Studies on the mechanism by which antigen-specific IgG suppresses primary antibody responses: Evidence for epitope masking and decreased localization of antigen in the spleen

Scandinavian Journal of Immunology

Volumn 70, Issue 3, 2009, Pages 277-287

  Getahun, A ^a,b   Heyman, B ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b DEPARTMENT OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; EPITOPE; IMMUNOGLOBULIN G; OVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIGEN SPECIFICITY; ARTICLE; ASSAY; B LYMPHOCYTE; BLOOD FLOW; CONTROLLED STUDY; IMMUNIZATION; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SHEEP ERYTHROCYTE; SPLEEN; T LYMPHOCYTE;

ADOPTIVE TRANSFER; ANIMALS; ANTIBODY FORMATION; ANTIGENS; CD4-POSITIVE T-LYMPHOCYTES; EPITOPES; ERYTHROCYTES; IMMUNOGLOBULIN G; MICE; MICE, INBRED BALB C; NITROHYDROXYIODOPHENYLACETATE; SHEEP; SPLEEN;

EID: 69149085824     PISSN: 03009475     EISSN: 13653083     Source Type: Journal    
DOI: 10.1111/j.1365-3083.2009.02298.x     Document Type: Article

References (46)

1. von Behring E, Wernicke E. About immunization and cure of experimental animals having diphtheria. Z Hyg Infektionskrankheit 1892 12 : 10 44.
2. Uhr JW, Möller G. Regulatory effect of antibody on the immune response. Adv Immunol 1968 8 : 81 127.
3. Heyman B. Regulation of antibody responses via antibodies, complement, and Fc receptors. Annu Rev Immunol 2000 18 : 709 737.
4. Heyman B. Antibody feedback suppression: towards a unifying concept? Immunol Lett 1999 68 : 41 5.
5. Getahun A, Heyman B. How antibodies act as natural adjuvants. Immunol Lett 2006 104 : 38 45.
6. Bystryn JC, Graf MW, Uhr JW. Regulation of antibody formation by serum antibody. II. Removal of specific antibody by means of exchange transfusion. J Exp Med 1970 132 : 1279 1287.
7. Heyman B, Wigzell H. Specific IgM enhances and IgG inhibits the induction of immunological memory in mice. Scand J Immunol 1985 21 : 255 266.
8. Obukhanych TV, Nussenzweig MC. T-independent type II immune responses generate memory B cells. J Exp Med 2006 203 : 305 310.
9. Bowman JM. The prevention of Rh immunization. Transfus Med Rev 1988 2 : 129 150.
10. Siegrist CA. Mechanisms by which maternal antibodies influence infant vaccine responses: review of hypotheses and definition of main determinants. Vaccine 2003 21 : 3406 3412.
11. Phillips NE, Parker DC. Cross-linking of B lymphocyte Fc gamma receptors and membrane immunoglobulin inhibits anti-immunoglobulin-induced blastogenesis. J Immunol 1984 132 : 627 632.
12. Muta T, Kurosaki T, Misulovin Z, Sanchez M, Nussenzweig MC, Ravetch JV. A 13-amino-acid motif in the cytoplasmic domain of FcγRIIB modulates B-cell receptor signalling. Nature 1994 369 : 340.
13. Amigorena S, Bonnerot C, Drake JR et al. Cytoplasmic domain heterogeneity and functions of IgG Fc receptors in B lymphocytes. Science 1992 256 : 1808 1812.
14. Takai T, Ono M, Hikida M, Ohmori H, Ravetch JV. Augmented humoral and anaphylactic responses in FcγRII-deficient mice. Nature 1996 379 : 346 349.
15. Getahun A, Dahlstrom J, Wernersson S, Heyman B. IgG2a-mediated enhancement of antibody and T cell responses and its relation to inhibitory and activating Fc-gamma receptors. J Immunol 2004 172 : 5269 5276.
16. Sinclair NR. Fc-signalling in the modulation of immune responses by passive antibody. Scand J Immunol 2001 53 : 322 330.
17. Karlsson MC, Wernersson S, Diaz de Ståhl T, Gustavsson S, Heyman B. Efficient IgG-mediated suppression of primary antibody responses in Fcγ receptor-deficient mice. Proc Natl Acad Sci USA 1999 96 : 2244 2249.
18. Karlsson MC, Getahun A, Heyman B. FcγRIIB in IgG-mediated suppression of antibody responses: different impact in vivo and in vitro. J Immunol 2001 167 : 5558 5564.
19. Heyman B, Wiersma E, Nose M. Complement activation is not required for IgG-mediated suppression of the antibody response. Eur J Immunol 1988 18 : 1739 1743.
20. Walker JG, Siskind GW. Studies on the control of antibody synthesis. Effect of antibody affinity upon its ability to suppress antibody formation. Immunology 1968 14 : 21 8.
21. Brüggemann M, Rajewsky K. Regulation of the antibody response against hapten-coupled erythrocytes by monoclonal anti-hapten antibodies of various isotypes. Cell Immunol 1982 71 : 365 373.
22. Quintana IZ, Silveira AV, Möller G. Regulation of the antibody response to sheep erythrocytes by monoclonal IgG antibodies. Eur J Immunol 1987 17 : 1343 1349.
23. Möller G, Wigzell H. Antibody sythesis at the cellular level: antibody-induced suppression of 19S and 7S antibody response. J Exp Med 1965 15 : 409 412.
24. Karlsson MC, De Stahl TD, Heyman B. IgE-mediated suppression of primary antibody responses in vivo. Scand J Immunol 2001 53 : 381 385.
25. Tao TW, Uhr JW. Capacity of pepsin-digested antibody to inhibit antibody formation. Nature 1966 212 : 208 209.
26. Cerottini JC, McConahey PJ, Dixon FJ. The immunosuppressive effect of passively administered antibody IgG fragments. J Immunol 1969 102 : 1008 1015.
27. Na D, Kim D, Lee D. Mathematical modeling of humoral immune response suppression by passively administered antibodies in mice. J Theor Biol 2006 241 : 830 851.
28. Brody NI, Walker JG, Siskind GW. Studies on the control of antibody synthesis. Interaction of antigenic competition and suppression of antibody formation by passive antibody on the immune response. J Exp Med 1967 126 : 81 91.
29. Möller G. Antibody-mediated suppression of the immune response is determinant specific. Eur J Immunol 1985 15 : 409 412.
30. Heyman B, Wigzell H. Immunoregulation by monoclonal sheep erythrocyte-specific IgG antibodies: suppression is correlated to level of antigen binding and not to isotype. J Immunol 1984 132 : 1136 1143.
31. Kappler JW, Hoffmann M, Dutton RW. Regulation of the immune response. I. Differential effect of passively administered antibody on the thymus-derived and bone marrow-derived lymphocytes. J Exp Med 1971 134 : 577 587.
32. Enriquez Rincon F, Klaus GG. Differing effects of monoclonal anti-hapten antibodies on humoral responses to soluble or particulate antigens. Immunology 1984 52 : 129 136.
33. Murphy KM, Heimberger AB, Loh DY. Induction by antigen of intrathymic apoptosis of CD4 + CD8 + TCRlo thymocytes in vivo. Science 1990 250 : 1720 1723.
34. Ey PL, Prowse SJ, Jenkin CR. Isolation of pure IgG1, IgG2a and IgG2b immunoglobulins from mouse serum using protein A-Sepharose. Immunochemistry 1978 15 : 429 436.
35. Gustavsson S, Kinoshita T, Heyman B. Antibodies to murine complement receptor 1 and 2 can inhibit the antibody response in vivo without inhibiting T helper cell induction. J Immunol 1995 154 : 6524 6528.
36. Haskins K, Kubo R, White J, Pigeon M, Kappler J, Marrack P. The major histocompatibility complex-restricted antigen receptor on T cells. I. Isolation with a monoclonal antibody. J Exp Med 1983 157 : 1149 1169.
37. Kearney ER, Pape KA, Loh DY, Jenkins MK. Visualization of peptide-specific T cell immunity and peripheral tolerance induction in vivo. Immunity 1994 1 : 327 339.
38. Lee WT, Pasos G, Cecchini L, Mittler JN. Continued antigen stimulation is not required during CD4+ T cell clonal expansion. J Immunol 2002 168 : 1682 1689.
39. Borek F. Previously unrecognized functions of the spleen: development and mainenance of immune competence and regulation. Crit Rev Immunol 1986 6 : 287 293.
40. Watts C, Lanzavecchia A. Suppressive effect of antibody on processing of T cell epitopes. J Exp Med 1993 178 : 1459 1463.
41. Manca F, Fenoglio D, Li Pira G, Kunkl A, Celada F. Effect of antigen/antibody ratio on macrophage uptake, processing, and presentation to T cells of antigen complexed with polyclonal antibodies. J Exp Med 1991 173 : 37 48.
42. Brinc D, Le-Tien H, Crow AR, Freedman J, Lazarus AH. IgG-mediated immunosuppression is not dependent on erythrocyte clearance or immunological evasion: implications for the mechanism of action of anti-D in the prevention of haemolytic disease of the newborn? Br J Haematol 2007 139 : 275 279.
43. Crowe JEJ, Firestone CY, Murphy BR. Passively acquired antibodies suppress humoral but not cell-mediated immunity in mice immunized with live attenuated respiratory syncytial virus vaccines. J Immunol 2001 167 : 3910 3918.
44. Gans HA, Maldonado Y, Yasukawa LL et al. IL-12, IFN-gamma, and T cell proliferation to measles in immunized infants. J Immunol 1999 162 : 5569 5575.
45. Chan PL, Sinclair NR. Regulation of the immune response. VI. Inability of F(ab′) 2 antibody to terminate established immune responses and its ability to interfere with IgG antibody-mediated immunosuppression. Immunology 1973 24 : 289 301.
46. Kumpel BM. On the immunologic basis of Rh immune globulin (anti-D) prophylaxis. Transfusion 2006 46 : 1652 1656.