Role of protein tyrosine kinase and Erk1/2 activities in the toll-like receptor 2-induced cellular activation of murine B cells by neisserial porin

Clinical and Vaccine Immunology

Volumn 15, Issue 4, 2008, Pages 630-637

  MacLeod, Heather ^a,b   Bhasin, Navneet ^a   Wetzler, Lee M ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CD40 LIGAND; CD86 ANTIGEN; CELL PROTEIN; DIMETHYL SULFOXIDE; GENISTEIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOLOGICAL ADJUVANT; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGENIC AGENT; OUTER MEMBRANE PROTEIN; PATTERN RECOGNITION RECEPTOR; PORIN; PROTEIN PORB; TOLL LIKE RECEPTOR 2;

ANIMAL CELL; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE ACTIVATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME PHOSPHORYLATION; INNATE IMMUNITY; LYMPHOCYTE PROLIFERATION; MOUSE; NEISSERIA MENINGITIDIS; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANTIGENS, CD86; B-LYMPHOCYTES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEISSERIA MENINGITIDIS; NF-KAPPA B; PHOSPHORYLATION; PORINS; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; UP-REGULATION;

EID: 47049108203     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00435-07     Document Type: Article

References (69)

1. Barois, N., F. Forquet, and J. Davoust. 1997. Selective modulation of the major histocompatibility complex class II antigen presentation pathway following B cell receptor ligation and protein kinase C activation. J. Biol. Chem. 272:3641-3647.
2. Bhasin, N., Y. Ho, and L. M. Wetzler. 2001. Neisseria meningitidis lipopolysaccharide modulates the specific humoral immune response to neisserial porins but has no effect on porin-induced upregulation of costimulatory ligand B7-2. Infect. Immun. 69:5031-5036.
3. Bjune, G., E. A. Hoiby, J. K. Gronnesby, O. Arnesen, J. H. Fredriksen, A. Halstensen, E. Holten, A.-K. Lindbak, H. Nokleby, E. Rosenquist, L. K. Solberg, O. Closs, J. Eng, L. O. Froholm, A. Lystad, L. S. Bakketeig, and B. Hareide. 1991. Effect of outer membrane vesicle vaccine against group B meningococcal disease in Norway. Lancet 338:1093-1096.
4. Blake, M. S., and E. C. Gotschlich. 1986. Functional and immunological properties of pathogenic neisserial surface proteins, p. 377-400. In M. Inouye (ed.), Bacterial outer membranes as model systems. John Wiley, New York, NY.
5. Bluestone, J. A. 1995. New perspectives of CD28-B7-mediated T cell costimulation. Immunity 2:555-559.
6. Boisleve, F., S. Kerdine-Romer, and M. Pallardy. 2005. Implication of the MAPK pathways in the maturation of human dendritic cells induced by nickel and TNF-alpha. Toxicology 206:233-244.
7. 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.
8. Coligan, J. E., A. M. Kruisbeek, D. H. Margulies, E. M. Shevach, and W. Strober (ed.). 2001. Current protocols in immunology, p. 5.0.1-5.8.8 and 11.0.1-11.10.6. John Wiley & Sons, Inc., New York, NY.
9. Dal Porto, J. M., S. B. Gauld, K. T. Merrell, D. Mills, A. E. Pugh-Bernard, and J. Cambier. 2004. B cell antigen receptor signaling 101. Mol. Immunol. 41:599-613.
10. Delude, R. L., M. J. Fenton, R. J. Savedra, P. Y. Perera, S. N. Vogel, R. Thieringer, and D. T. Golenbock. 1994. CD14-mediated translocation of nuclear factor-kappa B induced by lipopolysaccharide does not require tyrosine kinase activity. J. Biol. Chem. 269:22253-22260.
11. Donnelly, J. J., R. R. Deck, and M. A. Liu. 1990. Immunogenicity of a Haemophilus influenzae polysaccharide-Neisseria meningitidis outer membrane protein vaccine. J. Immunol. 145:3071-3079.
12. Dudley, D. T., L. Pang, S. J. Decker, A. J. Bridges, and A. R. Saltiel. 1995. A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA 92:7686-7689.
13. Francis, D. A., J. G. Karras, X. Y. Ke, R. Sen, and T. L. Rothstein. 1995. Induction of the transcription factors NF-kappa B, AP-1 and NF-AT during B cell stimulation through the CD40 receptor. Int. Immunol. 7:151-161.
14. Fusco, P. C., F. Michon, M. Laude-Sharp, C. A. Minetti, C. H. Huang, I. Heron, and M. S. Blake. 1998. Preclinical studies on a recombinant group B meningococcal porin as a carrier for a novel Haemophilus influenzae type b conjugate vaccine. Vaccine 16:1842-1849.
15. Geissler, J. F., P. Traxler, U. Regenass, B. J. Murray, J. L. Roesel, T. Meyer, E. McGlynn, A. Storni, and N. B. Lydon. 1990. Thiazolidine-diones. Biochemical and biological activity of a novel class of tyrosine protein kinase inhibitors. J. Biol. Chem. 265:22255-22261.
16. Ghosh, S., M. J. May, and E. B. Kopp. 1998. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16:225-260.
17. Guttormsen, H. K., L. M. Wetzler, and A. Naess. 1993. Humoral immune response to the class 3 outer membrane protein during the course of meningococcal disease. Infect. Immun. 61:4734-4742.
18. Harnett, M. M., E. Katz, and C. A. Ford. 2005. Differential signalling during B-cell maturation. Immunol. Lett. 98:33-44.
19. Hemmi, H., O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408:740-745.
20. Hertz, C. J., S. M. Kiertscher, P. J. Godowski, D. A. Bouis, M. V. Norgard, M. D. Roth, and R. L. Modlin. 2001. Microbial lipopeptides stimulate dendritic cell maturation via Toll-like receptor 2. J. Immunol. 166:2444-2450.
21. Hsing, Y., B. S. Hostager, and G. A. Bishop. 1997. Characterization of CD40 signaling determinants regulating nuclear factor-kappa B activation in B lymphocytes. J. Immunol. 159:4898-4906.
22. Hunninghake, G. W., B. G. Monks, L. J. Geist, M. M. Monick, M. A. Monroy, M. F. Stinski, A. C. Webb, J. M. Dayer, P. E. Auron, and M. J. Fenton. 1992. The functional importance of a cap site-proximal region of the human prointerleukin 1 gene is defined by viral protein trans-activation. Mol. Cell. Biol. 12:3439-3448.
23. Kaisho, T., and S. Akira. 2001. Dendritic-cell function in Toll-like receptor- and MyD88-knockout mice. Trends Immunol. 22:78-83.
24. Kehry, M. R., and B. E. Castle. 1994. Regulation of CD40 ligand expression and use of recombinant CD40 ligand for studying B cell growth and differentiation. Semin. Immunol. 6:287-294.
25. Kim, J., H. R. Kim, J. C. Lee, and Y. S. Jang. 2002. Involvement of ERK, p38 MAP kinase, and PKC in MHC class II-mediated signal transduction in a resting B cell line. Biochem. Biophys. Res. Commun. 291:139-145.
26. Kohm, A. P., A. Mozaffarian, and V. M. Sanders. 2002. B cell receptor- and beta 2-adrenergic receptor-induced regulation of B7-2 (CD86) expression in B cells. J. Immunol. 168:6314-6322.
27. Krieg, A. M. 2000. Signal transduction induced by immunostimulatory CpG DNA. Springer Semin. Immunopathol. 22:97-105.
28. Lenschow, D. J., A. I. Sperling, M. P. Cooke, G. Freeman, L. Rhee, D. C. Decker, G. Gray, L. M. Nadler, C. C. Goodnow, and J. A. Bluestone. 1994. Differential up-regulation of the B7-1 and B7-2 costimulatory molecules after Ig receptor engagement by antigen. J. Immunol. 153:1990-1997.
29. Li, Q., and I. M. Verma. 2002. NF-kappaB regulation in the immune system. Nat. Rev. Immunol. 2:725-734.
30. Lien, E., T. J. Sellati, A. Yoshimura, T. H. Flo, G. Rawadi, R. W. Finberg, J. D. Carroll, T. Espevik, R. R. Ingalls, J. D. Radolf, and D. T. Golenbock. 1999. Toll-like receptor 2 functions as a pattern recognition receptor for diverse bacterial products. J. Biol. Chem. 274:33419-33425.
31. Liu, J. L., T. C. Chiles, R. J. Sen, and T. L. Rothstein. 1991. Inducible nuclear expression of NF-kappa B in primary B cells stimulated through the surface Ig receptor. J. Immunol. 146:1685-1691.
32. Livingston, P. O., M. J. Calves, F. Helling, W. D. Zollinger, M. S. Blake, and G. H. Lowell. 1993. GD3/proteosome vaccines induce consistent IgM antibodies against the ganglioside GD3. Vaccine 11:1199-1204.
33. Lowell, G. H. 1990. Proteosomes, hydrophobic anchors, iscoms, and liposomes for improved presentation of peptides and protein vaccines, p. 141-160. In G. C. Woodrow and M. M. Levine (ed.), New generation vaccines. Marcel Dekker, Inc., New York, NY.
34. Lowell, G. H., W. R. Ballou, L. F. Smith, R. A. Wirtz, W. D. Zollinger, and W. T. Hockmeyer. 1988. Proteosome-lipopeptide vaccines: enhancement of immunogenicity for malaria CS peptides. Science 240:800-802.
35. Mackinnon, F. G., Y. Ho, M. S. Blake, F. Michon, A. Chandraker, M. H. Sayegh, and L. M. Wetzler. 1999. The role of B/T costimulatory signals in the immunopotentiating activity of neisserial porin. J. Infect. Dis. 180:755-761.
36. Massari, P., P. Henneke, Y. Ho, E. Latz, D. T. Golenbock, and L. M. Wetzler. 2002. Cutting edge: immune stimulation by neisserial porins is Toll-like receptor 2 and MyD88 dependent. J. Immunol. 168:1533-1537.
37. Massari, P., C. A. King, H. MacLeod, and L. M. Wetzler. 2005. Improved purification of native meningococcal porin PorB and studies on its structure/function. Protein Expr. Purif. 44:136-146.
38. Massari, P., A. Visintin, J. Gunawardana, K. A. Halmen, C. A. King, D. T. Golenbock, and L. M. Wetzler. 2006. Meningococcal porin PorB binds to TLR2 and requires TLR1 for signaling. J. Immunol. 176:2373-2380.
39. Matsumoto, M., S. Kikkawa, M. Kohase, K. Miyake, and T. Seya. 2002. Establishment of a monoclonal antibody against human Toll-like receptor 3 that blocks double-stranded RNA-mediated signaling. Biochem. Biophys. Res. Commun. 293:1364-1369.
40. Medzhitov, R., P. Preston-Hurlburt, and C. A. Janeway, Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388:394-397.
41. Medzhitov, R., P. Preston-Hurlburt, E. Kopp, A. Stadlen, C. Chen, S. Ghosh, and C. A. Janeway, Jr. 1998. MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol. Cell 2:253-258.
42. Melancon, J., R. A. Murgita, and I. W. DeVoe. 1983. Activation of murine B lymphocytes by Neisseria meningitidis and isolated meningococcal surface antigens. Infect. Immun. 42:471-479.
43. Ozinsky, A., D. M. Underhill, J. D. Fontenot, A. M. Hajjar, K. D. Smith, C. B. Wilson, L. Schroeder, and A. Aderem. 2000. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between Toll-like receptors. Proc. Natl. Acad. Sci. USA 97:13766-13771.
44. Pasare, C., and R. Medzhitov. 2005. Control of B-cell responses by Toll-like receptors. Nature 438:364-368.
45. Piatelli, M. J., C. Doughty, and T. C. Chiles. 2002. Requirement for a hsp90 chaperone-dependent MEK1/2-ERK pathway for B cell antigen receptor-induced cyclin D2 expression in mature B lymphocytes. J. Biol. Chem. 277:12144-12150.
46. Poltorak, A., X. He, I. Smirnova, M. Y. Liu, C. V. Huffel, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, M. Freudenberg, P. Ricciardi-Castagnoli, B. Layton, and B. Beutler. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085-2088.
47. Poolman, J. T. 1988. Meningococcal vaccines. J. Med. Microbiol. 26:170-172.
48. Purkerson, J. M., and D. C. Parker. 1998. Differential coupling of membrane Ig and CD40 to the extracellularly regulated kinase signaling pathway. J. Immunol. 160:2121-2129.
49. Ray, A., and T. Biswas. 2005. Porin of Shigella dysenteriae enhances Toll-like receptors 2 and 6 of mouse peritoneal B-2 cells and induces the expression of immunoglobulin M, immunoglobulin G2a and immunoglobulin A. Immunology 114:94-100.
50. Ray, A., P. Karmakar, and T. Biswas. 2004. Up-regulation of CD80-CD86 and IgA on mouse peritoneal B-1 cells by porin of Shigella dysenteriae is Toll-like receptors 2 and 6 dependent. Mol. Immunol. 41:1167-1175.
51. Richards, J. D., S. H. Dave, C. H. Chou, A. A. Mamchak, and A. L. DeFranco. 2001. Inhibition of the MEK/ERK signaling pathway blocks a subset of B cell responses to antigen. J. Immunol. 166:3855-3864.
52. Singleton, T. E., P. Massari, and L. M. Wetzler. 2005. Neisserial porin-induced dendritic cell activation is MyD88 and TLR2 dependent. J. Immunol. 174:3545-3550.
53. Snapper, C. M., M. R. Kehry, B. E. Castle, and J. J. Mond. 1995. Multivalent, but not divalent, antigen receptor cross-linkers synergize with CD40 ligand for induction of Ig synthesis and class switching in normal murine B cells. A redefinition of the TI-2 vs T cell-dependent antigen dichotomy. J. Immunol. 154:1177-1187.
54. Snapper, C. M., F. R. Rosas, M. R. Kehry, J. J. Mond, and L. M. Wetzler. 1997. Neisserial porins may provide critical second signals to polysaccharide-activated murine B cells for induction of immunoglobulin secretion. Infect. Immun. 65:3203-3208.
55. Sparkes, B. G. 1983. Dual effect of meningococcal antigens on T cell dependent immune response. Can. J. Microbiol. 29:1619-1625.
56. Sparkes, B. G. 1983. Immunomodulating activity of meningococcal antigens. Can. J. Microbiol. 29:1611-1618.
57. Takeuchi, O., K. Hoshino, T. Kawai, H. Sanjo, H. Takada, T. Ogawa, K. Takeda, and S. Akira. 1999. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 11:443-451.
58. Tasker, L., and S. Marshall-Clarke. 1997. Immature B cells from neonatal mice show a selective inability to up-regulate MHC class II expression in response to antigen receptor ligation. Int. Immunol. 9:475-484.
59. Tsai, C. M., and C. E. Frasch. 1982. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119:115-119.
60. Vordermeier, H. M., and W. G. Bessler. 1987. Polyclonal activation of murine B lymphocytes in vitro by Salmonella typhimurium porins. Immunobiology 175:245-251.
61. Vordermeier, H. M., H. Drexler, and W. G. Bessler. 1987. Polyclonal activation of human peripheral blood lymphocytes by bacterial porins and defined porin fragments. Immunol. Lett. 15:121-126.
62. Vordermeier, H. M., K. Stab, and W. G. Bessler. 1986. A defined fragment of bacterial protein I (OmpF) is a polyclonal B-cell activator. Infect. Immun. 51:233-239.
63. Wetzler, L. M. 1994. Specificity of murine humoral and T helper cell responses towards neisserial porins, p. 127-134. In C. J. Conde-Glez, S. A. Morse, P. A. Rice, P. F. Sparling, and E. Calderón (ed.), Pathobiology and immunobiology of Neisseriaceae. Instituto Nacional de Salud Pública, Cuernavaca, Morelos, Mexico.
64. Wetzler, L. M., M. S. Blake, K. Barry, and E. C. Gotschlich. 1992. Gonococcal porin vaccine evaluation: comparison of Por proteosomes, liposomes and blebs isolated from rmp deletion mutants. J. Infect. Dis. 166:551-555.
65. Wetzler, L. M., M. S. Blake, and E. C. Gotschlich. 1988. Characterization and specificity of antibodies to protein I of Neisseria gonorrhoeae produced by injection with various protein I-adjuvant preparations. J. Exp. Med. 168:1883-1897.
66. Wetzler, L. M., Y. Ho, and H. Reiser. 1996. Neisserial porins induce B lymphocytes to express costimulatory B7-2 molecules and to proliferate. J. Exp. Med. 183:1151-1159.
67. Wu, M., H. Lee, R. E. Bellas, S. L. Schauer, M. Arsura, D. Katz, M. J. FitzGerald, T. L. Rothstein, D. H. Sherr, and G. E. Sonenshein. 1996. Inhibition of NF-kappaB/Rel induces apoptosis of murine B cells. EMBO J. 15:4682-4690.
68. Yao, X. R., and D. W. Scott. 1993. Inhibition of protein tyrosine kinase activity by herbimycin A prevents anti-mu but not LPS-mediated cell cycle progression and differentiation of splenic B lymphocytes. Cell. Immunol. 149:364-375.
69. Zollinger, W. D. 1990. New and inproved vaccines against meningococcal disease, p. 325-348. In G. C. Woodrow and M. M. Levine (ed.), New generation vaccines. Marcel Dekker, Inc., New York, NY.