Selective control of membrane ruffling and actin plaque assembly by the Rho GTPases Rac1 and CDC42 in FcεRI-activated rat basophilic leukemia (RBL-2H3) cells

Journal of Cell Science

Volumn 110, Issue 18, 1997, Pages 2215-2225

  Guillemot, Jean Claude ^a,b   Montcourrier, Philippe ^a,b   Vivier, Eric ^a,b   Davoust, Jean ^a,b   Chavrier, Philippe ^a,b  

^a INSERM   (France)

^b CNRS   (France)

Author keywords

CDC42; Fc RI signalling; Mast cell; Rac1; Rat

Indexed keywords

ACTIN; FC RECEPTOR; GUANOSINE TRIPHOSPHATASE; VINCULIN;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MEMBRANE; DEGRANULATION; LEUKEMIA CELL LINE; MAST CELL; NONHUMAN; PRIORITY JOURNAL; RAT;

ACTINS; ANIMALS; CDC42 GTP-BINDING PROTEIN; CELL ADHESION; CELL CYCLE PROTEINS; CELL MEMBRANE; CELL SIZE; CYTOPLASMIC GRANULES; CYTOSKELETON; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GTP PHOSPHOHYDROLASES; GTP-BINDING PROTEINS; GTPASE-ACTIVATING PROTEINS; LEUKEMIA, BASOPHILIC, ACUTE; MICROSCOPY, ELECTRON, SCANNING; PROTEINS; RATS; RECEPTORS, IGE; SEROTONIN; SIGNAL TRANSDUCTION; TRANSFECTION; TUMOR CELLS, CULTURED; VINCULIN;

EID: 0030846186     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (60)

1. Barker, S. A., Caldwell, K. K., Hall, A., Martinez, A. M., Pfeiffer, J. R., Oliver, J. M. and Wilson, B. S. (1995). Wortmannin blocks lipid and protein kinase activities associated with PI 3-kinase and inhibits a subset of responses induced by Fe epsilon RI cross-linking. Mol. Biol. Cell 6, 1145-1158.
2. Basciano, L. K., Berebstein, E. H., Kmak, L. and Siraganian, R. (1986). Monoclonal antibodies that inhibit IgE binding. J. Biol. Chem. 261, 11823-11831.
3. Beaven, M. A. and Metzger, H. (1993). Signal transduction by Fe receptors: the Fe epsilon RI case. Immunol. Today 14, 222-226.
4. Benhamou, M., Ryba, N. P. J., Kihara, H., Nishikata, H. and Siraganian, R. P. (1993). Protein-tyrosine kinase p72syk in high affinity IgE receptor signaling. J. Biol. Chem. 268, 23318-23324.
5. Brunk, H., Collins, V. P. and Arro, E. (1980). The fixation, dehydration, drying and coating of cultured cells for SEM. J. Microsc. 123, 121-131.
6. Burridge, K. and Mangeat, P. (1984). An interaction between vinculin and talin. Nature 308, 744-746.
7. FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell Biol. 119, 893-903.
8. Gambier, J. C. (1995). Antigen and Fc receptor signaling, the awesome power of the immunoreceptor tyrosine-based activation motif (ITAM). J. Immunol. 154, 3281-3285.
9. Cerione, R. A. and Zheng, Y. (1996). The Dbl family of oncogenes. Curr. Opin. Cell Biol. 8, 216-222.
10. Cox, D., Chang, P., Kurosaki, T. and Greenberg, S. (1996). Syk tyrosine kinase is required for immunoreceptor tyrosine activation motif-dependent actin assembly. J. Biol. Chem. 271, 16597-16602.
11. Crespo, P., Schuebel, K. E., Ostrom, A. A., Gutkind, J. S. and Bustelo, X. R. (1997). Phosphotyrosine-dependent activation of RAc1 GDP/GTP exchange by the vav proto-oncogene product. Nature 285, 169-172.
12. Deanin, G. G., Cutts, J. L., Pfeiffer, J. R. and Oliver, J. M. (1991). Role of isoprenoid metabolism in IgE receptor-mediated signal transduction. J. Immunol. 146, 3528-3535.
13. Deckert, M., Tartare-Deckert, S., Couture, C., Mustelin, T. and Altman, A. (1996). Functional and physical interactions of Syk family kinases with the Vav proto-oncogene product. Immunity 5, 591-604.
14. Dutartre, H., Davoust, J., Gorvel, J. P. and Chavrier, P. (1996) Cytokinesis arrest and redistribution of actin-cytoskeleton regulatory components in cells expressing the rho GTPase CDC42Hs. J. Cell Sci. 109, 367-377.
15. Eiseman, E. and Bolen, J. B. (1992). Engagement of high-affinity IgE receptor activates src protein-related tyrosine kinase. Nature 355, 78-80.
16. Evan, G. I., Lewis, G. K., Ramsay, G. and Bishop, J. M. (1985). Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell Biol. 5, 3610-3616.
17. Fantl, W. J., Escobedo, J. A., Martin, G. A., Turck, C. W., del Rosario, M., McCormick, F. and Williams, L. T. (1992). Distinct phosphotyrosines on a growth factor receptor bind to specific molecules that mediates different signaling pathways. Cell 69, 413-423.
18. Flinn, H. M. and Ridley, A. J. (1996). Rho stimulates tyrosine phosphorylation of focal adhesion kinase, p130 and paxillin. J. Cell Sci. 109, 1133-1141.
19. Fuerst, T. R., Niles, E. G., Studier, E. G. and Moss, B. (1986) Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophages T7 RNA polymerase. Proc. Nat. Acad. Sci. USA 83, 8122-8126.
20. Hall, A. (1994). Small GTP-binding proteins and the regulation of the actin cytoskcleton. Annu. Rev. Cell Biol. 10, 31-54.
21. Hamawy, M. M., Oliver, C., Mergenhagen, S. E. and Siraganian, R. P. (1992). Adherence of rat basophilic leukemia (RBL-2H3) cells to fibronectin-coated surfaces enhances secretion. J. Immunol. 149, 615-621.
22. FAK by the aggregation of high affinity immunoglobulin E receptors requires cell adherence. J. Biol. Chem 268. 6851-6854.
23. Hamawy, M. M., Mergenhagen, S. E. and Siraganian, R. P. (1994a). Adhesion molecules as regulators of mast-cell and basophil function. Immunol. Today 15, 62-66.
24. Hamawy, M. M., Swaim, W. D., Minoguchi, K., de Feijter, A. W., Mergenhagen, S. E. and Siraganian, R. P. (1994b). The aggregation of the high affinity IgE Receptor induces tyrosine phosphorylation of paxillin, a focal adhesion protein. J. Immunol. 153, 4655-4662.
25. Hawkins, P. T., Eguinoa, A., Qiu, R. G., Stokoe, D., Cooke, F. T., Walters, R., Wennström, S., Claesson-Welsh, L., Evans, T., Symons, M. and et al, (1995). PDGF stimulates an increase in GTP-Rac via activation of phosphoinositide 3-kinase. Curr. Biol. 5, 393-403.
26. Heiman, A. S. and Crews, F. T. (1985). Characterization of the effects of phorbol esters on rat mast cells secretion. J. Immunol. 134, 548-555.
27. 2+ and guanine nucleotides in exocytotic secretion from permeabilized rat mast cells. J. Cell Biol. 105, 191-197.
28. Hutchcroft, J. K., Geahlen, R. L., Deanin, G. G. and Oliver, J. M. (1992). FceRI-mediated tyrosine phosphorylation and activation of the 72-kDa protein-tyrosine kinase, FFK72, in RBL-2H3 rat tumor mast cells. Proc. Nat. Acad. Sci. USA 89, 9107-9111.
29. Johnson, R. P. and Craig, S. W. (1995). F-actin binding site masked by the intramolecular association of vinculin head and tail domains. Nature 373, 261-264.
30. Jouvin, M. H., Adamczewski, M., Numerof, R., Letourneur, O., Valle, A. and Kinet, J. P. (1994). Differential control of the tyrosine kinases Lyn and Syk by the two signaling chains of the high affinity immunoglobulin E receptor. J. Biol Chem. 269, 5918-5925.
31. Jouvin, M. H., Numerof, R. P. and Kinet, J. P. (1995). Signal transduction through the conserved motifs of the high affinity IgE receptor Fc epsilon RI. Semin. Immunol. 7, 29-35.
32. Kashishian, A., Kazlauskas, A. and Cooper, J. A. (1992). Phosphorylation sites in the PDGF receptor with different specificities for binding GAP and P13 kinase in vim. EMBO J. 11, 1373-1382.
33. Katzav, S., Sutherland, M., Packham, G., Yi, T. and Weiss, A. (1994) The protein tyrosine kinase ZAP-70 can associate with the SH2 domain of proto-Vav. J. Biol. Chem. 269, 32579-32585.
34. Kihara, H. and Siraganian, R. P. (1994). Src homology 2 domains of Syk and Lyn bind to tyrosine-phosphorylated subunits of the high affinity IgE receptor. J. Biol. Chem. 269, 22427-22432.
35. Koffer, A., Tatham, P. E. and Gomperts, B. D. (1990). Changes in the state of actin during the exocytotic reaction of permeabilized rat mast cells. J. Cell Biol. 111, 919-927.
36. Kozma, R., Ahmed, S., Best, A. and Lim, L. (1995). The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol. Cell Biol. 15, 1942-1952.
37. Lang, P., Gesbert, F., Thiberge, J. M., Troalen, F., Dutartre, H., Chavrier, P. and Bertoglio, J. (1993). Characterization of a monoclonal antibody specific for the Ras-related GTP-binding protein Rho A. Biochem. Biophys. Res. Commun. 196, 1522-1528.
38. Li, W., Deanin, G. G., Margolis, B., Schlessinger, J. and Oliver, J. M. (1992) FceRI-mediated tyrosine phosphorylation of multiple proteins including phospholipase Cg1 and the receptor bg2 complex, in RBL-2H3 rat basophilic leukemia cells. Mol. Cell Biol. 12, 3176-3185.
39. Margolis, B., Hu, P., Katzav, S., Li, W., Oliver, J. M., Ullrich, A., Weiss, A. and Schlessinger, J. (1992) Tyrosine phosphorylation of vav proto-oncogene product containing SH2 domain and transcription factor motifs [see comments]. Nature 356, 71-74.
40. Meresse, S., Gorvel, J. P. and Chavrier, P. (1995) The rab7 GTPase resides on a vesicular compartment connected to lysosomes. J. Cell Sci. 108, 3349-3358.
41. Nobes, C. D., Hawkins, P., Stephens, L. and Hall, A. (1995). Activation of the small GTP-binding proteins rho and rac by growth factor receptors. J. Cell Sci. 108, 225-233.
42. Norman, J. C., Price, L. S., Ridley, A. J., Hall, A. and Koffer, A. (1994) Actin filament organization in activated mast cells is regulated by heterotrimeric and small GTP-binding proteins. J. Cell Biol. 126, 1005-1015.
43. Norman, J. C., Price, L. S., Ridley, A. J. and Koffer, A. (1996). The small GTP-binding proteins. Rac and Rho, regulate cytoskeletal organization and exocytosis in mast cells by parallel pathways. Mol. Biol. Cell 7, 1429-1442.
44. Oliver, J. M., Burg, D. L., Wilson, B. S., McLaughlin, J. L. and Geahlen, R. L. (1994). Inhibition of mast cell Fc epsilon RI-mediated signaling and effector function by the Syk-selective inhibitor, piceatannol. J. Biol. Chem. 269, 29697-29703.
45. Park, D. J., Min, H. K. and Rhee, S. G. (1991). IgE-induccd tyrosine phosphorylation of phospholipase C-gamma 1 in rat basophilic leukemia cells. J. Biol. Chem. 266, 24237-24240.
46. 2+ Influx. J. Biol. Chem. 271, 7883-7886.
47. Pfeiffcr, J. R., Deanin, G. G., Seagrave, J. C., Davis, B. H. and Oliver, J. M. (1985). Membrane and cytoskeletal changes associated with IgE-mediated scrotonin release in rat basophilic leukemia cells. J. Cell Biol. 101, 2145-2155.
48. Pfeiffer, J. R. and Oliver, J. M. (1994). Tyrosine kinase-dependent assembly of actin plaques linking Fc epsilon R1 cross-linking to increased cell substrate adhesion in RBL-2H3 tumor mast cells. J. Immunol. 152, 270-279.
49. Price, L. S., Norman, J. C., Ridley, A. J. and Koffer, A. (1995). The small GTPases Rac and Rho as regulators of secretion in mast cells. Curr. Biol. 5, 68-73.
50. Ridley, A. J. and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
51. Ridley, A. J., Paterson, H. F., Johnston, C. L., Dickmann, D. and Hall, A. (1992). The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70, 401-410.
52. Ridley, A. J. (1994). Membrane ruffling and signal transduction. BioEssays 16, 321-327.
53. Rivera, V. M. and Brugge, J. S. (1995). Clustering of Syk is sufficient to induce tyrosine phosphorylation and release of allergic mediators from rat basophilic leukemia cells. Mol. Cell Biol. 15, 1582-1590.
54. Sinnett-Smith, J., Zachary, I., Valverde, A. M. and Rozengurt, E. (1993) Bombesin stimulation of pp125 focal adhesion kinase tyrosine phosphorylation. J. Biol. Chem. 268, 14261-14268.
55. Turner, C. E., Glenney, J. R. and Burridge, K. (1990). Paxillin-a new vinculin-binding protein present in focal adhesions. J. Cell Biol. 111, 1059-1068.
56. Van Aelst, L., Joneson, T. and Bar-Sagi, U. (1996). Identification of a novel Rac1-interacting protein involved in membrane ruffling. EMBO J. 15, 3778-3786.
57. Vos, J. C. and Stunnenberg, H. G. (1988). Derepression of a novel class of vaccinia virus genes upon DNA replication. EMBO J. 11, 3487-3492.
58. Wennström, S., Hawkins, P., Cooke, F. T., Hara, K., Yonezawa, K., Kasuga, M., Jackson, T., Claesson-Welsh, L. and Stephens, S. (1994) Activation of phosphoinositide 3-kinase is required tor PDGF-stimulated membrane ruffling. Curr. Biol. 4, 385-393.
59. Yano, H., Nakanishi, S., Kimura, K., Hanai, N., Saitoh, Y., Fukui, Y., Nonomura, Y. and Matsuda, Y. (1993). Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBL-2H3 cells. J. Biol. Chem. 268, 25846-25856.
60. Zacharv, I., Sinnett-Smith, J., Turner, C. E. and Rozengurt, E. (1993). Bombesin, vasopressin and endothelin rapidly stimulate tyrosine phosphorylation of the focal adhesion-associated protein paxillin in Swiss3T3 cells. J. Biol. Chem. 268, 22060-22065.