Monovalent and multivalent ligation of the B cell receptor exhibit differential dependence upon Syk and Src family kinases

Science Signaling

Volumn 6, Issue 256, 2013, Pages

  Mukherjee, Sayak ^a   Zhu, Jing ^b   Zikherman, Julie ^b   Parameswaran, Ramya ^b   Kadlecek, Theresa A ^b   Wang, Qi ^c   Au Yeung, Byron ^b   Ploegh, Hidde ^d   Kuriyan, John ^c   Das, Jayajit ^a   Weiss, Arthur ^b  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; PROTEIN KINASE SYK; PROTEIN SH2; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL LINEAGE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; IN VITRO STUDY; MONTE CARLO METHOD; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBODIES, MONOCLONAL; B-LYMPHOCYTES; CLONING, MOLECULAR; COMPUTER SIMULATION; FEEDBACK, PHYSIOLOGICAL; HEK293 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, IMMUNOLOGICAL; MONTE CARLO METHOD; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; RECEPTORS, ANTIGEN, B-CELL; SF9 CELLS; SIGNAL TRANSDUCTION; SPODOPTERA; SRC-FAMILY KINASES; ULTRACENTRIFUGATION; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 84872585135     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2003220     Document Type: Article

References (66)

1. T. Kurosaki, H. Shinohara, Y. Baba, B cell signaling and fate decision. Annu. Rev. Immunol. 28, 21-55 (2010).
2. M. L. Hermiston, J. Zikherman, J. W. Zhu, CD45, CD148, and Lyp/Pep: Critical phosphatases regulating Src family kinase signaling networks in immune cells. Immunol. Rev. 228, 288-311 (2009).
3. L. Shiue, M. J. Zoller, J. S. Brugge, Syk is activated by phosphotyrosine-containing peptides representing the tyrosine-based activation motifs of the high affinity receptor for IgE. J. Biol. Chem. 270, 10498-10502 (1995).
4. T. Brdicka, T. A. Kadlecek, J. P. Roose, A. W. Pastuszak, A. Weiss, Intramolecular regulatory switch in ZAP-70: Analogy with receptor tyrosine kinases. Mol. Cell. Biol. 25, 4924-4933 (2005).
5. S. Deindl, T. A. Kadlecek, T. Brdicka, X. Cao, A. Weiss, J. Kuriyan, Structural basis for the inhibition of tyrosine kinase activity of ZAP-70. Cell 129, 735-746 (2007).
6. S. Deindl, T. A. Kadlecek, X. Cao, J. Kuriyan, A. Weiss, Stability of an autoinhibitory interface in the structure of the tyrosine kinase ZAP-70 impacts T cell receptor response. Proc. Natl. Acad. Sci. U.S.A. 106, 20699-20704 (2009).
7. J. M. Bradshaw, The Src, Syk, and Tec family kinases: Distinct types of molecular switches. Cell. Signal. 22, 1175-1184 (2010).
8. R. L. Geahlen, Syk and pTyr'd: Signaling through the B cell antigen receptor. Biochim. Biophys. Acta 1793, 1115-1127 (2009).
9. E. H. Palacios, A. Weiss, Function of the Src-family kinases, Lck and Fyn, in T-cell development and activation. Oncogene 23, 7990-8000 (2004).
10. K. Kishihara, J. Penninger, V. A. Wallace, T. M. Kündig, K. Kawai, A. Wakeham, E. Timms, K. Pfeffer, P. S. Ohashi, M. L. Thomas, C. Furlonger, C. J. Paige, T. W. Mak, Normal B lymphocyte development but impaired T cell maturation in CD45-exon6 protein tyrosine phosphatase-deficient mice. Cell 74, 143-156 (1993).
11. + thymocytes, and B cell maturation. J. Exp. Med. 183, 1707-1718 (1996).
12. P. J. Mee, M. Turner, M. A. Basson, P. S. Costello, R. Zamoyska, V. L. Tybulewicz, Greatly reduced efficiency of both positive and negative selection of thymocytes in CD45 tyrosine phosphatase-deficient mice. Eur. J. Immunol. 29, 2923-2933 (1999).
13. J. D. Stone, L. A. Conroy, K. F. Byth, R. A. Hederer, S. Howlett, Y. Takemoto, N. Holmes, D. R. Alexander, Aberrant TCR-mediated signaling in CD45-null thymocytes involves dysfunctional regulation of Lck, Fyn, TCR-ζ, and ZAP-70. J. Immunol. 158, 5773-5782 (1997).
14. N. S. van Oers, B. Lowin-Kropf, D. Finlay, K. Connolly, A. Weiss, αβ T cell development is abolished in mice lacking both Lck and Fyn protein tyrosine kinases. Immunity 5, 429-436 (1996).
15. F. Van Laethem, S. D. Sarafova, J. H. Park, X. Tai, L. Pobezinsky, T. I. Guinter, S. Adoro, A. Adams, S. O. Sharrow, L. Feigenbaum, A. Singer, Deletion of CD4 and CD8 coreceptors permits generation of αβT cells that recognize antigens independently of the MHC. Immunity 27, 735-750 (2007).
16. M. Takata, H. Sabe, A. Hata, T. Inazu, Y. Homma, T. Nukada, H. Yamamura, T. Kurosaki, Tyrosine kinases Lyn and Syk regulate B cell receptor-coupled Ca2+ mobilization through distinct pathways. EMBO J. 13, 1341-1349 (1994).
17. M. Turner, P. J. Mee, P. S. Costello, O. Williams, A. A. Price, L. P. Duddy, M. T. Furlong, R. L. Geahlen, V. L. Tybulewicz, Perinatal lethality and blocked B-cell development in mice lacking the tyrosine kinase Syk. Nature 378, 298-302 (1995).
18. A. M. Cheng, B. Rowley, W. Pao, A. Hayday, J. B. Bolen, T. Pawson, Syk tyrosine kinase required for mouse viability and B-cell development. Nature 378, 303-306 (1995).
19. R. J. Cornall, A. M. Cheng, T. Pawson, C. C. Goodnow, Role of Syk in B-cell development and antigen-receptor signaling. Proc. Natl. Acad. Sci. U.S.A. 97, 1713-1718 (2000).
20. K. Saijo, C. Schmedt, I. H. Su, H. Karasuyama, C. A. Lowell, M. Reth, T. Adachi, A. Patke, A. Santana, A. Tarakhovsky, Essential role of Src-family protein tyrosine kinases in NF-κB activation during B cell development. Nat. Immunol. 4, 274-279 (2003).
21. J. W. Zhu, T. Brdicka, T. R. Katsumoto, J. Lin, A. Weiss, Structurally distinct phosphatases CD45 and CD148 both regulate B cell and macrophage immunoreceptor signaling. Immunity 28, 183-196 (2008).
22. D. H. Chu, H. Spits, J. F. Peyron, R. B. Rowley, J. B. Bolen, A. Weiss, The Syk protein tyrosine kinase can function independently of CD45 or Lck in T cell antigen receptor signaling. EMBO J. 15, 6251-6261 (1996).
23. V. Rolli, M. Gallwitz, T. Wossning, A. Flemming, W. W. Schamel, C. Zürn, M. Reth, Amplification of B cell antigen receptor signaling by a Syk/ITAM positive feedback loop. Mol. Cell 10, 1057-1069 (2002).
24. O. El-Hillal, T. Kurosaki, H. Yamamura, J. P. Kinet, A. M. Scharenberg, syk kinase activation by a src kinase-initiated activation loop phosphorylation chain reaction. Proc. Natl. Acad. Sci. U.S.A. 94, 1919-1924 (1997).
25. N. E. Harwood, F. D. Batista, Early events in B cell activation. Annu. Rev. Immunol. 28, 185-210 (2010).
26. P. Tolar, J. Hanna, P. D. Krueger, S. K. Pierce, The constant region of the membrane immunoglobulin mediates B cell-receptor clustering and signaling in response to membrane antigens. Immunity 30, 44-55 (2009).
27. J. Yang, M. Reth, The dissociation activation model of B cell antigen receptor triggering. FEBS Lett. 584, 4872-4877 (2010).
28. B. Treanor, D. Depoil, A. Gonzalez-Granja, P. Barral, M. Weber, O. Dushek, A. Bruckbauer, F. D. Batista, The membrane skeleton controls diffusion dynamics and signaling through the B cell receptor. Immunity 32, 187-199 (2010).
29. W. Liu, T. Meckel, P. Tolar, H. W. Sohn, S. K. Pierce, Antigen affinity discrimination is an intrinsic function of the B cell receptor. J. Exp. Med. 207, 1095-1111 (2010).
30. E. Tsang, A. M. Giannetti, D. Shaw, M. Dinh, J. K. Tse, S. Gandhi, H. Ho, S. Wang, E. Papp, J. M. Bradshaw, Molecular mechanism of the Syk activation switch. J. Biol. Chem. 283, 32650-32659 (2008).
31. D. Qian, M. N. Mollenauer, A. Weiss, Dominant-negative zeta-associated protein 70 inhibits T cell antigen receptor signaling. J. Exp. Med. 183, 611-620 (1996).
32. D. H. Chu, C. T. Morita, A. Weiss, The Syk family of protein tyrosine kinases in T-cell activation and development. Immunol. Rev. 165, 167-180 (1998).
33. E. A. Ottinger, M. C. Botfield, S. E. Shoelson, Tandem SH2 domains confer high specificity in tyrosine kinase signaling. J. Biol. Chem. 273, 729-735 (1998).
34. F. D. Batista, E. Arana, P. Barral, Y. R. Carrasco, D. Depoil, J. Eckl-Dorna, S. Fleire, K. Howe, A. Vehlow, M. Weber, B. Treanor, The role of integrins and coreceptors in refining thresholds for B-cell responses. Immunol. Rev. 218, 197-213 (2007).
35. C. L. Adams, M. K. Macleod, E. James Milner-White, R. Aitken, P. Garside, D. I. Stott, Complete analysis of the B-cell response to a protein antigen, from in vivo germinal centre formation to 3-D modelling of affinity maturation. Immunology 108, 274-287 (2003).
36. T. B. Lavoie, W. N. Drohan, S. J. Smith-Gill, Experimental analysis by site-directed mutagenesis of somatic mutation effects on affinity and fine specificity in antibodies specific for lysozyme. J. Immunol. 148, 503-513 (1992).
37. S. J. Fleire, J. P. Goldman, Y. R. Carrasco, M. Weber, D. Bray, F. D. Batista, B cell ligand discrimination through a spreading and contraction response. Science 312, 738-741 (2006).
38. P. K. Tsourkas, W. Liu, S. C. Das, S. K. Pierce, S. Raychaudhuri, Discrimination of membrane antigen affinity by B cells requires dominance of kinetic proofreading over serial engagement. Cell. Mol. Immunol. 9, 62-74 (2012).
39. P. K. Tsourkas, C. D. Somkanya, P. Yu-Yang, W. Liu, S. K. Pierce, S. Raychaudhuri, Formation of BCR oligomers provides a mechanism for B cell affinity discrimination. J. Theor. Biol. 307, 174-182 (2012).
40. J. G. Monroe, ITAM-mediated tonic signalling through pre-BCR and BCR complexes. Nat. Rev. Immunol. 6, 283-294 (2006).
41. L. Srinivasan, Y. Sasaki, D. P. Calado, B. Zhang, J. H. Paik, R. A. DePinho, J. L. Kutok, J. F. Kearney, K. L. Otipoby, K. Rajewsky, PI3 kinase signals BCR-dependent mature B cell survival. Cell 139, 573-586 (2009).
42. J. Zikherman, R. Parameswaran, A. Weiss, Endogenous antigen tunes the responsiveness of naive B cells but not T cells. Nature 489, 160-164 (2012).
43. S. M. Abel, J. P. Roose, J. T. Groves, A. Weiss, A. K. Chakraborty, The membrane environment can promote or suppress bistability in cell signaling networks. J. Phys. Chem. B 116, 3630-3640 (2012).
44. K. Luby-Phelps, Cytoarchitecture and physical properties of cytoplasm: Volume, viscosity, diffusion, intracellular surface area. Int. Rev. Cytol. 192, 189-221 (2000).
45. A. C. Chan, M. Iwashima, C. W. Turck, A. Weiss, ZAP-70: A 70 kd protein tyrosine kinase that associates with the TCR ζ chain. Cell 71, 649-662 (1992).
46. M. Iwashima, B. A. Irving, N. S. van Oers, A. C. Chan, A. Weiss, Sequential interactions of the TCR with two distinct cytoplasmic tyrosine kinases. Science 263, 1136-1139 (1994).
47. S. A. Johnson, C. M. Pleiman, L. Pao, J. Schneringer, K. Hippen, J. C. Cambier, Phosphorylated immunoreceptor signaling motifs (ITAMs) exhibit unique abilities to bind and activate Lyn and Syk tyrosine kinases. J. Immunol. 155, 4596-4603 (1995).
48. D. Straus, A. Weiss, Genetic evidence for the involvement of the lck tyrosine kinase in signal transduction through the T cell antigen receptor. Cell 70, 585-593 (1992).
49. N. S. van Oers, N. Killeen, A. Weiss, Lck regulates the tyrosine phosphorylation of the T cell receptor subunits and ZAP-70 in murine thymocytes. J. Exp. Med. 183, 1053-1062 (1996).
50. A. L. DeFranco, V. W. Chan, C. A. Lowell, Positive and negative roles of the tyrosine kinase Lyn in B cell function. Semin. Immunol. 10, 299-307 (1998).
51. J. H. Hanke, J. P. Gardner, R. L. Dow, P. S. Changelian, W. H. Brissette, E. J. Weringer, B. A. Pollok, P. A. Connelly, Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 271, 695-701 (1996).
52. N. Yamamoto, K. Takeshita, M. Shichijo, T. Kokubo, M. Sato, K. Nakashima, M. Ishimori, H. Nagai, Y. F. Li, T. Yura, K. B. Bacon, The orally available spleen tyrosine kinase inhibitor 2-[7-(3,4-dimethoxyphenyl)-imidazo[1,2-c] pyrimidin-5-ylamino]nicotinamide dihydrochloride (BAY 61-3606) blocks antigen-induced airway inflammation in rodents. J. Pharmacol. Exp. Ther. 306, 1174-1181 (2003).
53. C. C. Goodnow, J. Crosbie, S. Adelstein, T. B. Lavoie, S. J. Smith-Gill, R. A. Brink, H. Pritchard-Briscoe, J. S. Wotherspoon, R. H. Loblay, K. Raphael, R. J. Trent, A. Basten, Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 334, 676-682 (1988).
54. Y. M. Kim, J. Y. Pan, G. A. Korbel, V. Peperzak, M. Boes, H. L. Ploegh, Monovalent ligation of the B cell receptor induces receptor activation but fails to promote antigen presentation. Proc. Natl. Acad. Sci. U.S.A. 103, 3327-3332 (2006).
55. D. T. Gillespie, Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem. 81, 2340-2361 (1977).
56. M. Lis, M. N. Artyomov, S. Devadas, A. K. Chakraborty, Efficient stochastic simulation of reaction-diffusion processes via direct compilation. Bioinformatics 25, 2289-2291 (2009).
57. X. Zhang, J. Gureasko, K. Shen, P. A. Cole, J. Kuriyan, An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 125, 1137-1149 (2006).
58. B. B. Au-Yeung, S. Deindl, L. Y. Hsu, E. H. Palacios, S. E. Levin, J. Kuriyan, A. Weiss, The structure, regulation, and function of ZAP-70. Immunol. Rev. 228, 41-57 (2009).
59. D. H. Chu, N. S. van Oers, M. Malissen, J. Harris, M. Elder, A. Weiss, Pre-T cell receptor signals are responsible for the down-regulation of Syk protein tyrosine kinase expression. J. Immunol. 163, 2610-2620 (1999).
60. A. C. Chan, B. A. Irving, J. D. Fraser, A. Weiss, The ζ chain is associated with a tyrosine kinase and upon T-cell antigen receptor stimulation associates with ZAP-70, a 70-kDa tyrosine phosphoprotein. Proc. Natl. Acad. Sci. U.S.A. 88, 9166-9170 (1991).
61. W. Liu, H. W. Sohn, P. Tolar, S. K. Pierce, It's all about change: The antigen-driven initiation of B-cell receptor signaling. Cold Spring Harb. Perspect. Biol. 2, a002295 (2010).
62. T. W. McKeithan, Kinetic proofreading in T-cell receptor signal transduction. Proc. Natl. Acad. Sci. U.S.A. 92, 5042-5046 (1995).
63. P. K. Tsourkas, N. Baumgarth, S. I. Simon, S. Raychaudhuri, Mechanisms of B-cell synapse formation predicted by Monte Carlo simulation. Biophys. J. 92, 4196-4208 (2007).
64. G. Altan-Bonnet, R. N. Germain, Modeling T cell antigen discrimination based on feedback control of digital ERK responses. PLoS Biol. 3, e356 (2005).
65. Z. Zhang, K. Shen, W. Lu, P. A. Cole, The role of C-terminal tyrosine phosphorylation in the regulation of SHP-1 explored via expressed protein ligation. J. Biol. Chem. 278, 4668-4674 (2003).
66. J. R. Faeder, W. S. Hlavacek, I. Reischl, M. L. Blinov, H. Metzger, A. Redondo, C. Wofsy, B. Goldstein, Investigation of early events in FcεRI-mediated signaling using a detailed mathematical model. J. Immunol. 170, 3769-3781 (2003).