Requirement of Lyn and Syk tyrosine kinases for the prevention of apoptosis by cytokines in human eosinophils

doi:10.1084/jem.183.4.1407

This Article

	Full Text (PDF, 1448K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JEM
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Yousefi, S.
	Articles by Simon, H. U.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Yousefi, S.
	Articles by Simon, H. U.


Social Bookmarking

	What's this?

ARTICLES

Requirement of Lyn and Syk tyrosine kinases for the prevention of apoptosis by cytokines in human eosinophils

S Yousefi, DC Hoessli, K Blaser, GB Mills and HU Simon
Swiss Institute of Allergy and Asthma Research, University of Zurich, Switzerland.

In allergic diseases, the cytokines interleukin (IL)5 and granulocyte/macrophage colony-stimulating factor (GM-CSF) are upregulated and have been proposed to cause blood and tissue eosinophilia by inhibition of eosinophil apoptosis. We demonstrate herein, in freshly isolated human eosinophils, that the IL-3/IL-5/GM- CSF receptor beta subunit interacts with cytoplasmic tyrosine kinases to induce phosphorylation of several cellular substrates, including the beta subunit itself. The Lyn and Syk intracellular tyrosine kinases constitutively associate at a low level with the IL-3/IL-5/GM-CSF receptor beta subunit in human eosinophils. Stimulation with GM-CSF or IL-5 results in a rapid and transient increase in the amount of Lyn and Syk associated with the IL-3/IL-5/GM-CSF receptor beta subunit. Lyn is required for optimal tyrosine phosphorylation and activation of Syk. In contrast, Syk is not required for optimal tyrosine phosphorylation and activation of Lyn. These data suggest that Lyn is proximal to Syk in a tyrosine kinase cascade that transduces IL-3, IL-5, or GM-CSF signals. Compatible with this model, both Lyn and Syk are essential for the activation of the antiapoptotic pathway(s) induced through the IL-3/IL- 5/GM-CSF receptor beta subunit in human eosinophils.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Carlens, J., Wahl, B., Ballmaier, M., Bulfone-Paus, S., Forster, R., Pabst, O. (2009). Common {gamma}-Chain-Dependent Signals Confer Selective Survival of Eosinophils in the Murine Small Intestine. J. Immunol. 183: 5600-5607 [Abstract] [Full Text]
Ennaciri, J., Girard, D. (2009). IL-4R{alpha}, a New Member that Associates with Syk Kinase: Implication in IL-4-Induced Human Neutrophil Functions. J. Immunol. 183: 5261-5269 [Abstract] [Full Text]
Didichenko, S. A., Spiegl, N., Brunner, T., Dahinden, C. A. (2008). IL-3 induces a Pim1-dependent antiapoptotic pathway in primary human basophils. Blood 112: 3949-3958 [Abstract] [Full Text]
Ulanova, M., Asfaha, S., Stenton, G., Lint, A., Gilbertson, D., Schreiber, A., Befus, D. (2007). Involvement of Syk protein tyrosine kinase in LPS-induced responses in macrophages. Innate Immunity 13: 117-125 [Abstract]
von Gunten, S., Yousefi, S., Seitz, M., Jakob, S. M., Schaffner, T., Seger, R., Takala, J., Villiger, P. M., Simon, H.-U. (2005). Siglec-9 transduces apoptotic and nonapoptotic death signals into neutrophils depending on the proinflammatory cytokine environment. Blood 106: 1423-1431 [Abstract] [Full Text]
Moroni, M., Soldatenkov, V., Zhang, L., Zhang, Y., Stoica, G., Gehan, E., Rashidi, B., Singh, B., Ozdemirli, M., Mueller, S. C. (2004). Progressive Loss of Syk and Abnormal Proliferation in Breast Cancer Cells. Cancer Res. 64: 7346-7354 [Abstract] [Full Text]
Dai, Y., Rahmani, M., Corey, S. J., Dent, P., Grant, S. (2004). A Bcr/Abl-independent, Lyn-dependent Form of Imatinib Mesylate (STI-571) Resistance Is Associated with Altered Expression of Bcl-2. J. Biol. Chem. 279: 34227-34239 [Abstract] [Full Text]
Berro, A. I., Perry, G. A., Agrawal, D. K. (2004). Increased Expression and Activation of CD30 Induce Apoptosis in Human Blood Eosinophils. J. Immunol. 173: 2174-2183 [Abstract] [Full Text]
Altznauer, F., Conus, S., Cavalli, A., Folkers, G., Simon, H.-U. (2004). Calpain-1 Regulates Bax and Subsequent Smac-dependent Caspase-3 Activation in Neutrophil Apoptosis. J. Biol. Chem. 279: 5947-5957 [Abstract] [Full Text]
Shivakrupa, R., Radha, V., Sudhakar, Ch., Swarup, G. (2003). Physical and Functional Interaction between Hck Tyrosine Kinase and Guanine Nucleotide Exchange Factor C3G Results in Apoptosis, Which Is Independent of C3G Catalytic Domain. J. Biol. Chem. 278: 52188-52194 [Abstract] [Full Text]
BAUMANN, R., CASAULTA, C., SIMON, D., CONUS, S., YOUSEFI, S., SIMON, H.-U. (2003). Macrophage migration inhibitory factor delays apoptosis in neutrophils by inhibiting the mitochondria-dependent death pathway. FASEB J. 17: 2221-2230 [Abstract] [Full Text]
Cen, O., Gorska, M. M., Stafford, S. J., Sur, S., Alam, R. (2003). Identification of UNC119 as a Novel Activator of SRC-type Tyrosine Kinases. J. Biol. Chem. 278: 8837-8845 [Abstract] [Full Text]
Stenton, G. R., Ulanova, M., Dery, R. E., Merani, S., Kim, M.-K., Gilchrist, M., Puttagunta, L., Musat-Marcu, S., James, D., Schreiber, A. D., Befus, A. D. (2002). Inhibition of Allergic Inflammation in the Airways Using Aerosolized Antisense to Syk Kinase. J. Immunol. 169: 1028-1036 [Abstract] [Full Text]
Zangrilli, J. G. (2002). Regulation of Eosinophil Viability by Cytokines. Am. J. Respir. Cell Mol. Bio. 26: 388-390 [Full Text]
Ishikawa, H., Tsuyama, N., Abroun, S., Liu, S., Li, F.-J., Taniguchi, O., Kawano, M. M. (2002). Requirements of src family kinase activity associated with CD45 for myeloma cell proliferation by interleukin-6. Blood 99: 2172-2178 [Abstract] [Full Text]
Stafford, S., Lowell, C., Sur, S., Alam, R. (2002). Lyn Tyrosine Kinase Is Important for IL-5-Stimulated Eosinophil Differentiation. J. Immunol. 168: 1978-1983 [Abstract] [Full Text]
Bulanova, E., Budagian, V., Pohl, T., Krause, H., Durkop, H., Paus, R., Bulfone-Paus, S. (2001). The IL-15R{alpha} Chain Signals Through Association with Syk in Human B Cells. J. Immunol. 167: 6292-6302 [Abstract] [Full Text]
Horikawa, K., Kaku, H., Nakajima, H., Davey, H. W., Henninghausen, L., Iwamoto, I., Yasue, T., Kariyone, A., Takatsu, K. (2001). Essential Role of Stat5 for IL-5-Dependent IgH Switch Recombination in Mouse B Cells. J. Immunol. 167: 5018-5026 [Abstract] [Full Text]
Alam, R., Gorska, M. (2001). Genomic Microarrays . Arraying Order in Biological Chaos?. Am. J. Respir. Cell Mol. Bio. 25: 405-408 [Full Text]
Temple, R., Allen, E., Fordham, J., Phipps, S., Schneider, H.-C., Lindauer, K., Hayes, I., Lockey, J., Pollock, K., Jupp, R. (2001). Microarray Analysis of Eosinophils Reveals a Number of Candidate Survival and Apoptosis Genes. Am. J. Respir. Cell Mol. Bio. 25: 425-433 [Abstract] [Full Text]
Hashimoto, S.-i., Komuro, I., Yamada, M., Akagawa, K. S. (2001). IL-10 Inhibits Granulocyte-Macrophage Colony-Stimulating Factor-Dependent Human Monocyte Survival at the Early Stage of the Culture and Inhibits the Generation of Macrophages. J. Immunol. 167: 3619-3625 [Abstract] [Full Text]
Hall, D. J., Cui, J., Bates, M. E., Stout, B. A., Koenderman, L., Coffer, P. J., Bertics, P. J. (2001). Transduction of a dominant-negative H-Ras into human eosinophils attenuates extracellular signal-regulated kinase activation and interleukin-5-mediated cell viability. Blood 98: 2014-2021 [Abstract] [Full Text]
Dewson, G., Cohen, G. M., Wardlaw, A. J. (2001). Interleukin-5 inhibits translocation of Bax to the mitochondria, cytochrome c release, and activation of caspases in human eosinophils. Blood 98: 2239-2247 [Abstract] [Full Text]
Talapatra, S., Thompson, C. B. (2001). Growth Factor Signaling in Cell Survival: Implications for Cancer Treatment. J. Pharmacol. Exp. Ther. 298: 873-878 [Abstract] [Full Text]
Grishin, A. V., Azhipa, O., Semenov, I., Corey, S. J. (2001). Interaction between growth arrest-DNA damage protein 34 and Src kinase Lyn negatively regulates genotoxic apoptosis. Proc. Natl. Acad. Sci. USA 10.1073/pnas.191130798v1 [Abstract] [Full Text]
Bates, R. C., Edwards, N. S., Burns, G. F., Fisher, D. E. (2001). A CD44 Survival Pathway Triggers Chemoresistance via Lyn Kinase and Phosphoinositide 3-Kinase/Akt in Colon Carcinoma Cells. Cancer Res. 61: 5275-5283 [Abstract] [Full Text]
Yamada, T., Fujieda, S., Yanagi, S., Yamamura, H., Inatome, R., Yamamoto, H., Igawa, H., Saito, H. (2001). IL-1 Induced Chemokine Production Through the Association of Syk with TNF Receptor-Associated Factor-6 in Nasal Fibroblast Lines. J. Immunol. 167: 283-288 [Abstract] [Full Text]
Yousefi, S., Cooper, P. R, Potter, S. L, Mueck, B., Jarai, G. (2001). Cloning and expression analysis of a novel G-protein-coupled receptor selectively expressed on granulocytes. J. Leukoc. Biol. 69: 1045-1052 [Abstract] [Full Text]
Saita, N., Yamanaka, T., Kohrogi, H., Ando, M., Hirashima, M. (2001). Apoptotic response of eosinophils in chronic eosinophilic pneumonia. Eur Respir J 17: 190-194 [Abstract] [Full Text]
Yamada, T., Fujieda, S., Yanagi, S., Yamamura, H., Inatome, R., Sunaga, H., Saito, H. (2001). Protein-Tyrosine Kinase Syk Expressed in Human Nasal Fibroblasts and Its Effect on RANTES Production. J. Immunol. 166: 538-543 [Abstract] [Full Text]
Savoie, A., Lavastre, V., Pelletier, M., Hajto, T., Hostanska, K., Girard, D. (2000). Activation of human neutrophils by the plant lectin Viscum album agglutinin-I: modulation of de novo protein synthesis and evidence that caspases are involved in induction of apoptosis. J. Leukoc. Biol. 68: 845-853 [Abstract] [Full Text]
Lach-Trifilieff, E., Menear, K., Schweighoffer, E., Tybulewicz, V. L. J., Walker, C. (2000). Syk-deficient eosinophils show normal interleukin-5-mediated differentiation, maturation, and survival but no longer respond to Fcgamma R activation. Blood 96: 2506-2510 [Abstract] [Full Text]
Adachi, T., Choudhury, B. K., Stafford, S., Sur, S., Alam, R. (2000). The Differential Role of Extracellular Signal-Regulated Kinases and p38 Mitogen-Activated Protein Kinase in Eosinophil Functions. J. Immunol. 165: 2198-2204 [Abstract] [Full Text]
Bates, M. E., Green, V. L., Bertics, P. J. (2000). ERK1 and ERK2 Activation by Chemotactic Factors in Human Eosinophils Is Interleukin 5-dependent and Contributes to Leukotriene C4 Biosynthesis. J. Biol. Chem. 275: 10968-10975 [Abstract] [Full Text]
Stenton, G. R., Kim, M.-K., Nohara, O., Chen, C.-F., Hirji, N., Wills, F. L., Gilchrist, M., Hwang, P.-H., Park, J.-G., Finlay, W., Jones, R. L., Befus, A. D., Schreiber, A. D. (2000). Aerosolized Syk Antisense Suppresses Syk Expression, Mediator Release from Macrophages, and Pulmonary Inflammation. J. Immunol. 164: 3790-3797 [Abstract] [Full Text]
Kagami, S.-i., Nakajima, H., Kumano, K., Suzuki, K., Suto, A., Imada, K., Davey, H. W., Saito, Y., Takatsu, K., Leonard, W. J., Iwamoto, I. (2000). Both Stat5a and Stat5b are required for antigen-induced eosinophil and T-cell recruitment into the tissue. Blood 95: 1370-1377 [Abstract] [Full Text]
Dibbert, B., Weber, M., Nikolaizik, W. H., Vogt, P., Schoni, M. H., Blaser, K., Simon, H.-U. (1999). Cytokine-mediated Bax deficiency and consequent delayed neutrophil apoptosis: A general mechanism to accumulate effector cells in inflammation. Proc. Natl. Acad. Sci. USA 96: 13330-13335 [Abstract] [Full Text]
Kankaanranta, H., De Souza, P. M., Barnes, P. J., Salmon, M., Giembycz, M. A., Lindsay, M. A. (1999). SB 203580, an Inhibitor of p38 Mitogen-Activated Protein Kinase, Enhances Constitutive Apoptosis of Cytokine-Deprived Human Eosinophils. J. Pharmacol. Exp. Ther. 290: 621-628 [Abstract] [Full Text]
Adachi, T., Stafford, S., Sur, S., Alam, R. (1999). A Novel Lyn-Binding Peptide Inhibitor Blocks Eosinophil Differentiation, Survival, and Airway Eosinophilic Inflammation1, 2. J. Immunol. 163: 939-946 [Abstract] [Full Text]
Giembycz, M. A., Lindsay, M. A. (1999). Pharmacology of the Eosinophil. Pharmacol. Rev. 51: 213-340 [Abstract] [Full Text]
Adachi, T., Pazdrak, K., Stafford, S., Alam, R. (1999). The Mapping of the Lyn Kinase Binding Site of the Common {beta} Subunit of IL-3/Granulocyte-Macrophage Colony- Stimulating Factor/IL-5 Receptor. J. Immunol. 162: 1496-1501 [Abstract] [Full Text]
Duprez, V., Blank, U., Chretien, S., Gisselbrecht, S., Mayeux, P. (1998). Physical and Functional Interaction between p72syk and Erythropoietin Receptor. J. Biol. Chem. 273: 33985-33990 [Abstract] [Full Text]
Adachi, T., Alam, R. (1998). The mechanism of IL-5 signal transduction. Am. J. Physiol. Cell Physiol. 275: C623-C633 [Abstract] [Full Text]
Pazdrak, K., Olszewska-Pazdrak, B., Stafford, S., Garofalo, R. P., Alam, R. (1998). Lyn, Jak2, and Raf-1 Kinases Are Critical for the Antiapoptotic Effect of Interleukin 5, whereas only Raf-1 Kinase Is Essential for Eosinophil Activation and Degranulation. JEM 188: 421-429 [Abstract] [Full Text]
Dibbert, B., Daigle, I., Braun, D., Schranz, C., Weber, M., Blaser, K., Zangemeister-Wittke, U., Akbar, A. N., Simon, H.-U. (1998). Role for Bcl-xL in Delayed Eosinophil Apoptosis Mediated by Granulocyte-Macrophage Colony-Stimulating Factor and Interleukin-5. Blood 92: 778-783 [Abstract] [Full Text]
Simon, H.-U., Yousefi, S., Dibbert, B., Hebestreit, H., Weber, M., Branch, D. R., Blaser, K., Levi-Schaffer, F., Anderson, G. P. (1998). Role for Tyrosine Phosphorylation and Lyn Tyrosine Kinase in Fas Receptor-Mediated Apoptosis in Eosinophils. Blood 92: 547-557 [Abstract] [Full Text]
Kiefer, F., Brumell, J., Al-Alawi, N., Latour, S., Cheng, A., Veillette, A., Grinstein, S., Pawson, T. (1998). The Syk Protein Tyrosine Kinase Is Essential for Fcgamma Receptor Signaling in Macrophages and Neutrophils. Mol. Cell. Biol. 18: 4209-4220 [Abstract] [Full Text]
Gauvreau, G. M., O'Byrne, P. M., Moqbel, R., Velazquez, J., Watson, R. M., Howie, K. J., Denburg, J. A. (1998). Enhanced Expression of GM-CSF in Differentiating Eosinophils of Atopic and Atopic Asthmatic Subjects. Am. J. Respir. Cell Mol. Bio. 19: 55-62 [Abstract] [Full Text]
Chin, H., Arai, A., Wakao, H., Kamiyama, R., Miyasaka, N., Miura, O. (1998). Lyn Physically Associates With the Erythropoietin Receptor and May Play a Role in Activation of the Stat5 Pathway. Blood 91: 3734-3745 [Abstract] [Full Text]
Ogata, N., Kouro, T., Yamada, A., Koike, M., Hanai, N., Ishikawa, T., Takatsu, K. (1998). JAK2 and JAK1 Constitutively Associate With an Interleukin-5 (IL-5) Receptor alpha �and beta c Subunit, Respectively, and Are Activated Upon IL-5 Stimulation. Blood 91: 2264-2271 [Abstract] [Full Text]
Hebestreit, H., Dibbert, B., Balatti, I., Braun, D., Schapowal, A., Blaser, K., Simon, H.-U. (1998). Disruption of Fas Receptor Signaling by Nitric Oxide in Eosinophils. JEM 187: 415-425 [Abstract] [Full Text]
IVERSEN, P.�O., ROBINSON, D., YING, S., MENG, Q., BARRY KAY, A., CLARK-LEWIS, I., LOPEZ, A.�F. (1997). The GM-CSF Analogue E21R Induces Apoptosis of Normal and Activated Eosinophils. Am. J. Respir. Crit. Care Med. 156: 1628-1632 [Abstract] [Full Text]
Keel, M., Ungethum, U., Steckholzer, U., Niederer, E., Hartung, T., Trentz, O., Ertel, W. (1997). Interleukin-10 Counterregulates Proinflammatory Cytokine-Induced Inhibition of Neutrophil Apoptosis During Severe Sepsis. Blood 90: 3356-3363 [Abstract] [Full Text]
Phipps, D. J., Yousefi, S., Branch, D. R. (1997). Increased Enzymatic Activity of the T-Cell Antigen Receptor-Associated Fyn Protein Tyrosine Kinase in Asymptomatic Patients Infected With the Human Immunodeficiency Virus. Blood 90: 3603-3612 [Abstract] [Full Text]
Pazdrak, K., Adachi, T., Alam, R. (1997). Src Homology 2 Protein Tyrosine Phosphatase (SHPTP2)/Src Homology 2 Phosphatase 2 (SHP2) Tyrosine Phosphatase Is a Positive Regulator of the Interleukin 5 Receptor Signal Transduction Pathways Leading to the Prolongation of Eosinophil Survival. JEM 186: 561-568 [Abstract] [Full Text]
de Groot, R. P., van Dijk, T. B., Caldenhoven, E., Coffer, P. J., Raaijmakers, J. A.M., Lammers, J.-W. J., Koenderman, L. (1997). Activation of 12-O-Tetradecanoylphorbol-13-acetate Response Element- and Dyad Symmetry Element-dependent Transcription by Interleukin-5 Is Mediated by Jun N-terminal Kinase/Stress-activated Protein Kinase Kinases. J. Biol. Chem. 272: 2319-2325 [Abstract] [Full Text]
Grishin, A. V., Azhipa, O., Semenov, I., Corey, S. J. (2001). Interaction between growth arrest-DNA damage protein 34 and Src kinase Lyn negatively regulates genotoxic apoptosis. Proc. Natl. Acad. Sci. USA 98: 10172-10177 [Abstract] [Full Text]