The B Cell Antigen Receptor Controls Integrin Activity through Btk and PLCγ2

Journal of Experimental Medicine

Volumn 198, Issue 10, 2003, Pages 1539-1550

  Spaargaren, Marcel ^a,c   Beuling, Esther A ^a   Rurup, Mette L ^a   Meijer, Helen P ^a   Klok, Melanie D ^a   Middendorp, Sabine ^b   Hendriks, Rudolf W ^b   Pals, Steven T ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

B cell development; Germinal center; Lymphocyte adhesion; VCAM 1; X linked agammaglobulinaemia

Indexed keywords

ALPHA4 INTEGRIN; B CELL ANTIGEN RECEPTOR; CALCIUM ION; FIBRONECTIN; LYMPHOCYTE ANTIGEN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CALCIUM TRANSPORT; CELL ADHESION; CELL DIFFERENTIATION; CELL MATURATION; CYTOSKELETON; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN FUNCTION; X LINKED AGAMMAGLOBULINEMIA;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AGAMMAGLOBULINEMIA; ANIMALS; B-LYMPHOCYTES; CALCIUM; CELL ADHESION; DNA-BINDING PROTEINS; HUMANS; INTEGRINS; MICE; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA; PROTEIN KINASE C; PROTEIN-TYROSINE KINASES; RECEPTORS, ANTIGEN, B-CELL; VASCULAR CELL ADHESION MOLECULE-1;

EID: 0345016875     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20011866     Document Type: Article

References (75)

1. Miyake, K., I.L. Weissman, J.S. Greenberger, and P.W. Kincade. 1991. Evidence for a role of the integrin VLA-4 in lympho-hemopoiesis. J. Exp. Med. 173:599-607.
2. Leuker, C.E., M. Labow, W. Muller, and N. Wagner. 2001. Neonatally induced inactivation of the vascular cell adhesion molecule 1 gene impairs B cell localization and T cell-dependent humoral immune response. J. Exp. Med. 193:755-768.
3. Arroyo, A.G., J.T. Yang, H. Rayburn, and R.O. Hynes. 1996. Differential requirements for alpha4 integrins during fetal and adult hematopoiesis. Cell. 85:997-1008.
4. Arroyo, A.G., J.T. Yang, H. Rayburn, and R.O. Hynes. 1999. Alpha4 integrins regulate the proliferation/differentiation balance of multilineage hematopoietic progenitors in vivo. Immunity. 11:555-566.
5. Koni, P.A., S.K. Joshi, U.A. Temann, D. Olson, L. Burkly, and R.A. Flavell. 2001. Conditional vascular cell adhesion molecule 1 deletion in mice: impaired lymphocyte migration to bone marrow. J. Exp. Med. 193:741-754.
6. Berlin-Rufenach, C., F. Otto, M. Mathies, J. Westermann, M.J. Owen, A. Hamann, and N. Hogg. 1999. Lymphocyte migration in lymphocyte function-associated antigen (LFA)-1-deficient mice. J. Exp. Med. 189:1467-1478.
7. Butcher, E.C., and L.J. Picker. 1996. Lymphocyte homing and homeostasis. Science. 272:60-66.
8. Kunkel, E.J., and E.C. Butcher. 2002. Chemokines and the tissue-specific migration of lymphocytes. Immunity. 16:1-4.
9. Liu, Y.J., and C. Arpin. 1997. Germinal center development. Immunol. Rev. 156:111-126.
10. MacLennan, I.C. 1994. Germinal centers. Annu. Rev. Immunol. 12:117-139.
11. Lindhout, E., G. Koopman, S.T. Pals, and C. de Groot. 1997. Triple check for antigen specificity of B cells during germinal centre reactions. Immunol. Today. 18:573-577.
12. van Eijk, M., T. Defrance, A. Hennino, and C. de Groot. 2001. Death-receptor contribution to the germinal-center reaction. Trends Immunol. 22:677-682.
13. Freedman, A.S., J.M. Munro, G.E. Rice, M.P. Bevilacqua, C. Morimoto, B.W. McIntyre, K. Rhynhart, J.S. Pober, and L.M. Nadler. 1990. Adhesion of human B cells to germinal centers in vitro involves VLA-4 and INCAM-110. Science. 249:1030-1033.
14. Koopman, G., H.K. Parmentier, H.J. Schuumaan, W. Newman, C.J. Meijer, and S.T. Pals. 1991. Adhesion of human B cells to follicular dendritic cells involves both the lymphocyte function-associated antigen 1/intercellular adhesion molecule 1 and very late antigen 4/vascular cell adhesion molecule 1 pathways. J. Exp. Med. 173:1297-1304.
15. 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.
16. Koopman, G., R. M. Keehnen, E. Lindhout, W. Newman, Y. Shimizu, G.A. van Seventer, C. de Groot, and S.T. Pals. 1994. Adhesion through the LFA-1 (CD11a/CD18)-ICAM-1 (CD54) and the VLA-4 (CD49d)-VCAM-1 (CD106) pathways prevents apoptosis of germinal center B cells. J. Immunol. 152:3760-3767.
17. Koopman, G., R.M. Keehnen, E. Lindhout, D.F. Zhou, C. de Groot, and S.T. Pals. 1997. Germinal center B cells rescued from apoptosis by CD40 ligation or attachment to follicular dendritic cells, but not by engagement of surface immunoglobulin or adhesion receptors, become resistant to CD95-induced apoptosis. Eur. J. Immunol. 27:1-7.
18. Brakebusch, C., S. Fillatreau, A.J. Potocnik, G. Bungartz, P. Wilhelm, M. Svensson, P. Kearney, H. Korner, D. Gray, and R. Fassler. 2002. Beta1 integrin is not essential for hematopoiesis but is necessary for the T cell-dependent IgM antibody response. Immunity. 16:465-477.
19. Meffre, E., R. Casellas, and M.C. Nussenzweig. 2000. Antibody regulation of B cell development. Nat. Immunol. 1:379-385.
20. Niiro, H., and E.A. Clark. 2002. Regulation of B-cell fate by antigen-receptor signals. Nat. Rev. Immunol. 2:945-956.
21. Papavasiliou, F., Z. Misulovin, H. Suh, and M.C. Nussenzweig. 1995. The role of Ig beta in precursor B cell transition and allelic exclusion. Science. 268:408-411.
22. Torres, R.M., H. Flaswinkel, M. Reth, and K. Rajewsky. 1996. Aberrant B cell development and immune response in mice with a compromised BCR complex. Science. 272:1804-1808.
23. Kurosaki, T. 1999. Genetic analysis of B cell antigen receptor signaling. Annu. Rev. Immunol. 17:555-592.
24. Kurosaki, T. 2002. Regulation of B-cell signal transduction by adaptor proteins. Nat. Rev. Immunol. 2:354-363.
25. Hughes, P.E., and M. Pfaff. 1998. Integrin affinity modulation. Trends Cell Biol. 8:359-364.
26. van Kooyk, Y., and C.G. Figdor. 2000. Avidity regulation of integrins: the driving force in leukocyte adhesion. Curr. Opin. Cell Biol. 12:542-547.
27. van der Voort, R., T.E. Taher, V.J. Wielenga, M. Spaargaren, R. Prevo, L. Smit, G. David, G. Hartmann, E. Gherardi, and S.T. Pals. 1999. Heparan sulfate-modified CD44 promotes hepatocyte growth factor/scatter factor-induced signal transduction through the receptor tyrosine kinase c-Met. J. Biol. Chem. 274:6499-6506.
28. van der Voort, R., T.E. Taher, R.M. Keehnen, L. Smit, M. Groenink, and S.T. Pals. 1997. Paracrine regulation of germinal center B cell adhesion through the c-met-hepatocyte growth factor/scatter factor pathway. J. Exp. Med. 185:2121-2131.
29. 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.
30. Takata, M., Y. Homma, and T. Kurosaki. 1995. Requirement of phospholipase C-gamma 2 activation in surface immunoglobulin M-induced B cell apoptosis. J. Exp. Med. 182:907-914.
31. Sugawara, H., M. Kurosaki, M. Takata, and T. Kurosaki. 1997. Genetic evidence for involvement of type 1, type 2 and type 3 inositol 1,4,5-trisphosphate receptors in signal transduction through the B-cell antigen receptor. EMBO J. 16:3078-3088.
32. Hashimoto, A., H. Okada, A. Jiang, M. Kurosaki, S. Greenberg, E.A. Clark, and T. Kurosaki. 1998. Involvement of guanosine triphosphatases and phospholipase C-gamma2 in extracellular signal-regulated kinase, c-Jun NH2-terminal kinase, and p38 mitogen-activated protein kinase activation by the B cell antigen receptor. J. Exp. Med. 188:1287-1295.
33. Hendriks, R.W., M.F. de Bruijn, A. Maas, G.M. Dingjan, A. Karis, and F. Grosveld. 1996. Inactivation of Btk by insertion of lacZ reveals defects in B cell development only past the pre-B cell stage. EMBO J. 15:4862-4872.
34. Russell, D.M., Z. Dembic, G. Morahan, J.F. Miller, K. Burki, and D. Nemazee. 1991. Peripheral deletion of self-reactive B cells. Nature. 354:308-311.
35. Rolink, A., M. Streb, and F. Melchers. 1991. The kappa/lambda ratio in surface immunoglobulin molecules on B lymphocytes differentiating from DHJH-rearranged murine pre-B cell clones in vitro. Eur. J. Immunol. 21:2895-2898.
36. Dingjan, G.M., S. Middendorp, K. Dahlenborg, A. Maas, F. Grosveld, and R.W. Hendriks. 2001. Bruton's tyrosine kinase regulates the activation of gene rearrangements at the lambda light chain locus in precursor B cells in the mouse. J. Exp. Med. 193:1169-1178.
37. Gold, M.R., M.P. Scheid, L. Santos, M. Dang-Lawson, R.A. Roth, L. Matsuuchi, V. Duronio, and D.L. Krebs. 1999. The B cell antigen receptor activates the Akt (protein kinase B)/glycogen synthase kinase-3 signaling pathway via phosphatidylinositol 3-kinase. J. Immunol. 163:1894-1905.
38. Beitz, L.O., D.A. Fruman, T. Kurosaki, L.C. Cantley, and A.M. Scharenberg. 1999. SYK is upstream of phosphoinositide 3-kinase in B cell receptor signaling. J. Biol. Chem. 274:32662-32666.
39. Craxton, A., A. Jiang, T. Kurosaki, and E.A. Clark. 1999. Syk and Bruton's tyrosine kinase are required for B cell antigen receptor-mediated activation of the kinase Akt. J. Biol. Chem. 274:30644-30650.
40. Jiang, A., A. Craxton, T. Kurosaki, and E.A. Clark. 1998. Different protein tyrosine kinases are required for B cell antigen receptor-mediated activation of extracellular signal-regulated kinase, c-Jun NH2-terminal kinase 1, and p38 mitogen-activated protein kinase. J. Exp. Med. 188:1297-1306.
41. Pogue, S.L., T. Kurosaki, J. Bolen, and R. Herbst. 2000. B cell antigen receptor-induced activation of Akt promotes B cell survival and is dependent on Syk kinase. J. Immunol. 165:1300-1306.
42. Bannish, G., E.M. Fuentes-Panana, J.C. Cambier, W.S. Pear, and J.G. Monroe. 2001. Ligand-independent signaling functions for the B lymphocyte antigen receptor and their role in positive selection during B lymphopoiesis. J. Exp. Med. 194:1583-1596.
43. Middendorp, S., G.M. Dingjan, and R.W. Hendriks. 2002. Impaired precursor B cell differentiation in Bruton's tyrosine kinase-deficient mice. J. Immunol. 168:2695-2703.
44. Conley, M.E., and M.D. Cooper. 1998. Genetic basis of abnormal B cell development. Curr. Opin. Immunol. 10:399-406.
45. Nomura, K., H. Kanegane, H. Karasuyama, S. Tsukada, K. Agematsu, G. Murakami, S. Sakazume, M. Sako, R. Tanaka, Y. Kuniya, et al. 2000. Genetic defect in human X-linked agammaglobulinemia impedes a maturational evolution of pro-B cells into a later stage of pre-B cells in the B-cell differentiation pathway. Blood. 96:610-617.
46. 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.
47. Kitanaka, A., H. Mano, M.E. Conley, and D. Campana. 1998. Expression and activation of the nonreceptor tyrosine kinase Tec in human B cells. Blood. 91:940-948.
48. Guo, B., R. M. Kato, M. Garcia-Lloret, M.I. Wahl, and D.J. Rawlings. 2000. Engagement of the human pre-B cell receptor generates a lipid raft-dependent calcium signaling complex. Immunity. 13:243-253.
49. Kouro, T., K. Nagata, S. Takaki, S. Nisitani, M. Hirano, M.I. Wahl, O.N. Witte, H. Karasuyama, and K. Takatsu. 2001. Bruton's tyrosine kinase is required for signaling the CD79b-mediated pro-B to pre-B cell transition. Int. Immunol. 13:485-493.
50. Grabovsky, V., S. Feigelson, C. Chen, D.A. Bleijs, A. Peled, G. Cinamon, F. Baleux, F. Arenzana-Seisdedos, T. Lapidot, Y. van Kooyk, et al. 2000. Subsecond induction of alpha4 integrin clustering by immobilized chemokines stimulates leukocyte tethering and rolling on endothelial vascular cell adhesion molecule 1 under flow conditions. J. Exp. Med. 192:495-506.
51. Leitinger, B., and N. Hogg. 2000. Effects of I domain deletion on the function of the beta2 integrin lymphocyte function-associated antigen-1. Mol. Biol. Cell. 11:677-690.
52. van Kooyk, Y., S.J. van Vliet, and C.G. Figdor. 1999. The actin cytoskeleton regulates LFA-1 ligand binding through avidity rather than affinity changes. J. Biol. Chem. 274:26869-26877.
53. 2+-dependent protease, calpain. J. Cell Biol. 140:699-707.
54. Yauch, R.L., D.P. Felsenfeld, S.K. Kraeft, L.B. Chen, M.P. Sheetz, and M.E. Hemler. 1997. Mutational evidence for control of cell adhesion through integrin diffusion/clustering, independent of ligand binding. J. Exp. Med. 186:1347-1355.
55. Constantin, G., M. Majeed, C. Giagulli, L. Piccio, J.Y. Kim, E.C. Butcher, and C. Laudanna. 2000. Chemokines trigger immediate beta2 integrin affinity and mobility changes: differential regulation and roles in lymphocyte arrest under flow. Immunity. 13:759-769.
56. 2+ mobilization. J. Exp. Med. 186:1897-1910.
57. Pleiman, C.M., W.M. Hertz, and J.C. Cambier. 1994. Activation of phosphatidylinositol-3′ kinase by Src-family kinase SH3 binding to the p85 subunit. Science. 263:1609-1612.
58. 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.
59. Rose, D.M., P.M. Cardarelli, R.R. Cobb, and M.H. Ginsberg. 2000. Soluble VCAM-1 binding to alpha4 integrins is cell-type specific and activation dependent and is disrupted during apoptosis in T cells. Blood. 95:602-609.
60. (2+) or antibody activation. J. Biol. Chem. 276:48670-48678.
61. Leitinger, B., and N. Hogg. 2002. The involvement of lipid rafts in the regulation of integrin function. J. Cell Sci. 115:963-972.
62. Krauss, K., and P. Altevogt. 1999. Integrin leukocyte function-associated antigen-1-mediated cell binding can be activated by clustering of membrane rafts. J. Biol. Chem. 274:36921-36927.
63. 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.
64. Tomlinson, M.G., T. Kurosaki, A.E. Berson, G.H. Fujii, J.A. Johnston, and J.B. Bolen. 1999. Reconstitution of Btk signaling by the atypical tec family tyrosine kinases Bmx and Txk. J. Biol. Chem. 274:13577-13585.
65. 2+ following B-cell receptor activation. EMBO J. 17:1973-1985.
66. Ellmeier, W., S. Jung, M.J. Sunshine, F. Hatam, Y. Xu, D. Baltimore, H. Mano, and D.R. Littman. 2000. Severe B cell deficiency in mice lacking the tec kinase family members Tec and Btk. J. Exp. Med. 192:1611-1624.
67. Forssell, J., A. Nilsson, and P. Sideras. 2000. Reduced formation of phosphatidic acid upon B-cell receptor triggering of mouse B-lymphocytes lacking Bruton's tyrosine kinase. Scand. J. Immunol. 52:30-38.
68. Rigley, K.P., M.M. Harnett, R.J. Phillips, and G.G. Klaus. 1989. Analysis of signaling via surface immunoglobulin receptors on B cells from CBA/ N mice. Eur. J. Immunol. 19:2081-2086.
69. Fujimoto, M., J.C. Poe, A.B. Satterthwaite, M.I. Wahl, O.N. Witte, and T.F. Tedder. 2002. Complementary roles for CD19 and Bruton's tyrosine kinase in B lymphocyte signal transduction. J. Immunol. 168:5465-5476.
70. Cariappa, A., T.J. Kim, and S. Pillai. 1999. Accelerated emigration of B lymphocytes in the Xid mouse. J. Immunol. 162:4417-4423.
71. Martin, F., and J.F. Kearney. 2000. Positive selection from newly formed to marginal zone B cells depends on the rate of clonal production, CD19, and btk. Immunity. 12:39-49.
72. Dingjan, G.M., A. Maas, M.C. Nawijn, L. Smit, J.S. Voerman, F. Grosveld, and R.W. Hendriks. 1998. Severe B cell deficiency and disrupted splenic architecture in transgenic mice expressing the E41K mutated form of Bruton's tyrosine kinase. EMBO J. 17:5309-5320.
73. Ridderstad, A., G.J. Nossal, and D.M. Tarlinton. 1996. The xid mutation diminishes memory B cell generation but does not affect somatic hypermutation and selection. J. Immunol. 157:3357-3365.
74. Vinuesa, C.G., Y. Sunners, J. Pongracz, J. Ball, K.M. Toellner, D. Taylor, I.C. MacLennan, and M.C. Cook. 2001. Tracking the response of Xid B cells in vivo: TI-2 antigen induces migration and proliferation but Btk is essential for terminal differentiation. Eur. J. Immunol. 31:1340-1350.
75. Fruman, D.A., A.B. Satterthwaite, and O.N. Witte. 2000. Xid-like phenotypes: a B cell signalosome takes shape. Immunity. 13:1-3.