The innate immune response and activation of coagulation in ±1,3-galactosyltransferase gene-knockout xenograft recipients

Transplantation

Volumn 87, Issue 6, 2009, Pages 805-812

  Ezzelarab, Mohamed ^a   Garcia, Bertha ^b   Azimzadeh, Agnes ^c   Sun, Hongtao ^b   Lin, Chih Che ^a   Hara, Hidetaka ^a   Kelishadi, Sean ^c   Zhang, Tianshu ^c   Lin, Yih Jyh ^a   Tai, Hao Chi ^a   Wagner, Robert ^d   Thacker, Jnanesh ^e   Murase, Noriko ^a   McCurry, Kenneth ^a,e   Barth, Rolf N ^c   Ayares, David ^f   Pierson, Richard N ^c   Cooper, David K C ^a  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c UNIVERSITY OF MARYLAND   (United States)

^d UNIVERSITY OF PITTSBURGH   (United States)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^f REVIVICOR INC   (United States)

Author keywords

1,3 Galactosyltransferase gene knockout; Baboon; Consumptive coagulopathy; Costimulatory blockade; Heart; Kidney; Pig; Xenotransplantation

Indexed keywords

ABATACEPT; ALPHA 1,3 GALACTOSYLTRANSFERASE; CD40 LIGAND MONOCLONAL ANTIBODY; COBROTOXIN; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C4; COMPLEMENT COMPONENT C5B; COMPLEMENT COMPONENT C9; FIBRIN; HEPARIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M; IMMUNOGLOBULIN M ANTIBODY; IMMUNOSUPPRESSIVE AGENT; LEFLUNOMIDE; MESSENGER RNA; METHYLPREDNISOLONE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; THROMBOPLASTIN; THYMOCYTE ANTIBODY; GALACTOSYLTRANSFERASE;

ACUTE GRAFT REJECTION; ACUTE HUMORAL XENOGRAFT REJECTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BABOON; BLOOD CLOTTING; COMPLEMENT DEPOSITION; CONTROLLED STUDY; DISSEMINATED INTRAVASCULAR CLOTTING; DRUG DOSE REDUCTION; ENDOTHELIUM CELL; ENZYME ACTIVATION; GRAFT SURVIVAL; HEART GRAFT; HEART TRANSPLANTATION; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOGLOBULIN PRODUCTION; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; KIDNEY GRAFT; KIDNEY TRANSPLANTATION; KNOCKOUT GENE; LOW DRUG DOSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGAN TRANSPLANTATION; PRIMATE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SWINE; THROMBOCYTE AGGREGATION; THROMBOEMBOLISM; THROMBOTIC THROMBOCYTOPENIC PURPURA; TREATMENT OUTCOME; XENOTRANSPLANTATION; ANIMAL; B LYMPHOCYTE; GENETICS; HOMOZYGOTE; IMMUNOLOGY; PAPIO; PATHOLOGY; T LYMPHOCYTE; TRANSGENIC ANIMAL; XENOGRAFT;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; B-LYMPHOCYTES; GALACTOSYLTRANSFERASES; GRAFT SURVIVAL; HEART TRANSPLANTATION; HOMOZYGOTE; IMMUNITY, INNATE; IMMUNOSUPPRESSIVE AGENTS; KIDNEY TRANSPLANTATION; PAPIO; SWINE; T-LYMPHOCYTES; TRANSPLANTATION, HETEROLOGOUS;

EID: 65549162661     PISSN: 00411337     EISSN: None     Source Type: Journal    
DOI: 10.1097/TP.0b013e318199c34f     Document Type: Article

References (48)

1. Phelps CJ, Koike C, Vaught TD, et al. Production of alpha 1, 3-galactosyltransferase-deficient pigs. Science 2003; 299: 411.
2. Kolber-Simonds D, Lai L, Watt SR, et al. Production of alpha-1, 3-galactosyltransferase null pigs by means of nuclear transfer with fibroblasts bearing loss of heterozygosity mutations. Proc Natl Acad Sci USA 2004; 101: 7335.
3. 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.
4. Tseng YL, Kuwaki K, Dor FJ, et al. alpha1,3-Galactosyltransferase geneknockout pig heart transplantation in baboons with survival approaching 6 months. Transplantation 2005; 80: 1493.
5. Houser SL, Kuwaki K, Knosalla C, et al. Thrombotic microangiopathy and graft arteriopathy in pig hearts following transplantation into baboons. Xenotransplantation 2004; 11: 416.
6. Chen G, Qian H, Starzl T, et al. Acute rejection is associated with antibodies to non-Gal antigens in baboons using Gal-knockout pig kidneys. Nat Med 2005; 11: 1295.
7. Ezzelarab M, Hara H, Busch J, et al. Antibodies directed to pig non-Gal antigens in naive and sensitized baboons. Xenotransplantation 2006; 13: 400.
8. 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.
9. Rood PP, Hara H, Busch JL, et al. Incidence and cytotoxicity of antibodies in cynomolgus monkeys directed to nonGal antigens, and their relevance for experimental models. Transpl Int 2006; 19: 158.
10. 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.
11. Dai Y, Vaught TD, Boone J, et al. Targeted disruption of the alpha1,3- galactosyltransferase gene in cloned pigs. Nat Biotechnol 2002; 20: 251.
12. Cooper DKC, Ye Y, Niekrasz M. Heart transplantation in primates. In: Cramer DV, Podesta LG, Makowka L, eds. Handbook of animal models in transplantation research. Boca Raton, CRC Press 1994, pp 173.
13. 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.
14. Buhler L, Yamada K, Kitamura H, et al. Pig kidney transplantation in baboons: Anti-Gal(alpha)1-3Gal IgM alone is associated with acute humoral xenograft rejection and disseminated intravascular coagulation. Transplantation 2001; 72: 1743.
15. Knosalla C, Gollackner B, Buhler L, et al. Correlation of biochemical and hematological changes with graft failure following pig heart and kidney transplantation in baboons. Am J Transplant 2003; 3: 1510.
16. 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.
17. Buhler L, Awwad M, Basker M, et al. High-dose porcine hematopoietic cell transplantation combined with CD40 ligand blockade in baboons prevents an induced anti-pig humoral response. Transplantation 2000; 69: 2296.
18. Buhler L, Alwayn IP, Basker M, et al. CD40-CD154 pathway blockade requires host macrophages to induce humoral unresponsiveness to pig hematopoietic cells in baboons. Transplantation 2001; 72: 1759.
19. Buhler L, Basker M, Alwayn IP, et al. Coagulation and thrombotic disorders associated with pig organ and hematopoietic cell transplantation in nonhuman primates. Transplantation 2000; 70: 1323.
20. Ierino FL, Kozlowski T, Siegel JB, et al. Disseminated intravascular coagulation in association with the delayed rejection of pig-to-baboon renal xenografts. Transplantation 1998; 66: 1439.
21. Kawai T, Andrews D, Colvin RB, et al. Thromboembolic complications after treatment with monoclonal antibody against CD40 ligand. Nat Med 2000; 6: 114.
22. Knosalla C, Gollackner B, Cooper DK. Anti-CD154 monoclonal antibody and thromboembolism revisted. Transplantation 2002; 74: 416.
23. Tai HC, Campanile N, Ezzelarab M, et al. Measurement of anti-CD154 monoclonal antibody in primate sera by competitive inhibition ELISA. Xenotransplantation 2006; 13: 566.
24. Ezzelarab M, Cortese-Hassett A, Cooper DK, et al. Extended coagulation profiles of healthy baboons and of baboons rejecting GT-KO pig heart grafts. Xenotransplantation 2006; 13: 522.
25. Kuwaki K, Knosalla C, Dor FJ, et al. Suppression of natural and elicited antibodies in pig-to-baboon heart transplantation using a human anti-human CD154 mAb-based regimen. Am J Transplant 2004; 4: 363.
26. Kozlowski T, Monroy R, Xu Y, et al. Anti-Gal(alpha)1-3Gal antibody response to porcine bone marrow in unmodified baboons and baboons conditioned for tolerance induction. Transplantation 1998; 66: 176.
27. McGregor CG, Tazelaar HD, Rao VP, et al. Gene-knockout (GT-KO) heterotopic cardiac xenotransplantation: Are GT-KO pigs essential for successful clinical xenotransplantation? Xenotransplantation 2007; 14: 181.
28. McGregor CG, Teotia SS, Byrne GW, et al. Cardiac xenotransplantation: Progress toward the clinic. Transplantation 2004; 78: 1569.
29. Fox A, Harrison LC. Innate immunity and graft rejection. Immunol Rev 2000; 173: 141.
30. Cooper DK, Dorling A, Pierson RN III, et al. Alpha1,3- galactosyltransferase gene-knockout pigs for xenotransplantation: Where do we go from here? Transplantation 2007; 84: 1.
31. Tai HC, Ezzelarab M, Hara H, et al. Progress in xenotransplantation following the introduction of gene-knockout technology. Transpl Int 2007; 20: 107.
32. Shimizu A, Hisashi Y, Kuwaki K, et al. Thrombotic microangiopathy associated with humoral rejection of cardiac xenografts from alpha1,3- galactosyltransferase gene-knockout pigs in baboons. Am J Pathol 2008; 172: 1471.
33. Robson SC, Cooper DK, d'Apice AJ. Disordered regulation of coagulation and platelet activation in xenotransplantation. Xenotransplantation 2000; 7: 166.
34. Nagayasu T, Saadi S, Holzknecht RA, et al. Expression of tissue factor mRNA in cardiac xenografts: Clues to the pathogenesis of acute vascular rejection. Transplantation 2000; 69: 475.
35. Lin CC, Chen D, McVey JH, et al. Expression of tissue factor and initiation of clotting by human platelets and monocytes after incubation with porcine endothelial cells. Transplantation 2008; 86: 702.
36. al-Mohanna F, Collison K, Parhar R, et al. Activation of naive xenogeneic but not allogeneic endothelial cells by human naive neutrophils: A potential occult barrier to xenotransplantation. Am J Pathol 1997; 151: 111.
37. Al-Mohanna F, Saleh S, Parhar RS, et al. Human neutrophil gene expression profiling following xenogeneic encounter with porcine aortic endothelial cells: The occult role of neutrophils in xenograft rejection revealed. J Leukoc Biol 2005; 78: 51.
38. Mejia-Laguna JE, Martinez-Palomo A, Lopez-Soriano F, et al. Prolonged survival of kidney xenografts in leucopenic rabbits. Immunology 1971; 21: 879.
39. Richards AC, Tucker AW, Carrington CA, et al. Neutrophils and xenotransplantation. Lancet 1996; 348: 1596.
40. Wu G, Pfeiffer S, Schroder C, et al. Co-stimulation blockade targeting CD154 and CD28/B7 modulates the induced antibody response after a pig-to-baboon cardiac xenograft. Xenotransplantation 2005; 12: 197.
41. Yi S, Hawthorne WJ, Lehnert AM, et al. T cell-activated macrophages are capable of both recognition and rejection of pancreatic islet xenografts. J Immunol 2003; 170: 2750.
42. Todoroki H, Nakamura S, Higure A, et al. Neutrophils express tissue factor in a monkey model of sepsis. Surgery 2000; 127: 209.
43. Drake TA, Cheng J, Chang A, et al. Expression of tissue factor, thrombomodulin, and E-selectin in baboons with lethal Escherichia coli sepsis. Am J Pathol 1993; 142: 1458.
44. Drake TA, Morrissey JH, Edgington TS. Selective cellular expression of tissue factor in human tissues. Implications for disorders of hemostasis and thrombosis. Am J Pathol 1989; 134: 1087.
45. Wu G, Pfeiffer S, Schroder C, et al. Coagulation cascade activation triggers early failure of pig hearts expressing human complement regulatory genes. Xenotransplantation 2007; 14: 34.
46. Lupu C, Westmuckett AD, Peer G, et al. Tissue factor-dependent coagulation is preferentially up-regulated within arterial branching areas in a baboon model of Escherichia coli sepsis. Am J Pathol 2005; 167: 1161.
47. Strukova S. Blood coagulation-dependent inflammation. Coagulationdependent inflammation and inflammation-dependent thrombosis. Front Biosci 2006; 11: 59.
48. Suo Z, Citron BA, Festoff BW. Thrombin: A potential proinflammatory mediator in neurotrauma and neurodegenerative disorders. Curr Drug Targets Inflamm Allergy 2004; 3: 105.