Phosphatidylinositol 3-kinase is required for integrin-stimulated AKT and Raf-1/mitogen-activated protein kinase pathway activation

Molecular and Cellular Biology

Volumn 17, Issue 8, 1997, Pages 4406-4418

  King, Warren G ^a   Mattaliano, Mark D ^a   Chan, Tung O ^b   Tsichlis, Philip N ^b   Brugge, Joan S ^a  

^a ARIAD PHARMACEUTICALS INC   (United States)

^b FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ENZYME INHIBITOR; FIBRONECTIN; FOCAL ADHESION KINASE; GUANOSINE TRIPHOSPHATE; INTEGRIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN SERINE THREONINE KINASE; RAF PROTEIN; RAS PROTEIN; WORTMANNIN;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL SPREADING; CELL STRAIN COS1; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; FIBROBLAST; MUTAGENESIS; NONHUMAN; PHOSPHOINOSITIDE METABOLISM; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0030839766     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.8.4406     Document Type: Article

References (101)

1. Akimoto, K., R. Takahashi, S. Moriya, N. Nishioka, J. Takayanagi, K. Kimura, Y. Fukui, S. Osada, K. Mizuno, S. Hirai, A. Kazlauskas, and S. Ohno. 1996. EGF or PDGF receptors activate atypical PKCλ through phosphatidylinositol 3-kinase. EMBO J. 15:788-798.
2. Alessi, D. R., P. Cohen, A. Ashworth, S. Cowley, S. J. Leevers, and C. J. Marshall. 1995. Assay and expression of mitogen-activated protein kinase, MAP kinase kinase, and raf. Methods Enzymol. 255:279-290.
3. Attar, R. M., and M. Z. Gilman. 1992. Expression cloning of a novel zinc finger protein that binds to the c-fos serum response element. Mol. Cell. Biol. 12:2432-2443.
4. Auger, K. R., L. A. Serunian, S. P. Soltoff, P. Libby, and L. Cantley. 1989. PDGF-dependent tyrosine phosphorylation stimulates production of novel phosphoinositides in intact cells. Cell 57:167-175.
5. Burgering, B. M. T., and P. J. Coffer. 1995. Protein kinase B (c-akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature (London) 376:599-602.
6. Cai, H., U. Smola, V. Wixler, I. Eisenmann-Tappe, M. T. Diaz-Meco, J. Moscat, U. Rapp, and G. M. Cooper. 1997. Role of diacylglycerol-regulated protein kinase C isotypes in growth factor activation of the Raf-1 protein kinase. Mol. Cell. Biol. 17:732-741.
7. Carpenter, C. L., K. R. Auger, M. Chanudhuri, M. Yoakim, B. Schaffhausen, S. Shoelson, and L. C. Cantley. 1993. Phosphoinositide 3-kinase is activated by phosphopeptides that bind to the SH2 domains of the 85-kDa subunit. J. Biol. Chem. 268:9478-9483.
8. Carter, A. N., and C. P. Downes. 1992. Phosphatidylinositol 3-kinase is activated by nerve growth factor and epidermal growth factor in PC12 cells. J. Biol. Chem. 267:14563-14567.
9. Carter, A. N., R. Huang, A. Sorisky, C. P. Downes, and S. E. Rittenhouse. 1994. Phosphatidylinositol 3,4,5-trisphosphate is formed from phosphatidylinositol 4,5-bisphosphate in thrombin-stimulated platelets. Biochem. J. 301:415-420.
10. Chen, H.-C., P. A. Appeddu, H. Isoda, and J.-L. Guan. 1996. Phosphorylation of tyrosine 397 in focal adhesion kinase is required for binding of phosphatidylinositol 3-kinase. J. Biol. Chem. 271:26329-26334.
11. Chen, H.-C., and J.-L. Guan. 1994. Association of focal adhesion kinase with its potential substrate phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 91:10148-10152.
12. Chen, Q., M. S. Kinch, T. H. Lin, K. Burridge, and R. L. Julian. 1994. Integrin-mediated cell adhesion activates mitogen-activated protein kinases. J. Biol. Chem. 269:26602-26605.
13. Chen, Q., T. H. Lin, C. J. Der, and R. L. Juliano. 1996. Integrin-mediated activation of mitogen-activated protein (MAP) or extracellular signal-related kinase kinase (MEK) and kinase is independent of Ras. J. Biol. Chem. 271:18122-18127.
14. Chong, L. D., A. Traynor-Kaplan, G. M. Bokoch, and M. A. Schwartz. 1994. The small GTP-binding protein Rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells. Cell 79:507-513.
15. Chun, J. S., M. J. Ha, and B. S. Jacobson. 1996. Differential translocation of protein kinase C epsilon during HeLa cell adhesion to gelatin substratum. J. Biol. Chem. 271:13008-13012.
16. Chun, J. S., and B. S. Jacobson. 1993. Requirement for diacylglycerol and protein kinase C in HeLa cell-substratum adhesion and their feedback amplification of arachidonic acid production for optimum cell spreading. Mol. Biol. Cell 4:271-281.
17. Clark, E. A., and J. S, Brugge. 1995. Integrins and signal transduction pathways: the road taken. Science 268:233-239.
18. Clark, E. A., and R. O. Hynes. 1996. Ras activation is necessary for integrin-mediated activation of extracellular signal-regulated kinase 2 and cytosolic phospholipase A2 but not for cytoskeletal organization. J. Biol. Chem. 271:14814-14818.
19. Cowen, D. S., R. S. Sowers, and D. R. Manning. 1996. Activation of a mitogen-activated protein kinase (ERK-2) by the 5-hydroxytryptamine 1A receptor is sensitive not only to inhibitors of phosphatidylinositol 3-kinase, but to an inhibitor of phosphatidylcholine hydrolysis. J. Biol. Chem. 271: 22297-22300.
20. Cross, D. A. E., D. R. Alessi, J. R. Vandenheede, H. E. McDowell, H. S. Hundal, and P. Cohen. 1994. The inhibition of glycogen synthase kinase-3 by insulin or insulin-like growth factor 1 in the rat skeletal muscle cell line L6 is blocked by wortmannin, but not by rapamycin: evidence that wortmannin blocks activation of the mitogen-activated protein kinase pathway in L6 cells between Ras and Raf. Biochem. J. 303:21-26.
21. DePaolo, D., J. E.-B. Reusch, K. Carel, P. Bhuripanyo, J. W. Leitner, and B. Draznin. 1996. Functional interactions of phosphatidylinositol 3-kinase with GTPase-activating protein in 3T3-L1 adipocytes. Mol. Biol. Cell 16: 1450-1457.
22. Dhand, R., K. Hara, I. Hiles, B. Bax, I. Gout, G. Panayotou, M. J. Fry, K. Yonezawa, M. Kasuga, and M. D. Waterfield. 1994. PI 3-kinase: structural and functional analysis of intersubunit interactions. EMBO J. 13:511-521.
23. Dudek, H., R. D. Sandeep, T. F. Franke, M. J. Birnbaum, R. Yao, G. M. Cooper, R. A. Segal, D. R. Kaplan, and M. E. Greenberg. 1997. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275:661-664.
24. Escobedo, J. A., S. Navankasattusas, W. M. Kavanaugh, D. Milfay, V. A. Fried, and L. T. Williams. 1991. cDNA cloning of a novel 85 kd protein that has SH2 domains and regulates binding of PI 3-kinase to the PDGF β-receptor. Cell 65:75-82.
25. Fantl, W. J., J. A. Escobedo, G. A. Martin, C. W. Turck, M. Del Rosario, F. McCormick, and L. T. Williams. 1992. Distinct phosphotyrosines on a growth factor receptor bind to specific molecules that mediate different signaling pathways. Cell 69:413-423.
26. Franke, T. F., D. R. Kaplan, L. C. Cantley, and A. Toker. 1997, Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science 275:665-628.
27. Franke, T. F., S. I. Yang, T. O. Chan, K. Datta, A. Kazlauskas, D. K. Morrison, D. R. Kaplan, and P. N. Tsichlis. 1995. The protein kinase encoded by the AKT proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81:727-736.
28. Frisch, S. M., and H. Francis. 1994. Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 124:619-626.
29. Fukami, K., K. Furuhashi, M. Inagaki, T. Endo, S. Hatano, and T. Takenawa. 1992. Requirement of phosphatidylinositol 4,5-bisphosphate for alpha-actinin function. Nature (London) 359:150-152.
30. Gironcel, D., C. Racaud-Sultan, B. Payrastre, M. Haricot, G. Borchet, N. Kieffer, M. Breton, and H. Chap. 1996. AlphaIIb-beta 3-integrin mediated adhesion of human platelets to a fibrinogen matrix triggers phospholipase C activation and phosphatidylinositol 3′,4′-bisphosphate accumulation. FEBS Lett. 389:253-256.
31. Hartwig, J. H., G. M. Bokoch, C. L. Carpenter, P. A. Janmey, L. A. Taylor, A. Toker, and T. P. Stossel. 1995. Thrombin receptor ligation and activated Ras uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets. Cell 82:643-653.
32. Hartwig, J. H., S. Kung, T. Kovacsovics, P. A. Janmey, L. C. Cantley, T. P. Stossel, and A. Toker. 1996. D3 phosphoinositides and outside-in integrin signaling by glycoprotein IIb-IIIa mediate platelet actin assembly and filopodial extension induced by phorbol 12-myristate 13-acetate. J. Biol. Chem. 271:32986-32993.
33. Hawes, B. E., L. M. Luttrell, T. Van Biesen, and R. J. Lefkowitz. 1996. Phosphatidylinositol 3-kinase is an early intermediate in the G-beta gamma-mediated mitogen-activated protein kinase signaling pathway. J. Biol. Chem. 271:12133-12136.
34. 3, by osteopontin stimulates phosphatidylinositol 3-hydroxyl kinase activity. Ann. N. Y. Acad. Sci. 760:151-165.
35. Hu, Z. W., X. Y. Shi, R. Z. Lin, and B. B. Hoffman. 1996. Alpha1 adrenergic receptors activate phosphatidylinositol 3-kinase in human vascular smooth muscle cells. Role in mitogenesis. J. Biol. Chem. 271:8977-8982.
36. c-src in human platelets. J. Biol. Chem. 269:27093-27099.
37. James, S. R., C. P. Downes, R. Gigg, S. J. Grove, A. B. Holmes, and D. R. Alessi. 1996. Specific binding of the AKT-1 protein kinase to phosphatidylinositol 3,4,5-trisphosphate without subsequent activation. Biochem. J. 315: 709-713.
38. Janmey, P. A., and T. P. Stossel. 1989. Gelsolin-polyphosphoinositide interaction. Full expression of gelsolin-inhibiting function by polyphosphoinositides in vesicular form and inactivation by dilution, aggregation, or masking of the inositol head group. J. Biol. Chem. 264:4825-4831.
39. Janmey, P. A., and T. P. Stossel. 1987. Modulation of gelsolin function by phosphatidylinositol 4,5-bisphosphate. Nature (London) 325:362-364.
40. Juliano, R. L., and S. Haskill. 1993. Signal transduction from the extracellular matrix. J. Cell Biol. 120:577-585.
41. Karnitz, L. M., L. A. Burns, S. L. Sutor, J. Blenis, and R. T. Abraham. 1995. Interleukin-2 triggers a novel phosphatidylinositol 3-kinase-dependent MEK activation pathway. Mol. Cell. Biol. 15:3049-3057.
42. Kauffmann-Zeh, A., P. Rodriquez-Vicana, E. Ulrich, P. Coffer, J. Downward, and G. Evan. 1996. Suppression of c-Myc-induced apoptosis by Ras signaling through PI(3)K and PKB. Nature (London) 385:544-548.
43. Kazlauskas, A., and J. A. Cooper. 1990. Phosphorylation of the PDGF receptor beta subunit creates a tight binding site for phosphatidylinositol 3 kinase. EMBO J. 9:3279-3286.
44. Kennedy, S. G., A. J. Wagner, S. D. Conzen, J. Jordan, A. Bellacosa, P. N. Tsichlis, and N. Hay. 1997. The PI 3-kinase/akt signaling pathway delivers an anti-apoptotic signal. Genes Dev. 11:701-713.
45. Klempke, R. L., A. Cai, A. L. Gianni, P. J. Gallagher, P. DeLaneroller, and D. A. Cheresh. 1997. Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol. 137:481-492.
46. Klippel, A., J. A. Escobedo, Q. Hu, and L. T. Williams. 1993. A region of the 85-kilodalton (kDa) subunit of phosphatidylinositol 3-kinase binds the 110-KDa catalytic subunit in vivo. Mol. Cell Biol. 13:5560-5566.
47. Klippel. A., W. M. Kavanaugh, D. Pot, and L. T. Williams. 1997. A specific product of phosphatidylinositol 3-kinase directly activates the protein kinase Akt through its pleckstrin homology domain. Mol. Cell. Biol. 17:338-344.
48. Klippel, A., C. Reinhard, W. M. Kavanaugh, G. Apell, M.-A. Escobedo, and L. T. Williams. 1996. Membrane localization of phosphatidylinositol 3-kinase is sufficient to activate multiple signal-transducing kinase pathways. Mol. Cell. Biol. 16:4117-4127.
49. Knall, C., S. Young, J. A. Nick, A. M. Buhl, G. S. Worthen, and G. L. Johnson. 1996. Interleukin-8 regulation of the ras/raf/mitogen-activated protein kinase pathway in human neutrophils. J. Biol. Chem. 271:2832-2838.
50. Kolch, W., G. Heidecker, G. Kochs, R. Hummel, H. Vahidi, H. Mischak, G. Finkenzeller, D. Marme, and U. R. Rapp. 1993. Protein kinase C alpha activates Raf-1 by direct phosphorylation. Nature (London) 364:249-252.
51. Kotani, K., K. Yonezawa, K. Kara, H. Ueda, Y. Kitamura, H. Sakaue, A. Ando, A. Chavanieu, B. Calas, F. Grigorescu, M. Nishiyama, M. D. Waterfield, and M. Kasuga. 1994. Involvement of phosphoinositide 3-kinase in insulin-or IGF-1-induced membrane ruffling. EMBO J. 13:2313-2321.
52. Kucera, G. L., and S. E. Rittenhouse. 1990. Human platelets form 3-phosphorylated phosphoinositides in response to α-thrombin, U46619, or GTPγS. J. Biol. Chem. 265:5345-5348.
53. Kunkel, T. A., J. D. Roberts, and R. A. Zakour. 1987. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154:367-382.
54. Leevers, S. J., H. F. Paterson, and C. J. Marshall. 1994. Requirement for ras in rat activation is overcome by targeting raf to the plasma membrane. Nature (London) 369:411-414.
55. Liscovitch, M., and L. C. Cantley. 1994. Lipid second messengers. Cell 77:329-334.
56. Lofgren, R., J. Ng-Sikorski, A. Sjolander, and T. Andersson. 1993, beta2 Integrin engagement triggers actin polymerization and phosphatidylinositol triphosphate formation in non-adherent human neutrophils. J. Cell Biol. 123:1597-1605.
57. Macdonald, S. G., C. M. Crews, L. Wu, J. Driller, R. Clark, R. L. Erikson, and F. McCormick. 1993. Reconstitution of the Raf-1-MEK-ERK signal transduction pathway in vitro. Mol. Cell. Biol. 13:6615-6620.
58. Marais, R., Y. Light, H. F. Paterson, and C. J. Marshall. 1995. Ras recruits raf-1 to the plasma membrane for activation by tyrosine phosphorylation. EMBO J. 14:3136-3145.
59. McNamee, H. P., D. E. Ingber, and M. A. Schwartz. 1993. Adhesion to fibronectin stimulates inositol lipid synthesis and enhances PDGF-induced inositol lipid breakdown. J. Cell Biol 121:673-678.
60. Miyamoto, S., H. Teramoto, J. S. Gutkind, and K. M. Yamada. 1996. Integrins can collaborate with growth factors for phosphorylation of receptor tyrosine kinases and MAP kinase activation: roles of integrin aggregation and occupancy of receptors. J. Cell Biol. 135:1633-1642.
61. Nakamura, S., and Y. Nishizuka. 1994. Lipid mediators and protein kinase C activation for the intracellular signaling network. J. Biochem. 115:1029-1034.
62. Nakanishi, H., K. A. Brewer, and J. H. Exton. 1993. Activation of the ζ isozyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 268:13-16.
63. Niggli, V., and M. Gimona. 1993. Evidence for a ternary interaction between alpha-actinin, (meta)vinculin and acidic-phospholipid bilayers. Eur. J. Biochem. 213:1009-1015.
64. Nishioka, N., S. Hirai, K. Mizuno, S. Osada, A. Suzuki, K. Kosaka, and S. Ohno. 1995. Wortmannin inhibits the activation of MAP kinase following vasopressin V1 receptor stimulation. FEBS Lett. 377:393-398.
65. Otsu, M., I. Hiles, I. Gout, M. J. Fry, F. Ruiz-Larrea, G. Panayotou, A. Thompson, R. Dhand, J. Hsuan, N. Totty, A. D. Smith, S. J. Morgan, S. A. Courtneidge, P. J. Parker, and M. D. Waterfield. 1991. Characterization of two 85 kd proteins that associate with receptor tyrosine kinases, middle-T/ pp60c-src complexes, and PI 3-kinase. Cell 65:91-104.
66. Rankin, S., R. Hooshmand-Radi, L. Claesson-Welsh, and E. Rozengurt. 1996. Requirement for phosphatidylinositol 3′-kinase activity in platelet-derived growth factor-stimulated tyrosine phosphorylation of p 125 focal adhesion kinase and paxillin. J. Biol. Chem. 271:7829-7834.
67. Reuter, C. W. M., A. D. Catling, and M. J. Weber. 1995. Immune complex kinase assays for mitogen-activated protein kinase and MEK. Methods Enzymol. 255:245-256.
68. Ridley, A. J., and A. Hall. 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.
69. Roche, S., M. Koegl, and S. A. Courtneidge. 1994. Phosphatidylinositol 3-kinase is required for DNA synthesis by some, but not all, growth factors. Proc. Natl. Acad. Sci. USA 91:9185-9189.
70. Rodriquez-Viciana, P., P. H. Warne, R. Dhand, B. Vanhaesebroeck, I. Gout, M. J. Fry, M. D. Waterfield, and J. Downward. 1994. Phosphatidylinositol-3-OH kinase as a direct target of ras. Nature (London) 370:527-532.
71. Rodriquez-Viciana, P., P. H. Warne, B. Vanhaesebroeck, M. D. Waterfield, and J. Downward. 1996. Activation of phosphoinositide 3-kinase by interaction with ras and by point mutation. EMBO J. 15:2442-2451.
72. Ruoslahti, E., and J. C. Reed. 1994. Anchorage dependence, integrins, and apoptosis. Cell 77:477-478.
73. Saito, Y., S. Mori, K. Yokote, T. Kanzaki, Y. Saito, and N. Morisaki. 1996. Phosphatidylinositol 3-kinase is required for the activation process of focal adhesion kinase by platelet-derived growth factor receptor. Biochem. Biophys. Res. Commun. 224:23-26.
74. Schaller, M. D., C. A. Borgman, B. S. Cobb. R. R. Vines, A. B. Reynolds, and J. T. Parsons. 1992. pp125FAK, a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc. Natl. Acad. Sci. USA 89:5192-5196.
75. Schaller, M. D., and J. T. Parsons. 1994. Focal adhesion kinase and associated proteins. Curr. Opin. Cell Biol. 6:705-710.
76. 75a.Schlaepfer, D., and T. Hunter. Personal communication.
77. Schwartz, M. A., M. D. Schaller, and M. H. Ginsberg. 1995. Integrins: emerging paradigms of signal transduction. Annu. Rev. Cell. Dev. Biol. 11:549-599.
78. Shimizu, Y., J. L. Mobley, L. D. Finkelstein, and A. S. Chan. 1995. A role for phosphatidylinositol 3-kinase in the regulation of beta 1 integrin activity by CD2 antigen. J. Cell Biol. 131:1867-1880.
79. 3 in thrombin-stimulated platelets. Biochem. J. 286:581-584.
80. Sozeri, O., K. Vollmer, M. Liyanage, D. Frith, G. Kour, G. E. Mark, and S. Srabel. 1992. Activation of the c-raf protein kinase by protein kinase C phosphorylation. Oncogene 7:2259-2262.
81. Stephens, L. R., K. T. Hughes, and R. F. Irvine. 1991. Pathway of phosphatidylinositol(3.4,5)-trisphosphatc synthesis in activated neutrophils. Nature (London) 251:33-39.
82. Tanaka, M., and W. Herr. 1990. Differential transcriptional activation by Oct-1 and Oct-2: interdependent activation domains induce Oct-2 phosphorylation. Cell 60:375-386.
83. 3. J. Biol. Chem. 269:32358-32367.
84. Touhara, K., B. E. Hawes, T. van Biesen, and R. J. Lefkowitz. 1995. G protein beta gamma subunits stimulate phosphorylation of Shc adapter protein. Proc. Natl. Acad. Sci. USA 92:9284-9287.
85. Traynor-Kaplan, A. E., A. L. Harris, B. L. Thompson, P. Taylor, and L. A. Sklar. 1988. An inositol tetrakisphosphate-containing phospholipid in activated neutrophils. Nature (London) 334:353-356.
86. Turner, C. E. 1994. Paxillin: a cytoskeletal target for tyrosine kinases. Bioessays 16:47-52.
87. Uehara, T., Y. Tokumitsu, and Y. Nomura. 1995. Wortmannin inhibits insulin-induced ras and mitogen-activated protein kinase activation related to adipocyte differentiation in 3T3-L1 fibroblasts. Biochem. Biophys. Res. Commun. 210:574-580.
88. Ui, M., T. Okada, K. Hazeki, and O. Hazeki. 1995. Wortmannin as a unique probe for an intracellular signalling protein, phosphoinositide 3-kinase. Trends Biochem. Sci. 20:303-307.
89. Urich, M., M. Y. el Shemerly, D. Besser, Y. Nagamine, and K. Ballmer-Hofer. 1995. Activation and nuclear translocation of mitogen-activated protein kinases by polyomavirus middle-T or serum depend on phosphatidylinositol 3-kinase. J. Biol. Chem. 270:29286-29292.
90. Vaillancourt, R. R., A. E. Harwood, and S. Winitz. 1994. Analysis of guanine nucleotides associated with protooncogene Ras. Methods Enzymol. 238: 255-259.
91. Valius, M., and A. Kazlauskas. 1993. Phospholipase c-gamma-1 and phosphatidylinositol 3-kinase are downstream mediators of the PDGF receptor's mitogenic signal. Cell 73:321-334.
92. Von Willebrand, M., T. Jascur, N. Bonnefoy-Berard, H. Yano, A. Altman, Y. Matsuda, and T. Mustelin. 1996. Inhibition of phosphatidylinositol 3-kinase blocks T cell antigen receptor/CD3-induced activation of the mitogen-activated kinase erk-2. Eur. J. Biochem. 235:828-835.
93. Vuori, K., and E. Ruoslahti. 1993. Activation of protein kinase C precedes alpha5beta1 integrin-mediated cell spreading on fibronectin. J. Biol. Chem. 268:21459-21462.
94. Wadzinski, B. E., B. J. Eisfelder, M. C. Mumby, and G. L. Johnson. 1992. NH2-terminal modification of the phosphatase 2A catalytic subunit allows functional expression in mammalian cells. J. Biol. Chem. 267:16883-16888.
95. Wennstrom, S., P. Hawkins, C. F., K. Hara, K. Yonezawa, M. Kasuga, T. Jackson, L. Claesson-Welsh, and L. Stephens. 1994. Activation of phosphoinositide 3-kinase is required for PDGF-stimulated membrane ruffling. Curr. Biol. 4:385-393.
96. Woods, A., and J. R. Couchman. 1992. Protein kinase C involvement in focal adhesion formation. J. Cell. Sci. 101:277-290.
97. Woscholski, R., T. Kodaki, M. McKinnon, M. D. Waterfield, and P. J. Parker. 1994. A comparison of demethoxyviridin and wortmannin as inhibitors of phosphatidylinositol 3-kinase. FEBS Lett. 342:109-114.
98. Yao, R., and G. M. Cooper. 1995. Requirement for phosphatidylinositol-3 kinase in prevention of apoptosis by nerve growth factor. Science 267:2003-2005.
99. Zell, T., S. W. Hunt, J. L. Mobley, L. D. Finkelstein, and Y. Shimizu. 1996. CD28-mediated up-regulation of beta 1-integrin adhesion involves phosphatidylinositol 3-kinase. J. Immunol. 156:883-886.
100. Zhang, J., J. Zhang, S. J. Shattil, M. C. Cunningham, and S. E. Rittenhouse. 1996. Phosphoinositide 3-kinase gamma and p85/phosphoinositide 3-kinase in platelets. Relative activation by thrombin receptor or betaphorbol myristate acetate and roles in promoting the ligand-binding function of αIIb/β3 integrin. J. Biol. Chem. 271:6265-6272.
101. Zhu, X., and R. K. Assoian. 1995. Integrin-dependent activation of map kinase: a link to shape-dependent cell proliferation. Mol. Biol. Cell 6:273-282.