The protein tyrosine kinase Tec regulates mast cell function

European Journal of Immunology

Volumn 39, Issue 11, 2009, Pages 3228-3238

  Schmidt, Uwe ^a,d   Abramova, Anastasia ^a   Boucheron, Nicole ^a   Eckelhart, Eva ^a,b   Schebesta, Alexandra ^a   Bilic, Ivan ^a,e   Kneidinger, Michael ^b   Unger, Bernd ^a,c   Hammer, Martina ^b   Sibilia, Maria ^b   Valent, Peter ^b   Ellmeier, Wilfried ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c Nabriva Therapeutics AG ^*  (Austria)

^d Nabriva Therapeutics Inc   (Austria)

^e RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

Author keywords

Kinases; Knockout mice; Mast cells; Signal transduction

Indexed keywords

BRUTON TYROSINE KINASE; FC RECEPTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HISTAMINE; INTERLEUKIN 13; INTERLEUKIN 4; LEUKOTRIENE C4; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE TEC; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; HISTAMINE RELEASE; IMMUNOREGULATION; MALE; MAST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFECT; REGULATORY MECHANISM;

ANIMALS; CELL SEPARATION; CYTOKINES; FEMALE; FLOW CYTOMETRY; IMMUNOBLOTTING; MALE; MAST CELLS; MICE; MICE, KNOCKOUT; PROTEIN-TYROSINE KINASES;

EID: 70449374880     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200838839     Document Type: Article

References (60)

1. Galli, S. J., Kalesnikoff, J., Grimbaldeston, M. A., Piliponsky, A. M., Williams, C. M. and Tsai, M., Mast cells as "tunable" effector and immunoregulatory cells: recent advances. Annu. Rev. Immunol. 2005. 23: 749-786.
2. Greenhawt, M. and Akin, C., Mastocytosis and allergy. Curr. Opin. Allergy Clin. Immunol. 2007. 7: 387-392.
3. Prussin, C. and Metcalfe, D. D., 5. IgE, mast cells, basophils, and eosinophils. J. Allergy Clin. Immunol. 2006. 117: S450-S456.
4. Valent, P., Schernthaner, G. H., Sperr, W. R., Fritsch, G., Agis, H., Willheim, M., Buhring, H. J. et al., Variable expression of activation-linked surface antigens on human mast cells in health and disease. Immunol. Rev. 2001. 179: 74-81.
5. Lee, D. M., Friend, D. S., Gurish, M. F., Benoist, C., Mathis, D. and Brenner, M. B., Mast cells: a cellular link between autoantibodies and inflammatory arthritis. Science 2002. 297: 1689-1692. (Pubitemid 35000781)
6. Steinman, L., Multiple sclerosis: a two-stage disease. Nat. Immunol. 2001. 2: 762-764.
7. Rijnierse, A., Koster, A. S., Nijkamp, F. P. and Kraneveld, A. D., Critical role for mast cells in the pathogenesis of 2,4-dinitrobenzene-induced murine colonic hypersensitivity reaction. J. Immunol. 2006. 176: 4375-4384. (Pubitemid 44264418)
8. Supajatura, V., Ushio, H., Nakao, A., Okumura, K., Ra, C. and Ogawa, H., Protective roles of mast cells against enterobacterial infection are mediated by Toll-like receptor 4. J. Immunol. 2001. 167: 2250-2256. (Pubitemid 32747537)
9. Metz, M., Piliponsky, A. M., Chen, C. C., Lammel, V., Abrink, M., Pejler, G., Tsai, M. and Galli, S. J., Mast cells can enhance resistance to snake and honeybee venoms. Science 2006. 313: 526-530. (Pubitemid 44148458)
10. Stassen, M., Hultner, L. and Schmitt, E., Classical and alternative pathways of mast cell activation. Crit. Rev. Immunol. 2002. 22: 115-140.
11. Marshall, J. S., Mast-cell responses to pathogens. Nat. Rev. Immunol. 2004. 4: 787-799.
12. Abramson, J. and Pecht, I., Regulation of the mast cell response to the type 1 Fc epsilon receptor. Immunol. Rev. 2007. 217: 231-254.
13. Gilfillan, A. M. and Tkaczyk, C., Integrated signalling pathways for mast-cell activation. Nat. Rev. Immunol. 2006. 6: 218-230.
14. Kambayashi, T. and Koretzky, G. A., Proximal signaling events in Fc epsilon RI-mediated mast cell activation. J. Allergy Clin. Immunol. 2007. 119: 544-552; quiz 553-1544
15. Galli, S. J., Nakae, S. and Tsai, M., Mast cells in the development of adaptive immune responses. Nat. Immunol. 2005. 6: 135-142.
16. Bischoff, S. C., Role of mast cells in allergic and non-allergic immune responses: comparison of human and murine data. Nat. Rev. Immunol. 2007. 7: 93-104.
17. Schmidt, U., Boucheron, N., Unger, B. and Ellmeier, W., The role of Tec family kinases in myeloid cells. Int. Arch. Allergy Immunol. 2004. 134: 65-78.
18. Felices, M., Falk, M., Kosaka, Y. and Berg, L. J., Tec kinases in T cell and mast cell signaling. Adv. Immunol. 2007. 93: 145-184.
19. Kawakami, Y., Yao, L., Miura, T., Tsukada, S., Witte, O. N. and Kawakami, T., Tyrosine phosphorylation and activation of Bruton tyrosine kinase upon Fc epsilon RI cross-linking. Mol. Cell. Biol. 1994. 14: 5108-5113.
20. Kawakami, Y., Yao, L., Tashiro, M., Gibson, S., Mills, G. B. and Kawakami, T., Activation and interaction with protein kinase C of a cytoplasmic tyrosine kinase, Itk/Tsk/Emt, on Fc epsilon RI cross-linking on mast cells. J. Immunol. 1995. 155: 3556-3562.
21. Hata, D., Kawakami, Y., Inagaki, N., Lantz, C. S., Kitamura, T., Khan, W. N., Maeda-Yamamoto, M. et al., Involvement of Bruton's tyrosine kinase in FcepsilonRI-dependent mast cell degranulation and cytokine production. J. Exp. Med. 1998. 187: 1235-1247.
22. Setoguchi, R., Kinashi, T., Sagara, H., Hirosawa, K. and Takatsu, K., Defective degranulation and calcium mobilization of bone-marrow derived mast cells from Xid and Btk-deficient mice. Immunol. Lett. 1998. 64: 109-118.
23. Kawakami, Y., Kitaura, J., Satterthwaite, A. B., Kato, R. M., Asai, K., Hartman, S. E., Maeda-Yamamoto, M. et al., Redundant and opposing functions of two tyrosine kinases, Btk and Lyn, in mast cell activation. J. Immunol. 2000. 165: 1210-1219. (Pubitemid 30604546)
24. Iwaki, S., Tkaczyk, C., Satterthwaite, A. B., Halcomb, K., Beaven, M. A., Metcalfe, D. D. and Gilfillan, A. M., Btk plays a crucial role in the amplification of Fc epsilonRI-mediated mast cell activation by kit. J. Biol. Chem. 2005. 280: 40261-40270.
25. Forssell, J., Sideras, P., Eriksson, C., Malm-Erjefalt, M., Rydell-Tormanen, K., Ericsson, P. O. and Erjefalt, J. S., Interleukin-2- inducible T cell kinase regulates mast cell degranulation and acute allergic responses. Am. J. Respir. Cell. Mol. Biol. 2005. 32: 511-520.
26. Iyer, A. S. and August, A., The Tec family kinase, IL-2-inducible T cell kinase, differentially controls mast cell responses. J. Immunol. 2008. 180: 7869-7877.
27. Schaeffer, E. M., Yap, G. S., Lewis, C. M., Czar, M. J., McVicar, D. W., Cheever, A. W., Sher, A. and Schwartzberg, P. L., Mutation of Tec family kinases alters T helper cell differentiation. Nat. Immunol. 2001. 2: 1183-1188.
28. Mueller, C. and August, A., Attenuation of immunological symptoms of allergic asthma in mice lacking the tyrosine kinase ITK. J. Immunol. 2003. 170: 5056-5063. (Pubitemid 36559524)
29. Ellmeier, W., Jung, S., Sunshine, M. J., Hatam, F., Xu, Y., Baltimore, D., Mano, H. and Littman, D. R., Severe B cell deficiency in mice lacking the tec kinase familymembers Tec and Btk. J. Exp. Med. 2000. 192: 1611-1624.
30. Hantschel, O., Rix, U., Schmidt, U., Burckstummer, T., Kneidinger, M., Schutze, G., Colinge, J. et al., The Btk tyrosine kinase is a major target of the Bcr-Abl inhibitor dasatinib. Proc. Natl. Acad. Sci. USA 2007. 104: 13283-13288.
31. Takata, M. and Kurosaki, T., A role for Bruton's tyrosine kinase in B cell antigen receptor-mediated activation of phospholipase C-gamma 2. J. Exp. Med. 1996. 184: 31-40.
32. Fluckiger, A. C., Li, Z., Kato, R. M., Wahl, M. I., Ochs, H. D., Longnecker, R., Kinet, J. P. et al., Btk/Tec kinases regulate sustained increases in intracellular Ca21 following B-cell receptor activation. EMBO J. 1998. 17: 1973-1985. (Pubitemid 28154527)
33. Liu, K. Q., Bunnell, S. C., Gurniak, C. B. and Berg, L. J., T cell receptor-initiated calcium release is uncoupled from capacitative calcium entry in Itk-deficient T cells. J. Exp. Med. 1998. 187: 1721-1727.
34. Schaeffer, E. M., Broussard, C., Debnath, J., Anderson, S., McVicar, D. W. and Schwartzberg, P. L., Tec family kinases modulate thresholds for thymocyte development and selection. J. Exp. Med. 2000. 192: 987-1000.
35. Irvin, B. J., Williams, B. L., Nilson, A. E., Maynor, H. O. and Abraham, R. T., Pleiotropic contributions of phospholipase C-gamma1 (PLC-gamma1) to T-cell antigen receptor-mediated signaling: reconstitution studies of a PLC-gamma1-deficient Jurkat T-cell line. Mol. Cell. Biol. 2000. 20: 9149-9161.
36. Watanabe, D., Hashimoto, S., Ishiai, M., Matsushita, M., Baba, Y., Kishimoto, T., Kurosaki, T. and Tsukada, S., Four tyrosine residues in phospholipase C-gamma 2, identified as Btk-dependent phosphorylation sites, are required for B cell antigen receptor-coupled calcium signaling. J. Biol. Chem. 2001. 276: 38595-38601.
37. Kawakami, Y., Miura, T., Bissonnette, R., Hata, D., Khan, W. N., Kitamura, T., Maeda-Yamamoto, M. et al., Bruton's tyrosine kinase regulates apoptosis and JNK/SAPK kinase activity. Proc. Natl. Acad. Sci. USA 1997. 94: 3938-3942.
38. Murphy, R. C. and Gijon, M. A., Biosynthesis and metabolism of leukotrienes. Biochem. J. 2007. 405: 379-395.
39. Hirasawa, N., Santini, F. and Beaven, M. A., Activation of the mitogen-activated protein kinase/cytosolic phospholipase A2 pathway in a rat mast cell line. Indications of different pathways for release of arachidonic acid and secretory granules. J. Immunol. 1995. 154: 5391-5402.
40. Kuehn, H. S., Swindle, E. J., Kim, M. S., Beaven, M. A., Metcalfe, D. D. and Gilfillan, A. M., The phosphoinositide 3-kinase-dependent activation of Btk is required for optimal eicosanoid production and generation of reactive oxygen species in antigen-stimulated mast cells. J. Immunol. 2008. 181: 7706-7712.
41. Gomez, G., Gonzalez-Espinosa, C., Odom, S., Baez, G., Cid, M. E., Ryan, J. J. and Rivera, J., Impaired FcepsilonRI-dependent gene expression and defective eicosanoid and cytokine production as a consequence of Fyn deficiency in mast cells. J. Immunol. 2005. 175: 7602-7610. (Pubitemid 41713460)
42. Xiao, W., Nishimoto, H., Hong, H., Kitaura, J., Nunomura, S., Maeda-Yamamoto, M., Kawakami, Y. et al., Positive and negative regulation of mast cell activation by Lyn via the FcepsilonRI. J. Immunol. 2005. 175: 6885-6892. (Pubitemid 41598934)
43. Parravicini, V., Gadina, M., Kovarova, M., Odom, S., Gonzalez-Espinosa, C., Furumoto, Y., Saitoh, S. et al., Fyn kinase initiates complementary signals required for IgE-dependent mast cell degranulation. Nat. Immunol. 2002. 3: 741-748.
44. Uckun, F. M., Waddick, K. G., Mahajan, S., Jun, X., Takata, M., Bolen, J. and Kurosaki, T., BTK as a mediator of radiation-induced apoptosis in DT-40 lymphoma B cells. Science 1996. 273: 1096-1100. (Pubitemid 26278163)
45. Vassilev, A., Ozer, Z., Navara, C., Mahajan, S. and Uckun, F. M., Bruton's tyrosine kinase as an inhibitor of the Fas/CD95 death-inducing signaling complex. J. Biol. Chem. 1999. 274: 1646-1656.
46. Kawakami, Y., Inagaki, N., Salek-Ardakani, S., Kitaura, J., Tanaka, H., Nagao, K., Kawakami, Y. et al., Regulation of dendritic cell maturation and function by Bruton's tyrosine kinase via IL-10 and Stat3. Proc. Natl. Acad. Sci. USA 2006. 103: 153-158.
47. Horwood, N. J., Mahon, T., McDaid, J. P., Campbell, J., Mano, H., Brennan, F. M., Webster, D. and Foxwell, B. M., Bruton's tyrosine kinase is required for lipopolysaccharide-induced tumor necrosis factor alpha production. J. Exp. Med. 2003. 197: 1603-1611.
48. Sekiya, F., Poulin, B., Kim, Y. J. and Rhee, S. G., Mechanism of tyrosine phosphorylation and activation of phospholipase C-gamma 1. Tyrosine 783 phosphorylation is not sufficient for lipase activation. J. Biol. Chem. 2004. 279: 32181-32190.
49. Blank, U. and Rivera, J., The ins and outs of IgE-dependent mast-cell exocytosis. Trends Immunol. 2004. 25: 266-273. (Pubitemid 38501673)
50. Vig, M. and Kinet, J. P., Calcium signaling in immune cells. Nat. Immunol. 2009. 10: 21-27.
51. Boudreau, R. T., Hoskin, D. W. and Lin, T. J., Phosphatase inhibition potentiates IL-6 production by mast cells in response to FcepsilonRI-mediated activation: involvement of p38 MAPK. J. Leukoc. Biol. 2004. 76: 1075-1081.
52. Stassen, M., Klein, M., Becker, M., Bopp, T., Neudorfl, C., Richter, C., Heib, V. et al., p38 MAP kinase drives the expression of mast cell-derived IL-9 via activation of the transcription factor GATA-1. Mol. Immunol. 2007. 44: 926-933.
53. Turner, H. and Cantrell, D. A., Distinct Ras effector pathways are involved in Fc epsilon R1 regulation of the transcriptional activity of Elk-1 and NFAT in mast cells. J. Exp. Med. 1997. 185: 43-53.
54. Ishizuka, T., Terada, N., Gerwins, P., Hamelmann, E., Oshiba, A., Fanger, G. R., Johnson, G. L. and Gelfand, E. W., Mast cell tumor necrosis factor alpha production is regulated by MEK kinases. Proc. Natl. Acad. Sci. USA 1997. 94: 6358-6363.
55. Solymar, D. C., Agarwal, S., Bassing, C. H., Alt, F. W. and Rao, A., A 3' enhancer in the IL-4 gene regulates cytokine production by Th2 cells and mast cells. Immunity 2002. 17: 41-50. (Pubitemid 34874617)
56. Gross, B., Borggrefe, T., Wabl, M., Sivalenka, R. R., Bennett, M., Rossi, A. B. and Jessberger, R., SWAP-70-deficient mast cells are impaired in development and IgE-mediated degranulation. Eur. J. Immunol. 2002. 32: 1121-1128.
57. Sivalenka, R. R., Sinha, M. and Jessberger, R., SWAP-70 regulates mast cell FcepsilonRI-mediated signaling and anaphylaxis. Eur. J. Immunol. 2008. 38: 841-854.
58. Friedman, A. and Perrimon, N., A functional RNAi screen for regulators of receptor tyrosine kinase and ERK signalling. Nature 2006. 444: 230-234. (Pubitemid 44722065)
59. Gomez-Rodriguez, J., Readinger, J. A., Viorritto, I. C., Mueller, K. L., Houghtling, R. A. and Schwartzberg, P. L., Tec kinases, actin, and cell adhesion. Immunol. Rev. 2007. 218: 45-64.
60. Khan, W. N., Alt, F. W., Gerstein, R. M., Malynn, B. A., Larsson, I., Rathbun, G., Davidson, L. et al., Defective B cell development and function in Btk-deficient mice. Immunity 1995. 3: 283-299.