Immunogenicity of influenza virus vaccine is increased by anti-gal-mediated targeting to antigen-presenting cells

Journal of Virology

Volumn 81, Issue 17, 2007, Pages 9131-9141

  Abdel Motal, Ussama M ^a   Guay, Heath M ^a   Wigglesworth, Kim ^a   Welsh, Raymond M ^a   Galili, Uri ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; CARBOHYDRATE; CD4 ANTIGEN; CYTOKINE; EPITOPE; FC RECEPTOR; GALACTOSAMINE; IMMUNOGLOBULIN; IMMUNOGLOBULIN G; INFLUENZA VACCINE; VIRUS HEMAGGLUTININ;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY TITER; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; ENZYME ENGINEERING; ENZYME GLYCOSYLATION; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; IMMUNE RESPONSE; IMMUNOGENICITY; INFLUENZA VIRUS A; INTERNALIZATION; LYMPH NODE; MALE; NONHUMAN; OPSONIZATION; PRIORITY JOURNAL; SYNTHESIS; T LYMPHOCYTE ACTIVATION; VIRUS ENVELOPE; VIRUS STRAIN;

ANIMALS; ANTIBODIES, VIRAL; ANTIGEN-PRESENTING CELLS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; DISEASE MODELS, ANIMAL; DRUG DELIVERY SYSTEMS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HEMAGGLUTINATION INHIBITION TESTS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; INFLUENZA, HUMAN; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SURVIVAL ANALYSIS; TRISACCHARIDES;

AVES; MAMMALIA; MUS; ORTHOMYXOVIRIDAE;

EID: 34548157925     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00647-07     Document Type: Article

References (46)

1. Abdel-Motal, U., S. Wang, S. Lu, K. Wigglesworth, and U. Galili. 2006. Increased immunogenicity of human immunodeficiency virus gp120 engineered to express Galα1-3Galβ1-4GlcNAc-R epitopes. J. Virol. 80:6943-6951.
2. Bottrel, R. L. A., W. O. Dutra, F. A. Martins, B. Gontijo, E. Carvalho, M. Barral-Netto, A. Barral, R. P. Almeida, W. Mayrink, R. Locksley, and K. J. Gollob. 2001. Flow cytometric determination of cellular sources and frequencies of key cytokine-producing lymphocytes directed against recombinant LACK and soluble Leishmania antigen in human cutaneous leishmaniasis. Infect. Immun. 69:3232-3239.
3. 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.
4. Chen, Z. C., M. Tanemura, and U. Galili. 2001. Synthesis of α-Gal epitopes (Ga1α1-3Galβ1-4GlcNAc-R) on human tumor cells by recombinant α1,3galactosyltransferase produced in Pichia pastoris. Glycobiology 11:577-586.
5. 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.
6. 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.
7. Couch, R. B., W. A. Keitel, and T. R. Cate. 1997. Improvement of inactivated influenza virus vaccines. J Infect. Dis. 176(Suppl. 1):S38-S44.
8. Deriy, L., H. Ogawa, G. P. Gao, and U. Galili. 2005. In vivo targeting of vaccinating tumor cells to antigen-presenting cells by a gene therapy method with adenovirus containing the α1,3galactosyltransferase gene. Cancer Gene Ther. 12:528-539.
9. Fanger, N. A., K. Wardwell, L. Shen, T. F. Tedder, and P. M. Guyre. 1996. Type I (CD64) and type II (CD32) Fc gamma receptor-mediated phagocytosis by human blood dendritic cells. J. Immunol. 157:541-548.
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., J. Buehler, S. B. Shohet, and B. A. Macher. 1987. The human natural anti-Gal IgG. III. The subtlety of immune tolerance in man as demonstrated by crossreactivity between natural anti-Gal and anti-B antibodies. J. Exp. Med. 165:693-704.
13. 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 Galα1→3Gal epitope in primates. Proc. Natl. Acad. Sci. USA 84:1369-1373.
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., R. E. Mandrell, R. M. Hamadeh, S. B. Shohet, and J. M. Griffiss. 1988. Interaction between human natural anti-α-Galactosyl immunoglobulin G and bacteria of the human flora. Infect. Immun. 56:1730-1737.
17. 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.
18. 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.
19. 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.
20. Galili, U., and K. Swanson. 1991. Gene sequences suggest inactivation of α-1,3-Galactosyltransferase in catarrhines after the divergence of apes from monkeys. Proc. Natl. Acad. Sci. USA 88:7401-7404.
21. 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.
22. 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.
23. 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.
24. Joziasse, D. H., J. H. Shaper, D. H. Van den Eijnden, A. J. Van Tunen, and N. L. Shaper. 1989. Bovine α1-3-Galactosyltransferase: isolation and characterization of a cDNA clone. Identification of homologous sequences in human genomic DNA. J. Biol. Chem. 264:14290-14297.
25. Katz, J. M., J. Plowden, M. Renshaw-Hoelscher, X. Lu, T. M. Tumpey, and S. Sambhara. 2004. Immunity to influenza: the challenges of protecting an aging population. Immunol. Res. 29:113-124.
26. Keil, W., R. Geyer, J. Dabrowski, U. Dabrowski, H. Niemann, S. Stirm, and H. D. Klenk. 1985. Carbohydrates of influenza virus. Structural elucidation of the individual glycans of the FPV hemagglutinin by two-dimensional 1H n.m.r. and methylation analysis. EMBO J. 4:2711-2720.
27. Koike, C., J. J. Fung, D. A. Geller, R. Kannagi, T. Libert, P. Luppi, I. Nakashima, J. Profozich, W. Rudert, S. B. Sharma, T. E. Starzl, and M. Trucco. 2002. Molecular basis of evolutionary loss of the α1,3-Galactosyltransferase gene in higher primates. J. Biol. Chem. 277:10114-10120.
28. Lanteri, M., V. Giordanengo, F. Vidal, P. Gaudray, and J. C. Lefebvre. 2002. A complete α,3-Galactosyltransferase gene is present in the human genome and partially transcribed. Glycobiology 12:785-792.
29. Larsen, R. D., C. A. Rivera-Marrero, L. K. Ernst, R. D. Cummings, and J. B. Lowe. 1990. Frameshift and nonsense mutations in a human genomic sequence homologous to a murine UDP-Gal:β-D-Gal(1,4)-D- GlcNAc α(1,3)-Galactosyltransferase cDNA. J. Biol. Chem. 265:7055-7061.
30. 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.
31. 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.
32. Matsumoto, A., H. Yoshima, and A. Kobata. 1983. Carbohydrates of influenza virus hemagglutinin: structures of the whole neutral sugar chains. Biochemistry 22:188-196.
33. 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.
34. 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.
35. + CTL responses in vivo. J. Immunol. 168:2240- 2246.
36. Shen, Z., G. Reznikoff, G. Dranoff, and K. L. Rock. 1997. Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules. J. Immunol. 158:2723-2730.
37. Skehel, J. J., and M. D. Waterfield. 1975. Studies on the primary structure of the influenza virus hemagglutinin. Proc. Natl. Acad. Sci. USA 72:93-97.
38. Smith, D. F., R. D. Larsen, S. Mattox, J. B. Lowe, and R. D. Cummings. 1990. Transfer and expression of a murine UDP-Gal:β-D- Gal-α1,3-Galactosyltransferase gene in transfected Chinese hamster ovary cells. Competition reactions between the α1,3-Galactosyltransferase and the endogenous α2,3-sialyltransferase. J. Biol. Chem. 265:6225-6234.
39. 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. Transplantation 73:1859-1868.
40. 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.
41. 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.
42. 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.
43. Unkeless, J. C. 1989. Function and heterogeneity of human Fc receptors for immunoglobulin G. J. Clin. Investig. 83:355-361.
44. 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.
45. Webster, R. G. 2000. Immunity to influenza in the elderly. Vaccine 18:1686-1689.
46. Zinkernagel, R. M., S. Ehl, P. Aichele, S. Oehen, T. Kundig, and H. Hengartner. 1997. Antigen localisation regulates immune responses in a dose- and time-dependent fashion: a geographical view of immune reactivity. Immunol. Rev. 156:199-209.