Differential Signaling via Tumor Necrosis Factor-Associated Factors (TRAFs) by CD27 and CD40 in Mouse B Cells

  • Woo, So-Youn (Department of Microbiology, College of Medicine, Ewha Womans University) ;
  • Park, Hae-Kyung (Department of Microbiology, College of Medicine, Ewha Womans University) ;
  • Bishop, Gail A. (Department of Microbiology, College of Medicine, Ewha Womans University)
  • Published : 2004.09.30

Abstract

Background: CD27 is recently known as a memory B cell marker and is mainly expressed in activated T cells, some B cell population and NK cells. CD27 is a member of tumor necrosis factor receptor family. Like CD40 molecule, CD27 has (P/S/T/A) X(Q/E)E motif for interacting with TNF receptor-associated factors (TRAFs), and TRAF2 and TRAF5 bindings to CD27 in 293T cells were reported. Methods: To investigate the CD27 signaling effect in B cells, human CD40 extracellular domain containing mouse CD27 cytoplamic domain construct (hCD40-mCD27) was transfected into mouse B cell line CH12.LX and M12.4.1. Results: Through the stimulation of hCD40-mCD27 molecule via anti-human CD40 antibody or CD154 ligation, expression of CD11a, CD23, CD54, CD70 and CD80 were increased and secretion of IgM was induced, which were comparable to the effect of CD40 stimulation. TRAF2 and TRAF3 were recruited into lipid-enriched membrane raft and were bound to CD27 in M12.4.1 cells. CD27 stimulation, however, did not increase TRAF2 or TRAF3 degradation. Conclusion: In contrast to CD40 signaling pathway, TRAF2 and TRAF3 degradation was not observed after CD27 stimulation and it might contribute to prolonged B cell activation through CD27 signaling.

Keywords

References

  1. Locksley RM, Killeen N, Lenardo MJ: The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104;487-501, 2001 https://doi.org/10.1016/S0092-8674(01)00237-9
  2. Brink R, Lodish HF: Tumor necrosis factor receptor (TNFR)- associated factor 2A (TRAF2A), a TRAF2 splice variant with an extended RING finger domain that inhibits TNFR2- mediated NF-kappaB activation. J Biol Chem 273;4129-4134, 1998 https://doi.org/10.1074/jbc.273.7.4129
  3. Bradley JR, Pober JS: Tumor necrosis factor receptor- associated factors (TRAFs). Oncogene 20;6482-6491, 2001 https://doi.org/10.1038/sj.onc.1204788
  4. Calderhead DM, Kosaka Y, Manning EM, Noelle RJ: CD40-CD154 interactions in B-cell signaling. Curr Top MicrobiolImmunol 245;73-99, 2000
  5. Rothe M, Sarma V, Dixit VM, Goeddel DV: TRAF2- mediated activation of NF-kappa B by TNF receptor 2 and CD40. Science 269;1424-1427, 1995 https://doi.org/10.1126/science.7544915
  6. Hu HM, O'Rourke K, Boguski MS, Dixit VM: A novel RING finger protein interacts with the cytoplasmic domain of CD40. J Biol Chem 269;30069-30072, 1994
  7. Ishida TK, Tojo T, Aoki T, Kobayashi N, Ohishi T, Watanabe T, Yamamoto T, Inoue J: TRAF5, a novel tumor necrosis factor receptor-associated factor family protein, mediates CD40 signaling. Proc Natl Acad Sci USA 93;9437-9442, 1996 https://doi.org/10.1073/pnas.93.18.9437
  8. Ishida T, Mizushima S, Azuma S, Kobayashi N, Tojo T, Suzuki K, Aizawa S, Watanabe T, Mosialos G, Kieff E, Yamamoto T, Inoue J: Identification of TRAF6, a novel tumor necrosis factor receptor-associated factor protein that mediates signaling from an amino-terminal domain of the CD40 cytoplasmic region. J Biol Chem 271;28745-29748, 1996 https://doi.org/10.1074/jbc.271.46.28745
  9. Bishop GA, Hostager BS: Molecular mechanisms of CD40 signaling. Arch Immunol Ther Exp 49;129-137, 2001
  10. Ahonen C, Manning E, Erickson LD, O'Connor B, Lind EF, Pullen SS, Kehry MR, Noelle RJ: The CD40-TRAF6 axis controls affinity maturation and the generation of long-lived plasma cells. Nat Immunol 3;451-456, 2002 https://doi.org/10.1038/ni792
  11. van Lier RA, Borst J, Vroom TM, Klein H, Van Mourik P, Zeijlemaker WP, Melief CJ: Tissue distribution and biochemical and functional properties of Tp55 (CD27), a novel T cell differentiation antigen. J Immunol 139;1589-1596, 1987
  12. Klein U, Rajewsky K, Kuppers R: Human immunoglobulin (Ig)M+IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J Exp Med 188;1679-1689, 1998 https://doi.org/10.1084/jem.188.9.1679
  13. Zandvoort A, Lodewijk ME, de Boer NK, Dammers PM, Kroese FG, Timens W: CD27 expression in the human splenic marginal zone: the infant marginal zone is populated by naive B cells. Tissue Antigens 58;234-242, 2001 https://doi.org/10.1034/j.1399-0039.2001.580403.x
  14. Maurer D, Holter W, Majdic O, Fischer GF, Knapp W: CD27 expression by a distinct subpopulation of human B lymphocytes. Eur J Immunol 20;2679-2684, 1990 https://doi.org/10.1002/eji.1830201223
  15. Kobata T, Jacquot S, Kozlowski S, Agematsu K, Schlossman SF, Morimoto C: CD27-CD70 interactions regulate B-cell activation by T cells. Proc Natl Acad Sci USA 92;11249-11253, 1995 https://doi.org/10.1073/pnas.92.24.11249
  16. Akiba H, Nakano H, Nishinaka S, Shindo M, Kobata T, Atsuta M, Morimoto C, Ware CF, Malinin NL, Wallach D, Yagita H, Okumura K: CD27, a member of the tumor necrosis factor receptor superfamily, activates NF-kappaB and stress-activated protein kinase/c-Jun N-terminal kinase via TRAF2, TRAF5, and NF-kappaB-inducing kinase. J Biol Chem 273;13353-13358, 1998 https://doi.org/10.1074/jbc.273.21.13353
  17. Nagumo H, Agematsu K, Shinozaki K, Hokibara S, Ito S, Takamoto M, Nikaido T, Yasui K, Uehara Y, Yachie A, Komiyama A: CD27/CD70 interaction augments IgE secretion by promoting the differentiation of memory B cells into plasma cells. J Immunol 161;6496-6502, 1998
  18. Hamano T, Kim KJ, Leiserson WM, Asofsky R: Establishment of B cell hybridomas with B cell surface antigens. J Immunol 129;1403-1406, 1982
  19. Bishop GA, Haughton G: Induced differentiation of a transformed clone of Ly-1+ B cells by clonal T cells and antigen. Proc. Natl. Acad. Sci. (USA) 83;7410-414, 1986 https://doi.org/10.1073/pnas.83.19.7410
  20. Mercolino TJ, Arnold LW, Haughton G: Phosphatidyl choline is recognized by a series of Ly-1+ murine B cell lymphomas specific for erythrocyte membranes. J Exp Med 163;155-165, 1986 https://doi.org/10.1084/jem.163.1.155
  21. Bishop GA, Warren WD, Berton MT: Signaling via MHC class II molecules and antigen receptors enhances the B cell response to gp39/CD40 ligand. Eur J Immunol 25;1230-1238, 1995 https://doi.org/10.1002/eji.1830250515
  22. Warren WD, Berton MT: Induction of germ-line $\gamma$1 and $\varepsilon$ Ig gene expression in murine B cells. IL-4 and the CD40LCD40 interaction provide distinct but synergistic signals. J Immunol 155;5637-5646, 1995
  23. Bishop GA: Requirements of class II-mediated B cell differentiation for class II crosslinking and cAMP. J Immunol. 147;1107-1114, 1991
  24. Montixi C, Langlet C, Bernard AM, Thimonier J, Dubois C, Wurbel MA, Chauvin JP, Pierres M, He HT: Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J 17;5334-5348, 1998 https://doi.org/10.1093/emboj/17.18.5334
  25. Hostager BS, Catlett IM, Bishop GA: Recruitment of CD40, TRAF2 and TRAF3 to membrane microdomains during CD40 signaling. J Biol Chem 275;15392-15398, 2000 https://doi.org/10.1074/jbc.M909520199
  26. Hsing Y, Hostager BS, Bishop GA: Characterization of CD40 signaling determinants regulating NF-$\kappa$B activation in lymphocytes. J Immunol 159;4898-4906, 1997
  27. Rothe M, Sarma V, Dixit VM, Goeddel DV: TRAF2- mediated activation of NF-kB by TNF receptor 2 and CD40. Science 269;1424-1427, 1995 https://doi.org/10.1126/science.7544915
  28. Hostager BS, Bishop GA: Cutting Edge: Contrasting roles of TRAF2 and TRAF3 in CD40-mediated B lymphocyte activation. J Immunol 162;6307-6311, 1999
  29. Brown KD, Hostager BS, Bishop GA: Regulation of TRAF2 signaling by self-induced degradation. J Biol Chem in press; 2002
  30. Brown KD, Hostager BS, Bishop GA: Differential signaling and tumor necrosis factor receptor-associated factor (TRAF) degradation mediated by CD40 and the Epstein-Barr virus oncoprotein latent membrane protein 1 (LMP1). J Exp Med 193;943-954, 2001 https://doi.org/10.1084/jem.193.8.943