Genetically Engineered Pigs as a Source for Clinical Red Blood Cell Transfusion

Clinics in Laboratory Medicine

Volumn 30, Issue 2, 2010, Pages 365-380

  Cooper, David K C ^a   Hara, Hidetaka ^a   Yazer, Mark ^a,b  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b INSTITUTE FOR TRANSFUSION MEDICINE   (United States)

Author keywords

Erythrocytes; Pig; Red blood cells; Xenotransfusion; Xenotransplantation

Indexed keywords

ALLOANTIGEN; ALPHA 1,3 GALACTOSYLTRANSFERASE; ALPHA GALACTOSIDASE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; GALACTOSE; IMMUNOGLOBULIN M; N GLYCOLOYLNEURAMINIC ACID;

ANTIGEN ANTIBODY REACTION; ANTIGEN EXPRESSION; BLOOD BANK; BLOOD GROUP ABO INCOMPATIBILITY; BLOOD TRANSFUSION; COMPLEMENT DEPENDENT CYTOTOXICITY; DONOR SELECTION; ERYTHROCYTE TRANSFUSION; FOOD AND DRUG ADMINISTRATION; GENE INACTIVATION; GENETIC MANIPULATION; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; MACROPHAGE ACTIVATION; NONHUMAN; PRIMATE; PRIORITY JOURNAL; REVIEW; TRANSGENIC PIG; XENOTRANSFUSION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOOD BANKS; DISACCHARIDES; ERYTHROCYTE TRANSFUSION; ERYTHROCYTES; GALACTOSYLTRANSFERASES; HUMANS; IMMUNOGLOBULIN G; PAPIO; PHAGOCYTOSIS; SWINE; TRANSPLANTATION, HETEROLOGOUS;

EID: 77953329303     PISSN: 02722712     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cll.2010.02.001     Document Type: Review

References (95)

1. Olsson M.L., Clausen H. Modifying the red cell surface: towards an ABO-universal blood supply. Br J Haematol 2008, 140:3-12.
2. Whitaker B., Sullivan M. The 2007 nationwide blood collection and utilization survey report 2008, Department of Health and Human Services, Washington, DC.
3. Johnstone J.E., Maclaren L.A., Doucet J., et al. In vitro studies regarding the feasibility of bovine erythrocyte xenotransfusion. Xenotransplantation 2004, 11:11-17.
4. Cooper D.K.C., Gollackner B., Sachs D.H. Will the pig solve the transplantation backlog?. Annu Rev Med 2002, 53:133-147.
5. Cooper D.K.C., Lanza R.P. Xeno - the promise of transplanting animal organs into humans 2000, Oxford University Press, New York, p. 1-274.
6. Roux F.A., Sai P., Deschamps J.Y. Xenotransfusions, past and present. Xenotransplantation 2007, 14:208-216.
7. Lower R. The method observed in transfusing the blood out of one live animal into another. Monday December 17, 1666. Philos Trans R Soc Lond A 1666, 1:353-358.
8. Lower R. Tractatus de corde 1669, Danielem Elzevirium, London.
9. Denis J.B. Copie d'une lettre e crite a Monsieur de Montmor touchant une nouvelle maniere de gue rir plusieurs maladies par la transfusion du sang, confirme e par deux experiences faites sur des hommes. Le 15 juin 1667 1667, Jean Cusson, Paris.
10. Schmidt P.J., Leacock A.G. Forgotten transfusion history: John Leacock of Barbados. BMJ 2002, 325:1485-1487.
11. Blundell J. Successful case of transfusion. Lancet 1829, 1:431-432.
12. Landsteiner K. Zur Kentniss der antifermentativen lytischen und agglutinierenden Wirkungen des Blutserums und der Lymphe. Zentralblatt für Bakteriologie 1900, 28:357-362. [in German].
13. Pond W.G., Houpt K.A. The biology of the pig 1978, Comstock Pub Associates, Ithaca (NY).
14. Jandl J.H. Blood: textbook of hematology 1996, Little, Brown, Boston.
15. Zhu A. Introduction to porcine red blood cells: implications for xenotransfusion. Semin Hematol 2000, 37:143-149.
16. Cooper D.K.C. Porcine red blood cells as a source of blood transfusion in humans. Xenotransplantation 2003, 10:384-386.
17. Eckermann J.M., Buhler L.H., Zhu A., et al. Initial investigation of the potential of modified porcine erythrocytes for transfusion in primates. Xenotransplantation 2004, 11:18-26.
18. Sako F., Gasa S., Makita A., et al. Human blood group glycosphingolipids of porcine erythrocytes. Arch Biochem Biophys 1990, 278:228-237.
19. Smith D.M., Newhouse M., Naziruddin B., et al. Blood groups and transfusions in pigs. Xenotransplantation 2006, 13:186-194.
20. Yamamoto F., Yamamoto M. Molecular genetic basis of porcine histo-blood group AO system. Blood 2001, 97:3308-3310.
21. Katz D.S., White S.P., Huang W., et al. Structure determination of aquomet porcine hemoglobin at 2.8A resolution. J Mol Biol 1994, 244:541-553.
22. Rao M.J., Schneider K., Chait B.T., et al. Recombinant hemoglobin A produced in transgenic swine: structural equivalence with human hemoglobin A. Artif Cells Blood Substit Immobil Biotechnol 1994, 22:695-700.
23. Oostingh G.J., Davies H.F.S., Tang K.C.G., et al. Sensitization to swine leukocyte antigens in patients with broadly reactive HLA specific antibodies. Am J Transplant 2002, 2:267-273.
24. Patience C., Takeuchi Y., Weiss R.A. Zoonosis in xenotransplantation. Curr Opin Immunol 1998, 10:539-542.
25. Blusch J.H., Patience C., Martin U. Pig endogenous retroviruses and xenotransplantation. Xenotransplantation 2002, 9:242-251.
26. Roux F.A., Sai P., Deschamps J.-Y. Some ethical issues regarding xenotransfusion. Xenotransplantation 2007, 14:217-221.
27. Galili U., Shohet S.B., Kobrin E., et al. 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.
28. Cooper D.K.C. Depletion of natural antibodies in nonhuman primates - a step towards successful discordant xenografting in man. Clin Transplant 1992, 6:178-183.
29. Good A.H., Cooper D.K., Malcolm A.J., et al. Identification of carbohydrate structures that bind human antiporcine antibodies: implications for discordant xenografting in humans. Transplant Proc 1992, 24:559-562.
30. Doucet J., Gao Z.H., MacLaren L.A., et al. Modification of xenoantigens on porcine erythrocytes for xenotransfusion. Surgery 2004, 135:178-186.
31. Galili U., Mandrell R.E., Hamadeh R.M., et al. Interaction between human natural anti-α-galactosyl immunoglogulin G and bacteria of the human flora. Infect Immun 1988, 56:1730-1737.
32. Phelps C.J., Koike C., Vaught T.D., et al. Production of alpha 1,3-galactosyltransferase-deficientpigs. Science 2003, 299:411-414.
33. Kolber-Simonds D., Lai L., Watt S.R., 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.
34. Hara H., Ezzelarab M., Rood P.P., 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.
35. Rood P.P.M., Hara H., Busch J.L., et al. Incidence and cytotoxicity of antibodies in cynomolgus monkeys directed to nonGal antigens, and their relevance for experimental models. Transpl Int 2006, 19:158-165.
36. Ezzelarab M., Hara H., Busch J., et al. Antibodies directed to pig non-Gal antigens in naive and sensitized baboons. Xenotransplantation 2006, 13:400-407.
37. Zhu A., Hurst R. Anti-N-glycolylneuraminic acid antibodies identified in healthy human serum. Xenotransplantation 2002, 9:376-381.
38. Schauer R. Sialic acids, chemistry, metabolism, and function 1982, Springer, Vienna (Austria).
39. Asaoka H., Matsuda H. Detection of N-glycolylneuraminic acid-containing glycoproteins from various animal erythrocytes by chicken monoclonal antibody against Hanganutziu-Deicher antigens. J Vet Med Sci 1994, 56:375-377.
40. Varki A. Loss of N-glycolylneuraminic acid in humans: mechanisms, consequences, and implications for hominid evolution. Am J Phys Anthropol 2001, 116(Suppl 33):54-69.
41. Bouhours D., Pourcel C., Bouhours J.E. Simultaneous expression by porcine aorta endothelial cells of glycosphingolipids bearing the major epitope for human xenoreactive antibodies (Gal alpha 1-3Gal), blood group H determinant and N-glycolylneuraminic acid. Glycoconj J 1996, 13:947-953.
42. Yeh P, Ezzelarab M, Bovin N, et al. Investigation of potential carbohydrate antigen targets for human and baboon antibodies. Xenotransplantation, in press.
43. Blixt O., Kumagai-Braesch M., Tibell A., et al. Anticarbohydrate antibody repertoires in patients transplanted with fetal pig islets revealed by glycan arrays. Am J Transplant 2009, 9:83-90.
44. Zhu A. Binding of human natural antibodies to nonαGal xenoantigens on porcine erythrocytes. Transplantation 2000, 69:2422-2428.
45. Zhu A., Hurst R. Human natural antibodies that recognize nonalphaGal antigens on porcine red blood cells. Transplant Proc 2000, 32:872-873.
46. Zhu A., Goldstein J. Cloning and functional expression of a cDNA encoding coffee bean alpha-galactosidase. Gene 1994, 140:227-231.
47. Zhu A., Monahan C., Zhang Z., et al. High-level expression and purification of coffee bean alpha-galactosidase produced in the yeast Pichia pastoris. Arch Biochem Biophys 1995, 324:65-70.
48. Zhu A., Wang Z.K. Expression and characterization of recombinant alpha-galactosidase in baculovirus-infected insect cells. Eur J Biochem 1996, 235:332-337.
49. LaVecchio J.A., Dunne A.D., Edge A.S. Enzymatic removal of alpha-galactosyl epitopes from porcine endothelial cells diminishes the cytotoxic effect of natural antibodies. Transplantation 1995, 60:841-847.
50. Luo Y., Wen J., Luo C., et al. Pig xenogeneic antigen modification with green coffee bean α-galactosidase: working conditions and potential application in xenotransplantation. Xenotransplantation 1999, 6:238-248.
51. Kobayashi T., Taniguchi S., Neethling F.A., et al. Delayed xenograft rejection of pig-to-baboon cardiac transplants after cobra venom factor therapy. Transplantation 1997, 64:1255.
52. Xu Y., Lorf T., Sablinski T., et al. Removal of anti-porcine natural antibodies from human and nonhuman primate plasma in vitro and in vivo by a Galα1-3Galα1-4αGlc-X immunoaffinity column. Transplantation 1998, 65:172-179.
53. Kuwaki K., Knosalla C., Dor F.J., 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, 4:363-372.
54. Basker M., Alwayn I.P., Buhler L., et al. Clearance of mobilized porcine peripheral blood progenitor cells is delayed by depletion of the phagocytic reticuloendothelial system in baboons. Transplantation 2001, 72:1278-1285.
55. Tseng Y.-L., Sachs D.H., Cooper D.K.C. Porcine hematopoietic progenitor cell transplantation in nonhuman primates: a review of progress. Transplantation 2005, 79:1-9.
56. Dor F.J., Rouhani F.J., Cooper D.K. Transfusion of pig red cells into baboons. Xenotransplantation 2004, 11:295-297.
57. Llanes D., Nogal M.L., Prados F., et al. An erythroid species-specific antigen of swine detected by a monoclonal antibody. Hybridoma 1992, 11:757-764.
58. Rouhani F.J., Dor F.J., Cooper D.K. Investigation of red blood cells from alpha1,3-galactosyltransferase-knockout pigs for human blood transfusion. Transfusion 2004, 44:1004-1012.
59. MacLaren L.A., Riggs C.M., Johnstone J.E., et al. Evaluating porcine RBC and platelet alpha-galactosyl expression. Transfusion 2002, 42:1184-1188.
60. Cooper D.K.C. Xenoantigens and xenoantibodies. Xenotransplantation 1998, 5:6-17.
61. Ezzelarab M., Ayares D., Cooper D.K. Carbohydrates in xenotransplantation. Immunol Cell Biol 2005, 83:396-404.
62. Huflejt M.E., Vuskovic M., Vasiliu D., et al. Anti-carbohydrate antibodies of normal sera: findings, surprises and challenges. Mol Immunol 2009, 46:3037-3049.
63. 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.
64. Rees M.A., Butler A.J., Negus M.C., et al. Classical pathway complement destruction is not responsible for the loss of human erythrocytes during porcine liver perfusion. Transplantation 2004, 77:1416-1423.
65. Rees M.A., Butler A.J., Brons I.G., et al. Evidence of macrophage receptors capable of direct recognition of xenogeneic epitopes without opsonization. Xenotransplantation 2005, 12:13-19.
66. Oldenborg P.A., Zheleznyak A., Fang Y.F., et al. Role of CD47 as a marker of self on red blood cells. Science 2000, 288:2051-2054.
67. Oldenborg P.A., Gresham H.D., Lindberg F.P. CD47-signal regulatory protein alpha (SIRPalpha) regulates Fcgamma and complement receptor-mediated phagocytosis. J Exp Med 2001, 193:855-862.
68. Vernon-Wilson E.F., Kee W.J., Willis A.C., et al. CD47 is a ligand for rat macrophage membrane signal regulatory protein SIRP (OX41) and human SIRPalpha 1. Eur J Immunol 2000, 30:2130-2137.
69. Ide K., Ohdan H., Kobayashi T., et al. Antibody- and complement-independent phagocytotic and cytolytic activities of human macrophages toward porcine cells. Xenotransplantation 2005, 12:81-88.
70. Wang H., VerHalen J., Madariaga M.L., et al. Attenuation of phagocytosis of xenogeneic cells by manipulating CD47. Blood 2007, 109:836-842.
71. Ide K., Wang H., Tahara H., et al. Role for CD47-SIRPalpha signaling in xenograft rejection by macrophages. Proc Natl Acad Sci U S A 2007, 104:5062-5066.
72. Cooper D.K.C., Tseng Y.L., Saidman S.L. Alloantibody and xenoantibody cross-reactivity in transplantation. Transplantation 2004, 77:1-5.
73. Phelps C., Ball S., Vaught T., et al. Production and characterization of transgenic pigs expressing porcine CTLA4-Ig. Xenotransplantation 2009, 16:477-485.
74. Koike C., Kannagi R., Takuma Y., et al. Introduction of [alpha](1,2)- fucosyltransferase and its effect on [alpha]-Gal epitopes in transgenic pig. Xenotransplantation 1996, 3:81-86.
75. Sharma A., Okabe J., Birch P., et al. Reduction in the level of Gal(alpha1,3)Galα1,3Gal (Gal) in transgenic mice and pigs by the expression of an alpha(1,2)fucosyltransferase. Proc Natl Acad Sci U S A 1996, 93:7190-7195.
76. Osman N., Mckenzie I.F., Ostenried K., et al. Combined transgenic expression of alpha-galactosidase and alpha1,2-fucosyltransferase leads to optimal reduction in the major xenoepitope Gal alpha(1,3)Gal. Proc Natl Acad Sci U S A 1997, 94:14677-14682.
77. Chen C.G., Salvaris E.J., Romanella M., et al. Transgenic expression of human alpha1,2-fucosyltransferase (H-transferase) prolongs mouse heart survival in an ex vivo model of xenograft rejection. Transplantation 1998, 65:832-837.
78. Costa C., Zhao L., Burton W.V., et al. Expression of the human alpha1,2-fucosyltransferase in transgenic pigs modifies the cell surface carbohydrate phenotype and confers resistance to human serum-mediated cytolysis. FASEB J 1999, 13:1762-1773.
79. Ramsoondar J.J., Machaty Z., Costa C., et al. Production of alpha 1,3- galactosyltransferase-knockout cloned pigs expressing human alpha 1,2-fucosylosyltransferase. Biol Reprod 2003, 69:437-445.
80. Cozzi E., White D.J.G. The generation of transgenic pigs as potential organ donors for humans. Nat Med 1995, 1:964-969.
81. Diamond L.E., Quinn C.M., Martin M.J., et al. A human CD46 transgenic pig model system for the study of discordant xenotransplantation. Transplantation 2001, 71:132-142.
82. Adams D.H., Kadner A., Chen R.H., et al. Human membrane cofactor protein (MCP, CD 46) protects transgenic pig hearts from hyperacute rejection in primates. Xenotransplantation 2001, 8:36-40.
83. Loveland B.E., 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.
84. Hara H., Long C., Lin Y.J., et al. In vitro investigation of pig cells for resistance to human antibody-mediated rejection. Transpl Int 2008, 21:1163-1174.
85. Tadaki D.K., Craighead N., Saini A., et al. Costimulatory molecules are active in the human xenoreactive T-cell response but not in natural killer-mediated cytotoxicity. Transplantation 2000, 70:162-167.
86. Vaughan A.N., Malde P., Rogers N.J., et al. Porcine CTLA4-Ig lacks a MYPPPY motif, binds inefficiently to human B7 and specifically suppresses human CD4+ T cell responses costimulated by pig but not human B7. J Immunol 2000, 165:3175-3181.
87. Mirenda V., Golshayan D., Read J., et al. Achieving permanent survival of islet xenografts by independent manipulation of direct and indirect T-cell responses. Diabetes 2005, 54:1048-1055.
88. 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.
89. Jeong S.T., Byun S.M. Decreased agglutinability of methoxy-polyethylene glycol attached red blood cells: significance as a blood substitute. Artif Cells Blood Substit Immobil Biotechnol 1996, 24:503-511.
90. Scott M.D., Murad K.L., Koumpouras F., et al. Chemical camouflage of antigenic determinants: stealth erythrocytes. Proc Natl Acad Sci U S A 1997, 94:7566-7571.
91. Scott M.D., Bradley A.J., Murad K.L. Camouflaged blood cells: low-technology bioengineering for transfusion medicine?. Transfus Med Rev 2000, 14:53-63.
92. Scott M.D., Chen A.M. Beyond the red cell: pegylation of other blood cells and tissues. Transfus Clin Biol 2004, 11:40-46.
93. Murad K.L., Mahany K.L., Brugnara C., et al. Structural and functional consequences of antigenic modulation of red blood cells with methoxypoly (ethylene glycol). Blood 1999, 93:2121-2127.
94. Chen A.M., Scott M.D. Current and future applications of immunological attenuation via pegylation of cells and tissues. BioDrugs 2001, 15:833-847.
95. Garrity G. Modulating the red cell membrane to produce universal/stealth donor red cells suitable for transfusion. Vox Sang 2008, 94:87-95.