The immunoglobulin tail tyrosine motif upgrades memory-type BCRs by incorporating a Grb2-Btk signalling module

Nature Communications

Volumn 5, Issue , 2014, Pages

  Engels, Niklas ^a   König, Lars M ^a   Schulze, Wiebke ^a   Radtke, Daniel ^b   Vanshylla, Kanika ^a   Lutz, Johannes ^a   Winkler, Thomas H ^c   Nitschke, Lars ^b   Wienands, Jürgen ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; BRUTON TYROSINE KINASE; CALCIUM ION; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; IMMUNOGLOBULIN G; PROTEIN KINASE SYK; PROTEIN SH3; TYROSINE; AGAMMAGLOBULINAEMIA TYROSINE KINASE; CALCIUM; GRB2 PROTEIN, HUMAN; LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN TYROSINE KINASE;

AMINO ACID; ANATOMY; ANTIBODY; ANTIGEN; CYTOPLASM; MEMBRANE; MEMORY; SIGNALING;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CONTROLLED STUDY; ENZYME ACTIVITY; GENE AMPLIFICATION; HUMAN; HUMAN CELL; IMMUNOGLOBULIN GENE; MEMORY CELL; MOUSE; NONHUMAN; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SEQUENCE ALIGNMENT; T LYMPHOCYTE; VERTEBRATE; ANIMAL; B LYMPHOCYTE; C57BL MOUSE; CHEMISTRY; FEMALE; GENETICS; MALE; METABOLISM; SIGNAL TRANSDUCTION;

VERTEBRATA;

AMINO ACID MOTIFS; ANIMALS; B-LYMPHOCYTES; CALCIUM; FEMALE; GRB2 ADAPTOR PROTEIN; HUMANS; IMMUNOGLOBULIN G; MALE; MICE; MICE, INBRED C57BL; PROTEIN-TYROSINE KINASES; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION; TYROSINE;

EID: 84923291888     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6456     Document Type: Article

References (43)

1. Yoshida, T. et al. Memory B and memory plasma cells. Immunol. Rev. 237, 117-139 (2010).
2. Tangye, S. G. & Tarlinton, D. M. Memory B cells: effectors of long-lived immune responses. Eur. J. Immunol. 39, 2065-2075 (2009).
3. Dogan, I. et al. Multiple layers of B cell memory with different effector functions. Nat. Immunol. 10, 1292-1299 (2009).
4. Pape, K. A., Taylor, J. J., Maul, R. W., Gearhart, P. J. & Jenkins, M. K. Different B cell populations mediate early and late memory during an endogenous immune response. Science 331, 1203-1207 (2011).
5. Uhr, J. W. The Heterogeneity of the Immune Response. Science 145, 457-464 (1964).
6. Engels, N. et al. Recruitment of the cytoplasmic adaptor Grb2 to surface IgG and IgE provides antigen receptor-intrinsic costimulation to class-switched B cells. Nat. Immunol. 10, 1018-1025 (2009).
7. Liu, W., Meckel, T., Tolar, P., Sohn, H. W. & Pierce, S. K. Intrinsic properties of immunoglobulin IgG1 isotype-switched B cell receptors promote microclustering and the initiation of signaling. Immunity 32, 778-789 (2010).
8. Schamel, W. W. & Reth, M. Monomeric and oligomeric complexes of the B cell antigen receptor. Immunity 13, 5-14 (2000).
9. Tolar, P., Sohn, H. W. & Pierce, S. K. The initiation of antigen-induced B cell antigen receptor signaling viewed in living cells by fluorescence resonance energy transfer. Nat. Immunol. 6, 1168-1176 (2005).
10. Reth, M. Antigen receptor tail clue. Nature 338, 383-384 (1989).
11. Rolli, V. et al. Amplification of B cell antigen receptor signaling by a Syk/ITAM positive feedback loop. Mol. Cell 10, 1057-1069 (2002).
12. Engels, N., Wollscheid, B. & Wienands, J. Association of SLP-65/BLNK with the B cell antigen receptor through a non-ITAM tyrosine of Ig-alpha. Eur. J. Immunol. 31, 2126-2134 (2001).
13. Kabak, S. et al. The direct recruitment of BLNK to immunoglobulin alpha couples the B-cell antigen receptor to distal signaling pathways. Mol. Cell Biol. 22, 2524-2535 (2002).
14. Patterson, H. C., Kraus, M., Kim, Y. M., Ploegh, H. & Rajewsky, K. The B cell receptor promotes B cell activation and proliferation through a non-ITAM tyrosine in the Igalpha cytoplasmic domain. Immunity 25, 55-65 (2006).
15. Ishiai, M., Sugawara, H., Kurosaki, M. & Kurosaki, T. Cutting edge: association of phospholipase C-gamma 2 Src homology 2 domains with BLNK is critical for B cell antigen receptor signaling. J. Immunol. 163, 1746-1749 (1999).
16. Su, Y. W. et al. Interaction of SLP adaptors with the SH2 domain of Tec family kinases. Eur. J. Immunol. 29, 3702-3711 (1999).
17. Stork, B. et al. Grb2 and the non-T cell activation linker NTAL constitute a Ca(2+)-regulating signal circuit in B lymphocytes. Immunity 21, 681-691 (2004).
18. Engelke, M., Engels, N., Dittmann, K., Stork, B. & Wienands, J. Ca(2+) signaling in antigen receptor-activated B lymphocytes. Immunol. Rev. 218, 235-246 (2007).
19. Dellis, O. et al. Ca2+ entry through plasma membrane IP3 receptors. Science 313, 229-233 (2006).
20. Kaisho, T., Schwenk, F. & Rajewsky, K. The roles of gamma 1 heavy chain membrane expression and cytoplasmic tail in IgG1 responses. Science 276, 412-415 (1997).
21. Martin, S. W. & Goodnow, C. C. Burst-enhancing role of the IgG membrane tail as a molecular determinant of memory. Nat. Immunol. 3, 182-188 (2002).
22. Waisman, A. 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. 204, 747-758 (2007).
23. Liu, W. et al. The scaffolding protein synapse-associated protein 97 is required for enhanced signaling through isotype-switched IgG memory B cell receptors. Sci. Signal. 5, ra54 (2012).
24. Stork, B. et al. Subcellular localization of Grb2 by the adaptor protein Dok-3 restricts the intensity of Ca2+ signaling in B cells. Embo J. 26, 1140-1149 (2007).
25. Jang, I. K., Zhang, J. & Gu, H. Grb2, a simple adapter with complex roles in lymphocyte development, function, and signaling. Immunol. Rev. 232, 150-159 (2009).
26. Ackermann, J. A., Radtke, D., Maurberger, A., Winkler, T. H. & Nitschke, L. Grb2 regulates B-cell maturation, B-cell memory responses and inhibits B-cell Ca(2+) signalling. Embo J. 30, 1621-1633 (2011).
27. Otipoby, K. L., Draves, K. E. & Clark, E. A. CD22 regulates B cell receptor-mediated signals via two domains that independently recruit Grb2 and SHP-1. J. Biol. Chem. 276, 44315-44322 (2001).
28. Jang, I. K. et al. Growth-factor receptor-bound protein-2 (Grb2) signaling in B cells controls lymphoid follicle organization and germinal center reaction. Proc. Natl Acad. Sci. USA 108, 7926-7931 (2011).
29. Casola, S. et al. Tracking germinal center B cells expressing germ-line immunoglobulin gamma1 transcripts by conditional gene targeting. Proc. Natl Acad. Sci. USA 103, 7396-7401 (2006).
30. Neumann, K., Oellerich, T., Urlaub, H. & Wienands, J. The B-lymphoid Grb2 interaction code. Immunol. Rev. 232, 135-149 (2009).
31. Hawkins, E. D. et al. Regulation of asymmetric cell division and polarity by Scribble is not required for humoral immunity. Nat. Commun. 4, 1801 (2013).
32. Engels, N. & Wienands, J. The signaling tool box for tyrosine-based costimulation of lymphocytes. Curr. Opin. Immunol. 23, 324-329 (2011).
33. Vivier, E., Nunes, J. A. & Vely, F. Natural killer cell signaling pathways. Science 306, 1517-1519 (2004).
34. Raab, M. et al. p56Lck and p59Fyn regulate CD28 binding to phosphatidylinositol 3-kinase, growth factor receptor-bound protein GRB-2, and T cell-specific protein-tyrosine kinase ITK: implications for T-cell costimulation. Proc. Natl Acad. Sci. USA 92, 8891-8895 (1995).
35. Khan, W. N. et al. Defective B cell development and function in Btk-deficient mice. Immunity 3, 283-299 (1995).
36. Khan, A. Q., Sen, G., Guo, S., Witte, O. N. & Snapper, C. M. Induction of in vivo antipolysaccharide immunoglobulin responses to intact Streptococcus pneumoniae is more heavily dependent on Btk-mediated B-cell receptor signaling than antiprotein responses. Infect. Immun. 74, 1419-1424 (2006).
37. Ellmeier, W. et al. Severe B cell deficiency in mice lacking the tec kinase family members Tec and Btk. J. Exp. Med. 192, 1611-1624 (2000).
38. Hikida, M. et al. PLC-gamma2 is essential for formation and maintenance of memory B cells. J. Exp. Med. 206, 681-689 (2009).
39. Paus, D. et al. Antigen recognition strength regulates the choice between extrafollicular plasma cell and germinal center B cell differentiation. J. Exp. Med. 203, 1081-1091 (2006).
40. Phan, T. G. et al. High affinity germinal center B cells are actively selected into the plasma cell compartment. J. Exp. Med. 203, 2419-2424 (2006).
41. Chan, T. D. et al. Antigen affinity controls rapid T-dependent antibody production by driving the expansion rather than the differentiation or extrafollicular migration of early plasmablasts. J. Immunol. 183, 3139-3149 (2009).
42. Liu, W., Meckel, T., Tolar, P., Sohn, H. W. & Pierce, S. K. Antigen affinity discrimination is an intrinsic function of the B cell receptor. J. Exp. Med. 207, 1095-1111 (2010).
43. Kometani, K. et al. Repression of the transcription factor Bach2 contributes to predisposition of IgG1 memory B cells toward plasma cell differentiation. Immunity 39, 136-147 (2013).