Increased immunogenicity of human immunodeficiency virus gp120 engineered to express Galα1-3Galβ1-4GlcNAc-R epitopes

Journal of Virology

Volumn 80, Issue 14, 2006, Pages 6943-6951

  Abdel Motal, Ussama ^a   Wang, Shixia ^a   Lu, Shan ^a   Wigglesworth, Kim ^a   Galili, Uri ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 1,3 GALACTOSAMINE; ALPHA 1,3 GALACTOSYLTRANSFERASE; BETA 1,4 GALACTOSAMINE; EPITOPE; FC RECEPTOR; GALACTOSAMINE; GLYCOPROTEIN GP 120; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G; LIGAND; N ACETYLGLUCOSAMINE; NEUTRALIZING ANTIBODY; SIALIC ACID; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIGEN ANTIBODY COMPLEX; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; DRUG UPTAKE; ENZYME LINKED IMMUNOSPOT ASSAY; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNIZATION; IMMUNOGENICITY; KNOCKOUT MOUSE; LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; VACCINATION; VIRUS NEUTRALIZATION;

AIDS VACCINES; ANIMALS; ANTIBODY FORMATION; ANTIGEN-ANTIBODY COMPLEX; ANTIGEN-PRESENTING CELLS; CHO CELLS; CRICETINAE; CRICETULUS; GENE EXPRESSION; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HUMANS; IMMUNIZATION; IMMUNOGLOBULIN G; MICE; MICE, KNOCKOUT; POLYSACCHARIDES; PROTEIN ENGINEERING; RECEPTORS, IGG;

HUMAN IMMUNODEFICIENCY VIRUS;

EID: 33745785047     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00310-06     Document Type: Article

References (59)

1. Abdel-Motal, U. M., R. Friedline, B. Poligone, R. R. Pogue-Caley, J. A. Frelinger, and R. Tisch. 2001. Dendritic cell vaccination induces cross-reactive cytotoxic T lymphocytes specific for wild-type and natural variant human immunodeficiency virus type 1 epitopes in HLA-A*0201/Kb transgenic mice. Clin. Immunol. 101:51-58.
2. Abdel-Motal, U. M., J. Gillis, K. Manson, M. Wyand, D. Montefiori, K. Stefano-Cole, R. C. Montelaro, J. D. Altman, and R. P. Johnson. 2005. Kinetics of expansion of SIV Gag-specific CD8+ T lymphocytes following challenge of vaccinated macaques. Virology 333:226-238.
3. Berzofsky, J. A., J. D. Ahlers, J. Janik, J. Morris, S. Oh, M. Terabe, and I. M. Belyakov. 2004. Progress on new vaccine strategies against chronic viral infections. J. Clin. Investig. 114:450-462.
4. Buge, S. L., H. L. Ma, R. R. Amara, L. S. Wyatt, P. L. Earl, F. Villinger, D. C. Montefiori, S. I. Staprans, Y. Xu, E. Carter, S. P. O'Neil, J. G. Herndon, E. Hill, B. Moss, H. L. Robinson, and J. M. McNicholl. 2003. Gp120-alum boosting of a Gag-Pol-Env DNA/MVA AIDS vaccine: poorer control of a pathogenic viral challenge. AIDS Res. Hum. Retrovir. 19:891-900.
5. Burton, D. R., R. C. Desrosiers, R. W. Doms, W. C. Koff, P. D. Kwong, J. P. Moore, G. J. Nabel, J. Sodroski, I. A. Wilson, and R. T. Wyatt. 2004. HIV vaccine design and the neutralizing antibody problem. Nat. Immunol. 5:233-236.
6. Celis, E., and T. W. Chang. 1984. Antibodies to hepatitis B surface antigen potentiate the response of human T lymphocyte clones to the same antigen. Science 224:297-299.
7. Chen, Z. C., M. Tanemura, and U. Galili. 2001. Synthesis of α-gal epitopes (Galα1-3Galβ1-4GlcNAc-R) on human tumor cells by recombinant α1,3galactosyltransferase produced in Pichia pastoris. Glycobiology 11:577-586.
8. Clynes, R., Y. Takechi, Y. Moroi, A. Houghton, and J. V. Ravetch. 1998. Fc receptors are required in passive and active immunity to melanoma. Proc. Natl. Acad. Sci. USA 95:652-656.
9. Collins, B. H., A. H. Cotterell, K. R. McCurry, C. G. Alvarado, J. C. Magee, W. Parker, and J. L. Platt. 1995. Cardiac xenografts between primate species provide evidence for the importance of the α-galactosyl determinant in hyperacute rejection. J. Immunol. 154:5500-5510.
10. Galili, U. 1993. Evolution and pathophysiology of the human natural anti-α-galactosyl IgG (anti-Gal) antibody. Springer Semin. Immunopathol. 15: 155-171.
11. Galili, U. 1993. Interaction of the natural anti-Gal antibody with α-galactosyl epitopes: a major obstacle for xenotransplantation in humans. Immunol. Today 14:480-482.
12. Galili, U., M. R. Clark, S. B. Shohet, J. Buehler, and B. A. Macher. 1987. Evolutionary relationship between the natural anti-Gal antibody and the Gal α1-3Gal epitope in primates. Proc. Natl. Acad. Sci. USA 84:1369-1373.
13. Galili, U., and D. C. LaTemple. 1997. Natural anti-Gal antibody as a universal augmenter of autologous tumor vaccine immunogenicity. Immunol. Today 18:281-285.
14. Galili, U., D. C. LaTemple, and M. Z. Radic. 1998. A sensitive assay for measuring α-Gal epitope expression on cells by a monoclonal anti-Gal antibody. Transplantation 65:1129-1132.
15. Galili, U., B. A. Macher, J. Buehler, and S. B. Shohet. 1985. Human natural anti-α-galactosyl IgG. II. The specific recognition of α(1-3)-linked galactose residues. J. Exp. Med. 162:573-582.
16. Galili, U., E. A. Rachmilewitz, A. Peleg, and I. Flechner. 1984. A unique natural human IgG antibody with anti-α-galactosyl specificity. J. Exp. Med. 160:1519-1531.
17. Galili, U., P. M. Repik, F. Anaraki, K. Mozdzanowska, G. Washko, and W. Gerhard. 1996. Enhancement of antigen presentation of influenza virus hemagglutinin by the natural human anti-Gal antibody. Vaccine 14:321-328.
18. Galili, U., S. B. Shohet, E. Kobrin, C. L. Stults, and B. A. Macher. 1988. Man, apes, and Old World monkeys differ from other mammals in the expression of α-galactosyl epitopes on nucleated cells. J. Biol. Chem. 263: 17755-17762.
19. Geyer, H., C. Holschbach, G. Hunsmann, and J. Schneider. 1988. Carbohydrates of human immunodeficiency virus. Structures of oligosaccharides linked to the envelope glycoprotein 120. J. Biol. Chem. 263:11760-11767.
20. Good, A. H., D. K. Cooper, A. J. Malcolm, R. M. Ippolito, E. Koren, F. A. Neethling, Y. Ye, N. Zuhdi, and L. R. Lamontagne. 1992. Identification of carbohydrate structures that bind human antiporcine antibodies: implications for discordant xenografting in humans. Transplant. Proc. 24:559-562.
21. Gosselin, E. J., K. Wardwell, D. R. Gosselin, N. Alter, J. L. Fisher, and P. M. Guyre. 1992. Enhanced antigen presentation using human Fc gamma receptor (monocyte/macrophage)-specific immunogens. J. Immunol. 149:3477-3481.
22. Goulder, P. J., and D. I. Watkins. 2004. HIV and SIV CTL escape: implications for vaccine design. Nat. Rev. Immunol. 4:630-640.
23. Hamadeh, R. M., U. Galili, P. Zhou, and J. M. Griffiss. 1995. Anti-α-galactosyl immunoglobulin A (IgA), IgG, and IgM in human secretions. Clin. Diagn. Lab. Immunol. 2:125-131.
24. Henion, T. R., W. Gerhard, F. Anaraki, and U. Galili. 1997. Synthesis of α-gal epitopes on influenza virus vaccines, by recombinant α1,3galactosyltransferase, enables the formation of immune complexes with the natural anti-Gal antibody. Vaccine 15:1174-1182.
25. Henion, T. R., B. A. Macher, F. Anaraki, and U. Galili. 1994. Defining the minimal size of catalytically active primate α1,3 galactosyltransferase: structure-function studies on the recombinant truncated enzyme. Glycobiology 4:193-201.
26. Houston, W. E., R. J. Kremer, C. L. Crabbs, and R. O. Spertzel. 1977. Inactivated Venezuelan equine encephalomyelitis virus vaccine complexed with specific antibody: enhanced primary immune response and altered pattern of antibody class elicited. J. Infect. Dis. 135:600-610.
27. Kwong, P. D., M. L. Doyle, D. J. Casper, C. Cicala, S. A. Leavitt, S. Majeed, T. D. Steenbeke, M. Venturi, I. Chaiken, M. Fung, H. Katinger, P. W. Parren, J. Robinson, D. Van Ryk, L. Wang, D. R. Burton, E. Freire, R. Wyatt, J. Sodroski, W. A. Hendrickson, and J. Arthos. 2002. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420:678-682.
28. LaTemple, D. C., J. T. Abrams, S. Y. Zhang, and U. Galili. 1999. Increased immunogenicity of tumor vaccines complexed with anti-Gal: studies in knockout mice for α1,3galactosyltransferase. Cancer Res. 59:3417-3423.
29. LaTemple, D. C., and U. Galili. 1998. Adult and neonatal anti-Gal response in knock-out mice for α1,3galactosyltransferase. Xenotransplantation 5:191-196.
30. Leonard, C. K., M. W. Spellman, L. Riddle, R. J. Harris, J. N. Thomas, and T. J. Gregory. 1990. Assignment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant human immunodeficiency virus envelope glycoprotein (gp120) expressed in Chinese hamster ovary cells. J. Biol. Chem. 265:10373-10382.
31. Letvin, N. L. 2005. Progress toward an HIV vaccine. Annu. Rev. Med. 56:213-223.
32. Manca, F., D. Fenoglio, G. Li Pira, A. Kunkl, and F. Celada. 1991. Effect of antigen/antibody ratio on macrophage uptake, processing, and presentation to T cells of antigen complexed with polyclonal antibodies. J. Exp. Med. 173:37-48.
33. Manches, O., J. Plumas, G. Lui, L. Chaperot, J. P. Molens, J. J. Sotto, J. C. Bensa, and U. Galili. 2005. Anti-Gal-mediated targeting of human B lymphoma cells to antigen-presenting cells: a potential method for immunotherapy using autologous tumor cells. Haematologica 90:625-634.
34. Mizuochi, T., T. J. Matthews, M. Kato, J. Bamako, K. Titani, J. Solomon, and T. Feizi. 1990. Diversity of oligosaccharide structures on the envelope glycoprotein gp 120 of human immunodeficiency virus 1 from the lymphoblastoid cell line H9. Presence of complex-type oligosaccharides with bisecting N-acetylglucosamine residues. J. Biol. Chem. 265:8519-8524.
35. Mohiuddin, M. M., H. Ogawa, D. P. Yin, and U. Galili. 2003. Tolerance induction to a mammalian blood group-like carbohydrate antigen by syngeneic lymphocytes expressing the antigen. II. Tolerance induction on memory B cells. Blood 102:229-236.
36. Mohiuddin, M. M., H. Ogawa, D. P. Yin, J. Shen, and U. Galili. 2003. Antibody-mediated accommodation of heart grafts expressing an incompatible carbohydrate antigen. Transplantation 75:258-262.
37. Montefiori, D. C., G. Pantaleo, L. M. Fink, J. T. Zhou, J. Y. Zhou, M. Bilska, G. D. Miralles, and A. S. Fauci. 1996. Neutralizing and infection-enhancing antibody responses to human immunodeficiency virus type 1 in long-term nonprogressors. J. Infect. Dis. 173:60-67.
38. Ogawa, H., M. M. Mohiuddin, D. P. Yin, J. Shen, A. S. Chong, and U. Galili. 2004. Mouse-heart grafts expressing an incompatible carbohydrate antigen. II. Transition from accommodation to tolerance. Transplantation 77:366-373.
39. Ogawa, H., D. P. Yin, J. Shen, and U. Galili. 2003. Tolerance induction to a mammalian blood group-like carbohydrate antigen by syngeneic lymphocytes expressing the antigen. Blood 101:2318-2320.
40. Pantaleo, G., and R. A. Koup. 2004. Correlates of immune protection in HIV-1 infection: what we know, what we don't know, what we should know. Nat. Med. 10:806-810.
41. Pincus, S. H., K. Wehrly, E. Tschachler, S. F. Hayes, R. S. Buller, and M. Reitz. 1990. Variants selected by treatment of human immunodeficiency virus-infected cells with an immunotoxin. J. Exp. Med. 172:745-757.
42. Rafiq, K., A. Bergtold, and R. Clynes. 2002. Immune complex-mediated antigen presentation induces tumor immunity. J. Clin. Investig. 110:71-79.
43. Ravindran, B., A. K. Satapathy, and M. K. Das. 1988. Naturally-occurring anti-α-galactosyl antibodies in human Plasmodium falciparum infections-a possible role for autoantibodies in malaria. Immunol. Lett. 19:137-141.
44. Regnault, A., D. Lankar, V. Lacabanne, A. Rodriguez, C. Thery, M. Rescigno, T. Saito, S. Verbeek, C. Bonnerot, P. Ricciardi-Castagnoli, and S. Amigorena. 1999. Fcγ receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization. J. Exp. Med. 189:371-380.
45. Sandrin, M. S., H. A. Vaughan, P. L. Dabkowski, and I. F. McKenzie. 1993. Anti-pig IgM antibodies in human serum react predominantly with Gal(α1-3)Gal epitopes. Proc. Natl. Acad. Sci. USA 90:11391-11395.
46. Schuurhuis, D. H., A. Ioan-Facsinay, B. Nagelkerken, J. J. van Schip, C. Sedlik, C. J. Melief, J. S. Verbeek, and F. Ossendorp. 2002. Antigen-antibody immune complexes empower dendritic cells to efficiently prime specific CD8+ CTL responses in vivo. J. Immunol. 168:2240-2246.
47. Stager, S., J. Alexander, A. C. Kirby, M. Botto, N. V. Rooijen, D. F. Smith, F. Brombacher, and P. M. Kaye. 2003. Natural antibodies and complement are endogenous adjuvants for vaccine-induced CD8+ T-cell responses. Nat. Med. 9:1287-1292.
48. Tanemura, M., and U. Galili. 2000. Identification of B cells with receptors for α-Gal epitopes (Galα1-3Galβ1-4GlcNAc-R) in xenograft recipients. Transplant. Proc. 32:857-858.
49. Tanemura, M., H. Ogawa, D. P. Yin, Z. C. Chen, V. J. DiSesa, and U. Galili. 2002. Elimination of anti-Gal B cells by α-Gal ricin 1. Transplantation 73:1859-1868.
50. Tanemura, M., D. Yin, A. S. Chong, and U. Galili. 2000. Differential immune responses to α-gal epitopes on xenografts and allografts: implications for accommodation in xenotransplantation. J. Clin. Investig. 105:301-310.
51. Tearle, R. G., M. J. Tange, Z. L. Zannettino, M. Katerelos, T. A. Shinkel, B. J. Van Denderen, A. J. Lonie, I. Lyons, M. B. Nottle, T. Cox, C. Becker, A. M. Peura, P. L. Wigley, R. J. Crawford, A. J. Robins, M. J. Pearse, and A. J. d'Apice. 1996. The α-1,3-galactosyltransferase knockout mouse. Implications for xenotransplantation. Transplantation 61:13-19.
52. Thall, A. D., P. Maly, and J. B. Lowe. 1995. Oocyte Gal α1,3Gal epitopes implicated in sperm adhesion to the zona pellucida glycoprotein ZP3 are not required for fertilization in the mouse. J. Biol. Chem. 270:21437-21440.
53. Thomson, M. M., L. Perez-Alvarez, and R. Najera. 2002. Molecular epidemiology of HIV-1 genetic forms and its significance for vaccine development and therapy. Lancet Infect. Dis. 2:461-471.
54. Unkeless, J. C. 1989. Function and heterogeneity of human Fc receptors for immunoglobulin G. J. Clin. Investig. 83:355-361.
55. Villinger, F., A. E. Mayne, P. Bostik, K. Mori, P. E. Jensen, R. Ahmed, and A. A. Ansari. 2003. Evidence for antibody-mediated enhancement of simian immunodeficiency virus (SIV) Gag antigen processing and cross presentation in SIV-infected rhesus macaques. J. Virol. 77:10-24.
56. Wang, S., J. Arthos, J. M. Lawrence, D. Van Ryk, I. Mboudjeka, S. Shen, T. H. Chou, D. C. Montefiori, and S. Lu. 2005. Enhanced immunogenicity of gp120 protein when combined with recombinant DNA priming to generate antibodies that neutralize the JR-FL primary isolate of human immunodeficiency virus type 1. J. Virol. 79:7933-7937.
57. Watier, H., J. M. Guillaumin, I. Vallée, G. Thibault, Y. Gruel, Y. Lebranchu, and P. Bardos. 1996. Human NK cell-mediated direct and IgG-dependent cytotoxicity against xenogeneic porcine endothelial cells. Transplant Immunol. 4:293-299.
58. Wei, X., J. M. Decker, S. Wang, H. Hui, J. C. Kappes, X. Wu, J. F. Salazar-Gonzalez, M. G. Salazar, J. M. Kilby, M. S. Saag, N. L. Komarova, M. A. Nowak, B. H. Hahn, P. D. Kwong, and G. M. Shaw. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
59. Wood, C., E. A. Rabat, L. A. Murphy, and I. J. Goldstein. 1979. Immunochemical studies of the combining sites of the two isolectins, A4 and B4, isolated from Bandeiraea simplicifolia. Arch. Biochem. Biophys. 198:1-11.