This Article Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Kawakami, Y Articles by Kawakami, T Search for Related Content PubMed PubMed Citation Articles by Kawakami, Y Articles by Kawakami, T

Tyrosine phosphorylation and activation of Bruton tyrosine kinase upon Fc epsilon RI cross-linking.

Division of Immunobiology, La Jolla Institute for Allergy and Immunology, California 92037.

ABSTRACT

Tyrosine phosphorylation of several cellular proteins is one of the earliest signaling events induced by cross-linking of the high-affinity receptor for immunoglobulin E (Fc epsilon RI) on mast cells or basophils. Tyrosine kinases activated during this process include the Src family kinases, Lyn, c-Yes, and c-Src, and members of another subfamily, Syk and PTK72 (identical or highly related to Syk). Recently, some of us described two novel tyrosine kinases, Emb and Emt, whose expression was limited to subsets of hematopoietic cells, including mast cells. Emb turned out to be identical to Btk, a gene product defective in human X-linked agammaglobulinemia and in X-linked immunodeficient (xid) mice. Here we report that Fc epsilon RI cross-linking induced rapid phosphorylation on tyrosine, serine, and threonine residues and activation of Btk in mouse bone marrow-derived mast cells. A small fraction of Btk translocated from the cytosol to the membrane compartment following receptor cross-linking. Tyrosine phosphorylation of Btk was not induced by either a Ca2+ ionophore (A23187), phorbol 12-myristate 13-acetate, or a combination of the two reagents. Co-immunoprecipitation between Btk and receptor subunit beta or gamma was not detected. The data collectively suggest that Btk is not associated with Fc epsilon but that its activation takes place prior to protein kinase C activation and plays a novel role in the Fc epsilon RI signaling pathway.

This article has been cited by other articles:

• Kneidinger, M., Schmidt, U., Rix, U., Gleixner, K. V., Vales, A., Baumgartner, C., Lupinek, C., Weghofer, M., Bennett, K. L., Herrmann, H., Schebesta, A., Thomas, W. R., Vrtala, S., Valenta, R., Lee, F. Y., Ellmeier, W., Superti-Furga, G., Valent, P. (2008). The effects of dasatinib on IgE receptor-dependent activation and histamine release in human basophils. Blood 111: 3097-3107 [Abstract] [Full Text]  
• Yaghini, F. A., Li, F., Malik, K. U. (2007). Expression and Mechanism of Spleen Tyrosine Kinase Activation by Angiotensin II and Its Implication in Protein Synthesis in Rat Vascular Smooth Muscle Cells. J. Biol. Chem. 282: 16878-16890 [Abstract] [Full Text]  
• Yu, L., Mohamed, A. J., Vargas, L., Berglof, A., Finn, G., Lu, K. P., Smith, C. I. E. (2006). Regulation of Bruton Tyrosine Kinase by the Peptidylprolyl Isomerase Pin1. J. Biol. Chem. 281: 18201-18207 [Abstract] [Full Text]  
• Iwaki, S., Tkaczyk, C., Satterthwaite, A. B., Halcomb, K., Beaven, M. A., Metcalfe, D. D., Gilfillan, A. M. (2005). Btk Plays a Crucial Role in the Amplification of Fc{epsilon}RI-mediated Mast Cell Activation by Kit. J. Biol. Chem. 280: 40261-40270 [Abstract] [Full Text]  
• Kitaura, J., Eto, K., Kinoshita, T., Kawakami, Y., Leitges, M., Lowell, C. A., Kawakami, T. (2005). Regulation of Highly Cytokinergic IgE-Induced Mast Cell Adhesion by Src, Syk, Tec, and Protein Kinase C Family Kinases. J. Immunol. 174: 4495-4504 [Abstract] [Full Text]  
• Lesourne, R., Fridman, W. H., Daeron, M. (2005). Dynamic Interactions of Fc{gamma} Receptor IIB with Filamin-Bound SHIP1 Amplify Filamentous Actin-Dependent Negative Regulation of Fc{epsilon} Receptor I Signaling. J. Immunol. 174: 1365-1373 [Abstract] [Full Text]  
• Kawakami, Y., Nishimoto, H., Kitaura, J., Maeda-Yamamoto, M., Kato, R. M., Littman, D. R., Rawlings, D. J., Kawakami, T. (2004). Protein Kinase C {beta}II Regulates Akt Phosphorylation on Ser-473 in a Cell Type- and Stimulus-specific Fashion. J. Biol. Chem. 279: 47720-47725 [Abstract] [Full Text]  
• Maeda-Yamamoto, M., Inagaki, N., Kitaura, J., Chikumoto, T., Kawahara, H., Kawakami, Y., Sano, M., Miyase, T., Tachibana, H., Nagai, H., Kawakami, T. (2004). O-Methylated Catechins from Tea Leaves Inhibit Multiple Protein Kinases in Mast Cells. J. Immunol. 172: 4486-4492 [Abstract] [Full Text]  
• Kawakami, Y., Kitaura, J., Yao, L., McHenry, R. W., Kawakami, Y., Newton, A. C., Kang, S., Kato, R. M., Leitges, M., Rawlings, D. J., Kawakami, T. (2003). A Ras activation pathway dependent on Syk phosphorylation of protein kinase C. Proc. Natl. Acad. Sci. USA 100: 9470-9475 [Abstract] [Full Text]  
• Cooper, M. D., Lanier, L. L., Conley, M. E., Puck, J. M. (2003). Immunodeficiency Disorders. ASH Education Book 2003: 314-330 [Abstract] [Full Text]  
• Laederach, A., Cradic, K. W., Brazin, K. N., Zamoon, J., Fulton, D. B., Huang, X.-Y., Andreotti, A. H. (2002). Competing modes of self-association in the regulatory domains of Bruton's tyrosine kinase: Intramolecular contact versus asymmetric homodimerization. Protein Sci. 11: 36-57 [Abstract] [Full Text]  
• Lavens-Phillips, S. E., MacGlashan, D. W. Jr. (2000). The Tyrosine Kinases p53/56lyn and p72syk Are Differentially Expressed at the Protein Level but Not at the Messenger RNA Level in Nonreleasing Human Basophils. Am. J. Respir. Cell Mol. Bio. 23: 566-571 [Abstract] [Full Text]  
• Kikuchi, Y., Hirano, M., Seto, M., Takatsu, K. (2000). Identification and characterization of a molecule, BAM11, that associates with the pleckstrin homology domain of mouse Btk. Int Immunol 12: 1397-1408 [Abstract] [Full Text]  
• Shan, X., Czar, M. J., Bunnell, S. C., Liu, P., Liu, Y., Schwartzberg, P. L., Wange, R. L. (2000). Deficiency of PTEN in Jurkat T Cells Causes Constitutive Localization of Itk to the Plasma Membrane and Hyperresponsiveness to CD3 Stimulation. Mol. Cell. Biol. 20: 6945-6957 [Abstract] [Full Text]  
• Kitaura, J., Asai, K., Maeda-Yamamoto, M., Kawakami, Y., Kikkawa, U., Kawakami, T. (2000). Akt-dependent Cytokine Production in Mast Cells. J. Exp. Med. 192: 729-740 [Abstract] [Full Text]  
• Kawakami, Y., Kitaura, J., Hartman, S. E., Lowell, C. A., Siraganian, R. P., Kawakami, T. (2000). Regulation of protein kinase Cbeta I by two protein-tyrosine kinases, Btk and Syk. Proc. Natl. Acad. Sci. USA 10.1073/pnas.120175097v1 [Abstract] [Full Text]  
• Bunnell, S. C., Diehn, M., Yaffe, M. B., Findell, P. R., Cantley, L. C., Berg, L. J. (2000). Biochemical Interactions Integrating Itk with the T Cell Receptor-initiated Signaling Cascade. J. Biol. Chem. 275: 2219-2230 [Abstract] [Full Text]  
• Rohrer, J., Conley, M. E. (1999). Correction of X-Linked Immunodeficient Mice by Competitive Reconstitution With Limiting Numbers of Normal Bone Marrow Cells. Blood 94: 3358-3365 [Abstract] [Full Text]  
• Shan, X., Wange, R. L. (1999). Itk/Emt/Tsk Activation in Response to CD3 Cross-linking in Jurkat T Cells Requires ZAP-70 and Lat and Is Independent of Membrane Recruitment. J. Biol. Chem. 274: 29323-29330 [Abstract] [Full Text]  
• Yao, L., Janmey, P., Frigeri, L. G., Han, W., Fujita, J., Kawakami, Y., Apgar, J. R., Kawakami, T. (1999). Pleckstrin Homology Domains Interact with Filamentous Actin. J. Biol. Chem. 274: 19752-19761 [Abstract] [Full Text]  
• Novina, C. D., Kumar, S., Bajpai, U., Cheriyath, V., Zhang, K., Pillai, S., Wortis, H. H., Roy, A. L. (1999). Regulation of Nuclear Localization and Transcriptional Activity of TFII-I by Bruton's Tyrosine Kinase. Mol. Cell. Biol. 19: 5014-5024 [Abstract] [Full Text]  
• Baba, Y., Nonoyama, S., Matsushita, M., Yamadori, T., Hashimoto, S., Imai, K., Arai, S., Kunikata, T., Kurimoto, M., Kurosaki, T., Ochs, H. D., Yata, J.-i., Kishimoto, T., Tsukada, S. (1999). Involvement of Wiskott-Aldrich Syndrome Protein in B-Cell Cytoplasmic Tyrosine Kinase Pathway. Blood 93: 2003-2012 [Abstract] [Full Text]  
• Kawakami, Y., Hartman, S. E., Kinoshita, E., Suzuki, H., Kitaura, J., Yao, L., Inagaki, N., Franco, A., Hata, D., Maeda-Yamamoto, M., Fukamachi, H., Nagai, H., Kawakami, T. (1999). Terreic acid, a quinone epoxide inhibitor of Bruton's tyrosine kinase. Proc. Natl. Acad. Sci. USA 96: 2227-2232 [Abstract] [Full Text]  
• Ishizuka, T., Chayama, K., Takeda, K., Hamelmann, E., Terada, N., Keller, G. M., Johnson, G. L., Gelfand, E. W. (1999). Mitogen-Activated Protein Kinase Activation Through Fc{epsilon} Receptor I and Stem Cell Factor Receptor Is Differentially Regulated by Phosphatidylinositol 3-Kinase and Calcineurin in Mouse Bone Marrow-Derived Mast Cells. J. Immunol. 162: 2087-2094 [Abstract] [Full Text]  
• Debnath, J., Chamorro, M., Czar, M. J., Schaeffer, E. M., Lenardo, M. J., Varmus, H. E., Schwartzberg, P. L. (1999). rlk/TXK Encodes Two Forms of a Novel Cysteine String Tyrosine Kinase Activated by Src Family Kinases. Mol. Cell. Biol. 19: 1498-1507 [Abstract] [Full Text]  
• Suzuki, H., Terauchi, Y., Fujiwara, M., Aizawa, S., Yazaki, Y., Kadowaki, T., Koyasu, S. (1999). Xid-Like Immunodeficiency in Mice with Disruption of the p85 Subunit of Phosphoinositide 3-Kinase. Science 283: 390-392 [Abstract] [Full Text]  
• Miller, S. C., Furniss, M. J. (1998). Bruton's Tyrosine Kinase Activity and Inositol 1,4,5-Trisphosphate Production Are Not Altered in DT40 Lymphoma B Cells Exposed to Power Line Frequency Magnetic Fields. J. Biol. Chem. 273: 32618-32626 [Abstract] [Full Text]  
• Huber, M., Helgason, C. D., Damen, J. E., Liu, L., Humphries, R. K., Krystal, G. (1998). The src homology 2-containing inositol phosphatase (SHIP) is the gatekeeper of mast cell degranulation. Proc. Natl. Acad. Sci. USA 95: 11330-11335 [Abstract] [Full Text]  
• Kawakami, Y., Hartman, S. E., Holland, P. M., Cooper, J. A., Kawakami, T. (1998). Multiple Signaling Pathways for the Activation of JNK in Mast Cells: Involvement of Bruton's Tyrosine Kinase, Protein Kinase C, and JNK Kinases, SEK1 and MKK7. J. Immunol. 161: 1795-1802 [Abstract] [Full Text]  
• Deng, J., Kawakami, Y., Hartman, S. E., Satoh, T., Kawakami, T. (1998). Involvement of Ras in Bruton's Tyrosine Kinase-mediated JNK Activation. J. Biol. Chem. 273: 16787-16791 [Abstract] [Full Text]  
• Hata, D., Kitaura, J., Hartman, S. E., Kawakami, Y., Yokota, T., Kawakami, T. (1998). Bruton's Tyrosine Kinase-mediated Interleukin-2 Gene Activation in Mast Cells. DEPENDENCE ON THE c-Jun N-TERMINAL KINASE ACTIVATION PATHWAY. J. Biol. Chem. 273: 10979-10987 [Abstract] [Full Text]  
• Hata, D., Kawakami, Y., Inagaki, N., Lantz, C. S., Kitamura, T., Khan, W. N., Maeda-Yamamoto, M., Miura, T., Han, W., Hartman, S. E., Yao, L., Nagai, H., Goldfeld, A. E., Alt, F. W., Galli, S. J., Witte, O. N., Kawakami, T. (1998). Involvement of Bruton's Tyrosine Kinase in Fcepsilon RI-dependent Mast Cell Degranulation and Cytokine Production. J. Exp. Med. 187: 1235-1247 [Abstract] [Full Text]  
• Yamashita, Y., Watanabe, S., Miyazato, A., Ohya, K.-i., Ikeda, U., Shimada, K., Komatsu, N., Hatake, K., Miura, Y., Ozawa, K., Mano, H. (1998). Tec and Jak2 Kinases Cooperate to Mediate Cytokine-Driven Activation of c-fos Transcription. Blood 91: 1496-1507 [Abstract] [Full Text]  
• Csonga, R., Prieschl, E. E., Jaksche, D., Novotny, V., Baumruker, T. (1998). Common and Distinct Signaling Pathways Mediate the Induction of TNF-{alpha} and IL-5 in IgE Plus Antigen-Stimulated Mast Cells. J. Immunol. 160: 273-283 [Abstract] [Full Text]  
• Rohrer, J., Ellen Conley, M. (1998). Transcriptional Regulatory Elements Within the First Intron of Bruton's Tyrosine Kinase. Blood 91: 214-221 [Abstract] [Full Text]  
• Okazaki, H., Zhang, J., Hamawy, M. M., Siraganian, R. P. (1997). Activation of Protein-tyrosine Kinase Pyk2 Is Downstream of Syk in Fcepsilon RI Signaling. J. Biol. Chem. 272: 32443-32447 [Abstract] [Full Text]  
• Weil, D., Power, M.-A., Smith, S. I., Leung Li, C. (1997). Predominant Expression of Murine Bmx Tyrosine Kinase in the Granulo-Monocytic Lineage. Blood 90: 4332-4340 [Abstract] [Full Text]  
• Saharinen, P., Ekman, N., Sarvas, K., Parker, P., Alitalo, K., Silvennoinen, O. (1997). The Bmx Tyrosine Kinase Induces Activation of the Stat Signaling Pathway, Which Is Specifically Inhibited by Protein Kinase Cdelta. Blood 90: 4341-4353 [Abstract] [Full Text]  
• Satterthwaite, A. B., Cheroutre, H., Khan, W. N., Sideras, P., Witte, O. N. (1997). Btk dosage determines sensitivity to B cell antigen receptor cross-linking. Proc. Natl. Acad. Sci. USA 94: 13152-13157 [Abstract] [Full Text]  
• Fleming, T. J., Donnadieu, E., Song, C. H., Laethem, F. V., Galli, S. J., Kinet, J.-P. (1997). Negative Regulation of Fcepsilon RI-mediated Degranulation by CD81. J. Exp. Med. 186: 1307-1314 [Abstract] [Full Text]  
• August, A., Sadra, A., Dupont, B., Hanafusa, H. (1997). Src-induced activation of inducible T cell kinase (ITK) requires phosphatidylinositol 3-kinase activity and the Pleckstrin homology domain of inducible T cell kinase. Proc. Natl. Acad. Sci. USA 94: 11227-11232 [Abstract] [Full Text]  
• Wahl, M. I., Fluckiger, A.-C., Kato, R. M., Park, H., Witte, O. N., Rawlings, D. J. (1997). Phosphorylation of two regulatory tyrosine residues in the activation of Bruton's tyrosine kinase via alternative receptors. Proc. Natl. Acad. Sci. USA 94: 11526-11533 [Abstract] [Full Text]  
• Heyeck, S. D., Wilcox, H. M., Bunnell, S. C., Berg, L. J. (1997). Lck Phosphorylates the Activation Loop Tyrosine of the Itk Kinase Domain and Activates Itk Kinase Activity. J. Biol. Chem. 272: 25401-25408 [Abstract] [Full Text]  
• Wong, W. S. F., Koh, D. S. K., Koh, A. H. M., Ting, W. L., Wong, P. T. H. (1997). Effects of Tyrosine Kinase Inhibitors on Antigen Challenge of Guinea Pig Lung In Vitro. J. Pharmacol. Exp. Ther. 283: 131-137 [Abstract] [Full Text]  
• Ishizuka, T., Terada, N., Gerwins, P., Hamelmann, E., Oshiba, A., Fanger, G. R., Johnson, G. L., Gelfand, E. W. (1997). Mast cell tumor necrosis factor alpha  production is regulated by MEK kinases. Proc. Natl. Acad. Sci. USA 94: 6358-6363 [Abstract] [Full Text]  
• Yao, L., Suzuki, H., Ozawa, K., Deng, J., Lehel, C., Fukamachi, H., Anderson, W. B., Kawakami, Y., Kawakami, T. (1997). Interactions between Protein Kinase C and Pleckstrin Homology Domains. INHIBITION BY PHOSPHATIDYLINOSITOL 4,5-BISPHOSPHATE AND PHORBOL 12-MYRISTATE 13-ACETATE. J. Biol. Chem. 272: 13033-13039 [Abstract] [Full Text]  
• Kawakami, Y., Miura, T., Bissonnette, R., Hata, D., Khan, W. N., Kitamura, T., Maeda-Yamamoto, M., Hartman, S. E., Yao, L., Alt, F. W., Kawakami, T. (1997). Bruton's tyrosine kinase regulates apoptosis and JNK/SAPK kinase activity. Proc. Natl. Acad. Sci. USA 94: 3938-3942 [Abstract] [Full Text]  
• Yel, L., Minegishi, Y., Coustan-Smith, E., Buckley, R. H., Trubel, H., Pachman, L. M., Kitchingman, G. R., Campana, D., Rohrer, J., Conley, M. E. (1996). Mutations in the Mu Heavy-Chain Gene in Patients with Agammaglobulinemia. NEJM 335: 1486-1493 [Abstract] [Full Text]  
• Song, J. S., Gomez, J., Stancato, L. F., Rivera, J. (1996). Association of a p95 Vav-containing Signaling Complex with the Fcepsilon RI gamma Chain in the RBL-2H3 Mast Cell Line. EVIDENCE FOR A CONSTITUTIVE IN VIVO ASSOCIATION OF Vav WITH Grb2, Raf-1, AND ERK2 IN AN ACTIVE COMPLEX. J. Biol. Chem. 271: 26962-26970 [Abstract] [Full Text]  
• Bunnell, S. C., Henry, P. A., Kolluri, R., Kirchhausen, T., Rickles, R. J., Berg, L. J. (1996). Identification of Itk/Tsk Src Homology 3Domain Ligands. J. Biol. Chem. 271: 25646-25656 [Abstract] [Full Text]  
• Ishizuka, T., Oshiba, A., Sakata, N., Terada, N., Johnson, G. L., Gelfand, E. W. (1996). Aggregation of the Fcepsilon RI on Mast Cells Stimulates c-Jun Amino-terminal Kinase Activity. A RESPONSE INHIBITED BY WORTMANNIN. J. Biol. Chem. 271: 12762-12766 [Abstract] [Full Text]  
• Gibson, S., August, A., Branch, D., Dupont, B., Mills, G. B. (1996). Functional LCK Is Required for Optimal CD28-mediated Activation of the TEC Family Tyrosine Kinase EMT/ITK. J. Biol. Chem. 271: 7079-7083 [Abstract] [Full Text]  
• Swieter, M., Berenstein, E. H., Swaim, W. D., Siraganian, R. P. (1995). Aggregation of IgE Receptors in Rat Basophilic Leukemia 2H3 Cells Induces Tyrosine Phosphorylation of the Cytosolic Protein-tyrosine Phosphatase HePTP. J. Biol. Chem. 270: 21902-21906 [Abstract] [Full Text]  
• Yang, W., Malek, S. N., Desiderio, S. (1995). An SH3-binding Site Conserved in Bruton's Tyrosine Kinase and Related Tyrosine Kinases Mediates Specific Protein Interactions in Vitro and in Vivo. J. Biol. Chem. 270: 20832-20840 [Abstract] [Full Text]  
• Hamawy, M. M., Minoguchi, K., Swaim, W. D., Mergenhagen, S. E., Siraganian, R. P. (1995). A 77-kDa Protein Associates with pp125[IMAGE] in Mast Cells and Becomes Tyrosine-phosphorylated by High Affinity IgE Receptor Aggregation. J. Biol. Chem. 270: 12305-12309 [Abstract] [Full Text]  
• Turner, H., Reif, K., Rivera, J., Cantrell, D. A. (1995). Regulation of the Adapter Molecule Grb2 by the Fc[IMAGE]R1 in the Mast Cell Line RBL2H3. J. Biol. Chem. 270: 9500-9506 [Abstract] [Full Text]  
• Jui, H.-Y., Tseng, R.-J., Wen, X., Fang, H.-I, Huang, L.-M., Chen, K.-Y., Kung, H.-J., Ann, D. K., Shih, H.-M. (2000). Protein-tyrosine Phosphatase D1, a Potential Regulator and Effector for Tec Family Kinases. J. Biol. Chem. 275: 41124-41132 [Abstract] [Full Text]  
• Egloff, A. M., Desiderio, S. (2001). Identification of Phosphorylation Sites for Bruton's Tyrosine Kinase within the Transcriptional Regulator BAP/TFII-I. J. Biol. Chem. 276: 27806-27815 [Abstract] [Full Text]  
• Kawakami, Y., Kitaura, J., Hartman, S. E., Lowell, C. A., Siraganian, R. P., Kawakami, T. (2000). Regulation of protein kinase Cbeta I by two protein-tyrosine kinases, Btk and Syk. Proc. Natl. Acad. Sci. USA 97: 7423-7428 [Abstract] [Full Text]