Bruton's tyrosine kinase links the B cell receptor to nuclear factor κB activation

Journal of Experimental Medicine

Volumn 191, Issue 10, 2000, Pages 1735-1744

  Bajpai, Urmila D ^a   Zhang, Keming ^a   Teutsch, Mark ^a   Sen, Ranjan ^b   Wortis, Henry H ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BRANDEIS UNIVERSITY   (United States)

Author keywords

B cell activation; B cell receptor; CD40; Transcription factor; X linked immunodeficiency

Indexed keywords

IMMUNOGLOBULIN M; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; B LYMPHOCYTE; CELL FUNCTION; CELL LINE; CHICKEN; DNA BINDING; ENZYME ACTIVITY; GENE ACTIVATION; IMMUNE DEFICIENCY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; X LINKED AGAMMAGLOBULINEMIA;

ANIMALS; ANTIGENS, CD40; B-LYMPHOCYTES; BASE SEQUENCE; CHICKENS; DNA; DNA PRIMERS; IMMUNOGLOBULIN M; IMMUNOLOGIC DEFICIENCY SYNDROMES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, MUTANT STRAINS; NF-KAPPA B; POINT MUTATION; PROTEIN-TYROSINE KINASES; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION;

EID: 0034657235     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.191.10.1735     Document Type: Article

References (77)

1. Tsukada, S., D.C. Saffran, D.J. Rawlings, O. Parolini, R.C. Allen, I. Klisak, R.S. Sparkes, H. Kubagawa, T. Mohandas, S. Quan, et al. 1993. Deficient expression of a B cell cytoplasmic tyrosine kinase in human X-linked agammaglobulinemia. Cell. 72:279-290.
2. Rawlings, D.J., D.C. Saffran, S. Tsukada, D.A. Largaespada, J.C. Grinialdi, L. Cohen, R.N. Mohr, J.F. Bazan, M. Howard, N.G. Copeland, et al. 1993. Mutation of unique region of Bruton's tyrosine kinase in immunodeficient XID mice. Science. 261:358-361.
3. Thomas, J.D., P. Sideras, C.I. Smith, I. Vorechovsky, V. Chapman, and W.E. Paul. 1993. Colocalization of X-linked agammaglobulinemia and X-linked immunodeficiency genes. Science. 261:355-358.
4. Conley, M.E., O. Parolini, J. Rohrer, and D. Campana. 1994. X-linked agammaglobulinemia: new approaches to old questions based on the identification of the defective gene. Immunol. Rev. 138:5-21.
5. Rawlings, D.J., and O.N. Witte. 1994. Bruton's tyrosine kinase is a key regulator in B-cell development. Immunol. Rev. 138:105-119.
6. Khan, W.N., F.W. Alt, R.M. Gerstein, B.A. Malynn, I. Larsson, G. Rathbun, L. Davidson, S. Muller, A.B. Kantor, L.A. Herzenberg, et al. 1995. Defective B cell development and function in Btk-deficient mice. Immunity. 3:283-299.
7. Kerner, J.D., M.W. Appleby, R.N. Mohr, S. Chien, D.J. Rawlings, C.R. Maliszewski, O.N. Witte, and R.M. Perlmutter. 1995. Impaired expansion of mouse B cell progenitors lacking Btk. Immunity. 3:301-312.
8. Vihinen, M., B.H. Belohradsky, R.N. Haire, E. Holinski-Feder, S.P. Kwan, I. Lappalainen, H. Lehvaslaiho, T. Lester, A. Meindl, H.D. Ochs, et al. 1997. BTKbase, mutation database for X-linked agammaglobulinemia (XLA). Nucleic Acids Res. 25:166-171.
9. Rawlings, D.J., and O.N. Witte. 1995. The Btk subfamily of cytoplasmic tyrosine kinases: structure, regulation and function. Semin. Immunol. 7:237-246.
10. de Weers, M., M.C. Verschuren, M.E. Kraakman, R.G. Mensink, R.K. Schuurnan, J.J. van Dongen, and R.W. Hendriks. 1993. The Bruton's tyrosine kinase gene is expressed throughout B cell differentiation, from early precursor B cell stages preceding immunoglobulin gene rearrangement up to mature B cell stages. Eur. J. Immunol. 23:3109-3114.
11. Koike, M., Y. Kikuchi, A. Tominaga, S. Takaki, K. Akagi, J. Miyazaki, K. Yamamura, and K. Takatsu. 1995. Defective IL-5-receptor-mediated signaling in B cells of X-linked immunodeficient mice. Int. Immunol. 7:21-30.
12. Go, N.F., B.E. Castle, R. Barrett, R. Kastelein, W. Dang, T.R. Mosmann, K.W. Moore, and M. Howard. 1990. Interleukin 10, a novel B cell stimulatory factor: unresponsiveness of X chromosome-linked immunodeficiency B cells. J. Exp. Med. 172:1625-1631.
13. Santos-Argumedo, L., F.E. Lund, A.W. Heath, N. Solvason, W.W. Wu, J.C. Grimaldi, R.M. Parkhouse, and M. Howard. 1995. CD38 unresponsiveness of xid B cells implicates Bruton's tyrosine kinase (btk) as a regular of CD38 induced signal transduction. Int. Immunol. 7:163-170.
14. Hata, D., Y. Kawakami, N. Inagaki, C.S. Lantz, T. Kitamura, W.N. Khan, M. Maeda-Yamamoto, T. Miura, W. Han, S.E. Hartman, et al. 1998. Involvement of Bruton's tyrosine kinase in FcεRI-dependent mast cell degranulation and cytokine production. J. Exp. Med. 187:1235-1247.
15. Setoguchi, R., T. Kinashi, H. Sagara, K. Hirosawa, and K. Takatsu. 1998. Defective degranulation and calcium mobilization of bone-marrow derived mast cells from Xid and Btk-deficient mice. Immunol. Lett. 64:109-118.
16. Bona, C., J.J. Mond, and W.E. Paul. 1980. Synergistic genetic defect in B-lymphocyte function. I. Defective responses to B-cell stimulants and their genetic basis. J. Exp. Med. 151: 224-234.
17. de Weers, M., G.S. Brouns, S. Hinshelwood, C. Kinnon, R.K. Schuurman, R.W. Hendriks, and J. Borst. 1994. B-cell antigen receptor stimulation activates the human Bruton's tyrosine kinase, which is deficient in X-linked agammaglobulinemia. J. Biol. Chem. 269:23857-23860.
18. Aoki, Y., K.J. Isselbacher, and S. Pillai. 1994. Bruton tyrosine kinase is tyrosine phosphorylated and activated in pre-B lymphocytes and receptor-ligated B cells. Proc. Natl. Acad. Sci. USA. 91:10606-10609.
19. Rawlings, D.J., A.M. Scharenberg, H. Park, M.I. Wahl, S. Lin, R.M. Kato, A.C. Fluckiger, O.N. Witte, and J.P. Kinet. 1996. Activation of BTK by a phosphorylation mechanism initiated by SRC family kinases. Science. 271:822-825.
20. Park, H., M.I. Wahl, D.E. Afar, C.W. Turck, D.J. Rawlings, C. Tam, A.M. Scharenberg, J.P. Kinet, and O.N. Witte. 1996. Regulation of Btk function by a major autophosphorylation site within the SH3 domain. Immunity. 4:515-525.
21. Salim, K., M.J. Bottomley, E. Querfurth, M.J. Zvelebil, I. Gout, R. Scaife, R.L. Margolis, R. Gigg, C.I. Smith, P.C. Driscoll, et al. 1996. Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton's tyrosine kinase. EMBO (Eur. Mol. Biol. Organ.) J. 15:6241-6250.
22. Gupta, N., A.M. Scharenberg, D.A. Fruman, L.C. Cantley, J.P. Kinet, and E.O. Long. 1999. The SH2 domain-containing inositol 5′-phosphatase (SHIP) recruits the p85 subunit of phosphoinositide 3-kinase during FcgammaRIIb1-mediated inhibition of B cell receptor signaling. J. Biol. Chem. 274: 7489-7494.
23. Yang, W., and S. Desiderio. 1997. BAP-135, a target for Bruton's tyrosine kinase in response to B cell receptor engagement. Proc. Natl. Acad. Sci. USA. 94:604-609.
24. Johannes, F., A. Hausser, P. Storz, L. Truckenmüller, G. Link, T. Kawakami, and K. Pfizenmaier. 1999. Bruton's tyrosine kinase (Btk) associates with protein kinase C mu. PEBS Lett. 461:68-72.
25. Baba, Y., S. Nonoyama, M. Matsushita, T. Yamadori, S. Hashimoto, K. Imai, S. Arai, T. Kunikata, M. Kurimoto, T. Kurosaki, et al. 1999. Involvement of Wiskott-Aldrich syndrome protein in B-cell cytoplasmic tyrosine kinase pathway. Blood. 93:2003-2012.
26. Guinamard, R., M. Fougereau, and P. Seckinger. 1997. The SH3 domain of Bruton's tyrosine kinase interacts with Vav, Sam68 and EWS. Scand. J. Immunol. 45:587-595.
27. Cory, G.O., R.C. Lovering, S. Hinshelwood, L. MacCarthy-Morrogh, R.J. Levinsky, and C. Kinnon. 1995. The protein product of the c-cbl protooncogene is phosphorylated after B cell receptor stimulation and binds the SH3 domain of Bruton's tyrosine kinase. J. Exp. Med. 182:611-615.
28. Hashimoto, S., A. Iwamatsu, M. Ishiai, K. Okawa, T. Yamadori, M. Matsushita, Y. Baba, T. Kishimoto, T. Kurosaki, and S. Tsukada. 1999. Identification of the SH2 domain binding protein of Bruton's tyrosine kinase as BLNK - functional significance of Btk-SH2 domain in B-cell antigen receptor-coupled calcium signaling. Blood. 94:2357-2364.
29. 2+ following B-cell receptor activation. EMBO (Eur. Mol. Biol. Organ.) J. 17:1973-1985.
30. Takata, M., and T. Kurosaki. 1996. A role for Bruton's tyrosine kinase in B cell antigen receptor-mediated activation of phospholipase C-gamma 2. J. Exp. Med. 184:31-40.
31. Scharenberg, A.M., O. El-Hillal, D.A. Fruman, L.O. Beitz, Z. Li, S. Lin, I. Gout, L.C. Cantley, D.J. Rawlings, and J.P. Kinet. 1998. Phosphatidylinositol-3,4,5-trisphosphate (Pt-dIns-3,4,5-P3)/Tec kinase-dependent calcium signaling pathway: a target for SHIP-mediated inhibitory signals. EMBO (Eur. Mol. Biol. Organ.) J. 17:1961-1972.
32. Hawrylowicz, C.M., K.D. Keeler, and G.G. Klaus. 1984. Activation and proliferation signals in mouse B cells. 1. A comparison of the capacity of anti-Ig antibodies or phorbol myristic acetate to activate B cells from CBA/N or normal mice into G1. Eur. J. Immunol. 14:244-250.
33. Anderson, J.S., M. Teutsch, Z. Pong, and H.H. Wortis. 1996. An essential role for Bruton's [corrected] tyrosine kinase in the regulation of B-cell apoptosis [published erratum appears in Proc. Natl. Acad. Sci. USA. 1996, 93:15522]. Proc. Natl. Acad. Sci. USA. 93:10966-10971.
34. Brorson, K., M. Brunswick, S. Ezhevsky, D.G. Wei, R. Berg, D. Scott, and K.E. Stein. 1997. xid affects events leading to B cell cycle entry. J. Immunol. 159:135-143.
35. 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.
36. Francis, D.A., R. Sen, N. Rice, and T.L. Rothstein. 1998. Receptor-specific induction of NF-kappaB components in primary B cells. Int. Immunol. 10:285-293.
37. 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.
38. Kontgen, F., R.J. Grumont, A. Strasser, D. Metcalf, R. Li, D. Tarlinton, and S. Gerondakis. 1995. Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev. 9:1965-1977.
39. Doi, T.S., T. Takahashi, O. Taguchi, T. Azuma, and Y. Obata. 1997. NF-kappa B RelA-deficient lymphocytes: normal development of T cells and B cells, impaired production of IgA and IgG1 and reduced proliferative responses. J. Exp. Med. 185:953-961.
40. Bendall, H.H., M.L. Sikes, D.W. Ballard, and E.M. Oltz. 1999. An intact NF-kappa B signaling pathway is required for maintenance of mature B cell subsets. Mol. Immunol. 36: 187-195.
41. Sutherland, C.L., D.L. Krebs, and M.R. Gold. 1999. An 11-amino acid sequence in the cytoplasmic domain of CD40 is sufficient for activation of c-Jun N-terminal kinase, activation of MAHKAP kinase-2, phosphorylation of I kappa B alpha, and protection of WEHI-231 cells from anti-1gM-induced growth arrest. J. Immunol. 162:4720-4730.
42. Kosaka, Y., D.M. Calderhead, E.M. Manning, J.E. Hambor, A. Black, R. Geleziunas, K.B. Marcu, and R.J. Noelle. 1999. Activation and regulation of the IkappaB kinase in human B cells by CD40 signaling. Eur. J. Immunol. 29:1353-1362.
43. 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.
44. Gerondakis, S., R. Grumont, I. Rourke, and M. Grossmann. 1998. The regulation and roles of Rel/NF-kappa B transcription factors during lymphocyte activation. Curr. Opin. Immunol. 10:353-359.
45. Teutsch, M., M. Higer, D. Wang, and H.W. Wortis. 1995. Induction of CD5 on B and T cells is suppressed by cyclosporin A, FK-520 and rapamycin. Int. Immunol. 7:381-392.
46. Lane, P.J., and T. Brocker. 1999. Developmental regulation of dendritic cell function. Curr. Opin. Immunol. 11:308-313.
47. Petit, P.X., H. Lecoeur, E. Zorn, C. Dauguet, B. Mignotte, and M.L. Gougeon. 1995. Alterations in mitochondrial structure and function are early events of dexamethasone-induced thymocyte apoptosis. J. Cell Biol. 130:157-167.
48. 2+ mobilization through distinct pathways. EMBO (Eur. Mol. Biol. Organ.) J. 13:1341-1349.
49. Berland, K., and H.H. Wortis. 1998. An NFAT-dependent enhancer is necessary for anti-IgM-mediated induction of murine CD5 expression in primary splenic B cells. J. Immunol. 161:277-285.
50. Mauxion, F., C. Jamieson, M. Yoshida, K. Arai, and R. Sen. 1991. Comparison of constitutive and inducible transcriptional enhancement mediated by kappa B-related sequences: modulation of activity in B cells by human T-cell leukemia vims type I tax gene. Proc. Natl. Acad. Sci. USA. 88:2141-2145.
51. Rice, N.R., and M.K. Ernst. 1993. In vivo control of NF-kappa B activation by I kappa B alpha. EMBO (Eur. Mol. Biol. Organ.) J. 12:4685-4695.
52. Grumont, R.J., I.B. Richardson, C. Gaff, and S. Gerondakis. 1993. rel/NF-kappa B nuclear complexes that bind kB sites in the murine c-rel promoter are required for constitutive c-rel transcription in B-cells. Cell Growth Differ. 4:731-743.
53. Whiteside, S.T., and A. Israel. 1997. I kappa B proteins: structure, function and regulation. Semin. Cancer Biol. 8:75-82.
54. Li, H.L, M.S. Forman, T. Kurosaki, and E. Pure. 1997. Syk is required for BCR-mediated activation of p90Rsk, but not p70S6k, via a mitogen-activated protein kinase-independent pathway in B cells. J. Biol. Chem. 272:18200-18208.
55. Sidorenko, S.P., C.L. Law, S.J. Klaus, K.A. Chandran, M. Takata, T. Kurosaki, and E.A. Clark. 1996. Protein kinase C mu (PKC mu) associates with the B cell antigen receptor complex and regulates lymphocyte signaling. Immunity. 5:353-363.
56. Novina, C.D., S. Kumar, U. Bajpai, V. Cheriyath, K. Zhang, S. Pillai, H.H. Wortis, and A.L. Roy. 1999. Regulation of nuclear localization and transcriptional activity of TFII-I by Bruton's tyrosine kinase. Mol. Cell. Biol. 19:5014-5024.
57. Varnai, P., K.I. Rother, and T. Balla. 1999. Phosphatidylinositol 3-kinase-dependent membrane association of the Bruton's tyrosine kinase pleckstrin homology domain visualized in single living cells. J. Biol. Chem. 274:10983-10989.
58. Li, T., D.J. Rawlings, H. Park, R.M. Kato, O.N. Witte, and A.B. Satterthwaite. 1997. Constitutive membrane association potentiates activation of Bruton tyrosine kinase. Ocogene. 15:1375-1383.
59. Schauer, S.L., Z. Wang, G.E. Sonenshein, and T.L. Rothstein. 1996. Maintenance of nuclear factor-kappa B/Rel and c-myc expression during CD40 ligand rescue of WEHI 231 early B cells from receptor-mediated apoptosis through modulation of I kappa B proteins. J. Immunol. 157:81-86.
60. Lee, H.H., H. Dadgostar, Q. Cheng, J. Shu, and G. Cheng. 1999. NF-kappaB-mediated up-regulation of Bcl-x and Bfl-1/A1 is required for CD40 survival signaling in B lymphocytes. Proc. Natl. Acad. Sci. USA. 96:9136-9141.
61. L permits anti-immunoglobulin (Ig)-induced proliferation in xid B cells. J. Exp. Med. 187:1081-1091.
62. Klaus, G.G., M. Holman, C. Johnson-Leger, C. Elgueta-Karstegl, and C. Atkins. 1997. A re-evaluation of the effects of X-linked immunodeficiency (xid) mutation on B cell differentiation and function in the mouse. Eur. J. Immunol. 27: 2749-2756.
63. Cariappa, A., T.J. Kim, and S. Pillai. 1999. Accelerated emigration of B lymphocytes in the Xid mouse. J. Immunol. 162: 4417-4423.
64. Lindsberg, M.L., M. Brunswick, H. Yamada, A. Lees, J. Innian, C.H. June, and J.J. Mond. 1991. Biochemical analysis of the immune B cell defect in xid mice. J. Immunol. 147: 3774-3779.
65. Rawlings, D.J. 1999. Bruton's tyrosine kinase controls a sustained calcium signal essential for B lineage development and function, Clin. Immunol. 91:243-253.
66. Kurosaki, T. 1997. Molecular mechanisms in B cell antigen receptor signaling. Curr. Opin. Immunol. 9:309-318.
67. Heilker, R., F. Freuler, R. Pulfer, F. Di Padova, and J. Eder. 1999. All three IkappaB isoforms and most Rel family members are stably associated with the IkappaB kinase 1/2 complex. Eur. J. Biochem. 259:253-261.
68. Pomerantz, J.L., and D. Baltimore. 1999. NF-kappaB activation by a signaling complex containing TRAF2, TANK and TBK1, a novel IKK-related kinase. EMBO (Eur. Mol. Biol. Organ.) J. 18:6694-6704.
69. Akiba, H., H. Nakano, S. Nishinaka, M. Shindo, T. Kobata, M. Atsuta, C. Morimoto, C.F. Ware, N.L. Malinin, D. Wallach, et al. 1998. 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.
70. Karras, J.G., Z. Wang, L. Huo, D.A. Frank, and T.L. Rothstein. 1997. Induction of STAT protein signaling through the CD40 receptor in B lymphocytes: distinct STAT activation following surface Ig and CD40 receptor engagement. J. Immunol. 159:4350-4355.
71. Foote, L.C., T.J. Schneider, G.M. Fischer, J.K. Wang, B. Rasmussen, K.A. Campbell, D.H. Lynch, S.T. Ju, A. Marshak-Rothstein, and T.L. Rothstein. 1996. Intracellular signaling for inducible antigen receptor-mediated Fas resistance in B cells. J. Immunol. 157:1878-1885.
72. Sakata, N., H. Kawasome, N. Terada, P. Gerwins, G.L. Johnson, and E.W. Gelfand. 1999. Differential activation and regulation of mitogen-activated protein kinases through the antigen receptor and CD40 in human B cells. Eur. J. Immunol. 29:2999-3008.
73. Wortis, H.H., M. Teutsch, M. Higer, J. Zheng, and D.C. Parker. 1995. B-cell activation by crosslinking of surface IgM or ligation of CD40 involves alternative signal pathways and results in different B-cell phenotypes. Proc. Natl. Acad. Sci. USA. 92:3348-3352.
74. Venkataraman, L., W. Wang, and R. Sen. 1996. Differential regulation of c-Rel translocation in activated B and T cells. J. Immunol. 157:1149-1155.
75. Venkataraman, L., S.J. Burakoff, and R. Sen. 1995. FK506 inhibits antigen receptor-mediated induction of c-rel in B and T lymphoid cells. J. Exp. Med. 181:1091-1099.
76. Lin, S.C., H.H. Wortis, and J. Stavnezer. 1998. The ability of CD40L, but not lipopolysaccharide, to initiate immunoglobulin switching to immmunoglobulin G1 is explained by differential induction of NF-kappaB/Rel proteins. Mol. Cell. Biol. 18:5523-5532.
77. Whiteside, S.T., J.C. Epinat, N.R. Rice, and A. Israel. 1997. I kappa B epsilon, a novel member of the I kappa B family, controls RelA and cRel NF-kappa B activity. EMBO (Eur. Mol. Biol. Organ.) J. 16:1413-1426.