Human complement-activating immunoglobulin (Ig)G3 antibodies are essential for porcine endothelial cell activation

Xenotransplantation

Volumn 13, Issue 3, 2006, Pages 215-223

  Sæthre, Marit ^a   Lea, Tor ^a   Borgen, Merethe S ^a   Fiane, Arnt E ^a   Michaelsen, Terje E ^b,c   Thorsby, Erik ^a   Haraldsen, Guttorm ^a   Mollnes, Tom E ^a  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

Acute vascular rejection; Complement system; Immunoglobulin; Porcine endothelial cell

Indexed keywords

IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN G4;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CORRELATION ANALYSIS; ENDOTHELIUM CELL; FLOW CYTOMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; WESTERN BLOTTING;

ANIMALS; AORTA; CELL CULTURE TECHNIQUES; COMPLEMENT ACTIVATION; COMPLEMENT INACTIVATING AGENTS; DISACCHARIDES; E-SELECTIN; ENDOTHELIUM, VASCULAR; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GRAFT REJECTION; GUANIDINES; GUINEA PIGS; HUMANS; IMMUNOGLOBULIN G; PRIMATES; STAPHYLOCOCCAL PROTEIN A; SWINE; TRANSPLANTATION, HETEROLOGOUS;

EID: 33744773774     PISSN: 0908665X     EISSN: 13993089     Source Type: Journal    
DOI: 10.1111/j.1399-3089.2006.00289.x     Document Type: Article

References (49)

1. Hammer C Thein E. Physiological aspects of xenotransplantation, 2001. Xenotransplantation 2002 9 : 303.
2. 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.
3. Galili U. Evolution and pathophysiology of the human natural anti-alpha-galactosyl IgG (anti-Gal) antibody. Springer Semin Immunopathol 1993 15 : 155.
4. Galili U. The alpha-gal epitope (Gal alpha 1-3Gal beta 1-4GlcNAc-R) in xenotransplantation. Biochimie 2001 83 : 557.
5. Parker W Bruno D Holzknecht ZE Platt JL. Characterization and affinity isolation of xenoreactive human natural antibodies. J Immunol 1994 153 : 3791.
6. Johnston PS Wang MW Lim SM Wright LJ White DJ. Discordant xenograft rejection in an antibody-free model. Transplantation 1992 54 : 573.
7. Dalmasso AP Vercellotti GM Fischel RJ Bolman RM Bach FH Platt JL. Mechanism of complement activation in the hyperacute rejection of porcine organs transplanted into primate recipients. Am J Pathol 1992 140 : 1157.
8. 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. Lucchiari N Azimzadeh A Wolf P Regnault V Cinqualbre J. In vivo and in vitro optimization of depletion of IgM and IgG xenoantibodies by immunoadsorption using cell membrane proteins. Artif Organs 1997 21 : 278.
10. 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.
11. Cozzi E White DJ. The generation of transgenic pigs as potential organ donors for humans. Nat Med 1995 1 : 964.
12. Bach FH Winkler H Ferran C Hancock WW Robson SC. Delayed xenograft rejection. Immunol Today 1996 17 : 379.
13. Platt JL Lin SS McGregor CG. Acute vascular rejection. Xenotransplantation 1998 5 : 169.
14. 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.
15. Dorling A. Are anti-endothelial cell antibodies a pre-requisite for the acute vascular rejection of xenografts? Xenotransplantation 2003 10 : 16.
16. Saadi S Platt JL. Role of complement in xenotransplantation. Clin Exp Pharmacol Physiol 1999 26 : 1016.
17. Loss M Vangerow B Schmidtko J et al. Acute vascular rejection is associated with systemic complement activation in a pig-to-primate kidney xenograft model. Xenotransplantation 2000 7 : 186.
18. Zaidi A Schmoeckel M Bhatti F et al. Life-supporting pig-to-primate renal xenotransplantation using genetically modified donors. Transplantation 1998 65 : 1584.
19. Vangerow B Hecker JM Lorenz R et al. C1-Inhibitor for treatment of acute vascular xenograft rejection in cynomolgus recipients of h-DAF transgenic porcine kidneys. Xenotransplantation 2001 8 : 266.
20. Davis EA Pruitt SK Greene PS et al. Inhibition of complement, evoked antibody, and cellular response prevents rejection of pig-to-primate cardiac xenografts. Transplantation 1996 62 : 1018.
21. Selvan RS Kapadia HB Platt JL. Complement-induced expression of chemokine genes in endothelium: regulation by IL-1-dependent and -independent mechanisms. J Immunol 1998 161 : 4388.
22. Saadi S Holzknecht RA Patte CP Platt JL. Endothelial cell activation by pore-forming structures: pivotal role for interleukin-1alpha. Circulation 2000 101 : 1867.
23. Solvik UO Haraldsen G Fiane AE et al. Human serum-induced expression of E-selectin on porcine aortic endothelial cells in vitro is totally complement mediated. Transplantation 2001 72 : 1967.
24. Saethre M Solvik UO Haraldsen G et al. Human serum-induced porcine endothelial cell E-selectin expression is associated with IgG3 and IgM anti-Gal antibodies. Xenotransplantation 2002 9 : 350.
25. Sahu A Lambris JD. Structure and biology of complement protein C3, a connecting link between innate and acquired immunity. Immunol Rev 2001 180 : 35.
26. McMorrow IM Comrack CA Sachs DH DerSimonian H. Heterogeneity of human anti-pig natural antibodies cross-reactive with the Gal(alpha1,3)Galactose epitope. Transplantation 1997 64 : 501.
27. Galili U Rachmilewitz EA Peleg A Flechner I. A unique natural human IgG antibody with anti-alpha-galactosyl specificity. J Exp Med 1984 160 : 1519.
28. Barreau N Blancho G Boulet C et al. Natural anti-Gal antibodies constitute 0.2% of intravenous immunoglobulin and are equally retained on a synthetic disaccharide column or on an immobilized natural glycoprotein. Transplant Proc 2000 32 : 882.
29. Chiang TR Fanget L Gregory R et al. Anti-Gal antibodies in humans and 1,3alpha-galactosyltransferase knock-out mice. Transplantation 2000 69 : 2593.
30. 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.
31. Gerber B Tinguely C Bovin NV Rieben R Nydegger UE. Differences between synthetic oligosaccharide immunoabsorbents in depletion capacity for xenoreactive anti-Galalpha1-3Gal antibodies from human serum. Xenotransplantation 2001 8 : 106.
32. Phelps CJ Koike C Vaught TD et al. Production of alpha 1,3-galactosyltransferase-deficient pigs. Science 2003 299 : 411.
33. Lai L Kolber-Simonds D Park KW et al. Production of alpha-1,3- galactosyltransferase knockout pigs by nuclear transfer cloning. Science 2002 295 : 1089.
34. 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.
35. 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.
36. Baumann BC Forte P Hawley RJ Rieben R Schneider MK Seebach JD. Lack of galactose-alpha-1,3-galactose expression on porcine endothelial cells prevents complement-induced lysis but not direct xenogeneic NK cytotoxicity. J Immunol 2004 172 : 6460.
37. Michaelsen TE Frangione B Franklin EC. Primary structure of the "hinge" region of human IgG3. Probable quadruplication of a 15-amino acid residue basic unit. J Biol Chem 1977 252 : 883.
38. Ishizaka T Ishizaka K Salmon S Fudenberg H. Biologic activities of aggregated gamma-globulin. 8. Aggregated immunoglobulins of different classes. J Immunol 1967 99 : 82.
39. Schumaker VN Calcott MA Spiegelberg HL Muller-Eberhard HJ. Ultracentifuge studies of the binding of IgG of different subclasses to the Clq subunit of the first component of complement. Biochemistry 1976 15 : 5175.
40. Michaelsen TE Garred P Aase A. Human IgG subclass pattern of inducing complement-mediated cytolysis depends on antigen concentration and to a lesser extent on epitope patchiness, antibody affinity and complement concentration. Eur J Immunol 1991 21 : 11.
41. Michaelsen TE Ihle O Beckstrom KJ et al. Binding properties and anti-bacterial activities of V-region identical, human IgG and IgM antibodies, against group B Neisseria meningitidis. Biochem Soc Trans 2003 31 : 1032.
42. Yu PB Parker W Everett ML Fox IJ Platt JL. Immunochemical properties of anti-Gal alpha 1-3Gal antibodies after sensitization with xenogeneic tissues. J Clin Immunol 1999 19 : 116.
43. Yu PB Holzknecht ZE Bruno D Parker W Platt JL. Modulation of natural IgM binding and complement activation by natural IgG antibodies: a role for IgG anti-Gal alpha1-3Gal antibodies. J Immunol 1996 157 : 5163.
44. Yin D Zeng H Ma L et al. Cutting edge: NK cells mediate IgG1-dependent hyperacute rejection of xenografts. J Immunol 2004 172 : 7235.
45. Michaelsen TE Kolberg J Aase A Herstad TK Hoiby EA. The four mouse IgG isotypes differ extensively in bactericidal and opsonophagocytic activity when reacting with the P1.16 epitope on the outer membrane PorA protein of neisseria meningitidis. Scand J Immunol 2004 59 : 34.
46. Fujii S Hitomi Y. New synthetic inhibitors of C1r, C1 esterase, thrombin, plasmin, kallikrein and trypsin. Biochim Biophys Acta 1981 661 : 342.
47. Ikari N Sakai Y Hitomi Y Fujii S. New synthetic inhibitor to the alternative complement pathway. Immunology 1983 49 : 685.
48. Miyagawa S Shirakura R Matsumiya G et al. Prolonging discordant xenograft survival with anticomplement reagents K76COOH and FUT175. Transplantation 1993 55 : 709.
49. Blum MG Collins BJ Chang AC Zhang JP Knaus SA Pierson RN III.. Complement inhibition by FUT-175 and K76-COOH in a pig-to-human lung xenotransplant model. Xenotransplantation 1998 5 : 35.