Recipient tissue factor expression is associated with consumptive coagulopathy in pig-to-primate kidney xenotransplantation

American Journal of Transplantation

Volumn 10, Issue 7, 2010, Pages 1556-1568

  Lin, C C ^a,b   Ezzelarab, M ^a   Shapiro, R ^a   Ekser, B ^a   Long, C ^a   Hara, H ^a   Echeverri, G ^a   Torres, C ^a   Watanabe, H ^a   Ayares, D ^c   Dorling, A ^d   Cooper, D K C ^a  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^c REVIVICOR INC   (United States)

^d GUY S HOSPITAL   (United Kingdom)

Author keywords

Baboon; coagulation; PBMC; pig; platelets; tissue factor; xenotransplantation

Indexed keywords

ALPHA 1,3 GALACTOSYLTRANSFERASE; CD40 LIGAND MONOCLONAL ANTIBODY; COBROTOXIN; MEMBRANE COFACTOR PROTEIN; METHYLPREDNISOLONE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; THROMBIN; THROMBOPLASTIN; THYMOCYTE ANTIBODY;

ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; DISSEMINATED INTRAVASCULAR CLOTTING; FIBRIN DEPOSITION; HISTOPATHOLOGY; HUMORAL IMMUNITY; IMMUNE RESPONSE; KIDNEY FUNCTION; KIDNEY GRAFT; KIDNEY GRAFT REJECTION; KIDNEY TRANSPLANTATION; LEUKOCYTE AGGREGATION; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIMATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SWINE; THROMBOCYTE AGGREGATION; TREATMENT OUTCOME; XENOTRANSPLANTATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTILYMPHOCYTE SERUM; CD40 LIGAND; DISSEMINATED INTRAVASCULAR COAGULATION; FAMOTIDINE; GALACTOSYLTRANSFERASES; GENE KNOCKOUT TECHNIQUES; GRAFT REJECTION; HISTAMINE H2 ANTAGONISTS; IMMUNOSUPPRESSIVE AGENTS; KIDNEY TRANSPLANTATION; PAPIO; PLATELET ACTIVATION; PLATELET AGGREGATION; SWINE; THROMBIN; THROMBOPLASTIN; TRANSPLANTATION, HETEROLOGOUS;

EID: 77954079584     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2010.03147.x     Document Type: Article

References (43)

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. 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.
3. Gollackner B, Mueller NJ, Houser S et al. Porcine cytomegalovirus and coagulopathy in pig-to-primate xenotransplantation. Transplantation 2003 75 : 1841 1847.
4. Blakely ML, Van Der Werf WJ, Berndt MC, Dalmasso AP, Bach FH, Hancock WW. Activation of intragraft endothelial and mononuclear cells during discordant xenograft rejection. Transplantation 1994 58 : 1059 1066.
5. Bach FH, Robson SC, Winkler H et al. Barriers to xenotransplantation. Nat Med 1995 1 : 869 873.
6. Gollackner B, Goh SK, Qawi I et al. Acute vascular rejection of xenografts: Roles of natural and elicited xenoreactive antibodies in activation of vascular endothelial cells and induction of procoagulant activity. Transplantation 2004 77 : 1735 1741.
7. Morrissey JH. Tissue factor: An enzyme cofactor and a true receptor. Thromb Haemost 2001 86 : 66 74.
8. Mackman N. Role of tissue factor in hemostasis, thrombosis, and vascular development. Arterioscler Thromb Vasc Biol 2004 24 : 1015 1022.
9. Warr TA, Rao LV, Rapaport SI. Disseminated intravascular coagulation in rabbits induced by administration of endotoxin or tissue factor: Effect of anti-tissue factor antibodies and measurement of plasma extrinsic pathway inhibitor activity. Blood 1990 75 : 1481 1489.
10. Liu Y, Pelekanakis K, Woolkalis MJ. Thrombin and tumor necrosis factor alpha synergistically stimulate tissue factor expression in human endothelial cells: Regulation through c-Fos and c-Jun. J Biol Chem 2004 279 : 36142 36147.
11. Keller TT, Mairuhu AT, de Kruif MD et al. Infections and endothelial cells. Cardiovasc Res 2003 60 : 40 48.
12. Moosbauer C, Morgenstern E, Cuvelier SL et al. Eosinophils are a major intravascular location for tissue factor storage and exposure. Blood 2007 109 : 995 1002.
13. Redecha P, Franzke CW, Ruf W, Mackman N, Girardi G. Neutrophil activation by the tissue factor/Factor VIIa/PAR2 axis mediates fetal death in a mouse model of antiphospholipid syndrome. J Clin Invest 2008 118 : 3453 3461.
14. Giesen PL, Rauch U, Bohrmann B et al. Blood-borne tissue factor: Another view of thrombosis. Proc Natl Acad Sci U S A 1999 96 : 2311 2315.
15. Monroe DM, Key NS. The tissue factor-factor VIIa complex: Procoagulant activity, regulation, and multitasking. J Thromb Haemost 2007 5 : 1097 1105.
16. Panes O, Matus V, Saez CG, Quiroga T, Pereira J, Mezzano D. Human platelets synthesize and express functional tissue factor. Blood 2007 109 : 5242 5250.
17. Schwertz H, Tolley ND, Foulks JM et al. Signal-dependent splicing of tissue factor pre-mRNA modulates the thrombogenicity of human platelets. J Exp Med 2006 203 : 2433 2440.
18. Langer F, Holstein K, Eifrig B, Bokemeyer C. Haemostatic aspects in clinical oncology. Hamostaseologie 2008 28 : 472 480.
19. Mackman N. Tissue-specific hemostasis: Role of tissue factor. J Thromb Haemost 2008 6 : 303 305.
20. Johansson H, Lukinius A, Moberg L et al. Tissue factor produced by the endocrine cells of the islets of Langerhans is associated with a negative outcome of clinical islet transplantation. Diabetes 2005 54 : 1755 1762.
21. Bennet W, Groth CG, Larsson R, Nilsson B, Korsgren O. Isolated human islets trigger an instant blood mediated inflammatory reaction: Implications for intraportal islet transplantation as a treatment for patients with type 1 diabetes. Ups J Med Sci 2000 105 : 125 133.
22. Berman DM, Cabrera O, Kenyon NM et al. Interference with tissue factor prolongs intrahepatic islet allograft survival in a nonhuman primate marginal mass model. Transplantation 2007 84 : 308 315.
23. Lin CC, Chen D, McVey JH, Cooper DK, Dorling A. Expression of tissue factor and initiation of clotting by human platelets and monocytes after incubation with porcine endothelial cells. Transplantation 2008 86 : 702 709.
24. Phelps CJ, Koike C, Vaught TD et al. Production of alpha 1,3-galactosyltransferase-deficient pigs. Science 2003 299 : 411 414.
25. Hara H, Long C, Lin YJ et al. in vitro investigation of pig cells for resistance to human antibody-mediated rejection. Transpl Int 2008 21 : 1163 1174.
26. Ezzelarab M, Garcia B, Azimzadeh A et al. The innate immune response and activation of coagulation in alpha1,3-galactosyltransferase gene-knockout xenograft recipients. Transplantation 2009 87 : 805 812.
27. Yamada K, Yazawa K, Shimizu A et al. Marked prolongation of porcine renal xenograft survival in baboons through the use of alpha1,3-galactosyltransferase gene-knockout donors and the cotransplantation of vascularized thymic tissue. Nat Med 2005 11 : 32 34.
28. Hara H, Ezzelarab M, Rood PP et al. Allosensitized humans are at no greater risk of humoral rejection of GT-KO pig organs than other humans. Xenotransplantation 2006 13 : 357 365.
29. Bach FH, Robson SC, Ferran C et al. Endothelial cell activation and thromboregulation during xenograft rejection. Immunol Rev 1994 141 : 5 30. (Pubitemid 24333756)
30. Schouten M, Wiersinga WJ, Levi M, Van Der Poll T. Inflammation, endothelium, and coagulation in sepsis. J Leukoc Biol 2008 83 : 536 545.
31. Niessen F, Schaffner F, Furlan-Freguia C et al. Dendritic cell PAR1-S1P3 signalling couples coagulation and inflammation. Nature 2008 452 : 654 658.
32. Kopp CW, Robson SC, Siegel JB et al. Regulation of monocyte tissue factor activity by allogeneic and xenogeneic endothelial cells. Thromb Haemost 1998 79 : 529 538.
33. Li N. Platelet-lymphocyte cross-talk. J Leukoc Biol 2008 83 : 1069 1078.
34. Falati S, Liu Q, Gross P et al. Accumulation of tissue factor into developing thrombi in vivo is dependent upon microparticle P-selectin glycoprotein ligand 1 and platelet P-selectin. J Exp Med 2003 197 : 1585 1598.
35. Chou J, Mackman N, Merrill-Skoloff G, Pedersen B, Furie BC, Furie B. Hematopoietic cell-derived microparticle tissue factor contributes to fibrin formation during thrombus propagation. Blood 2004 104 : 3190 3197.
36. Kawai T, Andrews D, Colvin RB, Sachs DH, Cosimi AB. Thromboembolic complications after treatment with monoclonal antibody against CD40 ligand. Nat Med 2000 6 : 114.
37. Schulte am Esch J, II., 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.
38. Schulte Am Esch J, II., Robson SC, Knoefel WT, Hosch SB, Rogiers X. O-linked glycosylation and functional incompatibility of porcine von Willebrand factor for human platelet GPIb receptors. Xenotransplantation 2005 12 : 30 37.
39. Cantu E, Balsara KR, Li B et al. Prolonged function of macrophage, von Willebrand factor-deficient porcine pulmonary xenografts. Am J Transplant 2007 7 : 66 75.
40. Thomas GM, Panicot-Dubois L, Lacroix R, Dignat-George F, Lombardo D, Dubois C. Cancer cell-derived microparticles bearing P-selectin glycoprotein ligand 1 accelerate thrombus formation in vivo. J Exp Med 2009 206 : 1913 1927.
41. Yamamoto S, Lavelle JM, Vagefi PA et al. Vascularized thymic lobe transplantation in a pig-to-baboon model: A novel strategy for xenogeneic tolerance induction and T cell reconstitution. Transplantation 2005 80 : 1783 1790.
42. Kozlowski T, Shimizu A, Lambrigts D et al. Porcine kidney and heart transplantation in baboons undergoing a tolerance induction regimen and antibody adsorption. Transplantation 1999 67 : 18 30.
43. Cozzi E, Vial C, Ostlie D et al. Maintenance triple immunosuppression with cyclosporin A, mycophenolate sodium and steroids allows prolonged survival of primate recipients of hDAF porcine renal xenografts. Xenotransplantation 2003 10 : 300 310.