Viral superantigen drives extrafollicular and follicular B cell differentiation leading to virus-specific antibody production

Journal of Experimental Medicine

Volumn 185, Issue 3, 1997, Pages 551-562

  Luther, Sanjiv A ^a   Gulbranson Judge, Adam ^b   Acha Orbea, Hans ^a   MacLennan, Ian C M ^b,c  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY DEPARTMENT OF MEDICINE   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; HAPTEN; IMMUNOGLOBULIN; SUPERANTIGEN; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE ACTIVATION; B LYMPHOCYTE DIFFERENTIATION; CONTROLLED STUDY; GERMINAL CENTER; IMMUNOHISTOLOGY; LYMPH FOLLICLE; LYMPHOCYTE PROLIFERATION; MOUSE; MOUSE MAMMARY TUMOR ONCOVIRUS; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIBODIES, VIRAL; B-LYMPHOCYTES; CELL DIFFERENTIATION; CHICKENS; GAMMA-GLOBULINS; LYMPHOCYTE ACTIVATION; MAMMARY TUMOR VIRUS, MOUSE; MICE; MICE, INBRED BALB C; RATS; SUPERANTIGENS; T-LYMPHOCYTES;

EID: 0031041305     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.185.3.551     Document Type: Article

References (58)

1. Acha-Orbea, H., and H.R. MacDonald. 1995. Superantigens of mouse mammary tumor virus. Annu. Rev. Immunol. 13: 459-486.
2. Held, W., G.A. Waanders, A.N. Shakhov, L. Scarpellino, H. Acha-Orbea, and H.R. MacDonald. 1993. Superantigen-induced immune stimulation amplifies mouse mammary tumor virus infection and allows virus transmission. Cell. 74:529-540.
3. Karapetian, O., A.N. Shakhov, J.P. Kraehenbuhl, and H. Acha-Orbea. 1994. Retroviral infection of neonatal Peyer's patch lymphocytes: the mouse mammary tumor virus model. J. Exp. Med. 180:1511-1516.
4. Webb, S., C. Morris, and J. Sprent. 1990. Extrathymic tolerance of mature T cells: clonal elimination as a consequence of immunity. Cell. 63:1249-1256.
5. + T cells in mice tolerant to staphylococcus aureus enterotoxin B. Nature (Lond.). 349:245-248.
6. + peripheral T cells responding to staphylococcal encerotoxin B in vivo. Eur. J. Immunol. 21:1963-1966.
7. a (Mtv7). J. Exp. Med. 175:1623-1633.
8. + T cells are required to stimulate B cells after infection with mouse mammary tumor virus. J. Exp. Med. 177:359-366.
9. Luther, S., A.N. Shakhov, I. Xenarios, S. Haga, S. Imai, and H. Acha-Orbea. 1994. New infectious mammary tumor virus superantigen with Vβ-specificity identical to staphylococcal enterotoxin B (SEB). Eur. J. Immunol. 24:1757-1764.
10. Steinmann, R.M. 1991. The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 9:271-296.
11. MacLennan, I.C.M., Y.-J. Liu, S. Oldfield, J. Zhang, and P.J.L. Lane. 1990. The evolution of B cell clones. Curr. Topics Microbiol. Immunol. 159:37-64.
12. Liu, Y.-J., J. Zhang, P.L.J. Lane, E.Y.-T. Chan, and I.C.M. MacLennan. 1991. Sires of specific B cell activation in primary and secondary responses to T cell-dependent and T cell-independent antigens. Eur. J. Immunol. 21:2951-2962.
13. Jacob, J., R. Kassir, and G. Kelsoe. 1991. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. I. The architecture and dynamics of responding cell populations. J. Exp. Med. 173:1165-1175.
14. Kearney, E.R., K.A. Pape, D.Y. Loh, and M.K. Jenkins. 1994. Visualization of peptide-specific T cell immunity and peripheral tolerance induction in vivo. Immunity. 1:327-339.
15. Jacob, J., and G. Kelsoe. 1992. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. II. A common clonal origin for periarteriolar lymphoid sheath-associated foci and germinal centers. J. Exp. Med. 176:679-688.
16. McHeyzer-Williams, M.G., M.J. McLean, P.A. Lalor, and G.J.V. Nossal. 1993. Antigen-driven B cell differentiation in vivo. J. Exp. Med. 178:295-307.
17. Ho, F., J. Lortan, M. Khan, and I.C.M. MacLennan. 1986. Distinct short-lived and long-lived antibody-producing cell populations. Eur. J. Immunol. 16:1297-1301.
18. Smith, K.G., T.D. Hewitson, G.J.V. Nossal, and D.M. Tarlinton. 1996. The phenotype and fate of the antibody-forming cells of the splenic foci. Eur. J. Immunol. 26:444-448.
19. Toellner, K.-M., A. Gulbranson-Judge, D.R. Taylor, M.-Y. Sze, and I.C.M. MacLennan. 1996. Immunoglobulin switch transcript production in vivo related to the site and time of antigen-specific B cell activation. J. Exp. Med. 183:2303-2312.
20. Kosco, M.H., G.F. Burton, Z.F. Kapasi, A.K. Szakal, and J.G. Tew. 1989. Antibody forming cell induction during an early phase ot germinal center development and its delay with aging. Immunology. 68:312-318.
21. MacLennan, I.C.M., and D. Gray. 1986. Antigen-driven selection of virgin and memory B cells. Immunol. Rev. 91:61-85.
22. Jacob, J., G. Kelsoe, K. Rajewsky, and U. Weiss. 1991. Intraclonal generation of antibody mutants in germinal centers. Nature (Lond.). 354:389-392.
23. Tew, J.G., R.M. DiLosa, G.F. Burton, M.H. Kosco, L.I. Kupp, A. Masuda, and A.K. Szakal. 1992. Germinal centers and antibody production in bone marrow. Immunol. Rev. 126: 99-112.
24. Coico, R.F., B.S. Bhogal, and G.J. Thorbecke. 1983. The relationship of germinal centers in lymphoid tissue to immunologic memory. IV. Transfer of B cell memory with lymph node cells fractionated according to their receptors for peanut agglutinin. J. Immunol. 131:2254-2257.
25. Nossal, G.J.V., and M. Karvelas. 1990. Soluble antigen abrogates the appearance of anti protein IgG1 forming cell precursors during primary immunization. Proc. Natl. Acad. Sci. USA. 87:1615-1619.
26. Payne, J., B.T. Huber, N.A. Cannon, R. Schneider, M.W. Schilham, H. Acha-Orbea, H.R. MacDonald, and H. Hengartner. 1988. Monoclonal rat antibodies with specificity for the beta-chain variable region Vβ6 of the murine T cell receptor. Proc. Nat. Acad. Sci. USA. 85:7695-7698.
27. + T cells. J. Exp. Med. 170:135-143.
28. Liu, Y.-J., S. Oldfield, and I.C.M. MacLennan. 1988. Memory B cells in T-cell dependent antibody responses colonize the splenic marginal zones. Eur. J. Immunol. 18:355-362.
29. Han, S., K. Hathcock, B. Zheng, T.B. Kepler, R. Hodes, and G. Kelsoe. 1995. Cellular interaction in germinal centers; roles of CD40 ligand and B7-2 in established germinal centers. J. Immunol. 155:556-567.
30. Gulbranson-Judge, A., and I.C.M. MacLennan. 1996. Sequential antigen-specific growth of T cells in the T zones and follicles in response to pigeon cytochrome c. Eur. J. Immunol. 26:1830-1837.
31. MacLennan, I.C.M. 1994. Germinal centers. Annu. Rev. Immunol. 12:117-139.
32. Gunzburg, W.H., N.E. Hynes, and B. Groner. 1984. The methylation pattern of endogenous mouse mammary tumor virus proviral genes is tissue specific and stably inherited. Virology. 138:212-224.
33. Cho, K., D.A. Ferrick, and D.W. Morris. 1995. Structure and biological activity of the subgenomic Mtv-6 endogenous provirus. Virology. 206:395-402.
34. Nemazee, D.A., and K. Bürki. 1989. Clonal deletion of autoreactive B lymphocytes in a transgenic mouse bearing anti-MHC class I antibody genes. Nature (Lond.). 337:562-566.
35. Hartley, S.B., J. Crosbie, R.A. Brink, A.B. Kantor, A. Basten, and C.C. Goodnow. 1991. Elimination from peripheral lymphoid tissues of self-reactive B lymphocytes recognising membrane-bound antigen. Nature (Lond.). 353:765-769.
36. Lortan, J.E., C.A. Roobottom, S. Oldfield, and I.C.M. MacLennan. 1987. Newly produced virgin B cells migrate to secondary lymphoid organs but their capacity to enter follicles is restricted. Eur. J. Immunol. 17:1311-1316.
37. Chan, E.Y.T., and I.C.M. MacLennan. 1993. Only a small proportion of splenic B-cells in adults are short-lived virgin cells. Eur. J. Immunol. 23:357-363.
38. Gray, D., I.C.M. MacLennan, and P.J.L. Lane. 1986. Virgin B cell recruitment and the lifespan of memory clones during antibody responses to 2,4-dinitrophenyl-hemocyanin. Eur. J. Immunol. 16:641-648.
39. Cyster, J.G., and C.C. Goodnow. 1995. Antigen-induced exclusion from follicles and anergy are separate and complementary processes that influence peripheral B cell fate. Immunity. 3:691-701.
40. Howard, J.C., S.V. Hunt, and J.L. Gowans. 1972. Identification of marrow-derived and thymus-derived small lymphocytes in the lymphoid tissues and thoracic duct lymph of normal rats. J. Exp. Med. 135:200-209.
41. Nieuwenhuis, P., and W.L. Ford. 1976. Comparative migration of T cells and B cells in the rat spleen and lymph nodes. Cell. Immunol. 23:254-267.
42. Ron, Y., and J. Sprent. 1987. T cell priming in vivo: a major role for B cells in presenting antigen to T cells in lymph nodes. J. Immunol. 138:2848-2856.
43. Epstein, M.M., F. Di Rosa, D. Jankovic, A. Sher, and P. Matzinger. 1995. Successful T cell priming in B cell-deficient mice. J. Exp. Med. 182:915-922.
44. Matzinger, P. 1994. Tolerance, danger and the extended family. Annu. Rev. Immunol. 12:991-1045.
45. Beutner, U., E. Kraus, D. Kitamura, K. Rajewsky, and B. Huber. 1994. B cells are essential for murine mammary tumor virus transmission, but not for presentation of endogenous superantigens. J. Exp. Med. 179:1457-1466.
46. Chervonsky, A.V., J. Xu, A. Barlow, M. Khery, R.A. Flavell, and C.A. Janeway. 1995. Direct physical interaction involving CD40 ligand on T cells and CD40 on B cells is required to propagate MMTV. Immunity. 3:139-146.
47. Pullen, A.M., P. Marrack, and J.W. Kappler. 1988 The T cell receptor is heavily influenced by tolerance to polymorphic self-antigens. Nature (Lond.). 335:796-801.
48. a J. Exp. Med. 170:595-600.
49. Modlin, C.S., G.T. Todd, T.D. Cohen, and R.L. Fairchild. 1995. Transfer of endogenous retroviral superantigen from donor to recipient B cells following priming to induce peripheral T cell tolerance. Cell. Immunol. 164:217-226.
50. Raposo, G., H.W. Nijman, W. Stoorvogel, R. Leijendekker, C.V. Harding, C.J.M. Melief, and H.J. Geuze. 1996. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 183:1161-1172.
51. Pulendran, B., G. Kannourakis, S. Nouri, K.G.C. Smith and G.J.V. Nossal. 1995. Soluble antigen can cause enhanced apoptosis of germinal center B cells. Nature (Lond) 375:331-334.
52. Shokat, K.M., and C.C. Goodnow. 1995. Antigen-induced B cell death and elimination during germinal center immune responses. Nature (Lond.). 375:334-338.
53. Han, S.H., B. Zheng, J.D. Porto, and G. Kelsoe. 1995. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. IV. Affinity-dependent, antigen-driven B-cell apoptosis in germinal centers as a mechanism for maintaining self-tolerance. J. Exp. Med. 182:1635-1644.
54. Bachmann, M.F., B. Odermatt, H. Hengartner, and R.M. Zinkernagel. 1996. Induction of long-lived germinal centers associated with persisting antigen after viral infection. J. Exp. Med. 183:2259-2269.
55. Champagne, E., L. Scarpellino, P. Lane, and H. Acha-Orbea 1996. CD28/CTLA4-B7 interaction is dispensable for T cell stimulation by mouse mammary tumor virus superantigen but not for B cell differentiation and virus dissemination. Eur. J. Immunol. 26:1595-1602.
56. Brocke, S., A. Gaur, C. Piercy, A. Gautam, K. Gijbels, C.G. Fathman, and L. Steinman. 1993. Induction of relapsing paralysis in experimental autoimmune encephalomyelitis by bacterial superantigen. Nature (Lond.). 365:642-644.
57. Schiffenbauer, J., H.M. Johnson, E.J. Butfiloski, L. Wegrzyn, and J.M. Soos. 1993. Staphilococcal enterotoxins can reactivate experimental allergic encephalomyelitis. Proc. Natl. Acad. Sci. USA. 90:8543-8546.
58. McCormack, J.E.J., Kappler, and P. Marrack. 1994. Stimulation with specific antigen can block superantigen-mediated deletion of T cells in vivo. Proc. Natl. Acad. Sci. USA. 91: 2086-2090.