A pilot study showing differences in glycosylation patterns of igg subclasses induced by pneumococcal, meningococcal, and two types of influenza vaccines

Immunity, Inflammation and Disease

Volumn 2, Issue 2, 2014, Pages 76-91

  Vestrheim, Anne Cathrine ^a,b   Moen, Anders ^b   Egge Jacobsen, Wolfgang ^b   Reubsaet, Leon ^b   Halvorsen, Trine Grønhaug ^b   Bratlie, Diane Bryant ^a   Paulsen, Berit Smestad ^b   Michaelsen, Terje Einar ^a,b  

^a NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

Antibodies; Human and glycosylation; Immunology; Vaccination

Indexed keywords

EID: 84973233335     PISSN: None     EISSN: 20504527     Source Type: Journal    
DOI: 10.1002/iid3.22     Document Type: Article

References (69)

1. Wang, S. M., M. H. Tsai, H. Y. Lei, J. R. Wang, C. C. Liu, 2012. The regulatory T cells in anti-influenza antibody response post influenza vaccination. Hum. Vaccin. Immunother. 8 (9):1243–1249.
2. Treanor, J. J., H. K. Talbot, S. E. Ohmit, L. A. Coleman, M. G. Thompson, P. Y. Cheng, et al. 2012. Effectiveness of seasonal influenza vaccines in the United States during a season with circulation of all three vaccine strains. Clin. Infect. Dis.
3. Westerink, M. A., H. W. Schroeder, Jr., M. H. Nahm, 2012. Immune Responses to pneumococcal vaccines in children and adults: rationale for age-specific vaccination. Aging Dis. 3 (1):51–67.
4. Nimmerjahn, F., J. V. Ravetch, 2008. Anti-inflammatory actions of intravenous immunoglobulin. Annu. Rev. Immunol. 26:513–533.
5. Anthony, R. M., F. Nimmerjahn, D. J. Ashline, V. N. Reinhold, J. C. Paulson, J. V. Ravetch, 2008. Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc. Science 320(5874):373–376.
6. Matsumoto, A., K. Shikata, F. Takeuchi, N. Kojima, T. Mizuochi, 2000. Autoantibody activity of IgG rheumatoid factor increases with decreasing levels of galactosylation and sialylation. J. Biochem. 128(4):621–628.
7. Arnold, J. N., M. R. Wormald, R. B. Sim, P. M. Rudd, R. A. Dwek, 2007. The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu. Rev. Immunol. 25:21–50.
8. Karsten, C. M., M. K. Pandey, J. Figge, R. Kilchenstein, P. R. Taylor, M. Rosas, et al. 2012. Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of FcgammaRIIB and dectin-1. Nat. Med. 18(9):1401–1406.
9. Shinkawa, T., K. Nakamura, N. Yamane, E. Shoji-Hosaka, Y. Kanda, M. Sakurada, et al. 2003. The absence of fucose but not the presence of galactose or bisecting N-acetylglucos-amine of human IgG1 complex-type oligosaccharides shows the critical role of enhancing antibody-dependent cellular cytotoxicity. J. Biol. Chem. 278(5):3466–3473.
10. Shields, R. L., J. Lai, R. Keck, L. Y. O’Connell, K. Hong, Y. G. Meng, S. H. Weikert, L. G. Presta, 2002. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J. Biol. Chem. 277(30):26733–26740.
11. Aase, A., T. E. Michaelsen, 1994. Opsonophagocytic activity induced by chimeric antibodies of the four human IgG subclasses with or without help from complement. Scand. J. Immunol. 39(6):581–587.
12. Hall, M. A., M. S. Edwards, C. J. Baker, 1992. Complement and antibody participation in opsonophagocytosis of type IV and V group B streptococci. Infect. Immun. 60(12):5030– 5035.
13. Raju, T. S., J. B. Briggs, S. M. Borge, A. J. Jones, 2000. Species-specific variation in glycosylation of IgG: evidence for the species-specific sialylation and branch-specific galactosylation and importance for engineering recombinant glycopro-tein therapeutics. Glycobiology 10(5):477–486.
14. Davies, J., L. Jiang, L. Z. Pan, M. J. LaBarre, D. Anderson, M. Reff, 2001. Expression of GnTIII in a recombinant anti-CD20 CHO production cell line: expression of antibodies with altered glycoforms leads to an increase in ADCC through higher affinity for FC gamma RIII. Biotechnol. Bioeng. 74 (4):288–294.
15. Hodoniczky, J., Y. Z. Zheng, D. C. James, 2005. Control of recombinant monoclonal antibody effector functions by Fc N-glycan remodeling in vitro. Biotechnol. Prog. 21(6):1644– 1652.
16. Lastra, G. C., S. J. Thompson, A. S. Lemonidis, C. J. Elson, 1998. Changes in the galactose content of IgG during humoral immune responses. Autoimmunity 28(1):25–30.
17. Guo, N., Y. Liu, Y. Masuda, M. Kawagoe, Y. Ueno, T. Kameda, T. Sugiyama, 2005. Repeated immunization induces the increase in fucose content on antigen-specific IgG N-linked oligosaccharides. Clin. Biochem. 38(2):149– 153.
18. Selman, M. H., S. E. de Jong, D. Soonawala, F. P. Kroon, A. A. Adegnika, A. M. Deelder, C. H. Hokke, M. Yazdanbakhsh, M. Wuhrer, 2012. Changes in antigen-specific IgG1 Fc N-glycosylation upon influenza and tetanus vaccination. Mol. Cell Proteomics. 11(4):014563-1-10.
19. Naess, L. M., T. Aarvak, A. Aase, F. Oftung, E. A. Hoiby, R. Sandin, T. E. Michaelsen, 1999. Human IgG subclass responses in relation to serum bactericidal and opsonic activities after immunization with three doses of the Norwegian serogroup B meningococcal outer membrane vesicle vaccine. Vaccine 17(7–8):754–764.
20. Mackell, S. M. 2003. Vaccinations for the pediatric traveler. Clin. Infect. Dis. 37(11):1508–1516.
21. Wuhrer, M., J. C. Stam, F. E. van de Geijn, C. A. Koeleman, C. T. Verrips, R. J. Dolhain, C. H. Hokke, A. M. Deelder, 2007. Glycosylation profiling of immunoglobulin G (IgG) subclasses from human serum. Proteomics 7(22):4070–4081.
22. Wuhrer, M., L. Porcelijn, R. Kapur, C. A. Koeleman, A. Deelder, H. M. de, M. de Haas, G. Vidarsson, 2009. Regulated glycosylation patterns of IgG during alloimmune responses against human platelet antigens. J. Proteome Res. 8(2):450– 456.
23. Stadlmann, J., M. Pabst, D. Kolarich, R. Kunert, F. Altmann, 2008. Analysis of immunoglobulin glycosylation by LC-ESI-MS of glycopeptides and oligosaccharides. Proteomics 8 (14):2858–2871.
24. Bjune, G., E. A. Hoiby, J. K. Gronnesby, O. Arnesen, J. H. Fredriksen, A. Halstensen, E. Holten, A. K. Lindbak, H. Nokleby, E. Rosenqvist, 1991. Effect of outer membrane vesicle vaccine against group B meningococcal disease in Norway. Lancet 338(8775):1093–1096.
25. Rosenqvist, E., E. A. Hoiby, G. Bjune, K. Bryn, O. Closs, B. Feiring, A. Klem, H. Nokleby, L. O. Frolm, 1991. Human antibody responses after vaccination with the Norwegian group B meningococcal outer membrane vesicle vaccine: results from ELISA studies. NIPH Ann. 14(2):169–179.
26. Hoiby, E. A., G. Bjune, L. O. Froholm, J. Eng, A. Halstensen, E. Rosenqvist, E. Ronnild, E. Wedege, 1991. The Norwegian meningococcal serogroup B outer membrane vesicle vaccine protection trials: case tracing, meningococcal antigen detection and serological diagnosis. NIPH Ann. 14(2):107–121.
27. Mashburn-Warren, L., R. J. McLean, M. Whiteley, 2008. Gram-negative outer membrane vesicles: beyond the cell surface. Geobiology 6(3):214–219.
28. Danzig, L. 2004. Meningococcal vaccines. Pediatr. Infect. Dis. J. 23(suppl.12):285–295.
29. Organization, W. H. 2009. Recommended composition of influenza virus vaccines for use in the 2010 influenza season (southern hemisphere winter). Wkly. Epidemiol. Rec. 84 (41):421–431.
30. Selman, M. H., R. J. Derks, A. Bondt, M. Palmblad, B. Schoenmaker, C. A. Koeleman, F. E. van de Geijn, R. J. Dolhain, A. M. Deelder, M. Wuhrer, 2012. Fc specific IgG glycosylation profiling by robust nano-reverse phase HPLC-MS using a sheath-flow ESI sprayer interface. J. Proteomics 75 (4):1318–1329.
31. Holland, M., H. Yagi, N. Takahashi, K. Kato, C. O. Savage, D. M. Goodall, R. Jefferis, 2006. Differential glycosylation of polyclonal IgG, IgG-Fc and IgG-Fab isolated from the sera of patients with ANCA-associated systemic vasculitis. Biochim. Biophys. Acta 1760(4):669–677.
32. Kaneko, Y., F. Nimmerjahn, J. V. Ravetch, 2006. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 313(5787):670–673.
33. Nimmerjahn, F., J. V. Ravetch, 2007. The antiinflammatory activity of IgG: the intravenous IgG paradox. J. Exp. Med. 204 (1):11–15.
34. Shibata-Koyama, M., S. Iida, H. Misaka, K. Mori, K. Yano, K. Shitara, M. Satoh, 2009. Nonfucosylated rituximab poten-tiates human neutrophil phagocytosis through its high binding for FcgammaRIIIb and MHC class II expression on the phagocytotic neutrophils. Exp. Hematol. 37(3):309–321.
35. Kazatchkine, M. D., S. V. Kaveri, 2001. Immunomodulation of autoimmune and inflammatory diseases with intravenous immune globulin. N. Engl. J. Med. 345(10):747–755.
36. Lendvai, N., X. W. Qu, W. Hsueh, A. Casadevall, 2000. Mechanism for the isotype dependence of antibody-mediated toxicity in Cryptococcus neoformans-infected mice. J. Immunol. 164(8):4367–4374.
37. Feldmesser, M., A. Mednick, A. Casadevall, 2002. Antibody-mediated protection in murine Cryptococcus neoformans infection is associated with pleotrophic effects on cytokine and leukocyte responses. Infect. Immun. 70(3):1571–1580.
38. Taborda, C. P., J. Rivera, O. Zaragoza, A. Casadevall, 2003. More is not necessarily better: prozone-like effects in passive immunization with IgG. J. Immunol. 170(7):3621–3630.
39. Casadevall, A., L. A. Pirofski, 2012. A new synthesis for antibody-mediated immunity. Nat. Immunol. 13(1):21–28.
40. Goins, C. L., C. P. Chappell, R. Shashidharamurthy, P. Selvaraj, J. Jacob, 2010. Immune complex-mediated enhancement of secondary antibody responses. J. Immunol. 184 (11):6293–6298.
41. Choi, J. H., J. Dekker, S. C. Schafer, J. John, C. E. Whitfill, C. S. Petty, E. E. Haddad, M. A. Croyle, 2012. Optimized adenovirus-antibody complexes stimulate strong cellular and humoral immune responses against an encoded antigen in naive mice and those with preexisting immunity. Clin. Vaccine Immunol. 19(1):84–95.
42. Vestrheim, A. C., A. Moen, W. Egge-Jacobsen, D. B. Bratlie, T. E. Michaelsen, 2013. Different glycosylation pattern of human IgG1 and IgG3 antibodies isolated from transiently as well as permanently transfected cell lines. Scand. J. Immunol. 77(5):419–428.
43. Reid, C. Q., A. Tait, H. Baldascini, A. Mohindra, A. Racher, S. Bilsborough, C. M. Smales, M. Hoare, 2010. Rapid whole monoclonal antibody analysis by mass spectrometry: an ultra scale-down study of the effect of harvesting by centrifugation on the post-translational modification profile. Biotechnol. Bioeng. 107(1):85–95.
44. Michaelsen, T. E., A. Aase, L. Norderhaug, I. Sandlie, 1992. Antibody dependent cell-mediated cytotoxicity induced by chimeric mouse-human IgG subclasses and IgG3 antibodies with altered hinge region. Mol. Immunol. 29(3):319–326.
45. Huck, S., P. Fort, D. H. Crawford, M. P. Lefranc, G. Lefranc, 1986. Sequence of a human immunoglobulin gamma 3 heavy chain constant region gene: comparison with the other human C gamma genes. Nucleic Acids Res. 14(4):1779–1789.
46. Michaelsen, T. E., B. Frangione, E. C. Franklin, 1977. Primary structure of the hinge region of human IgG3. Probable quadruplication of a 15-amino acid residue basic unit. J. Biol. Chem. 252(3):883–889.
47. Michaelsen, T. E., I. Sandlie, D. B. Bratlie, R. H. Sandin, O. Ihle, 2009. Structural difference in the complement activation site of human IgG1 and IgG3. Scand. J. Immunol. 70(6):553– 564.
48. Lai, R. P., M. S. Seaman, P. Tonks, F. Wegmann, D. J. Seilly, S. D. Frost, et al. 2012. Mixed adjuvant formulations reveal a new combination that elicit antibody response comparable to Freund’s adjuvants. PLoS ONE 7(4):e35083.
49. Petrovsky, N., J. C. Aguilar, 2004. Vaccine adjuvants: current state and future trends. Immunol. Cell Biol. 82(5):488– 496.
50. Launay, O., C. Desaint, C. Durier, P. Loulergue, X. Duval, C. Jacomet, et al. 2011. Safety and immunogenicity of a monovalent 2009 influenza A/H1N1v vaccine adjuvanted with AS03A or unadjuvanted in HIV-infected adults: a randomized, controlled trial. J. Infect. Dis. 204(1):124–134.
51. Pellegrini, M., U. Nicolay, K. Lindert, N. Groth, C. G. Della, 2009. MF59-adjuvanted versus non-adjuvanted influenza vaccines: integrated analysis from a large safety database. Vaccine 27(49):6959–6965.
52. Haeuptle, M. A., M. Welti, H. Troxler, A. J. Hulsmeier, T. Imbach, T. Hennet, 2011. Improvement of dolichol-linked oligosaccharide biosynthesis by the squalene synthase inhibitor zaragozic acid. J. Biol. Chem. 286(8):6085–6091.
53. Welti, M. 2013. Regulation of dolichol-linked glycosylation. Glycoconj. J. 30(1):51–56.
54. O’Hagan, D. T., G. S. Ott, G. V. Nest, R. Rappuoli, G. D. Giudice, 2013. The history of MF59((R)) adjuvant: a phoenix that arose from the ashes. Expert Rev. Vaccines 12(1):13–30.
55. Saso, L., B. Silvestrini, I. Zwain, A. Guglielmotti, M. R. Luparini, V. Cioli, C. Y. Cheng, 1992. Abnormal glycosylation of hemopexin in arthritic rats can be blocked by bindarit. J. Rheumatol. 19(12):1859–1867.
56. Breton, C., L. Snajdrova, C. Jeanneau, J. Koca, A. Imberty, 2006. Structures and mechanisms of glycosyltransferases. Glycobiology 16(2):29R–37R.
57. Durand, G., N. Seta, 2000. Protein glycosylation and diseases: blood and urinary oligosaccharides as markers for diagnosis and therapeutic monitoring. Clin. Chem. 46(6 Pt 1):795–805.
58. Wang, J., C. I. Balog, K. Stavenhagen, C. A. Koeleman, H. U. Scherer, M. H. Selman, A. M. Deelder, T. W. Huizinga, R. E. Toes, M. Wuhrer, 2011. Fc-glycosylation of IgG1 is modulated by B-cell stimuli. Mol. Cell Proteomics 10(5): M110.
59. Pucic, M., A. Knezevic, J. Vidic, B. Adamczyk, M. Novokmet, O. Polasek, et al. 2011. High throughput isolation and glycosylation analysis of IgG-variability and heritability of the IgG glycome in three isolated human populations. Mol. Cell Proteomics 10(10):010090-1-15.
60. Malaspina, A., B. S. Collins, A. Dell, G. Alter, T. M. Onami, 2013. Conference report: functional glycomics in HIV type 1 vaccine design workshop report, Bethesda, Maryland, April 30–May 1, 2012. AIDS Res. Hum. Retroviruses 29(11):1407– 1417.
61. Pittet, L. F., K. M. Posfay-Barbe, 2012. Pneumococcal vaccines for children: a global public health priority. Clin. Microbiol. Infect. 18(Suppl 5):25–36.
62. Lue, C., A. Tarkowski, J. Mestecky, 1988. Systemic immunization with pneumococcal polysaccharide vaccine induces a predominant IgA2 response of peripheral blood lymphocytes and increases of both serum and secretory anti-pneumococcal antibodies. J. Immunol. 140(11):3793–3800.
63. Lortan, J. E., A. Vellodi, E. S. Jurges, K. Hugh-Jones, 1992. Class-and subclass-specific pneumococcal antibody levels and response to immunization after bone marrow transplantation. Clin. Exp. Immunol. 88(3):512–519.
64. Meningococcal vaccines: polysaccharide and polysaccharide conjugate vaccines. 2002. Wkly Epidemiol Rec. 77(40):331– 339.
65. Soonawala, D., G. F. Rimmelzwaan, L. B. Gelinck, L. G. Visser, F. P. Kroon, 2011. Response to 2009 pandemic influenza A (H1N1) vaccine in HIV-infected patients and the influence of prior seasonal influenza vaccination. PLoS ONE 6(1):e16496.
66. Swanson, J., I. Goldschneider, 1969. The serum bactericidal system: ultrastructural changes in Neisseria meningitidis exposed to normal rat serum. J. Exp. Med. 129(1):51–79.
67. Aase, A., G. Bjune, E. A. Hoiby, E. Rosenqvist, A. K. Pedersen, T. E. Michaelsen. 1995. Comparison among opsonic activity, antimeningococcal immunoglobulin G response, and serum bactericidal activity against meningococci in sera from vaccinees after immunization with a serogroup B outer membrane vesicle vaccine. Infect. Immun. 63(9):3531– 3536.
68. Raju, T. S. 2008. Terminal sugars of Fc glycans influence antibody effector functions of IgGs. Curr. Opin. Immunol. 20 (4):471–478.
69. Sandbu, S., B. Feiring, P. Oster, O. S. Helland, H. S. Bakke, L. M. Naess, et al. 2007. Immunogenicity and safety of a combination of two serogroup B meningococcal outer membrane vesicle vaccines. Clin. Vaccine Immunol. 14 (9):1062–1069.