Differential phosphorylation of functional tyrosines in CD19 modulates B-lymphocyte activation

European Journal of Immunology

Volumn 40, Issue 4, 2010, Pages 1192-1204

  Ishiura, Nobuko ^a,b   Nakashima, Hiroko ^a,b   Watanabe, Rei ^a,b   Kuwano, Yoshihiro ^a,b   Adachi, Takahiro ^c   Takahashi, Yoshimasa ^d   Tsubata, Takeshi ^c   Okochi, Hitoshi ^b   Tamaki, Kunihiko ^a   Tedder, Thomas F ^e   Fujimoto, Manabu ^b,f  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

^f KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

Author keywords

B cell; Cell surface molecule; Signal transduction

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD19 ANTIBODY; CD19 ANTIGEN; CD40 ANTIGEN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOSPECIFIC ANTIBODY; PROTEIN KINASE B; VAV PROTEIN;

ANIMAL CELL; ANTIBODY SPECIFICITY; ARTICLE; B LYMPHOCYTE ACTIVATION; CELL MEMBRANE; CONTROLLED STUDY; KINETICS; LIPID RAFT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIGENS, CD19; ANTIGENS, CD40; B-LYMPHOCYTES; CELL LINE, TUMOR; CROSSES, GENETIC; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; LYMPHOCYTE ACTIVATION; LYMPHOMA, B-CELL; MEMBRANE MICRODOMAINS; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; PHOSPHOTYROSINE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-VAV; RECEPTORS, ANTIGEN, B-CELL; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SPECIFIC PATHOGEN-FREE ORGANISMS;

EID: 77951082776     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939848     Document Type: Article

References (49)

1. Kurosaki, T. and Hikida, M., Tyrosine kinases and their substrates in B lymphocytes. Immunol. Rev. 2009. 228: 132-148.
2. Fujimoto, M., Poe, J. C., Inaoki, M. and Tedder, T. F., CD19 regulates B lymphocyte responses to transmembrane signals. Semin. Immunol. 1998. 10: 267-277.
3. Fearon, D. T. and Carroll, M. C., Regulation of B lymphocyte responses to foreign and self-antigens by the CD19/CD21 complex. Annu. Rev. Immunol. 2000. 18: 393-422.
4. Carter, R. H. and Barrington, R. A., Signaling by the CD19/CD21 complex on B cells. Curr. Dir. Autoimmun. 2004. 7: 4-32.
5. Rickert, R. C., Regulation of B lymphocyte activation by complement C3 and the B cell coreceptor complex. Curr. Opin. Immunol. 2005. 17: 237-243.
6. Dempsey, P. W., Allison, M. E., Akkaraju, S., Goodnow, C. C. and Fearon, D. T., C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science 1996. 271: 348-350. (Pubitemid 3021509)
7. Zabel, M. D. and Weis, J. H., Cell-specific regulation of the CD21 gene. Int. Immunopharmacol. 2001. 1: 483-493.
8. Tedder, T. F., Poe, J. C., Fujimoto, M., Haas, K. M. and Sato, S., The CD19-CD21 signal transduction complex of B lymphocytes regulates the balance between health and autoimmune disease: systemic sclerosis as a model system. Curr. Dir. Autoimmun. 2005. 8: 55-90.
9. Engel, P., Zhou, L. J., Ord, D. C., Sato, S., Koller, B. and Tedder, T. F., Abnormal B lymphocyte development, activation, and differentiation in mice that lack or overexpress the CD19 signal transduction molecule. Immunity 1995. 3: 39-50.
10. Rickert, R. C., Rajewsky, K. and Roes, J., Impairment of T-cell-dependent B-cell responses and B-1 cell development in CD19-deficient mice. Nature 1995. 376: 352-355.
11. Anzelon, A. N., Wu, H. and Rickert, R. C., Pten inactivation alters peripheral B lymphocyte fate and reconstitutes CD19 function. Nat. Immunol. 2003. 4: 287-294.
12. Haas, K. M., Poe, J. C., Steeber, D. A. and Tedder, T. F., B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity 2005. 23: 7-18.
13. van Zelm, M. C., Reisli, I., van der Burg, M., Castano, D., van Noesel, C. J., van Tol, M. J.,Woellner, C. et al., An antibody-deficiency syndrome due to mutations in the CD19 gene. N Engl. J. Med. 2006. 354: 1901-1912.
14. Tedder, T. F. and Isaacs, C. M., Isolation of cDNAs encoding the CD19 antigen of human and mouse B lymphocytes. A new member of the immunoglobulin superfamily. J. Immunol. 1989. 143: 712-717.
15. Vigorito, E., Kovesdi, D. and Turner, M., Synergistic activation of PKD by the B cell antigen receptor and CD19 requires PI3K, Vav1 and PLCgamma. Cell. Signal. 2006. 18: 1455-1460. (Pubitemid 43832082)
16. Inabe, K. and Kurosaki, T., Tyrosine phosphorylation of B-cell adaptor for phosphoinositide 3-kinase is required for Akt activation in response to CD19 engagement. Blood 2002. 99: 584-589. (Pubitemid 34533096)
17. Beckwith, M., Jorgensen, G. and Longo, D. L., The protein product of the proto-oncogene c-cbl forms a complex with phosphatidylinositol 3-kinase p85 and CD19 in anti-IgM-stimulated human B-lymphoma cells. Blood 1996. 88: 3502-3507. (Pubitemid 26365585)
18. Tuveson, D. A., Carter, R. H., Soltoff, S. P. and Fearon, D. T., CD19 of B cells as a surrogate kinase insert region to bind phosphatidylinositol 3-kinase. Science 1993. 260: 986-989.
19. Brooks, S. R., Kirkham, P. M., Freeberg, L. and Carter, R. H., Binding of cytoplasmic proteins to the CD19 intracellular domain is high affinity, competitive, and multimeric. J. Immunol. 2004. 172: 7556-7564. (Pubitemid 38747619)
20. 2+ mobilization. J. Exp. Med. 1997. 186: 1897-1910.
21. Carter, R. H., Doody, G. M., Bolen, J. B. and Fearon, D. T., Membrane IgM-induced tyrosine phosphorylation of CD19 requires a CD19 domain that mediates association with components of the B cell antigen receptor complex. J. Immunol. 1997. 158: 3062-3069.
22. Buhl, A. M. and Cambier, J. C., Phosphorylation of CD19 Y484 and Y515, and linked activation of phosphatidylinositol 3-kinase, are required for B cell antigen receptor-mediated activation of Bruton's tyrosine kinase. J. Immunol. 1999. 162: 4438-4446.
23. Weng, W. K., Jarvis, L. and LeBien, T. W., Signaling through CD19 activates Vav/mitogen-activated protein kinase pathway and induces formation of a CD19/Vav/phosphatidylinositol 3-kinase complex in human B cell precursors. J. Biol. Chem. 1994. 269: 32514-32521.
24. Li, X., Sandoval, D., Freeberg, L. and Carter, R. H., Role of CD19 tyrosine 391 in synergistic activation of B lymphocytes by coligation of CD19 and membrane Ig. J. Immunol. 1997. 158: 5649-5657. (Pubitemid 127483968)
25. Vigorito, E., Bardi, G., Glassford, J., Lam, E.W., Clayton, E. and Turner, M., Vav-dependent and vav-independent phosphatidylinositol 3-kinase activation in murine B cells determined by the nature of the stimulus. J. Immunol. 2004. 173: 3209-3214. (Pubitemid 39142028)
26. O'Rourke, L. M., Tooze, R., Turner, M., Sandoval, D. M., Carter, R. H., Tybulewicz, V. L. and Fearon, D. T., CD19 as a membrane-anchored adaptor protein of B lymphocytes: costimulation of lipid and protein kinases by recruitment of Vav. Immunity 1998. 8: 635-645. (Pubitemid 28264754)
27. Wang, Y., Brooks, S. R., Li, X., Anzelon, A. N., Rickert, R. C. and Carter, R. H., The physiologic role of CD19 cytoplasmic tyrosines. Immunity 2002. 17: 501-514. (Pubitemid 35223538)
28. Wang, Y. and Carter, R. H., CD19 regulates B cell maturation, proliferation, and positive selection in the FDC zone of murine splenic germinal centers. Immunity 2005. 22: 749-761. (Pubitemid 40814505)
29. Fujimoto, M., Fujimoto, Y., Poe, J. C., Jansen, P. J., Lowell, C. A., DeFranco, A. L. and Tedder, T. F., CD19 regulates Src family protein tyrosine kinase activation in B lymphocytes through processive amplification. Immunity 2000. 13: 47-57.
30. Fujimoto, M., Poe, J. C., Jansen, P. J., Sato, S. and Tedder, T. F., CD19 amplifies B lymphocyte signal transduction by regulating Src-family protein tyrosine kinase activation. J. Immunol. 1999. 162: 7088-7094. (Pubitemid 29277677)
31. Roifman, C. M. and Ke, S., CD19 is a substrate of the antigen receptor-associated protein tyrosine kinase in human B cells. Biochem. Biophys. Res. Commun. 1993. 194: 222-225.
32. van Noesel, C. J., Lankester, A. C., van Schijndel, G. M. and van Lier, R. A., The CR2/CD19 complex on human B cells contains the src-family kinase Lyn. Int. Immunol. 1993. 5: 699-705.
33. Fujimoto, M., Poe, J. C., Satterthwaite, A. B., Wahl, M. I., Witte, O. N. and Tedder, T. F., Complementary roles for CD19 and Bruton's tyrosine kinase in B lymphocyte signal transduction. J. Immunol. 2002. 168: 5465-5476. (Pubitemid 34556124)
34. Martin, S. W. and Goodnow, C. C., Burst-enhancing role of the IgG membrane tail as a molecular determinant of memory. Nat. Immunol. 2002. 3: 182-188.
35. Kaisho, T., Schwenk, F. and Rajewsky, K., The roles of gamma 1 heavy chain membrane expression and cytoplasmic tail in IgG1 responses. Science 1997. 276: 412-415. (Pubitemid 27180702)
36. Wakabayashi, C., Adachi, T., Wienands, J. and Tsubata, T., A distinct signaling pathway used by the IgG-containing B cell antigen receptor. Science 2002. 298: 2392-2395. (Pubitemid 36014213)
37. Otero, D. C., Omori, S. A. and Rickert, R. C., Cd19-dependent activation of Akt kinase in B-lymphocytes. J. Biol. Chem. 2001. 276: 1474-1478.
38. Dykstra, M., Cherukuri, A., Sohn, H. W., Tzeng, S. J. and Pierce, S. K., Location is everything: lipid rafts and immune cell signaling. Annu. Rev. Immunol. 2003. 21: 457-481.
39. Cheng, P. C., Dykstra,M. L., Mitchell, R. N. and Pierce, S. K., A role for lipid rafts in B cell antigen receptor signaling and antigen targeting. J. Exp. Med. 1999. 190: 1549-1560.
40. Cherukuri, A., Cheng, P. C., Sohn, H. W. and Pierce, S. K., The CD19/CD21 complex functions to prolong B cell antigen receptor signaling from lipid rafts. Immunity 2001. 14: 169-179. (Pubitemid 32206519)
41. 2+ responses: a role for Lyn sequestration in extinguishing negative regulation. J. Biol. Chem. 2001. 276: 44820-44827.
42. Engels, N., Konig, L. M., Heemann, C., Lutz, J., Tsubata, T., Griep, S., Schrader, V. and Wienands, J., Recruitment of the cytoplasmic adaptor Grb2 to surface IgG and IgE provides antigen receptor-intrinsic costimulation to class-switched B cells. Nat. Immunol. 2009. 10: 1018-1025.
43. Waisman, A., Kraus, M., Seagal, J., Ghosh, S., Melamed, D., Song, J., Sasaki, Y. et al., IgG1 B cell receptor signaling is inhibited by CD22 and promotes the development of B cells whose survival is less dependent on Ig alpha/beta. J. Exp. Med. 2007. 204: 747-758.
44. Fujimoto, M. and Sato, S., B cell signaling and autoimmune diseases: CD19/CD22 loop as a B cell signaling device to regulate the balance of autoimmunity. J. Dermatol. Sci. 2007. 46: 1-9.
45. Monroe, J. G., ITAM-mediated tonic signalling through pre-BCR and BCR complexes. Nat. Rev. Immunol. 2006. 6: 283-294.
46. Okada, T., Maeda, A., Iwamatsu, A., Gotoh, K. and Kurosaki, T., BCAP: the tyrosine kinase substrate that connects B cell receptor to phosphoinositide 3-kinase activation. Immunity 2000. 13: 817-827. (Pubitemid 32041804)
47. Aiba, Y., Kameyama, M., Yamazaki, T., Tedder, T. F. and Kurosaki, T., Regulation of B-cell development by BCAP and CD19 through their binding to phosphoinositide 3-kinase. Blood 2008. 111: 1497-1503. (Pubitemid 351213438)
48. Zipfel, P. A., Grove, M., Blackburn, K., Fujimoto, M., Tedder, T. F. and Pendergast, A. M., The c-Abl tyrosine kinase is regulated downstream of the B cell antigen receptor and interacts with CD19. J. Immunol. 2000. 165: 6872-6879. (Pubitemid 32001156)
49. Fujimoto, M., Kuwano, Y., Watanabe, R., Asashima, N., Nakashima, H., Yoshitake, S., Okochi, H., Tamaki, K., Poe, J. C., Tedder, T. F., and Sato, S., B cell antigen receptor and CD40 differentially regulate CD22 tyrosine phosphorylation. J. Immunol. 2006. 176: 873-879. (Pubitemid 43099684)