Characteristics of protein-carbohydrate interactions as a basis for developing novel carbohydrate-based antirejection therapies

Immunology and Cell Biology

Volumn 83, Issue 6, 2005, Pages 694-708

  Holgersson, Jan ^a   Gustafsson, Anki ^a,b   Breimer, Michael E ^b  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

ABO incompatible allotransplantation; Antirejection therapy; Protein carbohydrate interaction; Xenotransplantation

Indexed keywords

ALPHA 1,3 GALACTOSYLTRANSFERASE; ANTIBODY; CARBOHYDRATE; CARBOHYDRATE ANTIGEN; CELL ANTIBODY; GALACTOSE; HYBRID PROTEIN; IMMUNOGLOBULIN; OLIGOSACCHARIDE; P SELECTIN GLYCOPROTEIN LIGAND 1; PROTEIN;

ALLOGRAFT; ALLOTRANSPLANTATION; BIOSYNTHESIS; BLOOD GROUP ABO INCOMPATIBILITY; CHEMICAL STRUCTURE; DONOR; HUMAN; IMMUNOADSORBENT; MULTIPLE ORGAN FAILURE; NONHUMAN; PLASMAPHERESIS; PROTEIN CARBOHYDRATE INTERACTION; REVIEW; TRANSPLANTATION; XENOGRAFT;

ANIMALS; ANTIBODIES; BLOOD GROUP INCOMPATIBILITY; CARBOHYDRATES; HUMANS; IMMUNOSUPPRESSION; PROTEIN BINDING; TRANSPLANTATION, HETEROLOGOUS;

EID: 30544448119     PISSN: 08189641     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1440-1711.2005.01373.x     Document Type: Review

References (164)

1. Lowe JB. Glycan-dependent leukocyte adhesion and recruitment in inflammation. Curr. Opin. Cell Biol 2003; 15: 531-8.
2. Karlsson KA. Pathogen-host protein-carbohydrate interactions as the basis of important infections. Adv. Exp. Med. Biol. 2001; 491: 431-43.
3. Rydberg L. ABO-incompatibility in solid organ transplantation. Transfus. Med. 2001; 11: 325-42.
4. Takahashi K. Accommodation in ABO-Incompatible Kidney Transplantation. Amsterdam: Elsevier, 2004.
5. Alwayn IP, Basker M, Buhler L, Cooper DK. The problem of anti-pig antibodies in pig-to-primate xenografting: current and novel methods of depletion and/or suppression of production of anti-pig antibodies. Xenotransplantation 1999; 6: 157-68.
6. Lloyd KO. Carbohydrate vaccines for the immunotherapy of cancer. Drug News Perspect. 2000; 13: 463-70.
7. Maeder T. Sweet medicines. Sci. Am. 2002; 287: 40-7.
8. Bundle D, Young M. Carbohydrate-protein interactions in antibodies and lectins. Curr. Opin. Struct. Biol. 1992; 2: 666-73.
9. Toone E. Structure and energetics of protein-carbohydrate complexes. Curr. Opin. Struct. Biol. 1994; 4: 719-28.
10. Garcia-Hernandez E, Zubillaga RA, Rojo-Dominguez A, Rodriguez-Romero A, Hernandez-Arana A. New insights into the molecular basis of lectin-carbohydrate interactions: a calorimetric and structural study of the association of hevein to oligomers of N-acetylglucosamine. Proteins 1997; 29: 467-77.
11. Garcia-Hernandez E, Hernandez-Arana A. Structural bases of lectin-carbohydrate affinities: comparison with protein-folding energetics. Protein Sci. 1999; 8: 1075-86.
12. Dam TK, Brewer CF. Thermodynamic studies of lectin-carbohydrate interactions by isothermal titration calorimetry. Chem. Rev. 2002; 102: 387-429.
13. Garcia-Hernandez E, Zubillaga RA, Rodriguez-Romero A, Hernandez-Arana A. Stereochemical metrics of lectin-carbohydrate interactions: comparison with protein-protein interfaces. Glycobiology 2000; 10: 993-1000.
14. Navarre N, Amiot N, van Oijen A et al. Synthesis and conformational analysis of a conformationally constrained trisaccharide, and complexation properties with concanavalin A. Chem. Eur. J. 1999; 5: 2281-94.
15. Dunitz JD. Win some, lose some: enthalpy-entropy compensation in weak intermolecular interactions. Chem. Biol. 1995; 2: 709-12.
16. Lemieux R. How water provides the impetus for molecular recognition in aqueous solution. Acc. Chem. Res. 1996; 29: 373-80.
17. Rand RP, Fuller NL, Butko P, Francis G, Nicholls P. Measured change in protein solvation with substrate binding and turnover. Biochemistry 1993; 32: 5925-9.
18. Garcia-Hernandez E, Zubillaga RA, Chavelas-Adame EA, Vazquez-Contreras E, Rojo-Dominguez A, Costas M. Structural energetics of protein-carbohydrate interactions: insights derived from the study of lysozyme binding to its natural saccharide inhibitors. Protein Sci. 2003; 12: 135-42.
19. Swaminathan C, Surolia N, Avadhesha S. Role of water in the specific binding of mannose and mannooligosaccharides to concanavalin A. J. Am. Chem. Soc. 1998; 120: 5153-259.
20. Bryce RA, Hillier IH, Naismith JH. Carbohydrate-protein recognition: molecular dynamics simulations and free energy analysis of oligosaccharide binding to concanavalin A. Biophys. J. 2001; 81: 1373-88.
21. Hardy RR, Hayakawa K. CD5 B cells, a fetal B cell lineage. Adv. Immunol. 1994; 55: 297-339.
22. Casali P, Schettino EW. Structure and function of natural antibodies. Curr. Top. Microbiol. Immunol. 1996; 210: 167-79.
23. Satapathy AK, Ravindran B. Naturally occurring alpha-galactosyl antibodies in human sera display polyreactivity. Immunol. Lett. 1999; 69: 347-51.
24. Ochsenbein AF, Fehr T, Lutz C et al. Control of early viral and bacterial distribution and disease by natural antibodies. Science 1999; 286: 2156-9.
25. Ochsenbein AF, Zinkernagel RM. Natural antibodies and complement link innate and acquired immunity. Immunol. Today 2000; 21: 624-30.
26. Boes M. Role of natural and immune IgM antibodies in immune responses. Mol. Immunol. 2000; 37: 1141-9.
27. Bohn J. Are natural antibodies involved in tumour defence? Immunol. Lett. 1999; 69: 317-20.
28. Kearns-Jonker M, Swensson J, Ghiuzeli C et al. The human antibody response to porcine xenoantigens is encoded by IGHV3-11 and IGHV3-74 IgVH germline progenitors. J. Immunol. 1999; 163: 4399-412.
29. Tinguely C, Schaller M, Carrel T, Nydegger UE. Spectrotype analysis and clonal characteristics of human anti-Gal alpha1-3Gal antibodies. Xenotransplantation 2002; 9: 252-9.
30. Watkins WM. The ABO blood group system: historical background. Transfus. Med. 2001; 11: 243-65.
31. Galili U. Evolution and pathophysiology of the human natural anti-alpha-galactosyl IgG (anti-Gal) antibody. Springer Semin. Immunopathol. 1993; 15: 155-71.
32. Sandrin MS, Vaughan HA, Dabkowski PL, McKenzie IF. Anti-pig IgM antibodies in human serum react predominantly with Gal(alpha 1-3) Gal epitopes. Proc. Natl Acad. Sci. USA 1993; 90: 11 391-5.
33. McKane W, Lee J, Preston R et al. Polymorphism in the human anti-pig natural antibody repertoire: implications for antigen-specific immunoadsorption. Transplantation 1998; 66: 626-33.
34. Yamamoto F. Review: ABO blood group system - ABH oligosaccharide antigens, anti-A and anti-B, A and B glycosyltransferases, and ABO genes. Immunohematology 2004; 20: 3-22.
35. Oriol R, Mollicone R, Coullin P, Dalix AM, Candelier JJ. Genetic regulation of the expression of ABH and Lewis antigens in tissues. APMIS Suppl. 1992; 27: 28-38.
36. Ravn V, Dabelsteen E. Tissue distribution of histo-blood group antigens. APMIS 2000; 108: 1-28.
37. Marionneau S, Cailleau-Thomas A, Rocher J et al. ABH and Lewis histo-blood group antigens, a model for the meaning of oligosaccharide diversity in the face of a changing world. Biochimie 2001; 83: 565-73.
38. Breton C, Mucha J, Jeanneau C. Structural and functional features of glycosyltransferases. Biochimie 2001; 83: 713-8.
39. Clausen H, Hakomori S. ABH and related histo-blood group antigens; immunochemical differences in carrier isotypes and their distribution. Vox Sang. 1989; 56: 1-20.
40. Newburg DS, Neubauer SH. Carbohydrates in milks: analysis, quantities, and significance. In: Jensen RG (ed.). Handbook of Milk Composition. New York: Academic Press, 1995: 273-349.
41. Holgersson J, Breimer ME, Samuelsson B. Basic biochemistry of cell surface carbohydrates and aspects of the tissue distribution of histo-blood group ABH and related glycosphingolipids. Acta Pathol. Microbiol. Immunol. Scand. Suppl. 1992; 27: 18-27.
42. 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: 17 755-62.
43. Rydberg L, Holgersson J, Samuelsson BE, Breimer ME. alpha-Gal epitopes in animal tissue glycoproteins and glycolipids. Subcell. Biochem. 1999; 32: 107-25.
44. 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: 533-45.
45. Hallberg EC, Holgersson J, Samuelsson BE. Glycosphingolipid expression in pig aorta: identification of possible target antigens for human natural antibodies. Glycobiology 1998; 8: 637-49.
46. 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 alphal->3 on the 3-linked antenna, expressed in porcine kidney. Glycoconj. J. 1998; 15: 1001-16.
47. Oriol R, Ye Y, Koren E, Cooper DK. Carbohydrate antigens of pig tissues reacting with human natural antibodies as potential targets for hyperacute vascular rejection in pig-to-man organ xenotransplantation. Transplantation 1993; 56: 1433-42.
48. Oriol R, Barthod F, Bergemer AM, Ye Y, Koren E, Cooper DK. Monomorphic and polymorphic carbohydrate antigens on pig tissues: implications for organ xenotransplantation in the pig-to-human model. Transpl. Int. 1994; 7: 405-13.
49. Alvarado CG, Cotterell AH, McCurry KR et al. Variation in the level of xenoantigen expression in porcine organs. Transplantation 1995; 59: 1589-96.
50. Holzknecht ZE, Platt JL. Identification of porcine endothelial cell membrane antigens recognized by human xenoreactive natural antibodies. J. Immunol. 1995; 154: 4565-75.
51. Everett ML, Lin SS, Worrell SS, Platt JL, Parker W. The footprint of antibody bound to pig cells: evidence of complex surface topology. Biochem. Biophys. Res. Commun. 2003; 301: 751-7.
52. Brockhausen I, Moller G, Merz G, Adermann K, Paulsen H. Control of mucin synthesis: the peptide portion of synthetic O-glycopeptide substrates influences the activity of O-glycan core 1 UDPgalactose: N-acetyl-alpha-galactosaminyl-R beta 3-Galactosyltransferase. Biochemistry 1990; 29: 10 206-12.
53. Hennet T. The galactosyltransferase family. Cell. Mol. Life Sci. 2002; 59: 1081-95.
54. Gerken TA, Zhang J, Levine J, Elhammer A. Mucin core O-glycosylation is modulated by neighboring residue glycosylation status. Kinetic modeling of the site-specific glycosylation of the apo-porcine submaxillary mucin tandem repeat by UDP-GalNAc: polypeptide N-acetylgalactosaminyltransferases T1 and T2. J. Biol. Chem. 2002; 277: 49850-62.
55. Oriol R, Danilovs J, Hawkins BR. A new gene model proposing that the Sc gene is a structural gene closely linked to the H gene. Am. J. Hum. Genet. 1981; 33: 421-31.
56. Rajan VP, Larsen RD, Ajmera S, Ernst LK, Lowe JB. A cloned human DNA restriction fragment determines expression of a GDP-L-fucose: beta-D-galactoside 2-alpha-L-fucosyltransferase in transfected cells. Evidence for isolation and transfer of the human H blood group locus. J. Biol. Chem. 1989; 264: 11 158-67.
57. Larsen RD, Ernst LK, Nair RP, Lowe JB. Molecular cloning, sequence, and expression of a human GDP-L-fucose: beta-D-galactoside 2-alpha-L- fucosyltransferase cDNA that can form the H blood group antigen. Proc. Natl Acad. Sci. USA 1990; 87: 6674-8.
58. Kelly RJ, Rouquier S, Giorgi D, Lennon GG, Lowe JB. Sequence and expression of a candidate for the human secretor blood group alpha (1,2) fucosyltransferase gene (FUT2). Homozygosity for an enzyme-inactivating nonsense mutation commonly correlates with the non-secretor phenotype. J. Biol. Chem. 1995; 270: 4640-9.
59. Rouquier S, Lowe JB, Kelly RJ, Fertitta AL, Lennon GG, Giorgi D. Molecular cloning of a human genomic region containing the H blood group alpha(1,2)fucosyltransferase gene and two H locus-related DNA restriction fragments. Isolation of a candidate for the human Secretor blood group locus. J. Biol. Chem. 1995; 270: 4632-9.
60. Prieto PA, Larsen RD, Cho M et al. Expression of human H-type alpha1,2-fucosyltransferase encoding for blood group H(O) antigen in Chinese hamster ovary cells. Evidence for preferential fucosylation and truncation of polylactosamine sequences. J. Biol. Chem. 1997; 272: 2089-97.
61. Liu YH, Fujitani N, Koda Y, Kimura H. Distribution of H type 1 and of H type 2 antigens of ABO blood group in different cells of human submandibular gland. J. Histochem. Cytochem. 1998; 46: 69-76.
62. Liu Y, Fujitani N, Koda Y, Soejima M, Kimura H. Presence of H type 3/4 chains of ABO histo-blood group system in serous cells of human submandibular gland and regulation of their expression by the secretor gene (FUT2). J. Histochem. Cytochem. 1999; 47: 889-94.
63. Lofling JC, Hauzenberger E, Holgersson J. Absorption of anti-blood group A antibodies on P-selectin glycoprotein ligand-1/ immunoglobulin chimeras carrying blood group A determinants: core saccharide chain specificity of the Se and H gene encoded alpha1,2 fucosyltransferases in different host cells. Glycobiology 2002; 12: 173-82.
64. Oriol R, LePendu J, Mollicone R. Genetics of ABO, H, Lewis, X and related antigens. Vox. Sang. 1986; 51: 161-71.
65. Kelly RJ, Ernst LK, Larsen RD, Bryant JG, Robinson JS, Lowe JB. Molecular basis for H blood group deficiency in Bombay (Oh) and para-Bombay individuals. Proc. Natl Acad. Sci. USA 1994; 91: 5843-7.
66. Furukawa K, Mattes MJ, Lloyd KO. A1 and A2 erythrocytes can be distinguished by reagents that do not detect structural differences between the two cell types. J. Immunol. 1985; 135: 4090-4.
67. Clausen H, Watanabe K, Kannagi R et al. Blood group A glycolipid (Ax) with globo-series structure which is specific for blood group A1 erythrocytes: one of the chemical bases for A1 and A2 distinction. Biochem. Biophys. Res. Commun. 1984; 124: 523-9.
68. Clausen H, Holmes E, Hakomori S. Novel blood group H glycolipid antigens exclusively expressed in blood group A and AB erythrocytes (type 3 chain H). II. Differential conversion of different H substrates by A1 and A2 enzymes, and type 3 chain H expression in relation to secretor status. J. Biol. Chem. 1986; 261: 1388-92.
69. Breimer ME, Samuelsson BE. The specific distribution of glycolipid-based blood group A antigens in human kidney related to A1/A2, Lewis, and secretor status of single individuals. A possible molecular explanation for the successful transplantation of A2 kidneys into O recipients. Transplantation 1986; 42: 88-91.
70. Holgersson J, Breimer ME, Jacobsson A, Svensson L, Ulfvin A, Samuelsson BE. Glycolipid- and glycoprotein-based blood group A antigen expression in human thrombocytes. A1/A2 difference. Glycoconj. J. 1990; 7: 601-8.
71. Joziasse DH, Shaper JH, Shaper NL. The alpha 1,3-galactosyltransferase gene. Subcell. Biochem. 1999; 32: 25-48.
72. Larsen RD, Rivera-Marrero CA, Ernst LK, Cummings RD, Lowe JB. Frameshift and nonsense mutations in a human genomic sequence homologous to a murine UDP-Gal: beta-D-Gal(1,4)-D-GlcNAc alpha(1,3)-galactosyltransferase cDNA. J. Biol. Chem. 1990; 265: 7055-61.
73. Joziasse DH, Shaper JH, Jabs EW, Shaper NL. Characterization of an alpha 1-3-galactosyltransferase homologue on human chromosome 12 that is organized as a processed pseudogene. J. Biol. Chem. 1991; 266: 6991-8.
74. Taylor SG, McKenzie IF, Sandrin MS. Characterization of the rat alpha(1,3)galactosyltransferase: evidence for two independent genes encoding glycosyltransferases that synthesize Galalpha(1,3)Gal by two separate glycosylation pathways. Glycobiology 2003; 13: 327-37.
75. Sharma A, Naziruddin B, Cui C et al. Pig cells that lack the gene for alpha1-3 galactosyltransferase express low levels of the gal antigen. Transplantation 2003; 75: 430-6.
76. Imberty A, Mikros E, Koca J, Mollicone R, Oriol R, Perez S. Computer simulation of histo-blood group oligosaccharides: energy maps of all constituting disaccharides and potential energy surfaces of 14 ABH and Lewis carbohydrate antigens. Glycoconj. J. 1995; 12: 331-49.
77. Corzana F, Bettler E, Herve du Penhoat C, Tyrtysh TV, Bovin NV, Imberty A. Solution structure of two xenoantigens: alpha Gal-LacNAc and alpha Gal-Lewis X. Glycobiology 2002; 12: 241-50.
78. Maaheimo H, Renkonen R, Turunen JP, Penttila L, Renkonen O. Synthesis of a divalent sialyl Lewis x O-glycan, a potent inhibitor of lymphocyte-endothelium adhesion. Evidence that multivalency enhances the saccharide binding to 1-selectin. Eur. J. Biochem. 1995; 234: 616-25.
79. Mammen M, Choi S, Whitesides G. Polyvalent interactions in biological systems: implications for design and use of multivalent ligands and inhibitors. Angew. Chem. Int. Ed. 1998; 37: 2754-94.
80. Lee RT, Lee YC. Affinity enhancement by multivalent lectin-carbohydrate interaction. Glycoconj. J. 2000; 17: 543-51.
81. Renkonen O, Toppila S, Penttila L et al. Synthesis of a new nanomolar saccharide inhibitor of lymphocyte adhesion: different polylactosamine backbones present multiple sialyl Lewis x determinants to 1-selectin in high-affinity mode. Glycobiology 1997; 7: 453-61.
82. Bovin NV. Polyacrylamide-based glycoconjugates as tools in glycobiology. Glycoconj. J. 1998; 15: 431-46.
83. Kitov PI, Sadowska JM, Mulvey G et al. Shiga-like toxins are neutralized by tailored multivalent carbohydrate ligands. Nature 2000; 403: 669-72.
84. Fulton DA, Stoddart JF. Neoglycoconjugates based on cyclodextrins and calixarenes. Bioconjug. Chem. 2001; 12: 655-72.
85. Totani K, Kubota T, Kuroda T et al. Chemoenzymatic synthesis and application of glycopolymers containing multivalent sialyloligosaccharides with a poly (1-glutamic acid) backbone for inhibition of infection by influenza viruses. Glycobiology 2003; 13: 315-26.
86. Fan E, Zhongsheng Z, Minke WE, Hou Z, Verlinde CLMJ, Hol WGJ. High-affinity pentavalent ligands of Escherichia coli heat-labile enterotoxin by modular structure-based design. J. Am. Chem. Soc. 2000; 122: 2663-4.
87. Dam TK, Roy R, Das SK, Oscarson S, Brewer CF. Binding of multivalent carbohydrates to concanavalin A and Dioclea grandiflora lectin. Thermodynamic analysis of the 'multivalency effect'. J. Biol. Chem. 2000; 275: 14223-30.
88. Dam TK, Roy R, Page D, Brewer CF. Thermodynamic binding parameters of individual epitopes of multivalent carbohydrates to concanavalin a as determined by 'reverse' isothermal titration microcalorimetry. Biochemistry 2002; 41: 1359-63.
89. Gleason R, Murray J. Report from kidney transplant registry: analysis of variables in the function of human kidney transplants. Blood group compatibility and splenectomy. Transplantation 1967; 5: 343-59.
90. Porter KA. The effects of antibodies on human renal allografts. Transplant. Proc. 1976; 8: 189-97.
91. Brynger H, Rydberg L, Samuelsson B, Blohmé I, Lindholm A, Sandberg L. Renal transplantation across a blood group barrier: A2 kidneys to O recipients. Proc. Eur. Dial. Transplant. Assoc. 1982; 19: 427-31.
92. Alexandre G, Squifflet J, De Bruyére M et al. Splenectomy as a prerequisite for successful human ABO-incompatible renal transplantation. Transplant. Proc. 1985; 17: 138-43.
93. Alexandre G, Squifflet J, De Bruyére M et al. ABO-incompatible related and unrelated living donor renal allografts. Transplant. Proc. 1986; 18: 452-5.
94. Squifflet J-P, De Meyer M, Malaise J, Latinne D, Pirson Y, Alexandre GPJ. Lessons learned from ABO-incompatible living donor kidney transplantation: 20 years later. Exp. Clin. Transplant. 2004; 2: 208-13.
95. Welsh KI, van Dam M, Koffman CG et al. Transplantation of blood group A2 kidneys into O or B recipients: the effect of pretransplant anti-A titers on graft survival. Transplant. Proc. 1987; 19: 4565-7.
96. Tanabe K, Takahashi K, Agishi T, Toma H, Ota K. Removal of anti-A/B antibodies for successful kidney transplantation between ABO blood type incompatible couples. Transfus. Sci. 1996; 17: 455-62.
97. Stegall MD, Dean PG, Gloor JM. ABO-incompatible kidney transplantation. Transplantation 2004; 78: 635-40.
98. Sonnenday CJ, Warren DS, Cooper M et al. Plasmapheresis, CMV hyperimmune globulin, and anti-CD20 allow ABO-incompatible renal transplantation without splenectomy. Am. J. Transplant. 2004; 4: 1315-22.
99. Tyden G, Kumlien G, Genberg H, Sandberg J, Lundgren T, Fehrman I. ABO incompatible kidney transplantations without splenectomy, using antigen-specific immunoadsorption and rituximab. Am. J. Transplant. 2005; 5: 145-8.
100. Warren DS, Zachary AA, Sonnenday CJ et al. Successful renal transplantation across simultaneous ABO incompatible and positive crossmatch barriers. Am. J. Transplant. 2004; 4: 561-8.
101. Calne RY. Organ transplantation between widely disparate species. Transplant. Proc. 1970; 2: 550-6.
102. Auchincloss H, Sachs DH. Xenogeneic transplantation. Annu. Rev. Immunol 1998; 16: 433-70.
103. 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: 432-45.
104. Bannett AD, McAlack RF, Raja R, Baquero A, Morris M. Experiences with known ABO-mismatched renal transplants. Transplant. Proc. 1987; 19: 4543-6.
105. Winkler H, Ferran C, Bach FH. Accommodation of xenografts: a concept revisited. Xenotransplantation 1995; 2: 53-6.
106. Palmer A, Taube D, Welsh K, Bewick M, Gjorstrup P, Thick M. Removal of anti-HLA antibodies by extracorporeal immunoadsorption to enable renal transplantation. Lancet 1989; 1: 10-2.
107. Galili U. Immune response, accommodation, and tolerance to transplantation carbohydrate antigens. Transplantation 2004; 78: 1093-8.
108. Alexandre G, Gianello P, Latinne D et al. Plasmapheresis and splenectomy in experimental renal xenotransplantation. In: Hardy MA (ed.). Xenograft 25. Amsterdam: Elsevier Science Publishers, 1989: 259-66.
109. Bach FH, Turman MA, Vercellotti GM, Platt JL, Dalmasso AP. Accommodation: a working paradigm for progressing toward clinical discordant xenografting. Transplant. Proc. 1991; 23: 205-7.
110. Rydberg L, Hallberg EC, Bjorck S et al. Studies on the removal of anti-pig xenoantibodies in the human by plasmapheresis/ immunoadsorption. Xenotransplantation 1995; 2: 253-63.
111. Breimer ME, Björck S, Svalander CT et al. Extracorporeal ('ex vivo') connection of pig kidneys to humans. 1. Clinical data and studies of platelet destruction. Xenotransplantation 1996; 3: 328-39.
112. Cairns TD, Taube DH, Stevens N, Binns R, Welsh KI. Xenografts: future prospects for clinical transplantation. Immunol. Lett. 1991; 29: 167-70.
113. Leventhal JR, John R, Fryer JP et al. Removal of baboon and human antiporcine IgG and IgM natural antibodies by immunoadsorption. Results of in vitro and in vivo studies. Transplantation 1995; 59: 294-300.
114. Pascher A, Poehlein C, Stangl M et al. Application of immuno-apheresis for delaying hyperacute rejection during isolated xenogeneic pig liver perfusion. Transplantation 1997; 63: 867-75.
115. Lin SS, Weidner BC, Byrne GW et al. The role of antibodies in acute vascular rejection of pig-to-baboon cardiac transplants. J. Clin. Invest. 1998; 101: 1745-56.
116. Ramos A, Ruiz JC, de Francisco AL, Gomez-Fleitas M, Arias M. Removal of xenoreactive antibodies by protein-A immunoadsorption: experience in 22 patients. Xenotransplantation 2000; 7: 14-20.
117. Haas M, Bohmig GA, Leko-Mohr Z et al. Peri-operative immunoadsorption in sensitized renal transplant recipients. Nephrol. Dial. Transplant. 2002; 17: 1503-8.
118. Lemieux R. Human blood groups and carbohydrate chemistry. Chem. Soc. Rev. 1978; 7: 423-52.
119. Bensinger WI, Baker DA, Buckner CD, Clift RA, Thomas ED. Immunoadsorption for removal of A and B blood-group antibodies. N. Engl. J. Med. 1981; 304: 160-2.
120. Blomberg L, Bratt T, Chester MA, Hansson B. Improved removal of anti-A and anti-B antibodies from plasma using blood-group-active haptens. Vox. Sang. 1993; 65: 126-35.
121. 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: 666-72.
122. Mohacsi P, Rieben R, Sigurdsson G et al. Successful management of a B-type cardiac allograft into an O-type man with 3(1/2)-year clinical follow-up. Transplantation 2001; 72: 1328-30.
123. Pierson RN, Loyd JE, Goodwin A et al. Successful management of an ABO-mismatched lung allograft using antigen-specific immunoadsorption, complement inhibition, and immunomodulatory therapy. Transplantation 2002; 74: 79-84.
124. Rydberg L, Breimer ME, Brynger H, Samuelsson BE. ABO incompatible kidney transplantation (A2 to O). Qualitative and semi-quantitative studies on the humoral immune response against different blood group A antigens. Transplantation 1990; 49: 954-60.
125. Rydberg L, Breimer ME, Holgersson J et al. Characterisation of the anti-A antibody response following an ABO incompatible (A2 to O) kidney transplantation. Mol. Immunol. 1992; 29: 547-60.
126. Taniguchi S, Neethling FA, Korchagina EY et al. In vivo immunoadsorption of antipig antibodies in baboons using a specific Gal (alpha)1-3Gal column. Transplantation 1996; 62: 1379-84.
127. Lin SS, Kooyman DL, Daniels LJ et al. The role of natural anti-Gal alpha 1-3Gal antibodies in hyperacute rejection of pig-to-baboon cardiac xenotransplants. Transpl. Immunol. 1997; 5: 212-8.
128. 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 Galalpha1-3Galbeta1 4betaGlc-X immunoaffinity column. Transplantation 1998; 65: 172-9.
129. Liaigre J, Dubreuil D, Pradere JP, Bouhours JF. A novel synthesis of alpha-D-Galp-(1->3)-beta-D-Galp-1-O-(CH2) 3-NH2, its linkage to activated matrices and absorption of anti-alphaGal xenoantibodies by affinity columns. Carbohydr. Res. 2000; 325: 265-77.
130. Manez R, Domenech N, Centeno A et al. Failure to deplete anti-Galalpha1-3Gal antibodies after pig-to-baboon organ xenotransplantation by immunoaffinity columns containing multiple Galalpha1-3Gal oligosaccharides. Xenotransplantation 2004; 11: 408-15.
131. Karoor S, Molina J, Buchmann CR, Colton C, Logan JS, Henderson LW. Immunoaffinity removal of xenoreactive antibodies using modified dialysis or microfiltration membranes. Biotechnol. Bioeng. 2003; 81: 134-48.
132. Watts A, Foley A, Awwad M et al. Plasma perfusion by apheresis through a Gal immunoaffinity column successfully depletes anti-Gal antibody: experience with 320 aphereses in baboons. Xenotransplantation 2000; 7: 181-5.
133. 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: 32-4.
134. 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.
135. Perper RJ, Najarian JS. Experimental renal heterotransplantation. I. In widely divergent species. Transplantation 1966; 4: 377-88.
136. Linn BS, Jennsen JA, Portal P, Snyder GB. Renal xenograft prolongation by suppression of natural antibody. J. Surg. Res. 1968; 8: 211-3.
137. Romano EL, Soyano A, Linares J, Lauzon GJ. Neutralization of ABO blood group antibodies by specific oligosaccharides. Transplant. Proc. 1987; 19: 4426-30.
138. Romano EL, Soyano A, Linares J. Preliminary human study of synthetic trisaccharide representing blood substance A. Transplant. Proc. 1987; 19: 4475-8.
139. Cooper DKC, Ye Y, Neiekrasz M et al. Specific intravenous carbohydrate therapy. Transplantation 1993; 56: 769-77.
140. Neethling FA, Taniguchi S, Li SF et al. Roles of anti-alpha-Gal antibody and oligosaccharide therapy in xenotransplantation. In: Kemp E, Cooper DKC, Platt JL, White DJG (eds). Xenotransplantation: the Transplantation of Organs and Tissues Between Species. Berlin: Springer Verlag, 1997: 340-59.
141. Neethling FA, Koren E, Ye Y et al. Protection of pig kidney (PK15) cells from the cytotoxic effect of anti-pig antibodies by alpha-galactosyl oligosaccharides. Transplantation 1994; 57: 959-63.
142. Cairns T, Lee J, Goldberg L et al. Inhibition of the pig to human xenograft reaction, using soluble Gal alpha 1-3Gal and Gal alpha 1-3Gal beta 1-4GlcNAc. Transplantation 1995; 60: 1202-7.
143. Rieben R, Korchagina EY, von Allmen E et al. In vitro evaluation of the efficacy and biocompatibility of new, synthetic ABO immunoabsorbents. Transplantation 1995; 60: 425-30.
144. Galili U, Matta KL. Inhibition of anti-Gal IgG binding to porcine endothelial cells by synthetic oligosaccharides. Transplantation 1996; 62: 256-62.
145. Nagasaka T, Kobayashi T, Muramatsu H et al. alpha-Galactosyl oligosaccharides conjugated with polyethylene glycol as potential inhibitors of hyperacute rejection upon xenotransplantation. Biochem. Biophys. Res. Commun. 1997; 232: 731-6.
146. Neethling FA, Joziasse D, Bovin N, Cooper DK, Oriol R. The reducing end of alpha Gal oligosaccharides contributes to their efficiency in blocking natural antibodies of human and baboon sera. Transplant. Int. 1996; 9: 98-101.
147. Simon PM, Neethling FA, Taniguchi S et al. Intravenous infusion of Galalpha1-3Gal oligosaccharides in baboons delays hyperacute rejection of porcine heart xenografts. Transplantation 1998; 65: 346-53.
148. Rieben R, Bovin NV, Korchagina EY et al. Xenotransplantation: in vitro analysis of synthetic alpha-galactosyl inhibitors of human anti-Galalpha1- >3Gal IgM and IgG antibodies. Glycobiology 2000; 10: 141-8.
149. Magnusson S, Strokan V, Molne J, Nilsson K, Rydberg L, Breimer ME. Blocking of human anti-pig xenoantibodies by soluble GAL alpha 1-3Gal and Gal alpha 1-2Gal disaccharides; studies in a pig kidney in vitro perfusion model. Transpl. Int. 2000; 13: 402-12.
150. 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: 330-7.
151. Romano E, Neethling FA, Nilsson K et al. Intravenous synthetic alphaGal saccharides delay hyperacute rejection following pig-to-baboon heart transplantation. Xenotransplantation 1999; 6: 36-42.
152. Gollackner B, Knosalla C, Houser S et al. Pig kidney transplantation in baboons treated intravenously with a bovine serum albumin-Galalpha1-3Gal conjugate. Xenotransplantation 2003; 10: 606-14.
153. Byrne GW, Schwarz A, Fesi JR et al. Evaluation of different alpha-Galactosyl glycoconjugates for use in xenotransplantation. Bioconjug. Chem. 2002; 13: 571-81.
154. Diamond LE, Byrne GW, Schwarz A, Davis TA, Adams DH, Logan JS. Analysis of the control of the anti-gal immune response in a non-human primate by galactose alpha1-3 galactose trisaccharide-polyethylene glycol conjugate. Transplantation 2002; 73: 1780-7.
155. Katopodis AG, Warner RG, Duthaler RO et al. Removal of anti-Galalpha1,3Gal xenoantibodies with an injectable polymer. J. Clin. Invest. 2002; 110: 1869-77.
156. Teranishi K, Alwayn IP, Buhler L et al. Depletion of anti-Gal antibodies by the intravenous infusion of Gal type 2 and 6 glycoconjugates in baboons. Xenotransplantation 2003; 10: 357-67.
157. Zhong R, Luo Y, Yang H et al. Improvement in human decay accelerating factor transgenic porcine kidney xenograft rejection with intravenous administration of gas914, a polymeric form of alphaGAL. Transplantation 2003; 75: 10-9.
158. Lam TT, Hausen B, Boeke-Purkis K et al. Hyperacute rejection of hDAF-transgenic pig organ xenografts in cynomolgus monkeys: influence of pre-existing anti-pig antibodies and prevention by the alpha GAL glycoconjugate GAS914. Xenotransplantation 2004; 11: 517-24.
159. Houser SL, Kuwaki K, Knosalla C et al. Thrombotic microangiopathy and graft arteriopathy in pig hearts following transplantation into baboons. Xenotransplantation 2004; 11: 416-25.
160. Ling H, Boodhoo A, Hazes B et al. Structure of the shiga-like toxin I B-pentamer complexed with an analogue of its receptor Gb3. Biochemistry 1998; 37: 1777-88.
161. Liu J, Qian Y, Holgersson J. Removal of xenoreactive human anti-pig antibodies by absorption on recombinant mucin-containing glycoproteins carrying the Gal alpha1,3Gal epitope. Transplantation 1997; 63: 1673-82.
162. Liu J, Gustafsson A, Breimer ME, Kussak A, Holgersson J. Anti-pig antibody adsorption efficacy of {alpha}-Gal carrying recombinant P-selectin glycoprotein ligand-1/immunoglobulin chimeras increases with core 2 beta 1,6-N-acetylglucosaminyltransferase expression. Glycobiology 2004; 15: 571-83.
163. Liu J, Weintraub A, Holgersson J. Multivalent Galalpha1,3Gal-substitution makes recombinant mucin-immunoglobulins efficient absorbers of anti-pig antibodies. Xenotransplantation 2003; 10: 149-63.
164. Kudryashov V, Glunz PW, Williams LJ, Hintermann S, Danishefsky SJ, Lloyd KO. Toward optimized carbohydrate-based anti-cancer vaccines: epitope clustering, carrier structure, and adjuvant all influence antibody responses to Lewis(y) conjugates in mice. Proc. Natl Acad. Sci. USA 2001; 98: 3264-9.