Terminal B cell differentiation is skewed by deregulated interleukin-6 secretion in β2 integrin-deficient mice

Journal of Leukocyte Biology

Volumn 80, Issue 3, 2006, Pages 599-607

  Peters, Thorsten ^a   Bloch, Wilhelm ^c   Wickenhauser, Claudia ^b   Tawadros, Samir ^b   Oreshkova, Tsvetelina ^a   Kess, Daniel ^a   Krieg, Thomas ^b   Müller, Werner ^d   Scharffetter Kochanek, Karin ^a  

^a UNIVERSITY OF ULM   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c Institute of Cardiovascular Research and Sports Medicine   (Germany)

^d HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

Animal models; Hypergammaglobulinemia; Mott cells; Proinflammatory cytokines

Indexed keywords

BETA2 INTEGRIN; CD18 ANTIGEN; IMMUNOGLOBULIN G; INTERLEUKIN 6; LIPOPOLYSACCHARIDE;

AMINO ACID BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL FUNCTION; CELL STRUCTURE; CONTROLLED STUDY; CYTOKINE RELEASE; GERMFREE ANIMAL; HISTOLOGY; HYPERGAMMAGLOBULINEMIA; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOGLOBULIN PRODUCTION; LEUKOCYTE ADHESION DEFICIENCY; LYMPHOID TISSUE; MOUSE; NONHUMAN; PHENOTYPE; PLASMA CELL; PLASMACYTOSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS;

ANIMALS; ANTIGENS, CD18; B-LYMPHOCYTES; CELL DIFFERENTIATION; DOWN-REGULATION; IMMUNOGLOBULIN G; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT;

ANIMALIA; BACTERIA (MICROORGANISMS);

EID: 33751502444     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1205740     Document Type: Article

References (61)

1. Anderson, D. C., Miller, L. J., Schmalstieg, F. C., Rothlein, R., Springer, T. A. (1986) Contributions of the Mac-1 glycoprotein family to adherence-dependent granulocyte functions: structure-function assessments employing subunit-specific monoclonal antibodies. J. Immunol. 137, 15-27.
2. Hynes, R. O. (1987) Integrins: a family of cell surface receptors. Cell 48, 549-554.
3. Arnaout, M. A. (1990) Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood 75, 1037-1050.
4. Van der Vieren, M., Le Trong, H., Wood, C. L., Moore, P. F., St John, T., Staunton, D. E., Gallatin, W. M. (1995) A novel leukointegrin, α d β 2, binds preferentially to ICAM-3. Immunity 3, 683-690.
5. Beatty, P. G., Ochs, H. D., Harlan, J. M., Price, T. H., Rosen, H., Taylor, R. F., Hansen, J. A., Klebanoff, S. J. (1984) Absence of monoclonal-antibody-defined protein complex in boy with abnormal leucocyte function. Lancet 1, 535-537.
6. Kishimoto, T. K., Hollander, N., Roberts, T. M., Anderson, D. C., Springer, T. A. (1987) Heterogeneous mutations in the β subunit common to the LFA-1, Mac-1, and p150,95 glycoproteins cause leukocyte adhesion deficiency. Cell 50, 193-202.
7. Kuijpers, T. W., Van Lier, R. A., Hamann, D., de Boer, M., Thung, L. Y., Weening, R. S., Verhoeven, A. J., Roos, D. (1997) Leukocyte adhesion deficiency type 1 (LAD-1)/variant. A novel immunodeficiency syndrome characterized by dysfunctional β2 integrins. J. Clin. Invest. 100, 1725-1733.
8. Fischer, A., Trung, P. H., Descamps-Latscha, B., Lisowska-Grospierre, B., Gerota, I., Perez, N., Scheinmetzler, C., Durandy, A., Virelizier, J. L., Griscelli, C. (1983) Bone-marrow transplantation for inborn error of phagocytic cells associated with defective adherence, chemotaxis, and oxidative response during opsonized particle phagocytosis. Lancet 2, 473-476.
9. Anderson, D. C., Schmalsteig, F. C., Finegold, M. J., Hughes, B. J., Rothlein, R., Miller, L. J., Kohl, S., Tosi, M. F., Jacobs, R. L., Waldrop, T. C., et al. (1985) The severe and moderate phenotypes of heritable Mac-1, LFA-1 deficiency: their quantitative definition and relation to leukocyte dysfunction and clinical features. J. Infect. Dis. 152, 668-689.
10. Ochs, H. D., Nonoyama, S., Zhu, Q., Farrington, M., Wedgwood, R. J. (1993) Regulation of antibody responses: the role of complement and adhesion molecules. Clin. Immunol. Immunopathol. 67, S33-S40.
11. Fischer, A., Durandy, A., Sterkers, G., Griscelli, C. (1986) Role of the LFA-1 molecule in cellular interactions required for antibody production in humans. J. Immunol. 136, 3198-3203.
12. Scharffetter-Kochanek, K., Lu, H., Norman, K., van Nood, N., Munoz, F., Grabbe, S., McArthur, M., Lorenzo, I., Kaplan, S., Ley, K., Smith, C. W., Montgomery, C. A., Rich, S., Beaudet, A. L. (1998) Spontaneous skin ulceration and defective T cell function in CD18 null mice. J. Exp. Med. 188, 119-131.
13. Peters, T., Sindrilaru, A., Hinz, B., Hinrichs, R., Menke, A., Al-Azzeh, E. A., Holzwarth, K., Oreshkova, T., Wang, H., Kess, D., Walzog, B., Sulyok, S., Sunderkotter, C., Friedrich, W., Wlaschek, M., Krieg, T., Scharffetter- Kochanek, K. (2005) Wound-healing defect of CD18(-/-) mice due to a decrease in TGF-β1 and myofibroblast differentiation. EMBO J. 24, 3400-3410.
14. Kishimoto, T. (1989) The biology of interleukin-6. Blood 74, 1-10.
15. Kishimoto, T., Taga, T., Yamasaki, K., Matsuda, T., Tang, B., Muraguchi, A., Horii, Y., Suematsu, S., Hirata, Y., Yawata, H., et al. (1989) Normal and abnormal regulation of human B cell differentiation by a new cytokine, BSF2/IL-6. Adv. Exp. Med. Biol. 254, 135-143.
16. Suematsu, S., Matsuda, T., Aozasa, K., Akira, S., Nakano, N., Ohno, S., Miyazaki, J., Yamamura, K., Hirano, T., Kishimoto, T. (1989) IgG1 plasmacytosis in interleukin 6 transgenic mice. Proc. Natl. Acad. Sci. USA 86, 7547-7551.
17. Hirano, T., Kishimoto, T. (1989c) Interleukin-6: possible implications in human diseases. Ric. Clin. Lab. 19, 1-10.
18. Markine-Goriaynoff, D., Nguyen, T. D., Bigaignon, G., Van Snick, J., Coutelier, J. P. (2001) Distinct requirements for IL-6 in polyclonal and specific Ig production induced by microorganisms. Int. Immunol. 13, 1185-1192.
19. Pabst, O., Peters, T., Czeloth, N., Bernhardt, G., Scharffetter-Kochanek, K., Forster, R. (2005) Cutting edge: egress of newly generated plasma cells from peripheral lymph nodes depends on β 2 integrin. J. Immunol. 174, 7492-7495.
20. Brandt, S. J., Bodine, D. M., Dunbar, C. E., Nienhuis, A. W. (1990) Dysregulated interleukin 6 expression produces a syndrome resembling Castleman's disease in mice. J. Clin. Invest. 86, 592-599.
21. Hirano, T., Kishimoto, T. (1989b) Interleukin-6 and plasma cell neoplasias. Prog. Growth Factor Res. 1, 133-142.
22. Yoshizaki, K., Matsuda, T., Nishimoto, N., Kuritani, T., Taeho, L., Aozasa, K., Nakahata, T., Kawai, H., Tagoh, H., Komori, T., et al. (1989) Pathogenic significance of interleukin-6 (IL-6/BSF-2) in Castleman's disease. Blood 74, 1360-1367.
23. Kopf, M., Baumann, H., Freer, G., Freudenberg, M., Lamers, M., Kishimoto, T., Zinkernagel, R., Bluethmann, H., Kohler, G. (1994) Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368, 339-342.
24. Harriman, G. R., Kunimoto, D. Y., Elliott, J. F., Paetkau, V., Strober, W. (1988) The role of IL-5 in IgA B cell differentiation. J. Immunol. 140, 3033-3039.
25. Sunderkötter, C., Kunz, M., Steinbrink, K., Meinardus-Hager, G., Goebeler, M., Bildau, H., Sorg, C. (1993) Resistance of mice to experimental Leishmaniasis is associated with more rapid appearance of mature macrophages in vitro and in vivo. J. Immunol. 151, 4891-4901.
26. Hope, J. C., Cumberbatch, M., Fielding, I., Dearman, R. J., Kimber, I., Hopkins, S. J. (1995) Identification of dendritic cells as a major source of interleukin-6 in draining lymph nodes following skin sensitization of mice. Immunology 86, 441-447.
27. Schnurr, M., Toy, T., Shin, A., Hartmann, G., Rothenfusser, S., Soellner, J., Davis, I. D., Cebon, J., Maraskovsky, E. (2004) Role of adenosine receptors in regulating chemotaxis and cytokine production of plasmacytoid dendritic cells. Blood 103, 1391-1397.
28. Nordan, R. P., Potter, M. (1986) A macrophage-derived factor required by plasmacytomas for survival and proliferation in vitro. Science 233, 566-569.
29. Coutelier, J. P., Coulie, P. G., Wauters, P., Heremans, H., van der Logt, J. T. (1990) In vivo polyclonal B-lymphocyte activation elicited by murine viruses. J. Virol. 64, 5383-5388.
30. Izui, S., Eisenberg, R. A., Dixon, F. J. (1981) Subclass-restricted IgG polyclonal antibody production in mice injected with lipid A-rich lipopolysaccharides. J. Exp. Med. 153, 324-338.
31. Vink, A., Coulie, P. G., Wauters, P., Nordan, R. P., Van Snick, J. (1988) B cell growth and differentiation activity of interleukin-HP1 and related murine plasmacytoma growth factors. Synergy with interleukin 1. Eur. J. Immunol. 18, 607-612.
32. Kawano, Y., Noma, T., Yata, J. (1994) Regulation of human IgG subclass production by cytokines. IFN-γ and IL-6 act antagonistically in the induction of human IgG1 but additively in the induction of IgG2. J. Immunol. 153, 4948-4958.
33. Grabbe, S., Varga, G., Beissert, S., Steinert, M., Pendl, G., Seeliger, S., Bloch, W., Peters, T., Schwarz, T., Sunderkotter, C., Scharffetter-Kochanek, K. (2002) β2 integrins are required for skin homing of primed T cells but not for priming naive T cells. J. Clin. Invest. 109, 183-192.
34. Kopf, M., Herren, S., Wiles, M. V., Pepys, M. B., Kosco-Vilbois, M. H. (1998) Interleukin 6 influences germinal center development and antibody production via a contribution of C3 complement component. J. Exp. Med. 188, 1895-1906.
35. Camacho, S. A., Kosco-Vilbois, M. H., Berek, C. (1998) The dynamic structure of the germinal center. Immunol. Today 19, 511-514.
36. Valetti, C., Grossi, C. E., Milstein, C., Sitia, R. (1991) Russell bodies: a general response of secretory cells to synthesis of a mutant immunoglobulin which can neither exit from, nor be degraded in, the endoplasmic reticulum. J. Cell Biol. 115, 983-994.
37. Jack, H. M., Beck-Engeser, G., Sloan, B., Wong, M. L., Wabl, M. (1992) A different sort of Mott cell. Proc. Natl. Acad. Sci. USA 89, 11688-11691.
38. Alanen, A., Pira, U., Lassila, O., Roth, J., Franklin, R. M. (1985) Mott cells are plasma cells defective in immunoglobulin secretion. Eur. J. Immunol. 15, 235-242.
39. Gebbers, J. O., Otto, H. F. (1976) Plasma cell alterations in ulcerative colitis. An electron microscopic study. Pathol. Eur. 11, 271-279.
40. Jiang, Y., Hirose, S., Hamano, Y., Kodera, S., Tsurui, H., Abe, M., Terashima, K., Ishikawa, S., Shirai, T. (1997) Mapping of a gene for the increased susceptibility of B1 cells to Mott cell formation in murine autoimmune disease. J. Immunol. 158, 992-997.
41. Walzog, B., Scharffetter-Kochanek, K., Gaehtgens, P. (1999) Impairment of neutrophil emigration in CD18-null mice. Am. J. Physiol. 276, G1125-G1130.
42. van Spriel, A. B., Leusen, J. H., van Egmond, M., Dijkman, H. B., Assmann, K. J., Mayadas, T. N., van de Winkel, J. G. (2001) Mac-1 (CD11b/CD18) is essential for Fc receptor-mediated neutrophil cytotoxicity and immunologic synapse formation. Blood 97, 2478-2486.
43. Carrasco, Y. R., Fleire, S. J., Cameron, T., Dustin, M. L., Batista, F. D. (2004) LFA-1/ICAM-1 interaction lowers the threshold of B cell activation by facilitating B cell adhesion and synapse formation. Immunity 20, 589-599.
44. Perez, O. D., Mitchell, D., Jager, G. C., South, S., Murriel, C., McBride, J., Herzenberg, L. A., Kinoshita, S., Nolan, G. P. (2003) Leukocyte functional antigen 1 lowers T cell activation thresholds and signaling through cytohesin-1 and Jun-activating binding protein 1. Nat. Immunol. 4, 1083-1092.
45. Matsumoto, G., Omi, Y., Lee, U., Nishimura, T., Shindo, J., Penninger, J. M. (2000) Adhesion mediated by LFA-1 is required for efficient IL-12-induced NK and NKT cell cytotoxicity. Eur. J. Immunol. 30, 3723-3731.
46. Riteau, B., Barber, D. F., Long, E. O. (2003) Vav1 phosphorylation is induced by β2 integrin engagement on natural killer cells upstream of actin cytoskeleton and lipid raft reorganization. J. Exp. Med. 198, 469-474.
47. Hamann, D., Baars, P. A., Rep, M. H., Hooibrink, B., Kerkhof-Garde, S. R., Klein, M. R., van Lier, R. A. (1997) Phenotypic and functional separation of memory and effector human CD8+ T cells. J. Exp. Med. 186, 1407-1418.
48. Huleatt, J. W., Lefrancois, L. (1996) β2 integrins and ICAM-1 are involved in establishment of the intestinal mucosal T cell compartment. Immunity 5, 263-273.
49. Weinmann, P., Scharffetter-Kochanek, K., Forlow, S. B., Peters, T., Walzog, B. (2003) A role for apoptosis in the control of neutrophil homeostasis in the circulation: insights from CD18-deficient mice. Blood 101, 739-746.
50. Ochsenbein, A. F., Fehr, T., Lutz, C., Suter, M., Brombacher, F., Hengartner, H., Zinkernagel, R. M. (1999) Control of early viral and bacterial distribution and disease by natural antibodies. Science 286, 2156-2159.
51. Goodman-Snitkoff, G., Mannino, R. J., McSharry, J. J. (1981) The glycoprotein isolated from vesicular stomatitis virus is mitogenic for mouse B lymphocytes. J. Exp. Med. 153, 1489-1502.
52. Chelvarajan, R. L., Collins, S. M., Doubinskaia, I. E., Goes, S., Van Willigen, J., Flanagan, D., De Villiers, W. J., Bryson, J. S., Bondada, S. (2004) Defective macrophage function in neonates and its impact on unresponsiveness of neonates to polysaccharide antigens. J. Leukoc. Biol. 75, 982-994.
53. Paterson, H. M., Murphy, T. J., Purcell, E. J., Shelley, O., Kriynovich, S. J., Lien, E., Mannick, J. A., Lederer, J. A. (2003) Injury primes the innate immune system for enhanced Toll-like receptor reactivity. J. Immunol. 171, 1473-1483.
54. Iwakoshi, N. N., Lee, A. H., Glimcher, L. H. (2003) The X-box binding protein-1 transcription factor is required for plasma cell differentiation and the unfolded protein response. Immunol. Rev. 194, 29-38.
55. Gunn, K. E., Gifford, N. M., Mori, K., Brewer, J. W. (2004) A role for the unfolded protein response in optimizing antibody secretion. Mol. Immunol. 41, 919-927.
56. Taga, T., Kawanishi, Y., Hardy, R. R., Hirano, T., Kishimoto, T. (1987) Receptors for B cell stimulatory factor 2. Quantitation, specificity, distribution, and regulation of their expression. J. Exp. Med. 166, 967-981.
57. Hirano, T., Taga, T., Yasukawa, K., Nakajima, K., Nakano, N., Takatsuki, F., Shimizu, M., Murashima, A., Tsunasawa, S., Sakiyama, F., et al. (1987) Human B-cell differentiation factor defined by an anti-peptide antibody and its possible role in autoantibody production. Proc. Natl. Acad. Sci. USA 84, 228-231.
58. Kawano, M., Hirano, T., Matsuda, T., Taga, T., Horii, Y., Iwato, K., Asaoku, H., Tang, B., Tanabe, O., Tanaka, H., et al. (1988) Autocrine generation and requirement of BSF-2/IL-6 for human multiple myelomas. Nature 332, 83-85.
59. Suzuki, H., Yasukawa, K., Saito, T., Goitsuka, R., Hasegawa, A., Ohsugi, Y., Taga, T., Kishimoto, T. (1992) Anti-human interleukin-6 receptor antibody inhibits human myeloma growth in vivo. Eur. J. Immunol. 22, 1989-1993.
60. Nishimoto, N., Sasai, M., Shima, Y., Nakagawa, M., Matsumoto, T., Shirai, T., Kishimoto, T., Yoshizaki, K. (2000) Improvement in Castleman's disease by humanized anti-interleukin-6 receptor antibody therapy. Blood 95, 56-61.
61. Weyand, C. M., Fulbright, J. W., Hunder, G. G., Evans, J. M., Goronzy, J. J. (2000) Treatment of giant cell arteritis: interleukin-6 as a biologic marker of disease activity. Arthritis Rheum. 43, 1041-1048.