 2002 2 : 520 525.
2. Cozzi E, Simioni P, Boldrin M et al. Effects of long-term administration of high-dose recombinant human antithrombin in immunosuppressed primate recipients of porcine xenografts. Transplantation 2005 80 : 1501 1510.
3. Byrne GW, Davies WR, Oi K et al. Increased immunosuppression, not anticoagulation, extends cardiac xenograft survival. Transplantation 2006 82 : 1787 1791.
4. Shimizu A, Meehan SM, Kozlowski T et al. Acute humoral xenograft rejection: Destruction of the microvascular capillary endothelium in pig-to-nonhuman primate renal grafts. Lab Invest 2000 80 : 815 830.
5. Shimizu A, Yamada K, Yamamoto S et al. Thrombotic microangiopathic glomerulopathy in human decay accelerating factor-transgenic swine-to-baboon kidney xenografts. J Am Soc Nephrol 2005 16 : 2732 2745.
6. Shimizu A, Yamada K. Pathology of renal xenograft rejection in pig to non-human primate transplantation. Clin Transplant 2006 20 (Suppl 15 46 52.
7. Shimizu A, Colvin RB. Pathological features of antibody-mediated rejection. Curr Drug Targets Cardiovasc Haematol Disord 2005 5 : 199 214.
8. Hisashi Y, Yamada K, Kuwaki K et al. Rejection of cardiac xenografts transplanted from alpha1,3-galactosyltransferase gene-knockout (GalT-KO) pigs to baboons. Am J Transplant 2008 8 : 2516 2526.
9. Robson S, Cooper D, d'Apice A. Disordered regulation of coagulation and platelet activation in xenotransplantation. Xenotransplantation 2001 7 : 166 176.
10. Yamada K, Yazawa K, Shimizu A et al. Marked prolongation of porcine renal xenograft survival in baboons through the use of a1,3-galactosyltransferase gene-knockout donors and the cotransplantation of vascularized thymic tissue. Nature Med 2005 11 : 32 34.
11. Schulte am EJ, Cruz MA, Siegel JB, Anrather J, Robson SC. Activation of human platelets by the membrane-expressed A1 domain of von Willebrand factor. Blood 1997 90 : 4425 4437.
12. Siegel JB, Grey ST, Lesnikoski B et al. Xenogeneic endothelial cells activate human prothrombin. Transplantation 1997 64 : 888 896.
13. Roussel JC, Moran CJ, Salvaris EJ, Nandurkar HH, d'Apice AJF, Cowan PJ. Pig thrombomodulin binds human thrombin but is a poor cofactor for activation of human protein C and TAFI. Am J Transplant 2008 8 : 1101 1112.
14. Broekmans AW, Veltkamp JJ, Bertina RM. Congenital protein C deficiency and venous thromboembolism. A study of three Dutch families. New Engl J Med 1983 309 : 340 344.
15. Laszik Z, Mitro A, Taylor FB Jr., Ferrell G, Esmon CT. Human protein C receptor is present primarily on endothelium of large blood vessels: Implications for the control of the protein C pathway. Circulation 1997 96 : 3633 3640.
16. Taylor FB Jr., Peer GT, Lockhart MS, Ferrell G, Esmon CT. Endothelial cell protein C receptor plays an important role in protein C activation in vivo. Blood 2001 97 : 1685 1688.
17. Cowan PJ. Coagulation and the xenograft endothelium. Xenotransplantation 2007 14 : 7 12.
18. Cowan PJ, d'Apice AJF. The coagulation barrier in xenotransplantation: incompatibilities and strategies to overcome them. Curr Opin Organ Transplant 2008 13 : 178 183.
19. Dwyer K. Intravascular Coagulation in Discordant Xenotransplantation. University Of Melbourne, Australia, 2003.
20. Dejana E, Callioni A, Quintana A, de Gaetano G. Bleeding time in laboratory animals. II-A comparison of different assay conditions in rats. Thromb Res 1979 15 : 191 197.
21. Dwyer KM, Robson SC, Nandurkar HH et al. Thromboregulatory manifestations in human CD39 transgenic mice and the implications for thrombotic disease and transplantation. J Clin Invest 2004 113 : 1440 1446.
22. Myers DD, Hawley AE, Farris DM et al. P-selectin and leukocyte microparticles are associated with venous thrombogenesis. J Vasc Surg 2003 38 : 1075 1089.
23. Galbusera M, Zoja C, Donadelli R et al. Fluid shear stress modulates von Willebrand factor release from human vascular endothelium. Blood 1997 90 : 1558 1564.
24. Lendrum AC, Fraser DS, Slidders DS, Henderson R. Studies on the character and staining of fibrin. J Clin Pathol 1962 15 : 401 413.
25. Chen D, Weber M, McVey JH et al. Complete inhibition of acute humoral rejection using regulated expression of membrane-tethered anticoagulants on xenograft endothelium. Am J Transplant 2004 4 : 1958 1963.
26. Bersztel A, Tufveson G, Gannedahl G, Johnsson C. A morphological sequential study of mouse-to-rat cardiac xenografts. Scand J Immunol 1998 48 : 485 490.
27. Cowan PJ, Shinkel TA, Aminian A et al. High-level co-expression of complement regulators on vascular endothelium in transgenic mice: CD55 and CD59 provide greater protection from human complement-mediated injury than CD59 alone. Xenotransplantation 1998 5 : 184 190.
28. Van de WM, Collen D, Conway EM. Thrombomodulin-protein C-EPCR system: Integrated to regulate coagulation and inflammation. Arterioscler Thromb Vasc Biol 2004 24 : 1374 1383.
29. Wang H, Yang H, Czura CJ, Sama AE, Tracey KJ. HMGB1 as a late mediator of lethal systemic inflammation. Am J Respir Crit Care Med 2001 164 (10 Pt 1 1768 1773.
30. Soares MP, Lin Y, Anrather J et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat Med 1998 4 : 1073 1077.
31. Lorant T, Engstrand M, Tufveson G, Johnsson C. Isolation of mouse-to-rat cardiac xenograft-infiltrating cells by ex vivo propagation. Xenotransplantation 2002 9 : 209 219.
32. Gannedahl G, Fellstrom B, Larsson E, Roos-Engstrand E, Tufveson G. Characteristics of mouse to rat xenograft heart transplantation. Eur Surg Res 1990 22 : 206 212. (Pubitemid 20350559)
33. Murase N, Starzl TE, Demetris AJ et al. Hamster-to-rat heart and liver xenotransplantation with FK506 plus antiproliferative drugs. Transplantation 1993 55 : 701 707.
34. Dwyer KM, Deaglio S, Crikis S et al. Salutary roles of CD39 in transplantation. Transplantation Reviews 2007 21 : 54 63.
35. Lwaleed BA, Bass PS. Tissue factor pathway inhibitor: Structure, biology and involvement in disease. J Pathol 2006 208 : 327 339.
36. Cowan P, Aminian A, Barlow H et al. Renal xenografts from triple-transgenic pigs are not hyperacutely rejected but cause coagulopathy in non-immunosuppressed baboons. Transplantation 2000 69 : 2504 2515.
37. Byrne G, McCurry KR, Martin MJ, McClellan SM, Platt JL, Logan JS. Transgenic pigs expressing human CD59 and decay-accelerating factor produce an intrinsic barrier to complement-mediated damage. Transplantation 1997 63 : 149 155.
38. McGregor CGA, Teotia SS, Byrne GW et al. Cardiac transplantation: Progress toward the clinic. Transplantation 2005 78 : 1569 1575.
39. Cowan PJ, d'Apice AJ. Complement activation and coagulation in xenotransplantation. Immunol Cell Biol 2009 advance online publication, 20 January 2009 doi :.
40. Nawa K, Itani T, Ono M, Sakano K, Marumoto Y, Iwamoto M. The glycosaminoglycan of recombinant human soluble thrombomodulin affects antithrombotic activity in a rat model of tissue factor-induced disseminated intravascular coagulation. Thromb Haemost 1992 67 : 366 370.
41. Aoki Y, Takei R, Mohri M et al. Antithrombotic effects of recombinant human soluble thrombomodulin (rhs-TM) on arteriovenous shunt thrombosis in rats. Am J Hematol 1994 47 : 162 166.
42. Mohri M, Suzuki M, Sugimoto E, Sata M, Yamamoto S, Maruyama I. Effects of recombinant human soluble thrombomodulin (rhs-TM) on clot-induced coagulation in human plasma. Thromb Haemost 1998 80 : 925 929.
43. Kumada T, Dittman WA, Majerus PW. A role for thrombomodulin in the pathogenesis of thrombin-induced thromboembolism in mice. Blood 1988 71 : 728 733.
44. Gomi K, Zushi M, Honda G et al. Antithrombotic effect of recombinant human thrombomodulin on thrombin-induced thromboembolism in mice. Blood 1990 75 : 1396 1399.
45. Mohri M. ART-123: Recombinant human soluble thrombomodulin. Cardiovasc Drug Rev 2000 18 : 312 325.
46. Nagato M, Okamoto K, Abe Y, Higure A, Yamaguchi K. Recombinant human soluble thrombomodulin decreases the plasma high-mobility group box-1 protein levels, whereas improving the acute liver injury and survival rates in experimental endotoxemia. Crit Care Med 2009 37 : 2181 2186.
47. Abeyama K, Stern DM, Ito Y et al. The N-terminal domain of thrombomodulin sequesters high-mobility group-B1 protein, a novel antiinflammatory mechanism. J Clin Invest 2005 115 : 1267 1274.
48. Dorling A, Chen D, Riesbeck K et al. Regulated endothelial cell expression of novel anticoagulants: A strategy for the prevention and therapy of intravascular thrombosis. Transplant Proc 2000 32 : 971.