Inhibition of phosphatidylinositol 3-kinase blocks T cell antigen receptor/CD3-induced activation of the mitogen-activated kinase Erk2

European Journal of Biochemistry

Volumn 235, Issue 3, 1996, Pages 828-835

  Von Willebrand, Maria ^a   Jascur, Thomas ^a   Bonnefoy Bérard, Nathalie ^a   Yano, Hiroshi ^b   Altman, Amnon ^a   Matsuda, Yuzuru ^b   Mustelin, Tomas ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b KYOWA HAKKO KOGYO CO LTD   (Japan)

Author keywords

Erk2; Mek; Phosphatidylinositol 3 kinase; Raf; Wortmannin

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; OKT 3; PHOSPHATIDYLINOSITOL KINASE; WORTMANNIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALIA;

EID: 0030024007     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1996.00828.x     Document Type: Article

References (66)

1. Lips, D. L. & Majerus, P. W. (1989) Phosphatidylinositol 3-phosphate is present in normal and transformed fibroblasts and is resistant to hydrolysis by bovine brain phospholipase C II, J. Biol. Chem. 264, 8759-8763.
2. 2 3-OH kinase, Nature 358, 157-159.
3. Ward, S. G., Ley, S. C., MacPhee, C. & Cantrell, D. A. (1992) Regulation of D-3 phosphoinositides during T cell activation via T cell antigen receptor/CD3 complex and CD2 antigens, Eur. J. Immunol. 22, 45-49.
4. Kucera, G. L. & Rittenhouse, S. E. (1990) Human platelets form 3-phosphorylated phosphoinositides in response to α-thrombin, U46619, or GTPγS, J. Biol. Chem. 265, 5345-5348.
5. lck tyrosine kinase, Eur. J. Immunol. 24, 234-238.
6. Gold, M. R., Chan, V. W.-F., Turck, C. & DeFranco, A. L. (1992) Membrane Ig cross-linking regulates phosphatidylinositol 3-kinase in B lymphocytes. J. Immunol. 148, 2012-2022.
7. Carpenter, C. L., Duckworth, B. C., Auger, K. R., Cohen, B., Schaffhausen, B. S. & Cantley, L. C. (1990) Purification and characterization of phosphoinositide 3-kinase from rat liver. J. Biol. Chem. 265, 19704-19711.
8. Escobedo, J. A., Navankasattusas, S., Kavanaugh, W. M., Milfay, D., Fried, V. A. & Williams, L. T. (1991) cDNA cloning of a novel 85 kd protein that has SH2 domains and regulates binding of PI3-kinase to the PDGF β-receptor, Cell 65, 75-82.
9. Skolnik, E. Y., Margolis, B., Mohammadi, M., Lowenstein, E., Fischer, R., Drepps, A., Ullrich, A. & Schlessinger, J. (1991) Cloning of PI3kinase-associated p85 utilizing a novel method for expression/cloning of target proteins for receptor tyrosine kinases, Cell 165, 83-90.
10. c-src complexes, and PI3-kinase, Cell 65, 91-104.
11. Hiles, I., Otsu, M., Volinia, S., Fry, M. J., Gout, I., Dhand, R., Panayotou, G., Ruiz-Larrea, F., Thompson, A., Totty, N., Hsuan, J., Courtneidge, S. A., Parker, P. J. & Waterfield, M. D. (1992) Phosphatidylinositol 3-kinase: structure and expression of the 110 kd catalytic subunit, Cell 70, 419-425.
12. Hu, P., Mondino, A., Skolnik, E. Y. & Schlessinger, J. (1993) Cloning of a novel, ubiquitously expressed human phosphatidylinositol 3-kinase and identification of its binding site on p85, Mol. Cell. Biol. 13, 7677-7688.
13. Kazlauskas, A. & Cooper, J. A. (1990) Phosphorylation of the PDGF receptor β subunit creates a tight binding site for phosphatidylinositol 3 kinase, EMBO J. 9, 3279-3285.
14. End, P., Gout, I., Fry, M. J., Panayotou, G., Dhand, R., Yonezawa, K., Kasuga, M. & Waterfield, M. D. (1993) A biosensor approach to probe the structure and function of the p85 α subunit of the phosphatidylinositol 3-kinase complex, J. Biol. Chem. 268, 10066-10075.
15. Klippel, A., Escobedo, J. A., Hu, Q. & Williams, L. T. (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.
16. Holt, K. H., Olson, A. L., Moye-Rowley, W. S. & Pessin, J. E. (1994) Phosphatidylinositol 3-kinase activation is mediated by high-affinity interactions between distinct domains within the p110 and p85 subunits, Mol. Cell. Biol. 14, 42-49.
17. P1K reveal a new regulatory subunit for phosphatidylinositol 3-kinase. Mol. Cell. Biol. 15, 4453-4465.
18. Schu, P. V., Takegawa, K., Fry, M. J., Stack, J. H., Waterfield, M. D. & Emr, S. D. (1993) Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting, Science 260, 88-91.
19. Volinia, S., Dhand, R., Vanhaesebroeck, B., MacDougall, L. K., Stein, R., Zvelebil, M. J., Domin, J., Panaretou, C. & Waterfield, M. D. (1995) A human phosphatidylinositol 3-kinase complex related to the yeast Vps34p-Vps15p protein sorting system, EMBO J. 14, 3339-3348.
20. Savitsky, K., Bar-Shira, A., Gilad, S., Rotman, G., Ziv, Y., Vanagaite, L., Tagle, D. A., Smith, S., Uziel, T., Sfez, S., Ashkenazi, M., Pecker, I., Frydman, M., Harnik, R., Patanjali, S. R., Simmons, A., Clines, G. A., Sartiel, A., Gatti, R. A., Chessa, L., Sanal, O., Lavin, M. F., Jaspers, N. G. J., Taylor, A. M. R., Arlett, C. F., Miki, T., Weissman, S. M., Lovett, M., Collins, F. S. & Shiloh, Y. (1995) A single ataxia telangiectasia gene with a product similar to P1-3 kinase, Science 268, 1749-1753.
21. Stoyanov, B., Volinia, S., Hanck, T., Rubio, I., Loubtchenkov, M., Malek, D., Stoyanova, S., Vanhaesebroeck, B., Dhand, R., Nürnberg, B., Gierschik, P., Seedorf, K., Hsuan, J. J., Waterfield, M. D. & Wetzker, R. (1995) Cloning and characterization of a G protein-activated phosphatidylinositol 3-kinase, Science 269, 690-693.
22. Auger, K. R. & Cantley, L. C. (1991) Novel polyphosphoinositides in cell growth and activation, Cancer Cells 3, 263-275.
23. Gold, M. R. & Aebersold, R. (1994) Both phosphatidylinositol 3-kinase and phosphatidylinositol 4-kinase products are increased by antigen receptor signaling in B cells, J. Immunol. 152, 42-50.
24. Coughlin, S. R., Escobedo, J. A. & Williams, L. T. (1989) Role of phosphatidylinositol kinase in PDGF receptor signal transduction, Science 243, 1191-1193.
25. Yamauchi, K., Holt, K. & Pessins, J. E. (1993) Phosphatidylinositol 3-kinase functions upstream of Ras and Raf in mediating insulin stimulation of c-fos transcription, J. Biol. Chem. 268, 14597-14600.
26. Rodriguez-Viciana, P., Warne, P. H., Dhand, R., Vanhaesebroeck, B., Gout, I., Fry, M. J., Waterfield, M. D. & Downward, J. (1994) Phosphatidylinositol-3-OH kinase as a direct target of Ras, Nature 370, 527-532.
27. Valius, M. & Kazlauskas, A. (1993) Phospholipase C-γ1 and phosphatidylinositol 3 kinase are the downstream mediators of the PDGF receptor's mitogenic signal, Cell 73, 321-334.
28. Cheatham, B., Vlahos, C. J., Cheatham, L., Wang, L., Blenis, J. & 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.
29. Yano, H., Nakanishi, S., Kimura, K., Hanai, N., Saitoh, Y., Fukui, Y., Nonomura, Y. & Matsuda, Y. (1993) Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBE-2H3 cells, J. Biol. Chem. 268, 25846-25856.
30. Ward, S. G., Wilson, A., Turner, L., Westwick, J. & Sansom, D. M. (1995) Inhibition of CD28-mediated T cell costimulation by the phosphoinositide 3-kinase inhibitor wortmannin, Eur. J. Immunol. 25, 526-532.
31. Nakanishi, H., Brewer, K. A. & Exton, J. H. (1993) Activation of the ζ isozyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate, J. Biol. Chem. 268, 13-16.
32. 3, J. Biol. Chem. 269, 32358-32367.
33. Franke, T. F., Yang, S.-I., Chan, T. O., Datta, K., Kazlauskas, A., Morrison, D., Kaplan, D. R. & Tsichlis, P. N. The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase, Cell 81, 727-736
34. Burgering, B. M. T. & Coffer, P. J. (1995) Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376, 599-602.
35. Nakanishi, S., Kakita, S., Takahashi, I., Kawahara, K., Tsukuda, E., Sano, T, Yamada, K., Yoshida, M., Kase, H. & Matsuda, Y. (1992) Wortmannin, a microbial product inhibitor of myosin light chain kinase, J. Biol. Chem. 267, 2157-2163.
36. Carrasco-Marin, E., Alvarez-Dominguez, C. & Leyva-Cobian, F. (1994) Wortmannin, an inhibitor of phospholipase D activation, selectively blocks major histocompatibility complex class II-restricted antigen presentation, Eur. J. Immunol. 24, 2031-2039.
37. Liu, Y.-C., Kawagishi, M., Mikayama, T., Inagaki, Y., Takeuchi, T. & Ohashi, H. (1995) Processing of a fusion protein by endoproteinase in COS-1 cells for secretion of mature peptide by using a chimeric expression vector, Proc. Natl Acad. Sci. USA 90, 8957-8961.
38. Izquierdo, M., Bowden, S. & Cantrell, D. A. (1992) The role of Raf-1 in regulation of extracellular signal-regulated kinase 2 by the T cell antigen receptor, J. Exp. Med. 180, 401-406.
39. + T cells by receptor activation, J. Immunol. 155, 3815-3822.
40. lck and that is defective in HPB-ALL, J. Immunol. 147, 1933-1939.
41. Nel, A. E., Hanekom, C., Rheeder, A., Williams, K., Pollack, S., Katz, R. & Landreth, G. (1990) Stimulation of MAP-2 kinase activity in T lymphocytes by anti-CD3 or anti-Ti monoclonal antibody is partially dependent on protein kinase C. J. Immunol. 144, 2683-2689.
42. Nel, A. E., Pollack, S., Landreth, G., Ledbetter, J. A., Hultin, L., Williams, K., Katz, R. & Akerley, B. (1990) CD-3-mediated activation of MAP-2 kinase can be modified by ligation of the CD4 receptor. Evidence for tyrosine phosphorylation during activation of this kinase. J. Immunol. 145, 971-979.
43. ras in activation of extracellular signal-regulated kinase 2, Nature 357, 602-604.
44. Hu, Q., Klippel, A., Muslin, A. J., Fantl, W. J. & Williams, L. T. (1995) Ras-dependent induction of cellular responses by constitutively active phosphatidylinositol 3-kinase, Science 268, 100-102.
45. Dhand, R., Hara, K., Hiles, I., Bax, B., Gout, I., Panayotou, G., Fry, M. J., Yonezawa, K., Kasuga, M. & Waterfield, M. D. (1994) Pl 3-kinase: structural and functional analysis of intersubunit interactions, EMBO J. 13, 511-521.
46. Ahn, N. G., Seger, R. & Krebs, E. G. (1992) The mitogen-activated protein kinase activator, Curr. Opin. Cell Biol. 4, 992-999.
47. Siegel, J. N., June, C. H., Yamada, H., Rapp, U. R. & Samelson, L. (1993) Rapid activation of c-Raf-1 after stimulation of the T-cell receptor or the muscarinic receptor type 1 in resting T cells, J. Immunol. 151, 4116-4121.
48. Yan, M. & Templeton, D. J. (1994) Identification of 2 serine residues of MEK-1 that are differentially phosphorylated during activation by raf and MEK kinase, J. Biol. Chem. 269, 19067-19073.
49. Storm, S. M., Cleveland, J. L. & Rapp, U. R. (1990) Expression of raf family proto-oncogenes in normal mouse tissues, Oncogene 5, 345-351.
50. Lange-Carter, C. A., Pleiman, C. M., Gardner, A. M., Blumer, K. J. & Johnson, G. L. (1993) A divergence in the MAP kinase regulatory network defined by MEK kinase and Raf, Science 260, 315-319.
51. Hsi, E. D., Siegel, J. N., Minami, Y., Luong, E. T., Klausner, R. D. & Samelson, L. E. (1989) T cell activation induces rapid tyrosine phosphorylation of a limited number of cellular substrates, J. Biol. Chem. 264, 10836-10842.
52. Mustelin, T., Coggeshall, K. M., Isakov, N. & Altman, A. (1990) Tyrosine phosphorylation is required for T cell antigen receptor-mediated activation of phospholipase C, Science 247, 1584-1587.
53. Siegel, J. N., Klausner, R. D., Rapp, U. R. & Samelson, L. E. (1990) T cell antigen receptor engagement stimulates c-raf phosphorylation and induces c-raf-associated kinase activity via a protein kinase C-dependent pathway, J. Biol. Chem. 265, 18472-18478.
54. Whitehurst, C. E., Boulton, T. G., Cobb, M. H. & Geppert, T. D. (1992) Extracellular signal-regulated kinase in T-cells. Anti-CD3 and 4β-phorbol 12-myristate and 13-acetate-induced phosphorylation and activation. J. Immunol. 148, 3230-3237.
55. Van Aelst, L., Barr, M., Marcus, S., Polverino, A. & Wigler, M. (1993) Complex formation between RAS and RAF and other protein kinases, Proc. Natl Acad. Sci. USA 90, 6213-6217.
56. Vojtek, A. B., Hollenberg, S. M. & Cooper, J. A. (1993) Mammalian Ras interacts directly with the serine/threonine kinase Raf, Cell 74, 205-214.
57. Morrison, D. K., Heidecker, G., Rapp, U. F. & Copeland, T. D. (1993) Identification of the major phosphorylation sites of the Raf-1 kinase, J. Biol. Chem. 268, 17309-17316.
58. Dent, P., Haser, W., Haystead, T. A. J., Vincent, L. A., Roberts, T. M. & Sturgill, T. W. (1992) Activation of mitogen-activated protein kinase kinase by v-Raf in NIH 3T3 cells and in vitro, Science 257, 1404-1407.
59. Kyriakis, J. M., App, H., Zhang, X. F., Banerjee, P., Brautigan, D. L., Rapp, U. R. & Avruch, J. (1992) Raf-1 activates MAP kinase-kinase, Nature 358, 417-421.
60. Alvarez, E., Northwood, I. C., Gonzalez, F. A., Latour, D. H., Seth, A., Abate, C., Curran, T. & Davis, R. J. (1991) Pro-Leu-Ser/Thr-Pro is a consensus primary sequence for substrate protein phosphorylation. Characterization of the phosphorylation of c-myc and c-jun proteins by an epidermal growth factor receptor threonine 669 protein kinase, J. Biol. Chem. 266, 15277-15285.
61. Pulverer, B. J., Kyriakis, J. M., Avruch, J., Nikolaki, E. & Woodgett, J. R. (1991) Phosphorylation of c-jun mediated by MAP kinases, Nature 353, 670-674.
62. Gille, H., Sharrocks, A. D. & Shaw, P. E. (1992) Phosphorylation of transcription factor p62TCF by MAP kinase stimulates ternary complex formation at c-fos promoter, Nature 358, 414-417.
63. Sturgill, T. W., Ray, L. B., Erikson, E. & Mailer, J. L. (1988) Insulin-stimulated MAP-2 kinase phosphorylates and activates ribosomal protein S6 kinase II, Nature 344, 715-718.
64. rsk activity, Proc. Natl Acad. Sci. USA 88, 4981-4985.
65. Ferby, I. M., Waga, I., Sakanaka, C., Kume, K. & Shimizu, T. (1994) Wortmannin inhibits mitogen-activated protein kinase activation induced by platelet-activating factor in guinea pig neutrophils. J. Biol. Chem. 269, 30485-30488.
66. Ward, Y., Gupta, S., Jensen, P., Wartmann, M., Davis, R. J. & Kelly, K. (1994) Control of MAP kinase activation by the mitogen-induced threonine/tyrosine phosphatase PAC1, Nature 367, 651-654.