Cross-linking of FcεRI causes Ca2+ mobilization via a sphingosine kinase pathway in a clathrin-dependent manner

Cell Calcium

Volumn 45, Issue 2, 2009, Pages 99-108

  Ryu, Seung Duk ^a   Lee, Hyun Sil ^a   Suk, Ho Young ^a   Park, Chang Shin ^b   Choi, Oksoon Hong ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Inha University School of Medicine   (South Korea)

Author keywords

Ca2+ signaling; Clathrin; Fc RI; Mast cell; Sphingosine kinase

Indexed keywords

ANTIGEN; CALCIUM ION; CLATHRIN; FC RECEPTOR; INOSITOL 1,4,5 TRISPHOSPHATASE; PHOSPHOLIPASE C GAMMA; PROTEIN KINASE SYK; PROTEIN P110; PROTEIN P85; SHORT HAIRPIN RNA; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE KINASE; CHLORPROMAZINE; CLATHRIN HEAVY CHAIN; CROSS LINKING REAGENT; IMMUNOGLOBULIN E RECEPTOR; INOSITOL 1,4,5 TRISPHOSPHATE; PHOSPHOTRANSFERASE; PHOSPHOTYROSINE;

ANIMAL CELL; ARTICLE; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CALCIUM TRANSPORT; COATED VESICLE; CONTROLLED STUDY; CROSS LINKING; DEGRANULATION; ENDOCYTOSIS; LIPID RAFT; MAST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; RECEPTOR AFFINITY; SIGNAL TRANSDUCTION; ANIMAL; CELL LINE; COATED PIT; CYTOLOGY; DRUG EFFECT; ENZYME ACTIVATION; ENZYMOLOGY; GENE SILENCING; METABOLISM; PHYSIOLOGY;

ANIMALS; CALCIUM SIGNALING; CELL DEGRANULATION; CELL LINE; CHLORPROMAZINE; CLATHRIN HEAVY CHAINS; COATED PITS, CELL-MEMBRANE; CROSS-LINKING REAGENTS; ENZYME ACTIVATION; GENE KNOCKDOWN TECHNIQUES; INOSITOL 1,4,5-TRISPHOSPHATE; MAST CELLS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PHOSPHOTYROSINE; RATS; RECEPTORS, IGE;

EID: 58549114380     PISSN: 01434160     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceca.2008.07.002     Document Type: Article

References (67)

1. Wedemeyer J., Tsai M., and Galli S.J. Roles of mast cells and basophils in innate and acquired immunity. Curr. Opin. Immunol. 12 (2000) 624-631
2. Choi O.H., Kim J.H., and Kinet J.P. Calcium mobilization via sphingosine kinase in signalling by the Fc epsilon RI antigen receptor. Nature 380 (1996) 634-636
3. Melendez A.J., and Khaw A.K. Dichotomy of Ca2+ Signals triggered by different phospholipid pathways in antigen stimulation of human mast cells. J. Biol. Chem. 277 (2002) 17255-17262
4. Lee H.S., Park C.S., Lee Y.M., Suk H.Y., Clemons T.C.M., and Choi O.H. Antigen-induced Ca2+ mobilization in RBL-2H3 cells: Role of I(1,4,5)P3 and S1P and necessity of I(1,4,5)P3 production. Cell Calcium 38 (2005) 581-592
5. Turner H., and Kinet J.P. Signalling through the high-affinity IgE receptor Fc epsilonRI. Nature 402 (1999) B24-B30
6. Rivera J. Molecular adapters in Fc varepsilon RI signaling and the allergic response. Curr. Opin. Immunol. 14 (2002) 688-693
7. Hla T., Lee M.J., Ancellin N., Paik J.H., and Kluk M.J. Lysophospholipids-receptor revelations. Science 294 (2001) 1875-1878
8. Spiegel S., and Milstien S. Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat. Rev. Mol. Cell Biol. 4 (2003) 397-407
9. Hla T. Signaling and biological actions of sphingosine 1-phosphate. Pharmacol. Res. 47 (2003) 401-407
10. Lee M.J., Van B.J., Thangada S., et al. Sphingosine-1-phosphate as a ligand for the G protein-coupled receptor EDG-1. Science 279 (1998) 1552-1555
11. An S., Bleu T., and Zheng Y. Transduction of intracellular calcium signals through G protein-mediated activation of phospholipase C by recombinant sphingosine 1-phosphate receptors. Mol. Pharmacol. 55 (1999) 787-794
12. Okajima F., Tomura H., Sho K., Nochi H., Tamoto K., and Kondo Y. Involvement of pertussis toxin-sensitive GTP-binding proteins in sphingosine 1-phosphate-induced activation of phospholipase C-Ca2+ system in HL60 leukemia cells. FEBS Lett. 379 (1996) 260-264
13. Sato K., Kon J., Tomura H., et al. Activation of phospholipase C-Ca2+ system by sphingosine 1-phosphate in CHO cells transfected with Edg-3, a putative lipid receptor. FEBS Lett. 443 (1999) 25-30
14. Melendez A.J., Floto R.A., Cameron A.J., Gillooly D.J., Harnett M.M., and Allen J.M. A molecular switch changes the signalling pathway used by the Fc gamma RI antibody receptor to mobilise calcium. Curr. Biol. 8 (1998) 210-221
15. Melendez A.J., Floto R.A., Gillooly D.J., Harnett M.M., and Allen J.M. FcgammaRI coupling to phospholipase D initiates sphingosine kinase-mediated calcium mobilization and vesicular trafficking. J. Biol. Chem. 273 (1998) 9393-9402
16. Chuang F.Y., Sassaroli M., and Unkeless J.C. Convergence of Fc gamma receptor IIA and Fc gamma receptor IIIB signaling pathways in human neutrophils. J. Immunol. 164 (2000) 350-360
17. Alemany R., Meyer Z.H., van Koppen C.J., and Jakobs K.H. Formyl peptide receptor signaling in HL-60 cells through sphingosine kinase. J. Biol. Chem. 274 (1999) 3994-3999
18. Meyer Heringdorf D., Lass H., Alemany R., et al. Sphingosine kinase-mediated Ca2+ signalling by G-protein-coupled receptors. EMBO J. 17 (1998) 2830-2837
19. Ghosh T.K., Bian J., and Gill D.L. Sphingosine 1-phosphate generated in the endoplasmic reticulum membrane activates release of stored calcium. J. Biol. Chem. 269 (1994) 22628-22635
20. Jolly P.S., Bektas M., Olivera A., et al. Transactivation of sphingosine-1-phosphate receptors by FcεRI triggering is required for normal mast cell degranulation and chemotaxis. J. Exp. Med. 199 (2004) 959-970
21. Mitra P., Oskeritzian C.A., Payne S.G., Beaven M.A., Milstien S., and Spiegel S. Role of ABCC1 in export of sphingosine-1-phosphate from mast cells. Proc. Natl. Acad. Sci. U.S.A. (2006) 16394-16399
22. Le Roy C., and Wrana J.L. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat. Rev. Mol. Cell Biol. 6 (2005) 112-126
23. Sorkin A., and Von Zastrow M. Signal transduction and endocytosis: close encounters of many kinds. Nat. Rev. Mol. Cell Biol. 3 (2002) 600-614
24. McPherson P.S., Kay B.K., and Hussain N.K. Signaling on the endocytic pathway. Traffic 2 (2001) 375-384
25. Di Fiore P.P., and De Camilli P. Endocytosis and signaling: an inseparable partnership. Cell 106 (2001) 1-4
26. Vieira A.V., Lamaze C., and Schmid S.L. Control of EGF receptor signaling by clathrin-mediated endocytosis. Science 274 (1996) 2086-2089
27. Ceresa B.P., Kao A.W., Santeler S.R., and Pessin J.E. Inhibition of clathrin-mediated endocytosis selectively attenuates specific insulin receptor signal transduction pathways. Mol. Cell Biol. 18 (1998) 3862-3870
28. Della Rocca G.J., Mukhin Y.V., Garnovskaya M.N., et al. Serotonin 5-HT1A receptor-mediated Erk activation requires calcium/calmodulin-dependent receptor endocytosis. J. Biol. Chem. 274 (1999) 4749-4753
29. Vogler O., Nolte B., Voss M., Schmidt M., Jakobs K.H., and van Koppen C.J. Regulation of muscarinic acetylcholine receptor sequestration and function by beta-arrestin. J. Biol. Chem. 274 (1999) 12333-12338
30. Ignatova E.G., Belcheva M.M., Bohn L.M., Neuman M.C., and Coscia C.J. Requirement of receptor internalization for opioid stimulation of mitogen-activated protein kinase: biochemical and immunofluorescence confocal microscopic evidence. J. Neurosci. 19 (1999) 56-63
31. Whistler J.L., and Von Zastrow M. Dissociation of functional roles of dynamin in receptor-mediated endocytosis and mitogenic signal transduction. J. Biol. Chem. 274 (1999) 24575-24578
32. Wilson B.S., Pfeiffer J.R., and Oliver J.M. Observing FcepsilonRI signaling from the inside of the mast cell membrane. J. Cell Biol. 149 (2000) 1131-1142
33. Field K.A., Holowka D., and Baird B. Structural aspects of the association of FcepsilonRI with detergent-resistant membranes. J. Biol. Chem. 274 (1999) 1753-1758
34. Wilson B., Pfeiffer J., and Oliver J. Fc varepsilon RI signaling observed from the inside of the mast cell membrane. Mol. Immunol. 38 (2002) 1259
35. Santini F., and Keen J.H. Endocytosis of activated receptors and clathrin-coated pit formation: deciphering the chicken or egg relationship. J. Cell Biol. 132 (1996) 1025-1036
36. Field K.A., Holowka D., and Baird B. Compartmentalized activation of the high affinity immunoglobulin E receptor within membrane domains. J. Biol. Chem. 272 (1997) 4276-4280
37. Sheets E.D., Holowka D., and Baird B. Critical Role for cholesterol in Lyn-mediated tyrosine phosphorylation of Fcepsilon RI and their association with detergent-resistant membranes. J. Cell Biol. 145 (1999) 877-887
38. Ali H., Richardson R.M., Tomhave E.D., DuBose R.A., Haribabu B., and Snyderman R. Regulation of stably transfected platelet activating factor receptor in RBL-2H3 cells. Role of multiple G proteins and receptor phosphorylation. J. Biol. Chem. 269 (1994) 24557-24563
39. Choi O.H., Lee J.H., Kassessinoff T., Cunha-Melo J.R., Jones S.V., and Beaven M.A. Antigen and carbachol mobilize calcium by similar mechanisms in a transfected mast cell line (RBL-2H3 cells) that expresses ml muscarinic receptors. J. Immunol. 151 (1993) 5586-5595
40. Jones S.V., Choi O.H., and Beaven M.A. Carbachol induces secretion in a mast cell line (RBL-2H3) transfected with the ml muscarinic receptor gene. FEBS Lett. 289 (1991) 47-50
41. Okamoto Y., Ninomiya H., Miwa S., and Masaki T. Cholesterol oxidation switches the internalization pathway of endothelin receptor Type A from caveolae to clathrin-coated pits in chinese hamster ovary cells. J. Biol. Chem. 275 (2000) 6439-6446
42. Okuyama M., Laman H., Kingsbury S.R., et al. Small-molecule mimics of an alpha-helix for efficient transport of proteins into cells. Nat. Methods (2007)
43. Vanden Broeck D., and De Wolf M.J. Selective blocking of clathrin-mediated endocytosis by RNA interference: epsin as target protein. BioTechniques 41 (2006) 475-484
44. Chatterjee S., Cao S., Peterson T.E., Simari R.D., and Shah V. Inhibition of GTP-dependent vesicle trafficking impairs internalization of plasmalemmal eNOS and cellular nitric oxide production. J. Cell Sci. 116 (2003) 3645-3655
45. Lecot S., Belouzard S., Dubuisson J., and Rouille Y. Bovine viral diarrhea virus entry is dependent on clathrin-mediated endocytosis. J. Virol. 79 (2005) 10826-10829
46. Blot V., and McGraw T.E. GLUT4 is internalized by a cholesterol-dependent nystatin-sensitive mechanism inhibited by insulin. EMBO J. 25 (2006) 5648-5658
47. Frankel D.J., Pfeiffer J.R., Surviladze Z., et al. Revealing the topography of cellular membrane domains by combined atomic force microscopy/fluorescence imaging. Biophys. J. 90 (2006) 2404-2413
48. Wettey F.R., Hawkins S.F.C., Stewart A., Luzio J.P., Howard J.C., and Jackson A.P. Controlled elimination of clathrin heavy-chain expression in DT40 lymphocytes. Science 297 (2002) 1521-1525
49. Wilson B.S., Steinberg S.L., Liederman K., et al. Markers for detergent-resistant lipid rafts occupy distinct and dynamic domains in Native membranes. Mol. Biol. Cell 15 (2004) 2580-2592
50. Rivera J., and Gilfillan A.M. Molecular regulation of mast cell activation. J. Allergy Clin. Immunol. 117 (2006) 1214-1225
51. Kuwahara K., Kawai T., Mitsuyoshi S., et al. Cross-linking of B cell antigen receptor-related structure of pre-B cell lines induces tyrosine phosphorylation of p85 and p110 subunits and activation of phosphatidylinositol 3-kinase. Int. Immunol. 8 (1996) 1273-1285
52. Craxton A., Jiang A., Kurosaki T., and Clark E.A. Syk and Bruton's tyrosine kinase are required for B cell antigen receptor-mediated activation of the kinase Akt. J. Biol. Chem. 274 (1999) 30644-30650
53. Mazerolles F., and Fischer A. Binding of CD4 ligands induces tyrosine phosphorylation of phosphatidylinositol-3 kinase p110 subunit. Int. Immunol. 10 (1998) 1897-1905
54. Jeschke M., Standke G.J.R., and Susa M. Fluoroaluminate induces activation and association of Src and Pyk2 tyrosine kinases in osteoblastic MC3T3-E1 cells. J. Biol. Chem. 273 (1998) 11354-11361
55. Parravicini V., Gadina M., Kovarova M., et al. Fyn kinase initiates complementary signals required for IgE-dependent mast cell degranulation. Nat. Immunol. 3 (2002) 741-748
56. Zhang W., Trible R.P., and Samelson L.E. LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation. Immunity 9 (1998) 239-246
57. Olivera A., Mizugishi K., Tikhonova A., et al. The sphingosine kinase-sphingosine-1-phosphate axis is a determinant of mast cell function and anaphylaxis. Immunity 26 (2007) 287-297
58. Tkaczyk C., and Gilfillan A.M. Fc(varepsilon)Ri-dependent signaling pathways in human mast cells. Clin. Immunol. 99 (2001) 198-210
59. Bischoff S.C. Role of mast cells in allergic and non-allergic immune responses: comparison of human and murine data. Nat. Rev. Immunol. 7 (2007) 93-104
60. Oskeritzian C.A., Alvarez S.E., Hait N.C., Price M.M., Milstien S., and Spiegel S. Distinct roles of sphingosine kinases 1 and 2 in human mast-cell functions. Blood 111 8 (2008) 4193-4200
61. Billich A., Bornancin F., Devay P., Mechtcheriakova D., Urtz N., and Baumruker T. Phosphorylation of the immunomodulatory drug FTY720 by sphingosine kinases. J. Biol. Chem. 278 (2003) 47408-47415
62. Park C.G., Lee H.S., Lee H.Y., Park C.S., and Choi O.H. Cloning and characterization of rat sphingosine kinase 1 with an N-terminal extension. Biochem. Biophys. Res. Commun. 364 (2007) 702-707
63. Beaven M.A. Division of labor: specialization of sphingosine kinases in mast cells. Immunity 26 (2007) 271-273
64. Mathes C., Fleig A., and Penner R. Calcium release-activated calcium current (ICRAC) is a direct target for sphingosine. J. Biol. Chem. 273 (1998) 25020-25030
65. van Rossum D.B., Patterson R.L., Kiselyov K., et al. Agonist-induced Ca2+ entry determined by inositol 1,4,5-trisphosphate recognition. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 2323-2327
66. Patterson R.L., van Rossum D.B., Ford D.L., et al. Phospholipase C-gamma is required for agonist-induced Ca2+ entry. Cell 111 (2002) 529-541
67. van Rossum D.B., Patterson R.L., Sharma S., et al. Phospholipase C[gamma]1 controls surface expression of TRPC3 through an intermolecular PH domain. Nature 434 (2005) 99-104