Pig thrombomodulin binds human thrombin but is a poor cofactor for activation of human protein C and TAFI

American Journal of Transplantation

Volumn 8, Issue 6, 2008, Pages 1101-1112

  Roussel, J C ^a   Moran, C J ^a   Salvaris, E J ^a   Nandurkar, H H ^a,b   D'Apice, A J F ^a,b   Cowan, P J ^a,b  

^a Immunology Research Centre   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Coagulation; Thrombosis; Xenotransplantation

Indexed keywords

PROTEIN C; PROTHROMBIN; THROMBIN ACTIVATABLE FIBRINOLYSIS INHIBITOR; THROMBOMODULIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SWINE;

ANIMALS; CARBOXYPEPTIDASE U; COENZYMES; ENZYME ACTIVATION; GRAFT REJECTION; HUMANS; MICROCIRCULATION; PROTEIN BINDING; PROTEIN C; SWINE; THROMBIN; THROMBOMODULIN; THROMBOSIS; TRANSPLANTATION, HETEROLOGOUS;

EID: 44449173082     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2008.02210.x     Document Type: Article

References (42)

1. Kuwaki K, Tseng YL, Dor FJ et al. Heart transplantation in baboons using alpha1,3-galactosyltransferase gene-knockout pigs as donors: Initial experience. Nat Med 2005 11 : 29 31.
2. Robson SC, Cooper DKC, d'Apice AJF. Disordered regulation of coagulation and platelet activation in xenotransplantation. Xenotransplantation 2000 7 : 166 176.
3. Fuentes-Prior P, Iwanaga Y, Huber R et al. Structural basis for the anticoagulant activity of the thrombin-thrombomodulin complex. Nature 2000 404 : 518 525.
4. Macias WL, Yan SB, Williams MD et al. New insights into the protein C pathway: Potential implications for the biological activities of drotrecogin alfa (activated). Crit Care 2005 9 (4 Suppl S38 S45.
5. Fukudome K, Ye X, Tsuneyoshi N et al. Activation mechanism of anticoagulant protein C in large blood vessels involving the endothelial cell protein C receptor. J Exp Med 1998 187 : 1029 1035.
6. Stearns-Kurosawa DJ, Kurosawa S, Mollica JS, Ferrell GL, Esmon CT. The endothelial cell protein C receptor augments protein C activation by the thrombin-thrombomodulin complex. Proc Natl Acad Sci USA 1996 93 : 10212 10216.
7. 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.
8. 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.
9. Esmon CT. Protein C anticoagulant pathway and its role in controlling microvascular thrombosis and inflammation. Crit Care Med 2001 29 (Suppl 7 S48 S51.
10. Esmon CT. Thrombomodulin as a model of molecular mechanisms that modulate protease specificity and function at the vessel surface. FASEB J 1995 9 : 946 955.
11. Bode W. The structure of thrombin, a chameleon-like proteinase. J Thromb Haemost 2005 3 : 2379 2388.
12. Overduin M, de BT. The plot thickens: How thrombin modulates blood clotting. Nat Struct Biol 2000 7 : 267 269.
13. Yang L, Manithody C, Rezaie AR. Activation of protein C by the thrombin-thrombomodulin complex: Cooperative roles of Arg-35 of thrombin and Arg-67 of protein C. Proc Natl Acad Sci USA 2006 103 : 879 884.
14. Koeppe JR, Seitova A, Mather T, Komives EA. Thrombomodulin tightens the thrombin active site loops to promote protein C activation. Biochemistry 2005 44 : 14784 14791.
15. Xu H, Bush LA, Pineda AO, Caccia S, Di Cera E. Thrombomodulin changes the molecular surface of interaction and the rate of complex formation between thrombin and protein C. J Biol Chem 2005 280 : 7956 7961.
16. Mosnier LO, Bouma BN. Regulation of fibrinolysis by thrombin activatable fibrinolysis inhibitor, an unstable carboxypeptidase B that unites the pathways of coagulation and fibrinolysis. Arterioscler Thromb Vasc Biol 2006 26 : 2445 2453.
17. Kokame K, Zheng X, Sadler JE. Activation of thrombin-activable fibrinolysis inhibitor requires epidermal growth factor-like domain 3 of thrombomodulin and is inhibited competitively by protein C. J Biol Chem 1998 273 : 12135 12139.
18. Schneider M, Nagashima M, Knappe S, Zhao L, Morser J, Nesheim M. Amino acid residues in the P6-P′3 region of thrombin-activable fibrinolysis inhibitor (TAFI) do not determine the thrombomodulin dependence of TAFI activation. J Biol Chem 2002 277 : 9944 9951.
19. Campbell WD, Lazoura E, Okada N, Okada H. Inactivation of C3a and C5a octapeptides by carboxypeptidase R and carboxypeptidase N. Microbiol Immunol 2002 46 : 131 134.
20. Shinohara T, Sakurada C, Suzuki T et al. Pro-carboxypeptidase R cleaves bradykinin following activation. Int Arch Allergy Immunol 1994 103 : 400 404.
21. Conway EM, Van de WM, Pollefeyt S et al. The lectin-like domain of thrombomodulin confers protection from neutrophil-mediated tissue damage by suppressing adhesion molecule expression via nuclear factor kappaB and mitogen-activated protein kinase pathways. J Exp Med 2002 196 : 565 577.
22. 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.
23. Siegel JB, Grey ST, Lesnikoski B-A et al. Xenogeneic endothelial cells activate human prothrombin. Transplantation 1997 64 : 888 896.
24. Kopp CW, Grey ST, Siegel JB et al. Expression of human thrombomodulin cofactor activity in porcine endothelial cells. Transplantation 1998 66 : 244 251.
25. Kawakatsu T, Ogita H, Fukuhara T et al. Vav2 as a Rac-GDP/GTP exchange factor responsible for the nectin-induced, c-Src- and Cdc42-mediated activation of Rac. J Biol Chem 2005 280 : 4940 4947.
26. Bendtsen JD, Nielsen H, von HG, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004 340 : 783 795.
27. Nagashima M, Lundh E, Leonard JC, Morser J, Parkinson JF. Alanine-scanning mutagenesis of the epidermal growth factor-like domains of human thrombomodulin identifies critical residues for its cofactor activity. J Biol Chem 1993 268 : 2888 2892.
28. Wood MJ, Sampoli Benitez BA, Komives EA. Solution structure of the smallest cofactor-active fragment of thrombomodulin. Nat Struct Biol 2000 7 : 200 204.
29. Wang W, Nagashima M, Schneider M, Morser J, Nesheim M. Elements of the primary structure of thrombomodulin required for efficient thrombin-activable fibrinolysis inhibitor activation. J Biol Chem 2000 275 : 22942 22947.
30. Gerlitz B, Hassell T, Vlahos CJ, Parkinson JF, Bang NU, Grinnell BW. Identification of the predominant glycosaminoglycan-attachment site in soluble recombinant human thrombomodulin: Potential regulation of functionality by glycosyltransferase competition for serine474. Biochem J 1993 295 (Pt 1 131 140.
31. Chen Y, Tan W, Lu X et al. Full-length cDNA cloning and protein three-dimensional structure modeling of porcine prothrombin. Blood Cells Mol Dis 2007 38 : 93 99.
32. Hall SW, Nagashima M, Zhao L, Morser J, Leung LL. Thrombin interacts with thrombomodulin, protein C, and thrombin-activatable fibrinolysis inhibitor via specific and distinct domains. J Biol Chem 1999 274 : 25510 25516.
33. Lawson JH, Daniels LJ, Platt JL. The evaluation of thrombomodulin activity in porcine to human xenotransplantation. Transplant Proc 1997 29 : 884 885.
34. Schulte am Esch EJ, Rogiers X, Robson SC. Molecular incompatibilities in hemostasis between swine and men-impact on xenografting. Ann Transplant 2001 6 : 12 16.
35. Kunz G, Ireland HA, Stubbs PJ, Kahan M, Coulton GC, Lane DA. Identification and characterization of a thrombomodulin gene mutation coding for an elongated protein with reduced expression in a kindred with myocardial infarction. Blood 2000 95 : 569 576.
36. Hasegawa N, Kandra TG, Husari AW et al. The effects of recombinant human thrombomodulin on endotoxin-induced multiple-system organ failure in rats. Am J Respir Crit Care Med 1996 153 (6 Pt 1 1831 1837.
37. Kaneko H, Joubara N, Yoshino M et al. Protective effect of human urinary thrombomodulin on ischemia- reperfusion injury in the canine liver. Eur Surg Res 2000 32 : 87 93.
38. Mohri M, Gonda Y, Oka M et al. The antithrombotic effects of recombinant human soluble thrombomodulin (rhsTM) on tissue factor-induced disseminated intravascular coagulation in crab-eating monkeys (Macaca fascicularis). Blood Coagul Fibrinolysis 1997 8 : 274 283.
39. Takahashi Y, Hosaka Y, Imada K, Adachi T, Niina H, Mochizuki H. Species specificity of the anticoagulant activity of human urinary soluble thrombomodulin. Thromb Res 1998 89 : 187 197.
40. Rose AG, Cooper DKC. Venular thrombosis is the key event in the pathogenesis of antibody-mediated cardiac rejection. Xenotransplantation 2000 7 : 31 41.
41. 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.
42. Shiraishi M, Oshiro T, Taira K et al. Improved hepatic microcirculation by human soluble urinary thrombomodulin in the xeno-perfused porcine liver. Transplantation 2001 71 : 1046 1050.