The dual phases of the response to neonatal exposure to a V(H) family- restricted staphylococcal B cell superantigen

Journal of Immunology

Volumn 161, Issue 10, 1998, Pages 5720-5732

  Silverman, Gregg J ^a,b   Nayak, Jayakar V ^a,c   Warnatz, Klaus ^a,d   Hajjar, Fred F ^a   Cary, Stephen ^a   Tighe, Helen ^a   Curtiss, Virginia E ^a  

^a San Diego   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

STAPHYLOCOCCUS PROTEIN A; SUPERANTIGEN;

ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; B LYMPHOCYTE; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; MOUSE; NEWBORN PERIOD; NONHUMAN; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; T LYMPHOCYTE;

ANIMALS; ANIMALS, NEWBORN; ANTIBODIES, BACTERIAL; B-LYMPHOCYTES; GENE REARRANGEMENT, B-LYMPHOCYTE, HEAVY CHAIN; GENES, IMMUNOGLOBULIN; IMMUNOGLOBULIN FAB FRAGMENTS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN M; IMMUNOGLOBULIN VARIABLE REGION; INJECTIONS, INTRAPERITONEAL; INJECTIONS, SUBCUTANEOUS; LYMPHOCYTE COUNT; MICE; MICE, INBRED BALB C; MULTIGENE FAMILY; STAPHYLOCOCCAL PROTEIN A; SUPERANTIGENS;

EID: 0032534042     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (98)

1. Goodnow, C. C., J. G. Cyster, S. B. Hartley, S. E. Bell, M. P. Cooke, J. I. Healy, S. Akkaraju, J. C. Rathmell, S. L. Pogue, and K. P. Shokat. 1995. Self-tolerance checkpoints in B lymphocyte development. Adv. Immunol. 59:279.
2. H3-restricted unconventional bacterial antigen. J. Immunol. 151:5840.
3. Silverman, G. J., P. Roben, J.-P. Bouvet, and M. Sasano. 1995. Superantigen properties of a human sialoprotein involved in gut-associated immunity. J. Clin. Invest. 96:417.
4. H family-specific binding interactions with human Igs. J. Immunol. 157:4496.
5. Pospisil, R., M. G. Fitts, and R. G. Mage. 1996. CD5 is a potential selecting ligand for B cell surface immunoglobulin framework region sequences. J. Exp. Med. 184:1279.
6. Silverman, G. J. 1997. B-cell superantigens. Immunol. Today 18:379.
7. H3 (D12 idiotope) B cells in vivo. J. Acquired Immune Defic. Syndr. 7:641.
8. H clonal deficit in human immunodeficiency virus-positive individuals reflects a B-cell maturational arrest. Blood 78:175.
9. Muller, S., H. Wang, G. J. Silverman, G. Bramlet, N. Haigwood, and H. Kohler. 1993. B-cell abnormalities in AIDS: stable and clonally-restricted antibody response in HIV-1 infection. Scand. J. Immunol. 38:327.
10. H1 gene expression in peripheral B cell IgM, IgD and IgG during HIV infection. Eur. J. Immunol. 25:1524.
11. Silverman, G. J. 1998. B cell Superantigens: possible roles in immunodeficiency and autoimmunity. Semin. Immunol. 10:43.
12. + B cells. J. Clin. Invest. 99:2488.
13. Sjodahl, J. 1977. Structural studies on the four repetitive Fc-binding regions in protein A from Staphylococcus aureus. Eur. J. Biochem. 78:471.
14. Lofdahl, S., B. Guss, M. Uhlen, L. Philipson, and M. Lindberg. 1983. Gene for staphylococcal protein A. Proc. Natl. Acad. Sci. USA 80:697.
15. Foster, T. J., and D. McDevitt. 1994. Surface-associated proteins of Staphylococcus aureus: their possible roles in virulence. FEMS. Microbiol. Lett. 118:199.
16. Patel, A. H., P. Nowlan, E. D. Weavers, and T. Foster. 1987. Virulence of protein A-deficient and α-toxin-deficient mutants of Staphylococcus aureus isolated by allele replacement. Infect. Immun. 55:3103.
17. Inganas, M., S. G. Johansson, and J. Sjoquist. 1981. Further characterization of the alternative protein-A interaction of immunoglobulins: demonstration of an Fc-binding fragment of protein A expressing the alternative reactivity. Scand. J. Immunol. 14:379.
18. 2-and Fc-mediated interactions of mammalian immunoglobulins with S. aureus and group C and G streptococci. Acta Pathol. Microbiol. Immunol. Scand. [B] 94: 377.
19. HIII H chains. J. Immunol. 142:2778.
20. Sasano, M., D. R. Burton, and G. J. Silverman. 1993. Molecular selection of human antibodies with an unconventional bacterial B cell superantigen. J. Immunol. 151:5822.
21. Silverman, G. J. 1992. Human antibody responses to bacterial antigens: studies of a model conventional antigen and a proposed model B cell superantigen. Int. Rev. Immunol. 9:57.
22. H3 immunoglobulin binding to staphylococcal protein A. J. Exp. Med. 178:331.
23. HIII subgroup. J. Immunol. 147:1877.
24. H3 antibodies bind domain D of staphylococcal protein A. J. Immunol. 154:6437.
25. H3-expressing B lymphocytes. J. Immunol. 153:2974.
26. H3 mRNA expression by protein A-binding B cells. J. Clin. Immunol. 15:145.
27. Kozlowski, L. M., W. Li, M. Goldschmidt, and A. I. Levinson. 1998. In vivo inflammatory response to a prototypic B cell superantigen: elicitation of an Arthus reaction by staphylococcal protein A. J. Immunol. 160:5246.
28. Myhre, E. B. 1990. Interaction of bacterial immunoglobulin receptors with sites in the Fab region. In Bacterial Immunoglobulin-Binding Proteins, Vol. 1. M. D. P. Boyle, ed. Academic Press, San Diego, p. 243.
29. H families S107 or J606 bind to protein A. J. Immunol. 145:2989.
30. Terres, G., and W. L. Hughes. 1959. Acquired immune tolerance in mice to crystalline bovine serum albumin. J. Immunol. 83:459.
31. Thorbecke, G. J., G. W. Siskind, and N. J. Goldberger. 1961. The induction in mice of sensitization and immunological unresponsiveness by neonatal injection of bovine γ-globulin. J. Immunol. 87:147.
32. Siskind, G. W., P. Y. Paterson, and L. Thomas. 1963. Induction of unresponsiveness and immunity in newborn and adult mice with pneumococcal polysaccharide. J. Immunol. 90:929.
33. Argyris, B. F. 1968. Role of macrophages in immunological maturation. J. Exp. Med. 128:459.
34. Lu, C. Y., E. G. Calamai, and E. R. Unanue. 1979. A defect in the antigen-presenting function of macrophages from neonatal mice. Nature 282:327.
35. Ridge, J. P., E. J. Fuchs, and P. Matzinger. 1996. Neonatal tolerance revisited: turning on newborn T cells with dendritic cells. Science 271:1723.
36. Chen, N., Q. Gao, and E. H. Field. 1995. Expansion of memory Th2 cells over Th1 cells in neonatal primed mice. Transplantation 60:1187.
37. Schurmans, S., C. H. Heusser, H. Y. Qin, J. Merino, G. Brighouse, and P. H. Lambert. 1990. In vivo effects of anti-IL-4 monoclonal antibody on neonatal induction of tolerance and on an associated autoimmune syndrome. J. Immunol. 145:2465.
38. Powell, T. J. J., and J. W. Streilein. 1990. Neonatal tolerance induction by class II alloantigens activates IL-4-secreting, tolerogen-responsive T cells. J. Immunol. 144:854.
39. Sarzotti, M., D. S. Robbins, and P. M. Hoffman. 1996. Induction of protective CTL responses in newborn mice by a murine retrovirus. Science 271:1726.
40. Forsthuber, T., H. C. Yip, and P. V. Lehmann. 1996. Induction of TH1 and TH2 immunity in neonatal mice. Science 271:1728.
41. Singh, R. R., B. H. Hahn, and E. E. Sercarz. 1996. Neonatal peptide exposure can prime T cells and, upon subsequent immunization, induce their immune deviation: implications for antibody vs. T cell-mediated autoimmunity. J. Exp. Med. 183:1613.
42. Dorsch, S., and B. Roser. 1975. T cells mediate transplantation tolerance. Nature 258:233.
43. Rieger, M., and I. Hilgert. 1977. The involvement of a suppressor mechanism in neonatally induced allograft tolerance in mice. J. Immunogenet. 4:61.
44. Rubinstein, L. J., B. Goldberg, J. Hiernaux, K. E. Stein, and C. A. Bona. 1983. Idiotype-antiidiotype regulation. V. The requirement for immunization with antigen or monoclonal antiidiotypic antibodies for the activation of beta 2 leads to 6 and beta 2 leads to 1 polyfructosan-reactive clones in BALB/c mice treated at birth with minute amounts of anti-A48 idiotype antibodies. J. Exp. Med. 158: 1129.
45. Accolla, R. S., P. J. Gearhart, N. H. Sigal, M. P. Cancro, and N. R. Klinman. 1977. Idiotype-specific neonatal suppression of phosphorylcholine-responsive B cells Eur. J. Immunol. 7:876.
46. Vakil, M., H. Sauter, C. Paige, and J. F. Kearney. 1986. In vivo suppression of perinatal multispecific B cells results in a distortion of the adult B cell repertoire. Eur. J. Immunol. 16:1159.
47. Mosier, D. E. 1978. Induction of B cell priming by neonatal injection of mice with thymic-independent (type 2) antigens. J. Immunol. 121:1453.
48. White, J., A. Herman, A. M. Pullen, R. Kubo, J. W. Kappler, and P. Marrack. 1989. The V β-specific superantigen staphylococcal enterotoxin B: stimulation of mature T cells and clonal deletion in neonatal mice. Cell 56:27.
49. Boussiotis, V. A., D. L. Barber, T. Nakarai, G. J. Freeman, J. G. Gribben, G. M. Bernstein, A. D. D'Andrea, J. Ritz, and L. M. Nadler. 1994. Prevention of T cell anergy by signaling through the γc chain of the IL-2 receptor. Science 266:1039.
50. Gimmi, C. D., G. J. Freeman, J. G. Gribben, G. Gray, and L. M. Nadler. 1993. Human T-cell clonal anergy is induced by antigen presentation in the absence of B7 costimulation. Proc. Natl. Acad. Sci. USA 90:6586.
51. Goodnow, C. C., R. Brink, and E. Adams. 1991. Breakdown of self-tolerance in anergic B lymphocytes. Nature 352:532.
52. Klinman, D. M., and T. B. Nutman. 1994. ELISPOT assay to detect cytokine-secreting murine and human cells. In Current Protocols in Immunology. J. E. Coligan, A. M. Kruisbeek, D. H. Margulies, E. M. Shevach, and W. Strober, eds. John Wiley & Sons, New York, p. 6.19.
53. Li, Y. S., K. Hayakawa, and R. R. Hardy. 1993. The regulated expression of B lineage associated genes during B cell differentiation in bone marrow and fetal liver. J. Exp. Med. 178:951.
54. Feeney, A. J. 1991. Predominance of the prototypic T15 anti-phosphorylcholine junctional sequence in neonatal pre-B cells. J. Immunol. 147:4343.
55. Feeney, A. J. 1990. Lack of N regions in fetal and neonatal mouse immunoglobulin V-D-J junctional sequences. J. Exp. Med. 172:1377.
56. Silverman, G. J., J. Nayak, and A. La Cava. 1997. B-cell superantigens: molecular and cellular implications. Int. Rev. Immunol. 14:259.
57. Silverman, G. J., P. Roben, R. Wagenknecht, J. Nayak, H. Tighe, and K. Warnatz. 1997. In vivo consequences of B-cell superantigen immunization. Ann. NY Acad. Sci. 815:105.
58. Carsetti, R., G. Kohler, and M. C. Lamers. 1995. Transitional B cells are the target of negative selection in the B cell compartment. J. Exp. Med. 181:2129.
59. Carsetti, R., G. Kohler, and M. C. Lamers. 1993. A role for immunoglobulin D: interference with tolerance induction. Eur. J. Immunol. 23:168.
60. Bos, N. A., C. G. Meeuwsen, H. Hooijkaas, R. Benner, B. S. Wostmann, and J. R. Pleasants. 1987. Early development of Ig-secreting cells in young of germ-free BALB/c mice fed a chemically defined ultrafiltered diet. Cell. Immunol. 105:235.
61. Agenes, F., M. M. Rosado, and A. A. Freitas. 1997. Independent homeostatic regulation of B cell compartments. Eur. J. Immunol. 27:1801.
62. Whitmer, K. J., C. G. Romball, and W. O. Weigle. 1997. Induction of tolerance to human γ-globulin in FcRγ-and FcγRII-deficient mice. J. Immunol. 159:644.
63. Shlomchik, M. J., D. Zharhary, T. Saunders, S. A. Camper, and M. G. Weigert. 1993. A rheumatoid factor transgenic mouse model of autoantibody regulation. Int. Immunol. 5:1329.
64. Roark, J. H., A. Bui, K. A. Nguyen, L. Mandik, and J. Erikson. 1997. Persistence of functionally compromised anti-double-stranded DNA B cells in the periphery of non-autoimmune mice. Int. Immunol. 9:1615.
65. Nguyen, K. A., L. Mandik, A. Bui, J. Kavaler, A. Norvell, J. G. Monroe, J. H. Roark, and J. Erikson. 1997. Characterization of anti-single-stranded DNA B cells in a non-autoimmune background. J. Immunol. 159:2633.
66. Rosenberg, Y. J., and J. M. Chiller. 1979. Ability of antigen-specific helper cells to effect a class-restricted increase in total Ig-secreting cells in spleens after immunization with the antigen. J. Exp. Med. 150:517.
67. Moticka, E. J. 1978. Antibody specificities generated during antigen-induced polyclonal hyperimmunoglobulinemia. Cell. Immunol. 36:151.
68. Clayton, J. P., G. M. Gammon, D. G. Ando, D. H. Kono, L. Hood, and E. E. Sercarz. 1989. Peptide-specific prevention of experimental allergic encephalomyelitis. Neonatal tolerance induced to the dominant T cell determinant of myelin basic protein. J. Exp. Med. 169:1681.
69. Gammon, G., K. Dunn, N. Shastri, A. Oki, S. Wilbur, and E. E. Sercarz. 1986. Neonatal T-cell tolerance to minimal immunogenic peptides is caused by clonal inactivation. Nature 319:413.
70. + cell subsets. J. Exp. Med. 178:1637.
71. H gene usage in adult mice. EMBO J. 8:2313.
72. H gene families. J. Immunol. 140:2436.
73. H gene family repertoire of resting B cells: preferential use of D-proximal families early in development may be due to distinct B cell subsets. J. Immunol. 143:2752.
74. H-D-JH sequences from B-1a, B-1b, and conventional B cells. J. Immunol. 158:1175.
75. Kavaler, J. A. J. Caton, L. M. Staudt, and W. Gerhard. 1991. A B cell population that dominates the primary response to influenza virus hemagglutinin does not participate in the memory response. Eur. J. Immunol. 21:2687.
76. Bachmann, M. F., U. H. Rohrer, T. M. Kundig, K. Burki, H. Hengartner, and R. M. Zinkernagel. 1993. The influence of antigen organization on B cell responsiveness. Science 262:1448.
77. Nadler, P. I., R. J. Klingenstein, and R. J. Hodes. 1980. Ontogeny of murine accessory cells: Ia antigen expression and accessory cell function in in vitro primary antibody responses. J. Immunol. 125:914.
78. Finkelman, F. D., A. Lees, R. Birnbaum, W. C. Gause, and S. C. Morris. 1996. Dendritic cells can present antigen in vivo in a tolerogenic or immunogenic fashion. J. Immunol. 157:1406.
79. Morris, S. C., A. Lees, J. M. Holmes, R. D. Jeffries, and F. D. Finkelman. 1994. Induction of B cell and T cell tolerance in vivo by anti-CD23 mAb. J. Immunol. 152:3768.
80. Eynon, E. E., and D. C. Parker. 1993. Parameters of tolerance induction by antigen targeted to B lymphocytes. J. Immunol. 151:2958.
81. Eynon, E. E., and D. C. Parker. 1992. Small B cells as antigen-presenting cells in the induction of tolerance to soluble protein antigens. J. Exp. Med. 175: 131.
82. Monroe, J. G. 1996. Tolerance sensitivity of immature-stage B cells: can developmentally regulated B cell antigen receptor (BCR) signal transduction play a role? J. Immunol. 156:2657.
83. Smith, R. T., and R. A. Bridges. 1958. Immunological unresponsiveness in rabbits produced by neonatal injection of defined antigens. J. Exp. Med. 108:227.
84. Tew, J. G., and T. E. Mandel. 1979. Prolonged antigen half-life in the lymphoid follicles of specifically immunized mice. Immunology 37:69.
85. Adelstein, S., H. Pritchard-Briscoe, T. A. Anderson, J. Crosbie, G. Gammon, R. H. Loblay, A. Basten, and C. C. Goodnow. 1991. Induction of self-tolerance in T cells but not B cells of transgenic mice expressing little self antigen. Science 251:1223.
86. Riley, R. L., and N. R. Klinman. 1986. The affinity threshold for antigenic triggering differs for tolerance susceptible immature precursors vs mature primary B cells. J. Immunol. 136:3147.
87. Nossal, G. J., B. L. Pike, and F. L. Battye. 1979. Mechanisms of clonal abortion tolerogenesis. II. Clonal behaviour of immature B cells following exposure to anti-mu chain antibody. Immunology 37:203.
88. Allman, D. M., S. E. Ferguson, and M. P. Cancro. 1992. Peripheral B cell maturation. I. Immature peripheral B cells in adults are heat-stable antigens and exhibit unique signaling characteristics. J. Immunol. 149:2533.
89. Metcalf, E. S., A. F. Schrater, and N. R. Klinman. 1979. Murine models of tolerance induction in developing and mature B cells. Immunol. Rev. 43:142.
90. Nossal, G. J., and M. Karvelas. 1990. Soluble antigen abrogates the appearance of anti-protein IgG1-forming cell precursors during primary immunization. Proc. Natl. Acad. Sci. USA 87:1615.
91. Linton, P. J., A. Rudie, and N. R. Klinman. 1991. Tolerance susceptibility of newly generating memory B cells. J. Immunol. 146:4099.
92. Karvelas, M., and G. J. Nossal. 1992. Memory cell generation ablated by soluble protein antigen by means of effects on T-and B-lymphocyte compartments. Proc. Natl. Acad. Sci. USA 89:3150.
93. Shokat, K. M., and C. C. Goodnow. 1995. Antigen-induced B-cell death and elimination during germinal-centre immune responses. Nature 375:334.
94. Pulendran, B., K. G. Smith, and G. J. Nossal. 1995. Soluble antigen can impede affinity maturation and the germinal center reaction but enhance extrafollicular immunoglobulin production. J. Immunol. 155:1141.
95. Malanchere, E., F. Huetz, and A. Coutinho. 1997. Maternal IgG stimulates B lineage cell development in the progeny. Eur. J. Immunol. 27:788.
96. Lam, K. P., R. Kuhn, and K. Rajewsky. 1997. In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid cell death. Cell 90:1073.
97. Neuberger, M. S. 1997. Antigen receptor signaling gives lymphocytes a long life. Cell 90:971.
98. Gu, H., D. Tarlington, W. Muller, K. Rajewsky, and L. Forster. 1991. Most peripheral B cells in mice are ligand selected. J. Exp. Med. 173:1357.