Structural characterization of α1,3-galactosyltransferase knockout pig heart and kidney glycolipids and their reactivity with human and baboon antibodies

Xenotransplantation

Volumn 17, Issue 1, 2010, Pages 48-60

  Diswall, Mette ^a   Ångström, Jonas ^a   Karlsson, Hasse ^b   Phelps, Carol J ^c   Ayares, David ^c   Teneberg, Susann ^b   Breimer, Michael E ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c REVIVICOR INC   (United States)

Author keywords

1,3 galactosyltransferase; Gal antigens; GalT KO; Glycolipids; Heart; Kidney; Knockout; Xenotransplantation

Indexed keywords

ALPHA 1,3 GALACTOSYLTRANSFERASE; ANTIBODY; GLYCOLIPID; IMMUNOGLOBULIN ANTIBODY; LECTIN; MONOCLONAL ANTIBODY; ANTIGEN; GALACTOSYLTRANSFERASE; N ACETYLLACTOSAMINIDE ALPHA 1,3 GALACTOSYLTRANSFERASE; N-ACETYLLACTOSAMINIDE ALPHA-1,3-GALACTOSYLTRANSFERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ARTICLE; CONTROLLED STUDY; GRAFT REJECTION; HEART; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYPERACUTE GRAFT REJECTION; IMMUNOREACTIVITY; INTESTINE LYMPHATIC TISSUE; KIDNEY; MASS SPECTROMETRY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; THIN LAYER CHROMATOGRAPHY; XENOTRANSPLANTATION; ANIMAL; BABOON; BLOOD; CARBOHYDRATE ANALYSIS; CHEMISTRY; GENETICS; HEART MUSCLE; HUMAN; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE; SWINE; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIBODIES; ANTIGENS; CARBOHYDRATE SEQUENCE; CHROMATOGRAPHY, THIN LAYER; GALACTOSYLTRANSFERASES; GLYCOLIPIDS; HUMANS; KIDNEY; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; MYOCARDIUM; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PAPIO; SWINE;

EID: 76349109490     PISSN: 0908665X     EISSN: 13993089     Source Type: Journal    
DOI: 10.1111/j.1399-3089.2009.00564.x     Document Type: Article

References (48)

1. 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 7340.
2. Phelps CJ, Koike C, Vaught TD et al. Production of alpha 1,3-galactosyltransferase-deficient pigs. Science 2003 299 : 411 414.
3. Cowan PJ. Coagulation and the xenograft endothelium. Xenotransplantation 2007 14 : 7 12.
4. 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.
5. 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.
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 1298.
7. Lam TT, Paniagua R, Shivaram G, Schuurman HJ, Borie DC, Morris RE. Anti-non-Gal porcine endothelial cell antibodies in acute humoral xenograft rejection of hDAF-transgenic porcine hearts in cynomolgus monkeys. Xenotransplantation 2004 11 : 531 535.
8. Buhler L, Xu Y, Li W, Zhu A, Cooper DK. An investigation of the specificity of induced anti-pig antibodies in baboons. Xenotransplantation 2003 10 : 88 93.
9. Christiansen D, Milland J, Mouhtouris E et al. Humans lack iGb3 due to the absence of functional iGb3-synthase: implications for NKT cell development and transplantation. PLoS Biol 2008 6 : e172.
10. Ezzelarab M, Ayares D, Cooper DK. Carbohydrates in xenotransplantation. Immunol Cell Biol 2005 83 : 396 404.
11. Diswall M, Angstrom J, Schuurman HJ, Dor FJ, Rydberg L, Breimer ME. Studies on glycolipid antigens in small intestine and pancreas from alpha1,3-galactosyltransferase knockout miniature swine. Transplantation 2007 84 : 1348 1356.
12. Holgersson J, Jovall PA, Samuelsson BE, Breimer ME. Structural characterization of non-acid glycosphingolipids in kidneys of single blood group O and A pigs. J Biochem 1990 108 : 766 777.
13. Breimer ME, Björck S, Svalander CT et al. Extracorporeal ("ex vivo") connection of pig kidneys to humans. I. Clinical data and studies of platelet destruction. Xenotransplantation 1996 3 : 328 339. (Pubitemid 126540933)
14. Ezzelarab M, Cortese-Hassett A, Cooper DK, Yazer MH. Extended coagulation profiles of healthy baboons and of baboons rejecting GT-KO pig heart grafts. Xenotransplantation 2006 13 : 522 528.
15. Holgersson J, Jovall PA, Breimer ME. Glycosphingolipids of human large intestine: detailed structural characterization with special reference to blood group compounds and bacterial receptor structures. J Biochem 1991 110 : 120 131.
16. Karlsson KA. Preparation of total nonacid glycolipids for overlay analysis of receptors for bacteria and viruses and for other studies. Methods Enzymol 1987 138 : 212 220.
17. Svennerholm L. Chromatographic separation of human brain gangliosides. J Neurochem 1963 10 : 613 623.
18. Clausen H, White T, Takio K et al. Isolation to homogeneity and partial characterization of a histo-blood group A defined Fuc alpha 1-2Gal alpha 1-3-N-acetylgalactosaminyltransferase from human lung tissue. J Biol Chem 1990 265 : 1139 1145.
19. Young WW Jr., Portoukalian J, Hakomori S. Two monoclonal anticarbohydrate antibodies directed to glycosphingolipids with a lacto-N-glycosyl type II chain. J Biol Chem 1981 256 : 10967 10972.
20. Rydberg L, Bengtsson A, Samuelsson O, Nilsson K, Breimer ME. In vitro assessment of a new ABO immunosorbent with synthetic carbohydrates attached to sepharose. Transpl Int 2005 17 : 666 672.
21. Morozumi K, Kobayashi T, Usami T et al. Significance of histochemical expression of Hanganutziu-Deicher antigens in pig, baboon and human tissues. Transplant Proc 1999 31 : 942 944.
22. 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.
23. Lindstrom K, Shanwell A, Jacobsson A, Lonnqvist B, Samuelsson BE. Alterations of glycosphingolipid-based blood group antigen expression on erythrocytes and in plasma studied on consecutive samples after a blood group O to A bone marrow transplantation. Glycobiology 1992 2 : 529 534.
24. Strokan V, Rydberg L, Hallberg EC, Molne J, Breimer ME. Characterisation of human natural anti-sheep xenoantibodies. Xenotransplantation 1998 5 : 111 121.
25. Teneberg S, Angstrom J, Jovall PA, Karlsson KA. Characterization of binding of Gal beta 4GlcNAc-specific lectins from Erythrina cristagalli and Erythrina corallodendron to glycosphinogolipids. Detection, isolation, and characterization of a novel glycosphinglipid of bovine buttermilk. J Biol Chem 1994 269 : 8554 8563.
26. Ito M, Yamagata T. Purification and characterization of glycosphingolipid-specific endoglycosidases (endoglycoceramidases) from a mutant strain of Rhodococcus sp. Evidence for three molecular species of endoglycoceramidase with different specificities. J Biol Chem 1989 264 : 9510 9519.
27. Angstrom J, Larsson T, Hansson GC, Karlsson KA, Henry S. Default biosynthesis pathway for blood group-related glycolipids in human small intestine as defined by structural identification of linear and branched glycosylceramides in a group O Le(a-b-) nonsecretor. Glycobiology 2004 14 : 1 12.
28. Backer AE, Holgersson J, Samuelsson BE, Karlsson H. Rapid and sensitive GC/MS characterization of glycolipid released Galalpha1,3Gal-terminated oligosaccharides from small organ specimens of a single pig. Glycobiology 1998 8 : 533 545.
29. Rydberg L, Holgersson J, Samuelsson BE, Breimer ME. alpha-Gal epitopes in animal tissue glycoproteins and glycolipids. Subcell Biochem 1999 32 : 107 125.
30. Smith DM, Newhouse M, Naziruddin B, Kresie L. Blood groups and transfusions in pigs. Xenotransplantation 2006 13 : 186 194.
31. Chai W, Piskarev V, Lawson AM. Negative-ion electrospray mass spectrometry of neutral underivatized oligosaccharides. Anal Chem 2001 73 : 651 657.
32. Robbe C, Capon C, Coddeville B, Michalski JC. Diagnostic ions for the rapid analysis by nano-electrospray ionization quadrupole time-of-flight mass spectrometry of O-glycans from human mucins. Rapid Commun Mass Spectrom 2004 18 : 412 420.
33. Thorn JJ, Levery SB, Salyan ME et al. Structural characterization of x2 glycosphingolipid, its extended form, and its sialosyl derivatives: accumulation associated with the rare blood group p phenotype. Biochemistry 1992 31 : 6509 6517.
34. Clausen H, Levery SB, Kannagi R, Hakomori S. Novel blood group H glycolipid antigens exclusively expressed in blood group A and AB erythrocytes (type 3 chain H). I. Isolation and chemical characterization. J Biol Chem 1986 261 : 1380 1387.
35. Teneberg S, Jovall PA, Karlsson H, Sjogren HO, Brodin T. Isolation and characterization of a rat testis glycosphingolipid based on gangliotetraosylceramide and having a blood group B determinant extended with beta 3-linked N-acetylgalactosamine. J Biochem 1994 116 : 697 703.
36. Clausen H, Levery SB, McKibbin JM, Hakomori S. Blood group A determinants with mono- and difucosyl type 1 chain in human erythrocyte membranes. Biochemistry 1985 24 : 3578 3586.
37. Bouhours D, Liaigre J, Lemoine J, Mayer-Posner F, Bouhours JF. Two novel isoneolacto-undecaglycosylceramides carrying Galalpha1 - >3Lewis(x) on the 6-linked antenna and N-acetylneuraminic acidalpha2 - >3 or Galactose alpha1 - >3 on the 3-linked antenna, expressed in porcine kidney. Glycoconj J 1998 15 : 1001 1016.
38. 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.
39. Parker W, Bruno D, Holzknecht ZE, Platt JL. Characterization and affinity isolation of xenoreactive human natural antibodies. J Immunol 1994 153 : 3791 3803. (Pubitemid 24313885)
40. Byrne GW, Stalboerger PG, Davila E et al. Proteomic identification of non-Gal antibody targets after pig-to-primate cardiac xenotransplantation. Xenotransplantation 2008 15 : 268 276.
41. Milland J, Christiansen D, Sandrin MS. Alpha1,3-galactosyltransferase knockout pigs are available for xenotransplantation: are glycosyltransferases still relevant? Immunol Cell Biol 2005 83 : 687 693.
42. Oriol R, Danilovs J, Hawkins BR. A new genetic model proposing that the Se gene is a structural gene closely linked to the H gene. Am J Hum Genet 1981 33 : 421 431.
43. Kannagi R, Fukuda MN, Hakomori S. A new glycolipid antigen isolated from human erythrocyte membranes reacting with antibodies directed to globo-N-tetraosylceramide (globoside). J Biol Chem 1982 257 : 4438 4442.
44. Siddiqui B, Hakomori S. A revised structure for the Forssman glycolipid hapten. J Biol Chem 1971 246 : 5766 5769.
45. Galili U, Clark MR, Shohet SB, Buehler J, Macher BA. Evolutionary relationship between the natural anti-Gal antibody and the Gal alpha 1-3Gal epitope in primates. Proc Natl Acad Sci USA 1987 84 : 1369 1373.
46. McCurry KR, Kooyman DL, Alvarado CG et al. Human complement regulatory proteins protect swine-to-primate cardiac xenografts from humoral injury. Nat Med 1995 1 : 423 427.
47. Magnusson S, Hallberg E, Mansson J et al. Ganglioside xenoantigens in pig lymphocytes and aorta. Transplant Proc 2000 32 : 848 850.
48. 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.