Initial in vitro studies on tissues and cells from GTKO/CD46/NeuGcKO pigs

Xenotransplantation

Volumn 23, Issue 2, 2016, Pages 137-150

  Lee, Whayoung ^a   Hara, Hidetaka ^a   Ezzelarab, Mohamed B ^a   Iwase, Hayato ^a   Bottino, Rita ^b   Long, Cassandra ^a   Ramsoondar, Jagdeece ^c   Ayares, David ^c   Cooper, David K C ^a  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b ALLEGHENY SINGER RESEARCH INSTITUTE   (United States)

^c REVIVICOR INC   (United States)

Author keywords

cytidine monophospho N acetylneuraminic acid hydroxylase; galactose 1,3 galactose; Islets; N glycolylneuraminic acid; pancreatic; Pig; Xenotransplantation; 1,3 galactosyltransferase gene knockout

Indexed keywords

IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; GALACTOSYLTRANSFERASE; MEMBRANE COFACTOR PROTEIN; N-GLYCOLYLNEURAMINIC ACID; NEURAMINIC ACID DERIVATIVE;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN BINDING; AORTA ENDOTHELIUM; AORTIC TISSUE; ARTICLE; CONTROLLED STUDY; CORNEA ENDOTHELIUM; CORNEAL TISSUE; ENDOTHELIUM CELL; ERYTHROCYTE; FEMALE; GENE; GENE EXPRESSION; HUMAN; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MALE; NEUGC GENE; NONHUMAN; NORMAL HUMAN; PANCREAS ISLET CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; T LYMPHOCYTE; THROMBOCYTE AGGREGATION; ANIMAL; CELL CULTURE; DEFICIENCY; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MONONUCLEAR CELL; PIG; PROCEDURES; TRANSGENIC ANIMAL; XENOGRAFT;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELLS, CULTURED; ENDOTHELIAL CELLS; GALACTOSYLTRANSFERASES; HUMANS; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE ACTIVATION; MEMBRANE COFACTOR PROTEIN; NEURAMINIC ACIDS; SWINE; TRANSPLANTATION, HETEROLOGOUS;

EID: 84961142164     PISSN: 0908665X     EISSN: 13993089     Source Type: Journal    
DOI: 10.1111/xen.12229     Document Type: Article

References (55)

1. Good AH, Cooper DK, Malcolm AJ, et al., Identification of carbohydrate structures that bind human antiporcine antibodies: implications for discordant xenografting in humans. Transplant Proc 1992; 24: 559-562.
2. Cooper DK, Good AH, Koren E, et al., Identification of alpha-galactosyl and other carbohydrate epitopes that are bound by human anti-pig antibodies: relevance to discordant xenografting in man. Transpl Immunol 1993; 1: 198-205.
3. Bouhours D, Pourcel C, Bouhours J-F,. Simultaneous expression by porcine aorta endothelial cells of glycosphingolipids bearing the major epitope for human xenoreactive antibodies (Galα1-3Gal), blood group H determinant and N-glycolylneuraminic acid. Glycoconj J 1996; 13: 947-953.
4. Zhu A, Hurst R,. Anti-N-glycolylneuraminic acid antibodies identified in healthy human serum. Xenotransplantation 2002; 9: 376-381.
5. Padler-Karavani V, Varki A,. Potential impact of the non-human sialic acid N-glycolylneuraminic acid on transplant rejection risk. Xenotransplantation 2011; 18: 1-5.
6. Galili U, Shohet SB, Kobrin E, Stults CL, Macher BA,. Man, apes, and Old World monkeys differ from other mammals in the expression of alpha-galactosyl epitopes on nucleated cells. J Biol Chem 1988; 263: 17755-17762.
7. Galili U,. Evolution of alpha 1,3galactosyltransferase and of the alpha-Gal epitope. Subcell Biochem 1999; 32: 1-23.
8. Basnet NB, Ide K, Tahara H, Tanaka Y, Ohdan H,. Deficiency of N-glycolylneuraminic acid and Galalpha1-3Galbeta1-4GlcNAc epitopes in xenogeneic cells attenuates cytotoxicity of human natural antibodies. Xenotransplantation 2010; 17: 440-448.
9. Tahara H, Ide K, Basnet NB, et al., Immunological property of antibodies against N-glycolylneuraminic acid epitopes in cytidine monophospho-N-acetylneuraminic acid hydroxylase-deficient mice. J Immunol 2010; 184: 3269-3275.
10. Lexer G, Cooper DK, Rose AG, et al., Hyperacute rejection in a discordant (pig to baboon) cardiac xenograft model. J Heart Transplant 1986; 5: 411-418.
11. Cooper DK, Human PA, Lexer G, et al., Effects of cyclosporine and antibody adsorption on pig cardiac xenograft survival in the baboon. J Heart Transplant 1988; 7: 238-246.
12. Ye Y, Neethling FA, Niekrasz M, et al., Evidence that intravenously administered alpha-galactosyl carbohydrates reduce baboon serum cytotoxicity to pig kidney cells (PK15) and transplanted pig hearts. Transplantation 1994; 58: 330-337.
13. Phelps CJ, Koike C, Vaught TD, et al., Production of alpha 1,3-galactosyltransferase-deficient pigs. Science 2003; 299: 411-414.
14. 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 U S A 2004; 101: 7335-7340.
15. 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.
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: 32-34.
17. Azimzadeh AM, Kelishadi SS, Ezzelarab MB, et al., Early graft failure of GalTKO pig organs in baboons is reduced by expression of a human complement pathway-regulatory protein. Xenotransplantation 2015; 22: 310-316.
18. McGregor CG, Ricci D, Miyagi N, et al., Human CD55 expression blocks hyperacute rejection and restricts complement activation in Gal knockout cardiac xenografts. Transplantation 2012; 93: 686-692.
19. Lutz AJ, Li P, Estrada JL, et al., Double knockout pigs deficient in N-glycolylneuraminic acid and galactose alpha-1,3-galactose reduce the humoral barrier to xenotransplantation. Xenotransplantation 2013; 20: 27-35.
20. Scobie L, Padler-Karavani V, Le Bas-Bernardet S, et al., Long-term IgG response to porcine Neu5Gc antigens without transmission of PERV in burn patients treated with porcine skin xenografts. J Immunol 2013; 191: 2907-2915.
21. Stone KR, Abdel-Motal UM, Walgenbach AW, Turek TJ, Galili U,. Replacement of human anterior cruciate ligaments with pig ligaments: a model for anti-non-gal antibody response in long-term xenotransplantation. Transplantation 2007; 83: 211-219.
22. Magnusson S, Mansson JE, Strokan V, et al., Release of pig leukocytes during pig kidney perfusion and characterization of pig lymphocyte carbohydrate xenoantigens. Xenotransplantation 2003; 10: 432-445.
23. Springer SA, Diaz SL, Gagneux P,. Parallel evolution of a self-signal: humans and new world monkeys independently lost the cell surface sugar Neu5Gc. Immunogenetics 2014; 66: 671-674.
24. Wang ZY, Burlak C, Estrada JL, et al., Erythrocytes from GGTA1/CMAH knockout pigs: implications for xenotransfusion and testing in non-human primates. Xenotransplantation 2014; 21: 376-384.
25. Burlak C, Paris LL, Lutz AJ, et al., Reduced binding of human antibodies to cells from GGTA1/CMAH KO pigs. Am J Transplant 2014; 14: 1895-1900.
26. Estrada JL, Martens G, Li P, et al., Evaluation of human and non-human primate antibody binding to pig cells lacking GGTA1/CMAH/beta4GalNT2 genes. Xenotransplantation 2015; 22: 194-202.
27. Cowan PJ, Roussel JC, D'Apice AJ,. The vascular and coagulation issues in xenotransplantation. Curr Opin Organ Transplant 2009; 14: 161-167.
28. Iwase H, Ekser B, Hara H, et al., Regulation of human platelet aggregation by genetically modified pig endothelial cells and thrombin inhibition. Xenotransplantation 2014; 21: 72-83.
29. 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.
30. van der Windt DJ, Marigliano M, He J, et al., Early islet damage after direct exposure of pig islets to blood: has humoral immunity been underestimated? Cell Transplant 2012; 21: 1791-1802.
31. Nagaraju S, Bertera S, Tanaka T, et al., In vitro exposure of pig neonatal isletlike cell clusters to human blood. Xenotransplantation 2015; 22: 317-324.
32. Loveland BE, Milland J, Kyriakou P, et al., Characterization of a CD46 transgenic pig and protection of transgenic kidneys against hyperacute rejection in non-immunosuppressed baboons. Xenotransplantation 2004; 11: 171-183.
33. 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.
34. Long C, Hara H, Pawlikowski Z, et al., Genetically engineered pig red blood cells for clinical transfusion: initial in vitro studies. Transfusion 2009; 49: 2418-2429.
35. Bottino R, Balamurugan AN, Smetanka C, et al., Isolation outcome and functional characteristics of young and adult pig pancreatic islets for transplantation studies. Xenotransplantation 2007; 14: 74-82.
36. Bottino R, Wijkstrom M, van der Windt DJ, et al., Pig-to-monkey islet xenotransplantation using multi-transgenic pigs. Am J Transplant 2014; 14: 2275-2287.
37. Fujita M, Mehra R, Lee SE, et al., Comparison of proliferative capacity of genetically-engineered pig and human corneal endothelial cells. Ophthalmic Res 2013: 49: 127-138.
38. Lee W, Miyagawa Y, Long C, et al., Expression of NeuGc on pig corneas and its potential significance in pig corneal xenotransplantation. Cornea 2016; 35: 105-113.
39. 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.
40. Wilhite T, Ezzelarab C, Hara H, et al., The effect of Gal expression on pig cells on the human T-cell xenoresponse. Xenotransplantation 2012; 19: 56-63.
41. Cohen D, Miyagawa Y, Mehra R, et al., Distribution of non-gal antigens in pig cornea: relevance to corneal xenotransplantation. Cornea 2014; 33: 390-397.
42. Byrne GW, Du Z, Stalboerger P, Kogelberg H, McGregor CG,. Cloning and expression of porcine beta1,4 N-acetylgalactosaminyl transferase encoding a new xenoreactive antigen. Xenotransplantation 2014; 21: 543-554.
43. Yeh P, Ezzelarab M, Bovin N, et al., Investigation of potential carbohydrate antigen targets for human and baboon antibodies. Xenotransplantation 2010; 17: 197-206.
44. Neethling F, Cooper DK, Xu H, Michler RE,. Newborn baboon serum anti-alpha galactosyl antibody levels and cytotoxicity to cultured pig kidney (PK15) cells. Transplantation 1995; 60: 520-521.
45. Dons EM, Montoya C, Long CE, et al., T-cell-based immunosuppressive therapy inhibits the development of natural antibodies in infant baboons. Transplantation 2012; 93: 769-776.
46. Rood PP, Tai HC, Hara H, et al., Late onset of development of natural anti-nonGal antibodies in infant humans and baboons: implications for xenotransplantation in infants. Transpl Int 2007; 20: 1050-1058.
47. Galili U, Mandrell RE, Hamadeh RM, Shohet SB, Griffiss JM,. Interaction between human natural anti-alpha-galactosyl immunoglobulin G and bacteria of the human flora. Infect Immun 1988; 56: 1730-1737.
48. Tangvoranuntakul P, Gagneux P, Diaz S, et al., Human uptake and incorporation of an immunogenic nonhuman dietary sialic acid. Proc Natl Acad Sci USA 2003; 100: 12045-12050.
49. Samraj AN, Pearce OM, Laubli H, et al., A red meat-derived glycan promotes inflammation and cancer progression. Proc Natl Acad Sci USA 2015; 112: 542-547.
50. Cooper DK, Koren E, Oriol R,. Genetically engineered pigs. Lancet 1993; 342: 682-683.
51. Miwa Y, Kobayashi T, Nagasaka T, et al., Are N-glycolylneuraminic acid (Hanganutziu-Deicher) antigens important in pig-to-human xenotransplantation? Xenotransplantation 2004; 11: 247-253.
52. Ezzelarab MB, Ayares D, Cooper DK,. Transgenic expression of human CD46: does it reduce the primate T-cell response to pig endothelial cells? Xenotransplantation 2015; 22: 487-489.
53. Buhler LH, Cooper DK,. How strong is the T cell response in the pig-to-primate model? Xenotransplantation 2005; 12: 85-87.
54. Ezzelarab MB, Ekser B, Echeverri G, et al., Costimulation blockade in pig artery patch xenotransplantation-a simple model to monitor the adaptive immune response in nonhuman primates. Xenotransplantation 2012; 19: 221-232.
55. Iwase H, Ekser B, Satyananda V, et al., Initial in vivo experience of pig artery patch transplantation in baboons using mutant MHC (CIITA-DN) pigs. Transpl Immunol 2015; 32: 99-108.