Early activation of sphingosine kinase in mast cells and recruitment to FcεRI are mediated by its interaction with Lyn kinase

Molecular and Cellular Biology

Volumn 24, Issue 19, 2004, Pages 8765-8777

  Urtz, Nicole ^a   Olivera, Ana ^b   Bofill Cardona, Elisa ^a   Csonga, Robert ^a   Billich, Andreas ^a   Mechtcheriakova, Diana ^a   Bornancin, Frederic ^a   Woisetschläger, Max ^a   Rivera, Juan ^b   Baumruker, Thomas ^a,c  

^a Novartis Inst BioMed Res Vienna   (Austria)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c Novartis Inst for Biomed Research   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN E RECEPTOR; IMMUNOGLOBULIN HEAVY CHAIN; LIPID PEROXIDASE; PROTEIN KINASE LYN; PROTEIN TYROSINE KINASE; SPHINGOLIPID; SPHINGOSINE KINASE; SPHINGOSINE KINASE TYPE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MAST CELL; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR AFFINITY; WILD TYPE;

ANIMALS; HELA CELLS; HUMANS; MAST CELLS; MICE; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RECEPTORS, IGE; SRC-FAMILY KINASES; TIME FACTORS;

ANIMALIA;

EID: 4544224536     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.19.8765-8777.2004     Document Type: Article

References (51)

1. Albrecht, B., M. Woisetschlager, and M. W. Robertson. 2000. Export of the high affinity IgE receptor from the endoplasmic reticulum depends on a glycosylation-mediated quality control mechanism. J. Immunol. 165:5686-5694.
2. Baumruker, T., G. G. Pendl, and E. E. Prieschl. 1997. Gene regulation after Fc epsilon RI stimulation in the murine mast cell line CPII. Int. Arch. Allergy Immunol. 113:39-41.
3. Baumruker, T., and E. E. Prieschl. 2002. Sphingolipids and the regulation of the immune response. Semin. Immunol. 14:57-63.
4. Billich, A., F. Bornancin, P. Devay, D. Mechtcheriakova, N. Urtz, and T. Baumruker. 2003. Phosphorylation of the immunomodulatory drug FTY720 by sphingosine kinases. J. Biol. Chem. 278:47408-47415.
5. Brinkmann, V., M. D. Davis, C. E. Heise, R. Albert, S. Cottens, R. Hof, C. Bruns, E. Prieschl, T. Baumruker, P. Hiestand, C. A. Foster, M. Zollinger, and K. R. Lynch. 2002. The immune modulator FTY720 targets sphingosine 1-phosphate receptors. J. Biol. Chem. 277:21453-21457.
6. Cantley, L. C. 2002. The phosphoinositide 3-kinase pathway. Science 296: 1655-1657.
7. Choi, O. H., J. H. Kim, and J. P. Kinet. 1996. Calcium mobilization via sphingosine kinase in signalling by the Fc epsilon RI antigen receptor. Nature 380:634-636.
8. Davis, R. J., N. Girones, and M. Faucher. 1988. Two alternative mechanisms control the interconversion of functional states of the epidermal growth factor receptor. J. Biol. Chem. 263:5373-5379.
9. Edsall, L. C., G. G. Pirianov, and S. Spiegel. 1997. Involvement of sphingosine-1-phosphate in nerve growth factor-mediated neuronal survival and differentiation. J. Neurosci. 17:6952-6960.
10. Eiseman, E., and J. B. Bolen. 1992. Engagement of the high-affinity IgE receptor activates src protein-related tyrosine kinases. Nature 355:78-80.
11. Field, K. A., D. Holowka, and B. Baird. 1995. FcεRI-mediated recruitment of p53/p56lyn to detergent-resistant membrane domains accompanies cellular signaling. Proc. Natl. Acad. Sci. USA 92:9201-9205.
12. Field, K. A., D. Holowka, and B. Baird. 1997. Compartmentalized activation of the high affinity immunoglobulin E receptor with membrane domains. J. Biol. Chem. 272:4276-4280.
13. Hayashi, S., T. Okada, N. Igarashi, T. Fujita, S. Jahangeer, and S. Nakamura. 2002. Identification and characterization of RPK118, a novel sphingosine kinase-1-binding protein. J. Biol. Chem. 277:33319-33324.
14. Hinkovska-Galcheva, V. T., L. A. Boxer, P. J. Mansfield, D. Harsh, A. Blackwood, and J. A. Shayman. 1998. The formation of ceramide-1-phosphate during neutrophil phagocytosis and its role in liposome fusion. J. Biol. Chem. 273:33203-33209.
15. Johnson, K. R., K. P. Becker, M. M. Facchinetti, Y. A. Hannun, and L. M. Obeid. 2002. PKC-dependent activation of sphingosine kinase 1 and translocation to the plasma membrane. Extracellular release of sphingosine-1-phosphate induced by phorbol 12-myristate 13-acetate (PMA). J. Biol. Chem. 277:35257-35262.
16. Jolly, P. S., M. Bektas, A. Olivera, C. Gonzalez-Espinosa, R. L. Proia, J. Rivera, S. Milstien, and S. Spiegel. 2004. Transactivation of sphingosine-1-phosphate receptors by FcεRI triggering is required for normal mast cell degranulation and chemotaxis. J. Exp. Med. 199:959-970.
17. Kawakami, Y., J. Kitaura, A. B. Satterthwaite, R. M. Kato, K. Asai, S. E. Hartman, M. Maeda-Yamamoto, C. A. Lowell, D. J. Rawlings, O. N. Witte, and T. Kawakami. 2000. Redundant and opposing functions of two tyrosine kinases, Btk and Lyn, in mast cell activation. J. Immunol. 165:1210-1219.
18. King, C. C., F. T. Zenke, P. E. Dawson, E. M. Dutil, A. C. Newton, B. A. Hemmings, and G. M. Bokoch. 2000. Sphingosine is a novel activator of 3-phosphoinositide-dependent kinase 1. J. Biol. Chem. 275:18108-18113.
19. Lacana, E., M. Maceyka, S. Milstien, and S. Spiegel. 2002. Cloning and characterization of a protein kinase A anchoring protein (AKAP)-related protein that interacts with and regulates sphingosine kinase 1 activity. J. Biol. Chem. 277:32947-32953.
20. Liu, H., M. Sugiura, V. E. Nava, L. C. Edsall, K. Kono, S. Poulton, S. Milstien, T. Kohama, and S. Spiegel. 2000. Molecular cloning and functional characterization of a novel mammalian sphingosine kinase type 2 isoform. J. Biol. Chem. 275:19513-19520.
21. Mazurek, N., T. Megidish, S. Hakomori, and Y. Igarashi. 1994. Regulatory effect of phorbol esters on sphingosine kinase in BALB/C 3T3 fibroblasts (variant A31): demonstration of cell type-specific response-a preliminary note. Biochem. Biophys. Res. Commun. 198:1-9.
22. McDonald, O. B., Y. A. Hannun, C. H. Reynolds, and N. Sahyoun. 1991. Activation of casein kinase II by sphingosine. J. Biol. Chem. 266:21773-21776.
23. Megidish, T., T. White, K. Takio, K. Titani, Y. Igarashi, and S. Hakomori. 1995. The signal modulator protein 14-3-3 is a target of sphingosine- or N,N-dimethylsphingosine-dependent kinase in 3T3(A31) cells. Biochem. Biophys. Res. Commun. 216:739-747.
24. Melendez, A., R. A. Floto, D. J. Gillooly, M. M. Harnett, and J. M. Allen. 1998. Fc gamma RI coupling to phospholipase D initiates sphingosine kinase-mediated calcium mobilization and vesicular trafficking. J. Biol. Chem. 273:9393-9402.
25. Melendez, A. J., and A. K. Khaw. 2002. Dichotomy of Ca2+ signals triggered by different phospholipid pathways in antigen stimulation of human mast cells. J. Biol. Chem. 277:17255-17262.
26. Meyer zu Heringdorf, D., H. Lass, R. Alemany, K. T. Laser, E. Neumann, C. Zhang, M. Schmidt, U. Rauen, K. H. Jakobs, and C. J. van Koppen. 1998. Sphingosine kinase-mediated Ca2+ signalling by G-protein-coupled receptors. EMBO J. 17:2830-2837.
27. Nishizumi, H., and T. Yamamoto. 1997. Impaired tyrosine phosphorylation and Ca2+ mobilization, but not degranulation, in lyn-deficient bone marrow-derived mast cells. J. Immunol. 158:2350-2355.
28. Odom, S., G. Gomez, M. Kovarova, Y. Furumoto, J. J. Ryan, H. V. Wright, C. Gonzales-Espinosa, M. L. Hibbs, K. W. Harder, and J. Rivera. 2004. Negative regulation of immunoglobulin E-dependent allergic responses by Lyn kinase. J. Exp. Med. 199:1491-1502.
29. Olivera, A., T. Kohama, L. Edsall, V. Nava, O. Cuvillier, S. Poulton, and S. Spiegel. 1999. Sphingosine kinase expression increases intracellular sphingosine-1-phosphate and promotes cell growth and survival. J. Cell Biol. 147:545-558.
30. Olivera, A., T. Kohama, Z. Tu, S. Milstien, and S. Spiegel. 1998. Purification and characterization of rat kidney sphingosine kinase. J. Biol. Chem. 273: 12576-12583.
31. Olivera, A., and S. Spiegel. 1993. Sphingosine-1-phosphate as second messenger in cell proliferation induced by PDGF and FCS mitogens. Nature 365:557-560.
32. Ortega, E., M. Lara, I. Lee, C. Santana, A. M. Martinez, J. R. Pfeiffer, R. J. Lee, B. S. Wilson, and J. M. Oliver. 1999. Lyn dissociation from phosphorylated Fc epsilon RI subunits: a new regulatory step in the Fc epsilon RI signaling cascade revealed by studies of Fc epsilon RI dimer signaling activity. J. Immunol. 162:176-185.
33. Parravicini, V., M. Gadina, M. Kovarova, S. Odom, C. Gonzalez-Espinosa, Y. Furumoto, S. Saitoh, L. E. Samelson, J. J. O'Shea, and J. Rivera. 2002. Fyn kinase initiates complementary signals required for IgE-dependent mast cell degranulation. Nat. Immunol. 3:741-748.
34. Pitson, S. M., R. J. D'Andrea, L. Vandeleur, P. A. Moretti, P. Xia, J. R. Gamble, M. A. Vadas, and B. W. Wattenberg. 2000. Human sphingosine kinase: purification, molecular cloning and characterization of the native and recombinant enzymes. Biochem. J. 350:429-441.
35. Pribluda, V. S., C. Pribluda, and H. Metzger. 1994. Transphosphorylation as the mechanism by which the high-affinity receptor for IgE is phosphorylated upon aggregation. Proc. Natl. Acad. Sci. USA 91:11246-11250.
36. Prieschl, E. E., and T. Baumruker. 2000. Sphingolipids: second messengers, mediators and raft constituents in signaling. Immunol. Today 21:555-560.
37. Prieschl, E. E., R. Csonga, V. Novotny, G. E. Kikuchi, and T. Baumruker. 1999. The balance between sphingosine and sphingosine-1-phosphate is decisive for mast cell activation after Fc epsilon receptor I triggering. J. Exp. Med. 190:1-8.
38. Prieschl, E. E., R. Csonga, V. Novotny, G. E. Kikuchi, and T. Baumruker. 2000. Glycosphingolipid-induced relocation of Lyn and Syk into detergent-resistant membranes results in mast cell activation. J. Immunol. 164:5389-5397.
39. Prieschl, E. E., G. G. Pendl, N. E. Harrer, and T. Baumruker. 1995. p21ras links Fc epsilon RI to NF-AT family member in mast cells. The AP3-like factor in this cell type is an NF-AT family member. J. Immunol. 155:4963-4970.
40. Saitoh, S., R. Arudchandran, T. S. Manetz, W. Zhang, C. L. Sommers, P. E. Love, J. Rivera, and L. E. Samelson. 2000. LAT is essential for Fc(epsilon)RI-mediated mast cell activation. Immunity 12:525-535.
41. Saitoh, S., S. Odom, G. Gomez, C. L. Sommers, H. A. Young, J. Rivera, and L. E. Samelson. 2003. The four distal tyrosines are required for LAT-dependent signaling in FcepsilonRI-mediated mast cell activation. J. Exp. Med. 198:831-843.
42. Spiegel, S., O. Cuvillier, L. C. Edsall, T. Kohama, R. Menzeleev, Z. Olah, A. Olivera, G. Pirianov, D. M. Thomas, Z. Tu, J. R. Van Brocklyn, and F. Wang. 1998. Sphingosine-1-phosphate in cell growth and cell death. Ann. N. Y. Acad. Sci. 845:11-18.
43. Suchard, S. J., V. Hinkovska-Galcheva, P. J. Mansfield, L. A. Boxer, and J. A. Shayman. 1997. Ceramide inhibits IgG-dependent phagocytosis in human polymorphonuclear leukocytes. Blood 89:2139-2147.
44. Tedeschi, A., M. Lorini, S. Gibelli, and A. Miadonna. 2000. Effects of protein kinase C and phospholipase C inhibitors on IgE-dependent and IgE-independent basophil histamine release. Inflamm. Res. 49:480-485.
45. Trieselmann, N. Z., J. Soboloff, and S. A. Berger. 2003. Mast cells stimulated by membrane-bound, but not soluble, steel factor are dependent on phospholipase C activation. Cell. Mol. Life Sci. 60:759-766.
46. Wang, F., J. R. Van Brocklyn, J. P. Hobson, S. Movafagh, Z. Zukowska-Grojec, S. Milstien, and S. Spiegel. 1999. Sphingosine 1-phosphate stimulates cell migration through a G(i)-coupled cell surface receptor. Potential involvement in angiogenesis. J. Biol. Chem. 274:35343-35350.
47. Xia, P., J. R. Gamble, K. A. Rye, L. Wang, C. S. Hii, P. Cockerill, Y. Khew-Goodall, A. G. Bert, P. J. Barter, and M. A. Vadas. 1998. Tumor necrosis factor-alpha induces adhesion molecule expression through the sphingosine kinase pathway. Proc. Natl. Acad. Sci. USA 95:14196-14201.
48. Xia, P., L. Wang, J. R. Gamble, and M. A. Vadas. 1999. Activation of sphingosine kinase by tumor necrosis factor-alpha inhibits apoptosis in human endothelial cells. J. Biol. Chem. 274:34499-34505.
49. Xia, P., L. Wang, P. A. Moretti, N. Albanese, F. Chai, S. M. Pitson, R. J. D'Andrea, J. R. Gamble, and M. A. Vadas. 2002. Sphingosine kinase interacts with TRAF2 and dissects tumor necrosis factor-alpha signaling. J. Biol. Chem. 277:7996-8003.
50. Yamashita, T., S. Y. Mao, and H. Metzger. 1994. Aggregation of the high-affinity IgE receptor and enhanced activity of p53/56lyn protein-tyrosine kinase. Proc. Natl. Acad. Sci. USA 91:11251-11255.
51. Young, R. M., D. Holowka, and B. Baird. 2003. A lipid raft environment enhances Lyn kinase activity by protecting the active site tyrosine from dephosphorylation. J. Biol. Chem. 278:20746-20752.