Nonredundant roles of Src-family kinases and Syk in the initiation of B-cell antigen receptor signaling

Journal of Immunology

Volumn 190, Issue 4, 2013, Pages 1807-1818

  Stepanek, Ondrej ^a   Draber, Peter ^a   Drobek, Ales ^a   Horejsi, Vaclav ^a   Brdicka, Tomas ^a  

^a INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD79A ANTIGEN; PROTEIN KINASE SYK; PROTEIN KINASE SYK INHIBITOR; PROTEIN TYROSINE KINASE; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CELL STIMULATION; CHICKEN; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; IMMUNE RESPONSE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPLEEN CELL;

ANIMALS; CELL LINE; CELL LINE, TUMOR; CELLS, CULTURED; CHICKENS; ENZYME ACTIVATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, ANIMAL; PRE-B CELL RECEPTORS; PROTEIN-TYROSINE KINASES; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 84873562250     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202401     Document Type: Article

References (75)

1. Shenoy-Scaria, A. M., L. K. Gauen, J. Kwong, A. S. Shaw, and D. M. Lublin. 1993. Palmitylation of an amino-terminal cysteine motif of protein tyrosine kinases p56lck and p59fyn mediates interaction with glycosyl-phosphatidylinositolanchored proteins. Mol. Cell. Biol. 13: 6385-6392.
2. Cross, F. R., E. A. Garber, D. Pellman, and H. Hanafusa. 1984. A short sequence in the p60src N terminus is required for p60src myristylation and membrane association and for cell transformation. Mol. Cell. Biol. 4: 1834-1842.
3. Lowell, C. A. 2004. Src-family kinases: rheostats of immune cell signaling. Mol. Immunol. 41: 631-643.
4. Zhu, J. W., T. Brdicka, T. R. Katsumoto, J. Lin, and A. Weiss. 2008. Structurally distinct phosphatases CD45 and CD148 both regulate B cell and macrophage immunoreceptor signaling. Immunity 28: 183-196.
5. Stepanek, O., T. Kalina, P. Draber, T. Skopcova, K. Svojgr, P. Angelisova, V. Horejsi, A. Weiss, and T. Brdicka. 2011. Regulation of Src family kinases involved in T cell receptor signaling by protein-tyrosine phosphatase CD148. J. Biol. Chem. 286: 22101-22112.
6. Sieh, M., J. B. Bolen, and A. Weiss. 1993. CD45 specifically modulates binding of Lck to a phosphopeptide encompassing the negative regulatory tyrosine of Lck. EMBO J. 12: 315-321.
7. Okada, M., and H. Nakagawa. 1989. A protein tyrosine kinase involved in regulation of pp60c-src function. J. Biol. Chem. 264: 20886-20893.
8. Piwnica-Worms, H., K. B. Saunders, T. M. Roberts, A. E. Smith, and S. H. Cheng. 1987. Tyrosine phosphorylation regulates the biochemical and biological properties of pp60c-src. Cell 49: 75-82.
9. Ingley, E. 2008. Src family kinases: regulation of their activities, levels and identification of new pathways. Biochim. Biophys. Acta 1784: 56-65.
10. Sun, G., L. Ramdas, W. Wang, J. Vinci, J. McMurray, and R. J. Budde. 2002. Effect of autophosphorylation on the catalytic and regulatory properties of protein tyrosine kinase Src. Arch. Biochem. Biophys. 397: 11-17.
11. Turner, M., E. Schweighoffer, F. Colucci, J. P. Di Santo, and V. L. Tybulewicz. 2000. Tyrosine kinase SYK: essential functions for immunoreceptor signalling. Immunol. Today 21: 148-154.
12. Iwashima, M., B. A. Irving, N. S. van Oers, A. C. Chan, and A. Weiss. 1994. Sequential interactions of the TCR with two distinct cytoplasmic tyrosine kinases. Science 263: 1136-1139.
13. Kurosaki, T., S. A. Johnson, L. Pao, K. Sada, H. Yamamura, and J. C. Cambier. 1995. Role of the Syk autophosphorylation site and SH2 domains in B cell antigen receptor signaling. J. Exp. Med. 182: 1815-1823.
14. Tsang, E., A. M. Giannetti, D. Shaw, M. Dinh, J. K. Tse, S. Gandhi, H. Ho, S. Wang, E. Papp, and J. M. Bradshaw. 2008. Molecular mechanism of the Syk activation switch. J. Biol. Chem. 283: 32650-32659.
15. Rolli, V., M. Gallwitz, T. Wossning, A. Flemming, W. W. Schamel, C. Zürn, and M. Reth. 2002. Amplification of B cell antigen receptor signaling by a Syk/ITAM positive feedback loop. Mol. Cell 10: 1057-1069.
16. Mócsai, A., J. Ruland, and V. L. Tybulewicz. 2010. The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat. Rev. Immunol. 10: 387-402.
17. Keshvara, L. M., C. C. Isaacson, T. M. Yankee, R. Sarac, M. L. Harrison, and R. L. Geahlen. 1998. Syk- and Lyn-dependent phosphorylation of Syk on multiple tyrosines following B cell activation includes a site that negatively regulates signaling. J. Immunol. 161: 5276-5283.
18. Furlong, M. T., A. M. Mahrenholz, K. H. Kim, C. L. Ashendel, M. L. Harrison, and R. L. Geahlen. 1997. Identification of the major sites of autophosphorylation of the murine protein-tyrosine kinase Syk. Biochim. Biophys. Acta 1355: 177-190.
19. Brdicka, T., T. A. Kadlecek, J. P. Roose, A. W. Pastuszak, and A. Weiss. 2005. Intramolecular regulatory switch in ZAP-70: analogy with receptor tyrosine kinases. Mol. Cell. Biol. 25: 4924-4933.
20. Bradshaw, J. M. 2010. The Src, Syk, and Tec family kinases: distinct types of molecular switches. Cell. Signal. 22: 1175-1184.
21. Zhang, J., T. Kimura, and R. P. Siraganian. 1998. Mutations in the activation loop tyrosines of protein tyrosine kinase Syk abrogate intracellular signaling but not kinase activity. J. Immunol. 161: 4366-4374.
22. Couture, C., S. Williams, N. Gauthier, P. Tailor, and T. Mustelin. 1997. Role of Tyr518 and Tyr519 in the regulation of catalytic activity and substrate phosphorylation by Syk protein-tyrosine kinase. Eur. J. Biochem. 246: 447-451.
23. Gold, M. R., L. Matsuuchi, R. B. Kelly, and A. L. DeFranco. 1991. Tyrosine phosphorylation of components of the B-cell antigen receptors following receptor crosslinking. Proc. Natl. Acad. Sci. USA 88: 3436-3440.
24. Weiss, A., and D. R. Littman. 1994. Signal transduction by lymphocyte antigen receptors. Cell 76: 263-274.
25. Molina, T. J., K. Kishihara, D. P. Siderovski, W. van Ewijk, A. Narendran, E. Timms, A. Wakeham, C. J. Paige, K. U. Hartmann, A. Veillette, et al. 1992. Profound block in thymocyte development in mice lacking p56lck. Nature 357: 161-164.
26. Hauck, F., C. Randriamampita, E. Martin, S. Gerart, N. Lambert, A. Lim, J. Soulier, Z. Maciorowski, F. Touzot, D. Moshous, et al. 2012. Primary T-cell immunodeficiency with immunodysregulation caused by autosomal recessive LCK deficiency. J. Allergy Clin. Immunol. 130: 1144-1152, e11.
27. Straus, D. B., and A. Weiss. 1992. Genetic evidence for the involvement of the lck tyrosine kinase in signal transduction through the T cell antigen receptor. Cell 70: 585-593.
28. 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.
29. Hibbs, M. L., D. M. Tarlinton, J. Armes, D. Grail, G. Hodgson, R. Maglitto, S. A. Stacker, and A. R. Dunn. 1995. Multiple defects in the immune system of Lyn-deficient mice, culminating in autoimmune disease. Cell 83: 301-311.
30. Chan, V. W., F. Meng, P. Soriano, A. L. DeFranco, and C. A. Lowell. 1997. Characterization of the B lymphocyte populations in Lyn-deficient mice and the role of Lyn in signal initiation and down-regulation. Immunity 7: 69-81.
31. Nishizumi, H., K. Horikawa, I. Mlinaric-Rascan, and T. Yamamoto. 1998. A double-edged kinase Lyn: a positive and negative regulator for antigen receptormediated signals. J. Exp. Med. 187: 1343-1348.
32. Xu, Y., K. W. Harder, N. D. Huntington, M. L. Hibbs, and D. M. Tarlinton. 2005. Lyn tyrosine kinase: accentuating the positive and the negative. Immunity 22: 9-18.
33. Saijo, K., C. Schmedt, I. H. Su, H. Karasuyama, C. A. Lowell, M. Reth, T. Adachi, A. Patke, A. Santana, and A. Tarakhovsky. 2003. Essential role of Src-family protein tyrosine kinases in NF-kappa B activation during B cell development. Nat. Immunol. 4: 274-279.
34. Hibbs, M. L., K. W. Harder, J. Armes, N. Kountouri, C. Quilici, F. Casagranda, A. R. Dunn, and D. M. Tarlinton. 2002. Sustained activation of Lyn tyrosine kinase in vivo leads to autoimmunity. J. Exp. Med. 196: 1593-1604.
35. + mobilization through distinct pathways. EMBO J. 13: 1341-1349.
36. Kurosaki, T. 1997. Molecular mechanisms in B cell antigen receptor signaling. Curr. Opin. Immunol. 9: 309-318.
37. Kulathu, Y., G. Grothe, and M. Reth. 2009. Autoinhibition and adapter function of Syk. Immunol. Rev. 232: 286-299.
38. Kurosaki, T., and M. Hikida. 2009. Tyrosine kinases and their substrates in B lymphocytes. Immunol. Rev. 228: 132-148.
39. Zoller, K. E., I. A. MacNeil, and J. S. Brugge. 1997. Protein tyrosine kinases Syk and ZAP-70 display distinct requirements for Src family kinases in immune response receptor signal transduction. J. Immunol. 158: 1650-1659.
40. Chu, D. H., H. Spits, J. F. Peyron, R. B. Rowley, J. B. Bolen, and A. Weiss. 1996. The Syk protein tyrosine kinase can function independently of CD45 or Lck in T cell antigen receptor signaling. EMBO J. 15: 6251-6261.
41. Sonoda, E., Y. Pewzner-Jung, S. Schwers, S. Taki, S. Jung, D. Eilat, and K. Rajewsky. 1997. B cell development under the condition of allelic inclusion. Immunity 6: 225-233.
42. Otáhal, P., S. Pata, P. Angelisová, V. Hořejší, and T. Brdička. 2011. The effects of membrane compartmentalization of csk on TCR signaling. Biochim. Biophys. Acta 1813: 367-376.
43. Kurebayashi, N., A. B. Harkins, and S. M. Baylor. 1993. Use of fura red as an intracellular calcium indicator in frog skeletal muscle fibers. Biophys. J. 64: 1934-1960.
44. Hanke, J. H., J. P. Gardner, R. L. Dow, P. S. Changelian, W. H. Brissette, E. J. Weringer, B. A. Pollok, and P. A. Connelly. 1996. 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.
45. Yamamoto, N., K. Takeshita, M. Shichijo, T. Kokubo, M. Sato, K. Nakashima, M. Ishimori, H. Nagai, Y. F. Li, T. Yura, and K. B. Bacon. 2003. 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.
46. + mobilizing signals when expressed on differentiated B lineage cells. J. Immunol. 144: 3272-3280.
47. Cumano, A., and K. Rajewsky. 1986. Clonal recruitment and somatic mutation in the generation of immunological memory to the hapten NP. EMBO J. 5: 2459-2468.
48. Schindler, T., F. Sicheri, A. Pico, A. Gazit, A. Levitzki, and J. Kuriyan. 1999. Crystal structure of Hck in complex with a Src family-selective tyrosine kinase inhibitor. Mol. Cell 3: 639-648.
49. Williams, N. K., I. S. Lucet, S. P. Klinken, E. Ingley, and J. Rossjohn. 2009. Crystal structures of the Lyn protein tyrosine kinase domain in its Apo- and inhibitor-bound state. J. Biol. Chem. 284: 284-291.
50. Zhu, X., J. L. Kim, J. R. Newcomb, P. E. Rose, D. R. Stover, L. M. Toledo, H. Zhao, and K. A. Morgenstern. 1999. Structural analysis of the lymphocytespecific kinase Lck in complex with non-selective and Src family selective kinase inhibitors. Structure 7: 651-661.
51. Allen, D., T. Simon, F. Sablitzky, K. Rajewsky, and A. Cumano. 1988. Antibody engineering for the analysis of affinity maturation of an anti-hapten response. EMBO J. 7: 1995-2001.
52. Bain, J., H. McLauchlan, M. Elliott, and P. Cohen. 2003. The specificities of protein kinase inhibitors: an update. Biochem. J. 371: 199-204.
53. Kurosaki, T., M. Takata, Y. Yamanashi, T. Inazu, T. Taniguchi, T. Yamamoto, and H. Yamamura. 1994. Syk activation by the Src-family tyrosine kinase in the B cell receptor signaling. J. Exp. Med. 179: 1725-1729.
54. Takata, M., and T. Kurosaki. 1995. The catalytic activity of Src-family tyrosine kinase is required for B cell antigen receptor signaling. FEBS Lett. 374: 407-411.
55. Pao, L. I., and J. C. Cambier. 1997. Syk, but not Lyn, recruitment to B cell antigen receptor and activation following stimulation of CD45-B cells. J. Immunol. 158: 2663-2669.
56. Gauld, S. B., J. M. Dal Porto, and J. C. Cambier. 2002. B cell antigen receptor signaling: roles in cell development and disease. Science 296: 1641-1642.
57. Kurosaki, T. 2011. Regulation of BCR signaling. Mol. Immunol. 48: 1287-1291.
58. Gauld, S. B., and J. C. Cambier. 2004. Src-family kinases in B-cell development and signaling. Oncogene 23: 8001-8006.
59. Johnson, S. A., C. M. Pleiman, L. Pao, J. Schneringer, K. Hippen, and J. C. Cambier. 1995. Phosphorylated immunoreceptor signaling motifs (ITAMs) exhibit unique abilities to bind and activate Lyn and Syk tyrosine kinases. J. Immunol. 155: 4596-4603.
60. Fujimoto, M., Y. Fujimoto, J. C. Poe, P. J. Jansen, C. A. Lowell, A. L. DeFranco, and T. F. Tedder. 2000. CD19 regulates Src family protein tyrosine kinase activation in B lymphocytes through processive amplification. Immunity 13: 47-57.
61. Hasegawa, M., M. Fujimoto, J. C. Poe, D. A. Steeber, C. A. Lowell, and T. F. Tedder. 2001. A CD19-dependent signaling pathway regulates autoimmunity in Lyn-deficient mice. J. Immunol. 167: 2469-2478.
62. Nika, K., C. Soldani, M. Salek, W. Paster, A. Gray, R. Etzensperger, L. Fugger, P. Polzella, V. Cerundolo, O. Dushek, et al. 2010. Constitutively active Lck kinase in T cells drives antigen receptor signal transduction. Immunity 32: 766-777.
63. El-Hillal, O., T. Kurosaki, H. Yamamura, J. P. Kinet, and A. M. Scharenberg. 1997. syk kinase activation by a src kinase-initiated activation loop phosphorylation chain reaction. Proc. Natl. Acad. Sci. USA 94: 1919-1924.
64. Flaswinkel, H., and M. Reth. 1994. Dual role of the tyrosine activation motif of the Ig-alpha protein during signal transduction via the B cell antigen receptor. EMBO J. 13: 83-89.
65. Pao, L. I., S. J. Famiglietti, and J. C. Cambier. 1998. Asymmetrical phosphorylation and function of immunoreceptor tyrosine-based activation motif tyrosines in B cell antigen receptor signal transduction. J. Immunol. 160: 3305-3314.
66. Gaul, B. S., M. L. Harrison, R. L. Geahlen, R. A. Burton, and C. B. Post. 2000. Substrate recognition by the Lyn protein-tyrosine kinase. NMR structure of the immunoreceptor tyrosine-based activation motif signaling region of the B cell antigen receptor. J. Biol. Chem. 275: 16174-16182.
67. Latour, S., L. M. Chow, and A. Veillette. 1996. Differential intrinsic enzymatic activity of Syk and Zap-70 protein-tyrosine kinases. J. Biol. Chem. 271: 22782-22790.
68. Zhang, J., and R. P. Siraganian. 1999. CD45 is essential for Fc epsilon RI signaling by ZAP70, but not Syk, in Syk-negative mast cells. J. Immunol. 163: 2508-2516.
69. Das, J., M. Ho, J. Zikherman, C. Govern, M. Yang, A. Weiss, A. K. Chakraborty, and J. P. Roose. 2009. Digital signaling and hysteresis characterize ras activation in lymphoid cells. Cell 136: 337-351.
70. Birtwistle, M. R., J. Rauch, A. Kiyatkin, E. Aksamitiene, M. Dobrzy-nski, J. B. Hoek, W. Kolch, B. A. Ogunnaike, and B. N. Kholodenko. 2012. Emergence of bimodal cell population responses from the interplay between analog single-cell signaling and protein expression noise. BMC Syst. Biol. 6: 109.
71. Poderycki, M., Y. Tomimori, T. Ando, W. Xiao, M. Maeda-Yamamoto, K. Sauer, Y. Kawakami, and T. Kawakami. 2010. A minor catalytic activity of Src family kinases is sufficient for maximal activation of mast cells via the high-affinity IgE receptor. J. Immunol. 184: 84-93.
72. Xiao, W., H. Nishimoto, H. Hong, J. Kitaura, S. Nunomura, M. Maeda-Yamamoto, Y. Kawakami, C. A. Lowell, C. Ra, and T. Kawakami. 2005. Positive and negative regulation of mast cell activation by Lyn via the FcepsilonRI. J. Immunol. 175: 6885-6892.
73. McCaig, A. M., E. Cosimo, M. T. Leach, and A. M. Michie. 2011. Dasatinib inhibits B cell receptor signalling in chronic lymphocytic leukaemia but novel combination approaches are required to overcome additional pro-survival microenvironmental signals. Br. J. Haematol. 153: 199-211.
74. Song, Z., P. Lu, R. R. Furman, J. P. Leonard, P. Martin, L. Tyrell, F. Y. Lee, D. M. Knowles, M. Coleman, and Y. L. Wang. 2010. Activities of SYK and PLCgamma2 predict apoptotic response of CLL cells to SRC tyrosine kinase inhibitor dasatinib. Clin. Cancer Res. 16: 587-599.
75. Riccaboni, M., I. Bianchi, and P. Petrillo. 2010. Spleen tyrosine kinases: biology, therapeutic targets and drugs. Drug Discov. Today 15: 517-530.