Interleukin 6 influences germinal center development and antibody production via a contribution of C3 complement component

Journal of Experimental Medicine

Volumn 188, Issue 10, 1998, Pages 1895-1906

  Kopf, Manfred ^a   Herren, Suzanne ^b,e   Wiles, Michael V ^c   Pepys, Mark B ^d   Kosco Vilbois, Marie H ^b,e  

^a BASEL INSTITUTE FOR IMMUNOLOGY   (Switzerland)

^b GLAXOSMITHKLINE   (United States)

^c MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^d HAMMERSMITH HOSPITAL   (United Kingdom)

^e SERONO PHARMACEUTICAL RES INSTITUTE   (Switzerland)

Author keywords

Antibody; Complement; Follicular dendritic cells; Germinal center; Interleukin 6

Indexed keywords

ANTIBODY; B7 ANTIGEN; COMPLEMENT COMPONENT C3; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN M; INTERLEUKIN 6;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY TITER; ANTIGEN EXPRESSION; ARTICLE; DENDRITIC CELL; DEVELOPMENT; GERMINAL CENTER; IMMUNE DEFICIENCY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBODIES; COMPLEMENT C3; CYTOKINES; GERMINAL CENTER; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-6; MICE; MICE, KNOCKOUT; RNA, MESSENGER; T-LYMPHOCYTES; TH1 CELLS; TH2 CELLS;

EID: 0032538991     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.188.10.1895     Document Type: Article

References (91)

1. van Snick, J. 1990. Interleukin-6: an overview. Annu. Rev. Immunol. 8:253-278.
2. Kishimoto, T., S. Akira, and T. Taga. 1992. Interleukin-6 and its receptor: a paradigm for cytokines. Science. 258:593-597.
3. Geiger, T., T. Andus, J. Klapproth, T. Hirano, T. Kishimoto, and P.C. Heinrich. 1988. Induction of rat acute-phase proteins by interleukin 6 in vivo. Eur. J. Immunol. 18:717-721.
4. Kopf, M., H. Baumann, G. Freer, M. Freudenberg, M. Lamers, T. Kishimoto, R. Zinkernagel, H. Bluethmann, and G. Kohler. 1994. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature. 368:339-342.
5. Helle, M., J.P. Brakenhoff, E.R. de Groot, and L.A. Aarden. 1988. Interleukin 6 is involved in interleukin 1-induced activities. Eur. J. Immunol. 18:957-959.
6. Marinkovic, S., G.P. Jahreis, G.G. Wong, and H. Baumann. 1989. Il-6 modulates the synthesis of a specific set of acute phase plasma proteins in vivo. J. Immunol. 142:808-812.
7. Hoang, T., A. Haman, O. Goncalves, G.G. Wong, and S.C. Clark. 1988. Interleukin-6 enhances growth factor-dependent proliferation of the blast cells of acute myeloblastic leukemia. Blood. 72:823-826.
8. Bot, F.J., L. van Eijk, L. Broeders, L.A. Aarden, and B. Lowenberg. 1989. Interleukin-6 synergizes with M-CSF in the formation of macrophage colonies from purified human marrow progenitor cells. Blood. 73:435-437.
9. Nordan, R.P., and M. Potter. 1986. A macrophage-derived factor required by plasmacytomas for survival and proliferation in vitro. Science. 233:566-569.
10. van Snick, J., A. Vink, S. Cayphas, and C. Uyttenhove. 1987. Interleukin-hp1, a T cell-derived hybridoma growth factor that supports the in vitro growth of murine plasmacytomas. J. Exp. Med. 165:641-649.
11. van Snick, J., S. Cayphas, A. Vink, C. Uyttenhove, P.G. Coulie, M.R. Rubira, and R.J. Simpson. 1986. Purification and NH2-terminal amino acid sequence of a T-cell-derived lymphokine with growth factor activity for B-cell hybridomas. Proc. Natl. Acad. Sci. USA. 83:9679-9683.
12. Weissenbach, J., Y. Chernajovsky, M. Zeevi, L. Shulman, H. Soreq, U. Nir, D. Wallach, M. Perricaudet, P. Tiollais, and M. Revel. 1980. Two interferon mRNAs in human fibroblasts: in vitro translation and Escherichia coli cloning studies. Proc. Natl. Acad. Sci. USA. 77:7152-7156.
13. Corbel, C., and F. Melchers. 1984. The synergism of accessory cells and of soluble alpha-factors derived from them in the activation of Bb cells to proliferation. Immunol. Rev. 78: 51-74.
14. Hirano, T., T. Taga, N. Nakano, K. Yasukawa, S. Kashiwamura, K. Shimizu, K. Nakajima, K.H. Pyun, and T. Kishimoto. 1985. Purification to homogeneity and characterization of human B-cell differentiation factor (BCDF or BSFP-2). Proc. Natl. Acad. Sci. USA. 82:5490-5494.
15. Burdin, N., L. Galibert, P. Garrone, I. Durand, J. Banchereau, and F. Rousset. 1996. Inability to produce IL-6 is a functional feature of human germinal center B lymphocytes. J. Immunol. 156:4107-4113.
16. de Vries, J.E., and G. Zurawski. 1995. Immunoregulatory properties of IL-13: its potential role in atopic disease. Int. Arch. Allergy Immunol. 106:175-179.
17. Taga, T., M. Hibi, Y. Hirata, K. Yamasaki, K. Yasukawa, T. Matsuda, T. Hirano, and T. Kishimoto. 1989. Interleukin-6 triggers the association of its receptor with a possible signal transducer, gp130. Cell. 58:573-581.
18. Kishimoto, T. 1989. The biology of interleukin-6. Blood. 74: 1-10.
19. Brandt, S.J., D.M. Bodine, C.E. Dunbar, and A.W. Nienhuis. 1990. Dysregulated interleukin 6 expression produces a syndrome resembling Castleman's disease in mice. J. Clin. Invest. 86:592-599.
20. Suematsu, S., T. Matsuda, K. Aozasa, S. Akira, N. Nakano, S. Ohno, J. Miyazaki, K. Yamamura, T. Hirano, and T. Kishimoto. 1989. IgG1 plasmacytosis in interleukin 6 transgenic mice. Proc. Natl. Acad. Sci. USA. 86:7547-7551.
21. Oka, Y., A.G. Rolink, S. Suematsu, T. Kishimoto, and F. Melchers. 1995. An interleukin-6 transgene expressed in B lymphocyte lineage cells overcomes the T cell-dependent establishment of normal levels of switched immunoglobulin isotypes. Eur. J. Immunol. 25:1332-1337.
22. 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.
23. 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. 176:679-687.
24. Kelsoe, G. 1995. In situ studies of the germinal center reaction. Adv. Immunol. 60:267-288.
25. MacLennan, I.C.M., A. Gulbranson-Judge, K.M. Toellner, M. Casamayor-Palleja, E. Chan, D.M.Y. Sze, S.A. Luther, and H. Acha Orbea. 1997. The changing preference of T and B cells for partners as T-dependent antibody responses develop. Immunol. Rev. 156:53-66.
26. Garside, P., E. Ingulli, R.R. Merica, J.G. Johnson, R.J. Noelle, and M.K. Jenkins. 1998. Visualization of specific B and T lymphocyte interactions in the lymph node. Science. 281: 96-99.
27. Kosco, M.H., A.K. Szakal, and J.G. Tew. 1988. In vivo obtained antigen presented by germinal center B cells to T cells in vitro. J. Immunol. 140:354-360.
28. Kosco-Vilbois, M.H., D. Gray, D. Scheidegger, and M. Julius. 1993. Follicular dendritic cells help resting B cells to become effective antigen-presenting cells: induction of B7/bb1 and upregulation of major histocompatibility complex class II molecules. J. Exp. Med. 178:2055-2066.
29. Guery, J.C., F. Ria, and L. Adorini. 1996. Dendritic cells but not B cells present antigenic complexes to class II-restricted T cells after administration of protein in adjuvant. J. Exp. Med. 183:751-757.
30. Kosco-Vilbois, M.H., J.Y. Bonnefoy, and Y. Chvatchko. 1997. The physiology of murine germinal center reactions. Immunol. Rev. 156:127-136.
31. Kosco-Vilbois, M.H., H. Zentgraf, J. Gerdes, and J.Y. Bonnefoy. 1997. To 'b' or not to 'b' a genal center. Immunol. Today. 18:225-230.
32. Tew, J.G., J. Wu, D. Qin, S. Helm, G.F. Burton, and A.K. Szakal. 1997. Follicular dendritic cells and presentation of antigen and costimulatory signals to B cells. Immunol. Rev. 156: 39-52.
33. Berek, C., A. Berger, and M. Apel. 1991. Maturation of the immune response in germinal centers. Cell. 67:1121-1129.
34. Jacob, J., G. Kelsoe, K. Rajewsky, and U. Weiss. 1991. Intraclonal generation of antibody mutants in germinal centres. Nature. 354:389-392.
35. MacLennan, I.C., and D. Gray. 1986. Antigen-driven selection of virgin and memory B cells. Immunol. Rev. 91:61-85.
36. Smith, K.G., G.J. Nossal, and D.M. Tarlinton. 1995. FAS is highly expressed in the germinal center but is not required for regulation of the B-cell response to antigen. Proc. Natl. Acad. Sci. USA. 92:11628-11632.
37. 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.
38. Pepys, M.B. 1972. Role of complement in induction of the allergic response. Nat. New Biol. 237:157-159.
39. Pepys, M.B. 1976. Role of complement in the induction of immunological responses. Transplant. Rev. 32:93-120.
40. Pepys, M.B. 1974. Role of complement in induction of antibody production in vivo. J. Exp. Med. 140:126-145.
41. Pepys, M.B. 1975. Studies in vivo of cobra venom factor and murine C3. Immunology. 28:369-377.
42. Papamichail, M., C. Gutierrez, P. Embling, P. Johnson, J. Holborow, and M. Pepys. 1975. Complement dependence of germinal center localization of aggregated γ-globulin. Scand. J. Immunol. 4:343-347.
43. Phillips, M.E., and G.J. Thorbecke. 1965. Serum protein formation of donor type in rat into mouse chimeras. Nature. 207:376-378.
44. Feldmann, M., and M.B. Pepys. 1974. Role of C3 in in vitro lymphocyte cooperation. Nature. 249:159-161.
45. Pepys, M. 1974. Complement-mediated mixed aggregation of murine spleen cells. Nature. 249:51-53.
46. Ahearn, J.M., M.B. Fischer, D. Croix, S. Goerg, M. Ma, J. Xia, X. Zhou, R.G. Howard, T.L. Rothstein, and M.C. Carroll. 1996. Disruption of the Cr2 locus results in a reduction in B-1a cells and in an impaired B cell response to T-dependent antigen. Immunity. 4:251-262.
47. Fischer, M.B., M. Ma, S. Goerg, X. Zhou, J. Xia, O. Finco, S. Han, G. Kelsoe, R.G. Howard, T.L. Rothstein, et al. 1996. Regulation of the B cell response to T-dependent antigen by classical pathway complement. J. Immunol. 157:549-556.
48. Fischer, M.B., M. Ma, N.C. Hsu, and M.C. Carroll. 1998. Local synthesis of C3 within the splenic lymphoid compartment can reconstitute the impaired immune response in C3 deficient mice. J. Immunol. 160:2619-2625.
49. Gray, D., M. Kosco, and B. Stockinger. 1991. Novel pathways of antigen presentation for the maintenance of memory. Int. Immunol. 3:141-148.
50. Baniyash, M., and Z. Eshhar. 1984. Inhibition of IgE binding to mast cells and basophils by monoclonal antibodies to murine IgE. Eur. J. Immunol. 14:799-807.
51. Coico, R.F., B.S. Bhogal, and G.J. Thorbecke. 1983. Relationship of germinal centers in lymphoid tissue to immunological memory. VI. Transfer of B cell memory with lymph node cells fractionalted according to their receptors for peanut agglutinin. J. Immunol. 131:2254-2257.
52. Szakal, A.K., J.K. Taylor, J.P. Smith, M.H. Kosco, G.F. Burton, and J.J. Tew. 1990. Kinetics of germinal center development in lymph nodes of young and aging immune mice. Anat. Rec. 227:475-485.
53. Kosco, M.H., E. Pflugfelder, and D. Gray. 1992. Follicular dendritic cell-dependent adhesion and proliferation of B cells in vitro. J. Immunol. 148:2331-2339.
54. Pepys, M.B., A.C. Dash, A.H. Fielder, and D.D. Mirjah. 1977. Isolation and study of murine c3. Immunology. 33: 491-499.
55. Kopf, M., F. Brombacher, G. Kohler, G. Kienzle, K.H. Widmann, K. Lefrang, C. Humborg, B. Ledermann, and W. Solbach. 1996. IL-4-deficient BALB/c mice resist infection with Leishmania major. J. Exp. Med. 184:1127-1136.
56. Heyman, B., E.J. Wiersma, and T. Kinoshita. 1990. In vivo inhibition of the antibody response by a complement receptor-specific monoclonal antibody. J. Exp. Med. 172:665-668.
57. Johansson, B.M., and M.V. Wiles. 1995. Evidence for involvement of activin a and bone morphogenetic protein 4 in mammalian mesoderm and hematopoietic development. Mol. Cell Biol. 15:141-151.
58. Keller, G., M. Kennedy, T. Papayannopoulou, and M.V. Wiles. 1993. Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol. Cell Biol. 13:473-486.
59. Kosco-Vilbois, M.H. 1997. Isolation and enrichment of follicular dendritic cells from murine lymphoid tissue. In Immunology Methods Manual. I. Lefkovits, editor. Academic Press, London, UK. 1468-1473.
60. + T cells. J. Exp. Med. 179:819-830.
61. Borriello, F., M.P. Sethna, S.D. Boyd, A.N. Schweitzer, E.A. Tivol, D. Jacoby, T.B. Strom, E.M. Simpson, G.J. Freeman, and A.H. Sharpe. 1997. B7-1 and B7-2 have overlapping, critical roles in immunoglobulin class switching and germinal center formation. Immunity. 6:303-313.
62. Kawabe, T., T. Naka, K. Yoshida, T. Tanaka, H. Fujiwara, S. Suematsu, N. Yoshida, T. Kishimoto, and H. Kikutani. 1994. The immune responses in CD40-deficient mice: impaired immunoglobulin class switching and germinal center formation. Immunity. 1:167-178.
63. Le Hir, M., H. Bluethmann, M.H. Kosco-Vilbois, M. Muller, F. di Padova, M. Moore, B. Ryffel, and H.P. Eugster. 1996. Differentiation of follicular dendritic cells and full antibody responses require tumor necrosis factor receptor-1 signaling. J. Exp. Med. 183:2367-2372.
64. Sethna, M.P., L. van Parijs, A.H. Sharpe, A.K. Abbus, and G.J. Freeman. 1994. A negative regulatory function of B7 revealed in B7-1 transgenic mice. Immunity. 1:415-421.
65. Carter, R.H., M.O. Spycher, Y.C. Ng, R. Hoffman, and D.T. Fearon. 1988. Synergistic interaction between complement receptor type 2 and membrane igm on B lymphocytes. J. Immunol. 141:457-463.
66. Carter, R.H., and D.T. Fearon. 1992. CD19: lowering the threshold for antigen receptor stimulation of B lymphocytes. Science. 256:105-107.
67. Morse, L., D. Chen, D. Franklin, Y. Xiong, and S. Chen-Kiang. 1997. Induction of cell cycle arrest and B cell terminal differentiation by cdk inhibitor p18(mk4c) and IL-6. Immunity. 6:47-56.
68. Kumanogoh, A., S. Marukawa, T. Kumanogoh, H. Hirota, K. Yoshida, I.S. Lee, T. Yasui, T. Taga, and T. Kishimoto. 1997. Impairment of antigen-specific antibody production in transgenic mice expressing a dominant-negative form of gp130. Proc. Natl. Acad. Sci. USA. 94:2478-2482.
69. Akira, S., K. Yoshida, T. Tanaka, T. Taga, and T. Kishimoto. 1995. Targeted disruption of the IL-6 related genes: gp130 and nf-IL-6. Immunol. Rev. 148:221-253.
70. Pepys, M., W. Brighton, B. Hewitt, D. Bryant, and J. Pepys. 1977. Complement in the induction of IgE antibody formation. Clin. Exp. Immunol. 27:397-400.
71. Rincón, M., J. Anguita, T. Nakamura, E. Fikrig, and R.A. Flavell. 1997. Interleukin (IL)-6 directs the differentiation of IL-4-producing CD4+ T cells. J. Exp. Med. 185:461-469.
72. Pulendran, B., R. van Driel, and G.J. Nossal. 1997. Immunological tolerance in germinal centres. Immunol. Today. 18:27-32.
73. Tew, J.G., M.H. Kosco, G.F. Burton, and A.K. Szakal. 1990. Follicular dendritic cells as accessory cells. Immunol. Rev. 117: 185-211.
74. Fang, Y., C. Xu, Y.X. Fu, V.M. Holers, and H. Molina. 1998. Expression of complement receptors 1 and 2 on follicular dendritic cells is necessary for the generation of a strong antigen-specific IgG response. J. Immunol. 160:5273-5279.
75. Fearon, D.T., and R.H. Carter. 1995. The CD19/CR2/ Tapa-1 complex of B lymphocytes: linking natural to acquired immunity. Annu. Rev. Immunol. 13:127-149.
76. Tedder, T.F., M. Inaoki, and S. Sato. 1997. The CD19-CD21 complex regulates signal transduction thresholds governing humoral immunity and autoimmunity. Immunity. 6:107-118.
77. Fischer, M.B., S. Goerg, L. Shen, A.P. Prodeus, C.C. Goodnow, G. Kelsoe, and M.C. Carroll. 1998. Dependence of germinal center B cells on expression of CD21/CD35 for survival. Science. 280:582-585.
78. Celada, A., M.J. Klemsz, and R.A. Maki. 1989. Interferon-γ activates multiple pathways to regulate the expression of the genes for major histocompatibility class II I-Aβ, tumor necrosis factor and complement component C3 in mouse macrophages. Eur. J. Immunol. 19:1103-1110.
79. Mitchell, T.J., M. Naughton, P. Norsworthy, K.A. Davies, M.J. Walport, and B.J. Morley. 1996. IFNγ up-regulates expression of complement components C3 and C4 by stabilization of mRNA. J. Immunol. 156:4429-4438.
80. Boettger, E.C., and D. Bitter-Suermann. 1987. Complement and the regulation of humoral immune responses. Immunol. Today. 8:261-265.
81. O'Neil, K.M., H.D. Ochs, S.R. Heller, L.C. Cork, J.M. Morris, and J.A. Winkelstein. 1988. Role of C3 in humoral immunity. Defective antibody production in C3-deficient dogs. J. Immunol. 140:1939-1945.
82. Ladel, C.H., C. Blum, A. Dreher, K. Reifenburg, M. Kopt, and S.H.E. Kaufmann. 1997. Lethal tuberculosis in IL-6 deficient mice. Infect. Immun. 65:4843-4849.
83. + T helper cell 1 development in interleukin 6-deficient mice infected with Candida albicans. J. Exp. Med. 183:1345-1355.
84. Ramsay, A.J., A.J. Husband, I.A. Ramshaw, S. Bao, K.I. Matthaei, G. Koehler, and M. Kopf. 1994. The role of interleukin-6 in mucosal IgA antibody responses in vivo. Science. 264:561-563.
85. Bromander, A.K., L. Ekman, M. Kopf, J.G. Nedrud, and N.Y. Lycke. 1996. IL-6-deficient mice exhibit normal mucosal IgA responses to local immunizations and helicobacter felis infection. J. Immunol. 156:4290-4297.
86. Cumberbatch, M., R.J. Dearman, and I. Kimber. 1996. Constitutive and inducible expression of interleukin-6 by Llangerhans cells and lymph node dendritic cells. Immunology. 87:513-518.
87. Steinman, R.M., M. Pack, and K. Inaba. 1997. Dendritic cells in the T cell areas of lymphoid organs. Immunol. Rev. 156:25-38.
88. Croix, D.A., J.M. Ahearn, A.M. Rosengard, S. Han, G. Kelsoe, M. Ma, and MC. Carroll. 1996. Antibody response to a T dependent antigen requires B cell expression of complement receptors. J. Exp. Med. 183:1857-1864.
89. Melchers, F., A. Erdei, T. Schulz, and M.P. Dierich. 1985. Growth control of activated, synchronized murine B cells by the C3d fragment of human complement. Nature. 317:264-267.
90. Cahen-Kramer, Y., I.L. Martensson, and F. Melchers. 1994. The structure of an alternate form of complement C3 that displays costimulatory growth factor activity for B lymphocytes. J. Exp. Med. 180:2079-2088.
91. Suematsu, S., T. Matsusaka, T. Matsuda, S. Ohno, J. Miyazaki, K. Yamamura, T. Hirano, and T. Kishimoto. 1992. Generation of plasmacytomas with the chromosomal translocation t(12;15) in interleukin 6 transgenic mice. Proc. Natl. Acad. Sci. USA. 89:232-235.