c-kit receptor signaling through its phosphatidylinositide-3'-kinase- binding site and protein kinase C: Role in mast cell enhancement of degranulation, adhesion, and membrane ruffling

Molecular Biology of the Cell

Volumn 8, Issue 5, 1997, Pages 909-922

  Vosseller, Keith ^a,b   Stella, Gregory ^a,b   Yee, Nelson S ^d   Besmer, Peter ^a,c  

^a Weill Cornell Graduate School of Biomedical Sciences   (United States)

^b HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d NONE

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CALCIUM ION; MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; STEM CELL FACTOR RECEPTOR;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BINDING SITE; CALCIUM CELL LEVEL; CELL ADHESION; CELL MEMBRANE; CONTROLLED STUDY; CYTOSKELETON; MAST CELL DEGRANULATION; MEMBRANE STRUCTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0030918253     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.8.5.909     Document Type: Article

References (70)

1. Arcaro, A., and Wymann, M.P. (1993). Wortmannin is a potent phosphatidylinositol 3-kinase inhibitor: the role of phosphatidylinositol 3,4,5-trisphosphate in neutrophil responses. Biochem. J. 296, 97-301.
2. 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 Fc∈RI cross-linking. Mol. Biol. Cell 6, 1145-1158.
3. Bennett, J.P., Cockcroft, S., and Gomperts, B.D. (1979). Ionomycin stimulates mast cell histamine secretion by forming a lipid-soluble calcium complex. Nature 282, 851-853.
4. Bischoff, S.C., and Clemens, D.A. (1992). c-kit ligand: a unique potentiator of mediator release by human lung mast cells. J. Exp. Med. 175, 237-244.
5. Blume-Jensen, P., Claesson-Welsh, L., Siegbahn, A., Zsebo, K.M., Westermark, B., and Heldin, C.H. (1991). Activation of the human c-kit product by ligand-induced dimerization mediates circular actin reorganization and chemotaxis. EMBO J. 10, 4121-4128.
6. Blume-Jensen, P., Ronnstrand, L., Gout, I., Waterfield, M.C., and Heldin, C.H. (1994). Modulation of Kit/Stem cell factor receptor-induced signaling by protein kinase C. J. Biol. Chem. 269, 21793-21802.
7. Blume-Jensen, P., Siegbahn, A., Stabel, S., Heldin, C.H., and Ronnstrand, L. (1993). Increased Kit/SCF receptor induced mitogenicity but abolished cell motility after inhibition of protein kinase C. EMBO J. 12, 4199-4209.
8. Bonnema, J.K., Karnitz, L.M., Schoon, R.A., Abraham, R.T., and Leibson, P.J. (1994). Fc receptor stimulation of phosphatidylinositol 3-kinase in natural killer cells is associated with protein kinase C-independent granule release and cell-mediated cytotoxicity. J. Exp. Med. 180, 1427-1435.
9. Brunn, G.J., Williams, J., Sabers, C., Wiederrecht, G., Lawrence, J.C., Jr., and Abraham, R.T. (1996). Direct inhibition of the signaling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002. EMBO J. 15, 5256-5267.
10. Burgering, B.M., and Coffer, P.J. (1995). Protein kinase B (C-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376, 599-602.
11. Chakravarty, N., Kjeldsen, B., Hansen, M., and Nielsen, E.H. (1990). The involvement of protein kinase C in exocytosis in mast cells. Exp. Cell Res. 186, 245-249.
12. Cheatham, B., Vlahos, C.J., Cheatham, L., Wang, L., Blenis, J., and Kahn, C.R. (1994). Phosphatidylinositol 3-kinase activation is required for insulin stimulation of Pp70 S6 kinase, DNA synthesis, and glucose transporter translocation. Mol. Cell. Biol. 14, 4902-4911.
13. Chung, J., Grammer, T.C., Lemon, K.P., Kazlauskas, A., and Blenis, J. (1994). PDGF-and insulin-dependent pp70S6K activation mediated by phosphatidylinositol-3-OH kinase. Nature 370, 71-75.
14. Coleman, J., Holliday, M.R., Kimber, I., Zsebo, K.M., and Galli, S.J. (1993). Regulation of mouse peritoneal mast cell secretory function by stem cell factor, IL-3 or IL-4. J. Immunol. 150, 556-562.
15. Coleman, J.W., Buckley, M.G., Holliday, M.R., and Morris, A.G. (1991). Interferon-γ inhibits serotonin release from mouse peritoneal mast cells. Eur. J. Immunol. 21, 2559-2564.
16. Condeelis, J., and Hall, A.L. (1991). Measurement of actin polymerization and cross-linking in agonist stimulated cells. Methods Enzymol., 196, 486-496.
17. Cooper, J.A. (1987). Effects of cytochalasin and phalloidin on actin. J. Cell Biol. 105, 1473-1478.
18. Dastych, J., and Metcalfe, D.D. (1994). Stem cell factor induces mast cell adhesion to fibronectin. J. Immunol. 152, 213-219.
19. Downey, G.P., Chan, C.K., Lea, P., Takei, A., and Grinstein, S. (1992). Phorbol ester-induced actin assembly in neutrophils: role of protein kinase C. J. Cell Biol. 116, 695-706.
20. Hartley, K.O., et al. (1995). DNA dependent protein kinase catalytic subunit: a relative of phosphatidylinositol 3-kinase and the ataxia telangiectasia gene product. Cell 82, 849-865.
21. Karasuyama, H., and Melchers, F. (1988). Establishment of mouse cell lines which constitutively secrete large quantities of interleukin 2, 3, 4 or 5, using modified cDNA expression vectors. Eur. J. Immunol. 18, 97-104.
22. Kinashi, T., and Springer, T.A. (1994). Steel factor and c-kit regulate cell-matrix adhesion. Blood 83, 1033-1038.
23. v mice and their increase by bone marrow transplantation. Blood 52, 447-452.
24. Kobayashi, E., Nakano, H., Morimoto, and Tamaoki, M., T. (1989). Calphostin C (UCN-1028C), a novel microbial compound, is a highly potent and specific inhibitor of protein kinase C. Biochem. Biophys. Res. Commun. 159, 548-553.
25. Koffer, A., Tatham, E.R., 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.
26. Koopmann, R., Jr., and Jackson, R.C. (1990). Calcium-and guanine-nucleotide-dependent exocytosis in permeabilized rat mast cells. Biochem. J. 265, 365-373.
27. Kotani, K., et al. (1994). Involvement of phosphoinositide 3-kinase in insulin-or IGF-induced membrane ruffling. EMBO J. 13, 2313-2321.
28. 1 integrins expressed on hematopoietic cell lines. Blood 85, 159-167.
29. Kovacsovics, T.J., Bachelot, C., Toker, A., Vlahos, C.J., Duckworth, B., Cantley, L.C., and Hartwig, J.H. (1995). Phosphoinositide 3-kinase inhibition spares actin assembly in activating platelets but reverses platelet aggregation. J. Biol. Chem. 270, 11358-11366.
30. Lev, S., Givol, D., and Yarden, Y. (1991). A specific combination of substrates is involved in signal transduction by the kit-encoded receptor. EMBO J. 10, 647-654.
31. Lindau, M., and Gomperts, B.D. (1991). Techniques and concepts in exocytosis. Biochim. Biophys. Acta 1071, 429-471.
32. Meininger, C.J., Yano, H., Rottapel, R., Bernstein, A., Zsebo, K.M., and Zetter, B.R. (1992). The c-kit receptor ligand functions as a mast cell chemoattractant. Blood 79, 958-963.
33. Monfar, M., Lemon, K.P., Grammer, T.C., Cheatham, L., Chung, J., Vlahos, C.J., and Blenis, J. (1995). Activation of Pp70/85 S6 kinases in interleukin-2-responsive lymphoid cells is mediated by phosphatidylinositol 3-kinase and inhibited by cyclic AMP. Mol. Cell. Biol. 15, 326-337.
34. Nakanishi, H., Brewer, K.A., and Exton, J.H. (1993). Activation of the isozyme of protein kinase C by phosphatidylinositol 3,4,5,-triphosphate. J. Biol. Chem. 268, 13-16..
35. Nakanishi, S., Catt, K.J., and Balla, T. (1995). A wortmannin-sensitive phosphatidylinositol 4-kinase that regulates hormone-sensitive pools of inositol phospholipids. Proc. Natl. Acad. Sci. USA 92, 5317-5321.
36. Nocka, K., Buck, J., Levi, E., and Besmer, P. (1990). Candidate ligand for the c-kit transmembrane kinase receptor: KL, a fibroblast derived growth factor stimulates mast cells and erythroid progenitors. EMBO J. 9, 3287-3294.
37. Okada, T., Kawano, Y., Sakakibar, T., Hazeki, O., and Ui, M. (1994). Essential role of phosphatidylinositol 3-kinase in insulin-induced glucose transport and antilipolysis in rat adipocytes. J. Biol. Chem. 269, 3568-3573.
38. 2+-independent isozymes of protein kinase C mediate exocytosis in antigen-stimulated rat basophilic RBL-2H3 cells. J. Biol. Chem. 268, 1749-1756.
39. Pfeiffer, J.R., and Oliver, J.M. (1994). Tyrosine kinase-dependent assembly of actin plaques linking Fc∈RI cross-linking to increased cell substrate adhesion in RBL-2H3 tumor mast cells. J. Immunol. 152, 270-279.
40. Pfeiffer, J.R., Seagrave, J.C., Davis, B.H., Deanin, G.G., and Oliver, J.M. (1985). Membrane and cytoskeletal changes associated with IgE-mediated serotonin release from rat basophilic leukemia cells. J. Cell Biol. 101, 2145-2155.
41. Pleiman, C.M., Hertz, W.M., and Cambier, J.C. (1994). Activation of phosphatidylinositol-3′ kinase by src-family kinase SH3 binding to the p85 subunit. Science 263, 1609-1612.
42. 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, 8-73.
43. Reith, A.D., Ellis, C., Lyman, S.D., Anderson, D.M., Williams, D.E., Bernstein, A., and Pawson, T. (1991). Signal transduction by normal isoforms and W mutant variants of the Kit receptor tyrosine kinase. EMBO J. 10, 2451-2459.
44. Ridley, A.J., and Hall, A. (1992). Distinct patterns of actin organization regulated by the small GTP-binding proteins rac and rho. Cold Spring Harbor Symp. Quant. Biol. 57, 61-671.
45. Rottapel, R., Reedijk, M., Williams, D.E., Lyman, S.D., Anderson, D.M., Pawson, T., and Bernstein, A. (1991). The Steel/W transduction pathway: Kit autophosphorylation and its association with a unique subset of cytoplasmic signaling proteins is induced by the steel factor. Mol. Cell. Biol. 11, 3043-3051.
46. Salim, K., et al. (1996). Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton's tyrosine kinase. EMBO J. 15, 6241-6250.
47. Serve, H., Hsu, Y., and Besmer, P. (1994). Tyrosine residue 719 of the c-kit receptor is essential for binding of the P85 subunit of phosphatidylinositol(PI) -kinase and for c-kit-associated PI 3-Kinase activity in COS-1 cells. J. Biol. Chem. 269, 6026-6030.
48. Serve, H., Yee, N.S., Stella, G., Sepp-Lerenzino, L., Tan, J.C., and Besmer, P. (1995). Differential roles of PI-3 kinase and Kit tyrosine 821 in Kit receptor-mediated proliferation, survival and cell adhesion in mast cells. EMBO J. 14, 473-483.
49. Sham, R.L., Packman, C.H., Abboud, C.N., and Lichtman, M.A. (1991). Signal transduction and the regulation of actin conformation during myeloid maturation studies in HL60 cells. Blood 77, 363-370.
50. Shimizu, Y., Mobley, J.L., Finkelstein, L.D., and Chan, A.S. (1995). A role for phosphatidylinositol 3-kinase in the regulation of beta 1 integrin activity by the CD2 antigen. J. Cell Biol. 131, 1867-1880.
51. Stack, J.H., and Emr, S.D. (1994). Vps34p required for yeast vacuolar protein sorting is a multiple specificity kinase that exhibits both protein kinase and phosphatidylinositol-specific PI 3-kinase activities. J. Biol. Chem. 269, 31552-31562.
52. Stack, J.H., Herman, P.K., Schu, P.V., and Emr, S.D. (1993). A membrane-associated complex containing the Vps15 protein kinase and the Vps34 PI 3-kinase is essential for protein sorting to the yeast lysosome-like vacuole. EMBO J. 12, 2195-2204.
53. Stossel, T.P. (1993). On the crawling of animal cells. Science 260, 1086-1094.
54. Tang, B., Mano, Yi, H., T., and Ihle, J.N. (1994). Tec kinase associates with c-kit and is tyrosine phosphorylated and activated following stem cell factor binding. Mol. Cell. Biol. 14, 8432-8437.
55. Tauchi, T., Feng, G.S., Marshall, M.S., Shen, R., Mantel, C., Pawson, T., and Broxmeyer, H.E. (1994). The ubiquitously expressed syp phosphatase interacts with c-kit and Grb2 in hematopoietic cells. J. Biol. Chem. 269, 25206-25211.
56. 3. J. Biol. Chem. 269, 32358-32367.
57. rsk and pp70S6 kinases in mouse mast cells by signaling through the c-kit receptor tyrosine kinase or Fc∈RI: rapamycin inhibits activation of pp70-S6 kinase and proliferation in mouse mast cells. Eur. J. Immunol. 23, 3286-3291.
58. Tsai, M., Takeishi, T., Thompson, H., Langley, K.E., Zsebo, K.M., Metcalfe, D.D., Geissler, E.N., and Galli, S.J. (1991). Induction of mast cell proliferation, maturation, and heparin synthesis by the rat c-kit ligand, stem cell factor. Proc. Natl. Acad. Sci. USA 88, 6382-6386.
59. Tsuji, K., et al. (1990). Effects of interleukin-3 and interleukin-4 on the development of connective tissue-type mast cells. Blood 75, 421-429.
60. Vlahos, C.J., Matter, W.F., Hui, K.Y., and Brown, R.F. (1994). A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269, 5241-5248.
61. Wennstrom, S., Hawkinsm P., Cooke, F., Hara, K., Yonezawa, K., Kasuga, M., Jackson, T., Claesson-Welsh, L., and Stephens, L. (1994). Activation of phosphoinositide 3-kinase is required for PDGF-stimulated membrane ruffling. Curr. Biol. 4, 385-393.
62. Wershil, B.K., Tsai, M., Geissler, E.N., Zsebo, K.M., and Galli, S.J. (1992). The rat c-kit ligand, stem cell factor, induces c-kit receptor-dependent mouse mast cell activation in vivo: evidence that signaling through the c-kit receptor can induce expression of cellular function. J. Exp. Med. 175, 245-255.
63. Wershil, B.K., Wang, Z.S., and Galli, S.J. (1991). Recruitment of neutrophils during IgE-dependent cutaneous late phase responses in the mouse is mast cell dependent: partial inhibition of the reaction with antiserum against tumor necrosis factor-alpha. J. Clin. Invest. 87, 446-453.
64. Wu, C., Keivens, V.M., O'Toole, T.E., McDonald, J.A., and Ginsberg, M.H. (1995). Integrin activation and cytoskeletal interaction are essential for the assembly of a fibronectin matrix. Cell 83, 715-724.
65. Yamanashi, Y., Fukui, Y., Wongsasant, W., Kinoshita, Y., Ichimori, Y., Toyoshima, K., and Yamamoto, T. (1992). Activation of Src-like protein tyrosine kinase lyn and its association with phosphatidylinositol 3-kinase upon B-cell antigen receptor-mediated signaling. Proc. Natl. Acad. Sci. USA 89, 1118-1122.
66. 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.
67. Yee, N.S., Hsiau, M.C., Serve, H., Vosseller, K., and Besmer, P. (1994). Mechanism of down-regulation of c-kit receptor. J. Biol. Chem. 269, 31991-31998.
68. Yee, N.S., Paek, I., and Besmer, P. (1994). Role of kit-ligand in proliferation and suppression of apoptosis in mast cells: basis for radiosensitivity of white spotting and steel mutant mice. J. Exp. Med. 179, 1777-1787.
69. Yi, T., and Ihle, J.N. (1993). Association of hematopoietic cell phosphatase with c-kit after stimulation with c-kit ligand. Mol. Cell. Biol. 13, 3350-3358.
70. Zhang, Y., Ramos, B.F., and Jakschik, B.A. (1991). Augmentation of reverse arthus reaction by mast cells in mice. J. Clin. Invest. 88, 841-846.