The α-galactosyl derivatives of ganglioside GD1b are essential for the organization of lipid rafts in RBL-2H3 mast cells

Experimental Cell Research

Volumn 314, Issue 13, 2008, Pages 2515-2528

  Silveira e Souza, Adriana Maria Mariano ^a   Mazucato, Vivian Marino ^a   de Castro, Rodrigo Orlandini ^a   Matioli, Fabiana ^a   Ciancaglini, Pietro ^a   de Paiva Paulino, Tony ^a   Jamur, Maria Célia ^a   Oliver, Constance ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Degranulation; Fce open RI; Gangliosides; Lipid rafts; Mast cells

Indexed keywords

ALPHA GALACTOSYL DERIVATIVE; BETA N ACETYLHEXOSAMINIDASE; CALCIUM IONOPHORE; GANGLIOSIDE GD 1B; GLYCOSPHINGOLIPID; IMMUNOGLOBULIN E RECEPTOR;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL ACTIVATION; CELL LINE; CELL MUTANT; CELL STRAIN RBL 2H3; DEGRANULATION; ENZYME ACTIVITY; LIPID RAFT; MAST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT;

EID: 47349116308     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2008.05.014     Document Type: Article

References (81)

1. Simons K., and Ikonen E. Functional rafts in cell membranes. Nature 387 (1997) 569-572
2. Gilfillan A., and Tkaczyk C. Integrated signaling pathways for mast-cell activation. Nat. Rev. Immunol. 6 (2006) 218-230
3. Hunter T. Signaling-2000 and beyond. Cell 100 (2000) 113-127
4. Simons K., and Toomre D. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1 (2000) 31-41
5. Holowka D., Gosse J.A., Hammond A.T., Han X., Sengupta P., Smith N.L., Wagenknecht-Wiesner A., Wu M., Young R.M., and Baird B. Lipid segregation and IgE receptor signaling: a decade of progress. Biochim. Biophys. Acta 20 (2005) 1-8
6. Allende M.L., and Proia R.L. Lubricating cell signaling pathways with gangliosides. Curr. Opin. Struct. Biol. 12 (2002) 587-592
7. Lyn to detergent-resistant membrane domains accompanies cellular signaling. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 9201-9205
8. Xavier R., Brennan T., Li Q., McCormack C., and Seed B. Membrane compartmentation is required for efficient T cell activation. Immunity 8 (1998) 723-732
9. Miceli M.C., Moran M., Chung C.D., Patel V.P., Low T., and Zinnanti W. Co-stimulation and counter-stimulation: lipid raft clustering controls TCR signaling and functional outcomes. Semin. Immunol. 13 (2001) 115-128
10. Cheng P.C., Cherukuri A., Dystra M., Malapati S., Sproul T., Chen M.R., and Pierce S.K. Floating the raft hypothesis: the roles of lipid rafts in B cell antigen receptor function. Semin. Immunol. 13 (2001) 107-114
11. Holowka D., and Baird B. FceRI as a paradigm for a lipid raft-dependent receptor in hematopoietic cells. Semin. Immunol. 13 (2001) 99-105
12. Metcalfe D.D., Baram D., and Mekori Y.A. Mast cells. Physiol. Rev. 77 (1997) 1033-1078
13. Rivera J., Arudchandran R., Gonzales-Espinosa C., Manetz T.S., and Xirasagar S. A perspective: regulation of IgE receptor-mediated mast cell responses by a LAT-organized plasma membrane-localized signaling complex. Int. Arch. Allergy Immunol. 124 (2001) 137-141
14. Rivera J., Gonzales-Espinosa C., Kovarova M., and Parracini V. The architecture of IgE-dependent mast cell signaling. A.C.I. International 14 (2002) 25-36
15. Siraganian R.P. Mast cell signal transduction from the high-affinity IgE receptor. Curr. Opin. Immunol. 15 (2003) 639-646
16. Galli S.J., Kaleniskoff J., Grimbaldeston M.A., Piliponsky A.M., Williams C.M.M., and Tsai M. Mast cell as "tunable" effector and immunoregulatory cells. Annu. Rev. Immunol. 23 (2005) 749-786
17. Field K.A., Apgar J.R., Hong-Geller E., Siraganian R.P., Baird B., and Holowka D. Mutant RBL mast cells defective in FceRI signaling and lipid raft biosynthesis are reconstituted by activated Rho-family GTPases. Mol. Biol. Cell 11 (2000) 3661-3673
18. Metzger H. It's spring, and thoughts turn to1/4allergies. Cell 97 (1999) 287-290
19. 3 in tyrosine phosphorylation of epidermal growth factor receptor. J. Biol. Chem. 263 (1988) 10915-10921
20. Weis F.M., and Davis R.J. Regulation of epidermal growth factor receptor signal transduction. Role of gangliosides. J. Biol. Chem. 265 (1990) 12059-12066
21. Baird B., Sheets E.D., and Holowka D. How does the plasma membrane participate in cellular signaling by receptor for immunoglobulin E?. Biophys. Chem. 82 (1999) 109-119
22. Wang X., Sun P., and Paller A.S. Ganglioside modulation regulates epithelial cell adhesion and spreading via ganglioside-specific effects on signaling. J. Biol. Chem. 277 (2002) 40410-40419
23. Stauffer T.P., and Meyer T. Compartmentalized IgE receptor-mediated signal transduction in living cell. J. Cell Biol. 139 (1997) 1447-1454
24. Holowka D., Sheets E.D., and Baird B. Interactions between FceRI and lipid rafts components are regulated by actin cytoskeleton. J. Cell Sci. 133 (2000) 1009-1019
25. Hakomori S. Structure and function of sphingolipids in transmembrane signaling and cell-cell interaction. Biochem. Soc. Trans. 21 (1993) 583-595
26. Brown D.A., and London E. Functions of lipid rafts in biological membranes. Annu. Rev. Immunol. 15 (1998) 371-404
27. Dráber P., and Dráberová L. Lipid rafts in mast cell signaling. Mol. Immunol. 38 (2001) 1247-1252
28. M.W. King, S. Marchesini, Metabolism of the sphingolipids, Available at: http://www.med.unids.it/~marchesi/lipsynth3.html, Search for "Lipid metabolism" from the opening page, Accessed February 14, 2002.
29. Pike L.J. Lipid Rafts: heterogeneity on the high seas. Biochem. J. 378 (2004) 281-292
30. Kolter T., Proia R.L., and Sandhoff K. Combinatorial ganglioside biosynthesis. J. Biol. Chem. 277 (2002) 25859-25862
31. Fishman P.H. Recent advances in identifying the functions of gangliosides. Chem. Phys. Lipides 42 (1986) 137-151
32. Bremer E.G., Schlessinger J., and Hakomori S. Ganglioside-mediated modulation of cell growth. J. Biol. Chem. 261 (1986) 2434-2440
33. Hunnan Y.A., and Bell R.M. Functions of sphingolipids and sphingolipids breakdown products in cellular regulation. Science 243 (1989) 500-507
34. Igarashi Y., Nojiri N., Hanai N., and Hakomori S. Gangliosides that modulate membrane protein function. Methods Enzym. 179 (1989) 521-541
35. Hakomori S. Bifunctional role of glycosphingolipids. J. Biol. Chem. 265 (1990) 18713-18716
36. Oliver C., Sahara N., Kitani S., Robbins A.R., Mertz L.M., and Siraganian R.P. Binding of monoclonal antibody AA4 to gangliosides on rat basophilic leukemia cells produces changes similar to those seen with Fce receptor activation. J. Cell Biol. 116 (1992) 635-646
37. Palestini P., Pitto M., Tedeschi G., Ferraretto A., Parenti M., Brunner J., and Masserini M. Tubulin anchoring to glycolipid-enriched, detergent-resistant domains of the neuronal plasma membrane. J. Biol. Chem. 276 (2000) 9978-9985
38. Metelmann W., Vukelić Ž., and Peter-Katalinić J. Nano-electrospray ionization time-of-flight mass spectrometry of gangliosides from human brain tissue. J. Mass Spectrom. 36 (2001) 21-29
39. Bremer E.G., Hakomori S., Bowen-Pope D.F., Raines E., and Ross R. Ganglioside-mediated modulation of cell growth, growth factor binding, and receptor phosphorylation. J. Biol. Chem. 259 (1984) 6818-6825
40. Wang X., Sun P., Al-Qamari A., Tai T., Kawashima L., and Paller A.S. Carbohydrate-Carbohydrate binding of ganglioside to integrin alpha(5) modulates alpha(5)beta(1) function. J. Biol. Chem. 276 (2001) 8436-8444
41. Martini F., Riondino S., Pignatelli P., Gazzaniga P.P., Ferroni P., and Lenti L. Involvement of GD3 in platelet activation, a novel association with Fcgamma receptor. Biochem. Biophys. Acta 8 (2002) 297-304
42. 1b. J. Biol. Chem. 264 (1989) 13267-13272
43. Sheets E.D., Holowka D., and Baird B. Membrane organization in immunoglobulin E receptor signaling. Curr. Opin. Chem. Biol. 3 (1999) 95-99
44. Pyenta P.S., Holowka D., and Baird B. Cross-correlation analysis of inner-leaflet-anchored green fluorescent protein co-redistributed with IgE receptors and leaflet lipid raft components. Biophys. J. 80 (2001) 2120-2132
45. Oliver C., Fujimura A., Silveira e Souza A.M.M., Orlandini de Castro R., Siraganian R.P., and Jamur M.C. Mast cell-specific gangliosides and FcepsilonRI follow the same endocytic pathway from lipid rafts in RBL-2H3 cells. J. Histochem. Cytochem. 55 (2007) 315-325
46. Basciano L.K., Berenstein E.H., Kmak L., and Siraganian R.P. Monoclonal antibodies that inhibit IgE binding. J. Biol. Chem. 261 (1986) 11823-11831
47. Swaim W.D., Minoguchi K., Oliver C., Hamawy M.M., Kihara H., Stephan V., Berenstein E.H., and Siraganian R.P. The anti-ganglioside monoclonal antibody AA4 induces protein tyrosine phosphorylations, but not degranulation, in rat basophilic leukemia cells. J. Biol. Chem. 269 (1994) 19466-19473
48. Stephan V., Seibt A., Dukanovic D., Skasa M., Swaim W.D., Berenstein E.H., Siraganian R.P., and Wahn V. Anti-ganglioside monoclonal antibody AA4 selectively inhibits IgE-induced signal transduction pathways in rat basophilic leukemia cells. Mol. Immunol. 34 (1997) 227-235
49. Stracke M.L., Basciano L.K., and Siraganian R.P. Binding properties and histamine release in variants of rat basophilic leukemia cells with changes in the IgE receptor. Immunol. Lett. 14 (1987) 287-292
50. 2+ mobilization and degranulation in mutant RBL mast cells. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 1154-1159
51. Barsumian E.L., Isersky C., Petrino M.G., and Siraganian R.P. IgE-induced histamine release from rat basophilic leukemia cell lines: isolation of releasing and nonreleasing clones. Eur. J. Immunol. 11 (1981) 317-323
52. Sahara N., Siraganian R.P., and Oliver C. Morphological changes induced by the calcium ionophore A23187 in rat basophilic leukemia (2H3) cells. J. Histochem. Cytochem. 38 (1990) 975-983
53. Crespo P.M., Zurita A.R., and Daniotti J.L. Effect of gangliosides on the distribution of a glycosylphosphatidylinositol-anchored protein in plasma membrane from Chinese hamster ovary-K1 cells. J. Biol. Chem. 277 (2002) 44731-44739
54. Radin N.S. Chemotherapy by slowing glucosphingolipid synthesis. Biochem. Pharmacol. 57 (1999) 589-595
55. Fischer P.B., Karlsson G.B., Butters T.D., Dwek R.A., and Platt F.M. N-Butyldeoxynojirimycin-mediated inhibition of human immunodeficiency virus entry correlates with changes in antibody recognition of the V1/V2 region of gp120. J. Virol. 7 (1996) 143-7152
56. Kato N., Nakanishi M., and Hirashima N. Cholesterol depletion inhibits store-operated calcium currents and exocytotic membrane fusion in RBL-2H3 cells. Biochemistry 42 (2003) 11808-11814
57. syk in high affinity IgE receptor signaling. J. Biol. Chem. 268 (1993) 23318-23324
58. Jamur M.C., Grodzki A.C.G., Berenstein E.H., Hamawy M.M., Siraganian R.P., and Oliver C. Identification and characterization of undifferentiated mast cells in mouse bone marrow. Blood 105 (2005) 4282-4289
59. Sada K., Zhang J., and Siraganian R.P. SH2 domain-mediated targeting, but not localization, of Syk in plasma membrane is critical for FceRI signaling. Blood 97 (2001) 1352-1359
60. Schnaar R.L. Isolation of glycosphingolipids. Methods Enzymol. 230 (1994) 348-370
61. Schnaar R.L., and Needham L.K. Thin-layer chromatography of glycosphingolipids. Methods Enzymol. 230 (1994) 371-389
62. Price L.S., Norman J.C., Ridley A.C., and Koffer A. The small GTPases Rac and Rho as regulators of secretion in mast cells. Curr. Biol. 5 (1995) 68-73
63. Norman J.C., Price L.S., Ridley A.J., and Koffer A. The small GTP-binding proteins, Rac and Rho, regulate cytoskeletal organization and exocytosis in mast cells by parallel pathways. Mol. Biol. Cell 7 (1996) 1429-1442
64. 3/calcium pathway in RBL-2H3 mast cells. J. Cell Biol. 148 (2000) 481-493
65. Yamashita T., Yamaguchi T., Murakami K., and Nagasawa S. Detergent resistant membrane domains are required for mast cell activation but dispensable for tyrosine phosphorylation upon aggregation of the high affinity receptor for IgE. J. Biochem. 129 (2001) 861-868
66. Janes P.W., Ley S.C., Magee A.I., and Kabouridis P.S. The role of lipid rafts in T cell antigen receptor (TCR) signaling. Semin. Immunol. 12 (2000) 23-34
67. Langlet C., Bernard A.M., Drevot P., and He H.T. Membrane rafts and signaling by the multichain immune recognition receptors. Curr. Opin. Immunol. 12 (2000) 250-255
68. Janes P.W., Ley S.C., and Magee A.I. Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 147 (1999) 447-461
69. Montixi C., Langlet C., Bernard A.M., Thimonier J., Dubois C., Werrbel M.A., Chauvin J.P., Pierres M., and He H.T. Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J. 17 (1998) 5334-5348
70. Tansey M.G., Baloh R.H., Milbrandt J., and Johnson Jr. E.M. GFRa-mediated localization of RET to lipid rafts is required for effective downstream signaling, differentiation, and neuronal survival. Neuron 25 (2000) 611-623
71. 1b in rat basophilic leukemia RBL-2H3 cells. J. Biol. Chem. 269 (1994) 5249-5254
72. Zhang W., Sloan-Lancaster J., Kitchen J., Trible R.P., and Samelson L.E. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 92 (1998) 83-92
73. Arudchandran R., Brown M.J., Peirce M.J., Song J.S., Zhang J., Siraganian R.P., Blank U., and Rivera J. The Src homology 2 domain of Vav is required for its compartmentation to the plasma membrane and activation of c-jun NH(2)-terminal kinase 1. J. Exp. Med. 191 (2000) 47-60
74. Segal D.M., Taurog J.D., and Metzger H. Dimeric immunoglobulin-E serves as a unit signal for mast cell degranulation. Proc. Natl. Acad. Sci. U .S. A. 74 (1977) 2993-2997
75. Fewtrell C., and Metzger H. Larger oligomers of IgE are more effective than dimers in stimulating rat basophilic leukemia cells. J. Immunol. 125 (1980) 701-710
76. Kihara H., and Siraganian R.P. Src homology 2 domains of Syk and Lyn bind tyrosine-phosphorylated subunits of the high affinity IgE receptor. J. Biol. Chem. 269 (1994) 22427-22432
77. Lin S., Cicala C., Scharenberg A.M., and Kinet J.P. The FceRI b subunit functions as an amplifier of FceRI g mediated cell activation signals. Cell 85 (1996) 985-995
78. Gelfand E.W., and Johnson G.L. Sequential protein kinase activation and the regulation of mast cell cytokine production. Mast Cell and Basophils (2000), Academic Press, San Diego 133-143
79. Beaven M.A., Rogers J., Moore J.P., Smith G.A., Hesketh T.R., and Metcalfe J.C. The mechanisms of the calcium signal and correlation with histamine release in 2H3 cells. J. Biol. Chem. 259 (1984) 7129-7138
80. Furuichi K., Rivera J., and Isersky C. The fate of IgE bound to rat basophilic leukemia cells III relationship between antigen-induced endocytosis and serotonin release. J. Immunol. 133 (1984) 1513-1519
81. Pfeiffer J.R., Seagrave J.C., Davis B.H., Deanin G.G., and Oliver J.M. Membrane and cytoskeletal changes associated with IgE-mediated serotonin release from rat basophilic leukemia cells. J. Cell Biol. 101 (1985) 2145-2155