4E-BP1, a repressor of mRNA translation, is phosphorylated and inactivated by the Akt(PKB) signaling pathway

Genes and Development

Volumn 12, Issue 4, 1998, Pages 502-513

  Gingras, Anne Claude ^a   Kennedy, Scott G ^b   O'Leary, Maura A ^b   Sonenberg, Nahum ^a   Hay, Nissim ^b,c  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

eIF4E; FRAP mTOR; Phosphorylation; PI 3 kinase; Protein kinase B; Protein synthesis

Indexed keywords

BINDING PROTEIN; INITIATION FACTOR 4E; INSULIN; MESSENGER RNA; MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; RAPAMYCIN; REPRESSOR PROTEIN; WORTMANNIN;

APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; KIDNEY CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RNA TRANSLATION; SIGNAL TRANSDUCTION; TRANSLATION REGULATION;

EID: 0032520009     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.12.4.502     Document Type: Article

References (67)

1. Ahmed, N.N., H.L. Grimes, A. Bellacosa, T.O. Chan, and P.N. Tsichlis. 1997. Transduction of interleukin-2 antiapoptotic and proliferative signal via Akt protein kinase. Proc. Natl. Acad. Sci. 94: 3627-3632.
2. 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 and PDGF receptors activate atypical PKC lambda through phosphatidylinositol 3-kinase. EMBO J. 15: 788-798.
3. Alessi, D., S. James, C.P. Downes, A. Holmes, P. Gaffney, C. Reese, and P. Cohen. 1997. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Bα. Curr. Biol. 7: 261-269.
4. Barbet, N.C., U. Schneider, S.B. Helliwell, I. Stansfield, M.F. Tuite, and M.N. Hall. 1996. Tor controls translation initiation and early G1 progression in yeast. Mol. Biol. Cell 7: 25-42.
5. Bellacosa, A., D.D. Feo, A.K. Godwin, D.W. Bell, J.Q. Cheng, D.A. Altomare, M. Wan, L. Dubeau, G. Scambia, V. Masciullo, G. Ferrandina, P.B. Panici, S. Mancuso, G. Neri, and J.R. Testa. 1995. Molecular alterations of the AKT2 oncogene in ovarian and breast carcinomas. Intern. J. Cancer 64: 280-285.
6. Beretta, L., A.C. Gingras, Y.V. Svitkin, M.N. Hall, and N. Sonenberg. 1996. Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation. EMBO J. 15: 658-664.
7. Brown, E.J. and S.L. Schreiber. 1996. A signaling pathway to translational control. Cell 86: 517-520.
8. Brown, E.J., P.A. Beal, C.T. Keith, J. Chen, T.B. Shin, and S.L. Schreiber. 1995. Control of p70 S6 kinase by kinase activity of FRAP in vivo. Nature 377: 441-446.
9. Brunn, G.J., J. Williams, C. Sabers, G. Wiederrecht, J.C.J. Lawrence, and R.T. Abraham. 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. Brunn, G.J., C.C. Hudson, A. Sekulic, J.M. Williams, H. Hosoi, P.J. Houghton, J. Lawrence, Jr., and R.T. Abraham. 1997. Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science 277: 99-101.
11. Burgering, B.M. and P.J. Coffer. 1995. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376: 599-602.
12. Cheng, J.Q., B. Ruggeri, W.M. Klein, G. Sonoda, D.A. Altomare, D.K. Watson, and J.R. Testa. 1996. Amplification of AKT2 in human pancreatic cells and inhibition of AKT2 expression and tumorigenicity by antisense RNA. Proc. Natl. Acad. Sci. 93: 3636-3641.
13. Cheng, J.Q., D.A. Altomare, M.A. Klein, W.C. Lee, G.D. Kruh, N.A. Lissy, and J.R. Testa. 1997. Transforming activity and mitosis-related expression of the AKT2 oncogene: Evidence suggesting a link between cell cycle regulation and oncogenesis. Oncogene 14: 2793-2801.
14. Chou, M.M. and J. Blenis. 1995. The 70 kDa S6 kinase: Regulation of a kinase with multiple roles in mitogenic signaling. Curr. Opin. Cell Biol. 7: 806-814.
15. Christofori, G., P. Nalik, and D. Hanahan. 1994. A second signal supplied by insulin-like growth factor II in oncogene-induced tumorigenesis. Nature 369: 414-418.
16. Chung, J., C.J. Kuo, G.R. Crabtree, and J. Blenis. 1992. Rapamycin-FKBP specifically blocks growth-dependent activation of and signaling by the 70 kd S6 protein kinases. Cell 69: 1227-1236.
17. Cohen, P., D.R. Alessi, and D.A.E. Cross. 1997. PDK1, one of the missing links in insulin signal transduction? Fed. Eur. Biochem. Soc. Lett. 410: 3-10.
18. Dudek, H., S.R. Datta, 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: 661-665.
19. Edery, I., M. Altmann, and N. Sonenberg. 1988. High-level synthesis in Escherichia coli of functional cap-binding eukaryotic initiation factor eIE-4E and affinity purification using a simplified cap-analog resin. Gene 74: 517-525.
20. Evan, G.I., A.H. Wyllie, C.S. Gilbert, T.D. Littlewood, H. Land, M. Brooks, C.M. Waters, L.Z. Penn, and D.C. Hancock. 1992. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69: 119-128.
21. Foote, L.C., T.J. Schneider, G.M. Fischer, J.K. Wang, B. Rasmussen, K.A. Campbell, D.H. Lynch, S.T. Ju, A. Marshak-Rothstein, and T.L. Rothstein. 1996. Intracellular signaling for inducible antigen receptor-mediated Fas resistance in B cells. J. Immunol. 157: 1878-1885.
22. Franke, T.F., S. 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.
23. Franke, T.F., D.R. Kaplan, and L.C. Cantley. 1997a. PI3K: Downstream AKTion blocks apoptosis. Cell 88: 435-437.
24. Franke, T.F., D.R. Kaplan, L.C. Cantley, and A.T. Toker. 1997b. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science 275: 665-667.
25. Gingras, A.C., Y. Svitkin, G.J. Belsham, A. Pause, and N. Sonenberg. 1996. Activation of the translational suppressor 4E-BP1 following infection with encephalomyocarditis virus and poliovirus. Proc. Natl. Acad. Sci. 93: 5578-5583.
26. Hall, M.N. 1996. The TOR signalling pathway and growth control in yeast. Biochem. Soc. Transac. 24: 234-239.
27. Hawkins, P.T., A. Eguinoa, R.G. Qui, D. Stokoe, F.T. Cooke, R. Walter, S. Wennstrom, W.L. Claesson, T. Evans, M. Symons, and L. Stephens. 1995. PDGF stimulates an increase in Rac-GTP via the activation of phosphoinositide 3-kinase. Curr. Biol. 5: 393-403.
28. Hemmings, B.A. 1997. Akt signaling: Linking membrane events to life and death decisions. Science 275: 628-630.
29. Hoekstra, M.F. 1997. Responses to DNA damage and regulation of cell cycle checkpoints by the ATM protein kinase family. Curr. Opin. Genet. Dev. 7: 170-175.
30. Karsan, A., E. Yee, and J.M. Harlan. 1996. Endothelial cell death induced by tumor necrosis factor- alpha is inhibited by the Bcl-2 family member, A1. J. Biol. Chem. 271: 27201-27204.
31. Kauffmann-Zeh, A., P. Rodriguez-Viciana, E. Ulrich, C. Gilbert, P. Coffer, J. Downward, and G. I. Evan. 1997. Suppression of c-Myc-induced apoptosis by Ras signalling through PI(3)K and PKB. Nature 385: 544-548.
32. 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.
33. Kerekatte, V., K. Smiley, B. Hu, A. Smith, F. Gelder, and A. De Benedetti. 1995. The proto-oncogene/translation factor eIF4E: A survey of its expression in breast carcinomas. Intern. J. Cancer 64: 27-31.
34. Khwaja, A., P. Rodriguez-Viciana, S. Wenstrom, P.H. Warne, and J. Downward. 1997. Matrix adhesion and Ras transformation both activate a phosphoinositide 3-OH kinase and protein kinase B/Akt cellular survival pathway. EMBO J. 16: 2783-2793.
35. Kimura, K.D., H.A. Tissenbaum, Y. Liu, and G. Ruvkun. 1997. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277: 942-946.
36. Kulik, G., A. Klippel, and M.J. Weber. 1997. Antiapoptotic signalling by the insulin-like growth factor I receptor, phosphatidylinositol 3-kinase, and Akt. Mol. Cell. Biol. 17: 1595-1606.
37. Lazaris-Karatzas, A., K.S. Montine, and N. Sonenberg. 1990. Malignant transformation by eukaryotic initiation factor subunit that binds to mRNA 5′ cap. Nature 345: 544-547.
38. Lin, T.A., X. Kong, T.A. Haystead, A. Pause, G. Belsham, N. Sonenberg, and J.C.J. Lawrence. 1994. PHAS-I as a link between mitogen-activated protein kinase and translation initiation. Science 266: 653-656.
39. Lin, T.A., X. Kong, A.R. Saltiel, P.J. Blackshear, and J.C.J. Lawrence. 1995. Control of PHAS-I by insulin in 3T3-L1 adipocytes. Synthesis, degradation, and phosphorylation by a rapamycin- sensitive and mitogen-activated protein kinase-independent pathway. J. Biol. Chem. 270: 18531-18538.
40. Marte, B.M. and J. Downward. 1997. PKB/Akt: Connecting phosphoinositide 3-kinase to cell survival and beyond. Trends Biochem. Sci. 22: 355-358.
41. Morris, J.Z., H.A. Tissenbaum, and G. Ruvkun. 1996. a phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382: 536-539.
42. Moser, B.A., P.B. Dennis, N. Pullen, R.B. Pearson, N.A. Williamson, R.E. Wettenhall, S.C. Kozma, and G. Thomas. 1997. Dual requirement for a newly identified phosphorylation site in p70s6k. Mol. Cell. Biol. 17: 5648-5655.
43. Nakanishi, H., K.A. Brewer, and J.H. Exton. 1993. Activation of the γ isozyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 268: 13-16.
44. Nathan, C.A., L. Liu, B.D. Li, F.W. Abreo, I. Nandy, and A. De Benedetti. 1997. Detection of the proto-oncogene eIF4E in surgical margins may predict recurrence in head and neck cancer. Oncogene 15: 579-584.
45. Natoli, G., A. Ianni, A. Costanzo, G. De Petrillo, I. Ilari, P. Chirillo, C. Balsano, and M. Levrero. 1995. Resistance to Fas-mediated apoptosis in human hepatoma cells. Oncogene 11: 1157-1164.
46. Nielsen, F.C., L. Ostergaard, J. Nielsen, and J. Christiansen. 1995. Growth-dependent translation of IGF-II mRNA by a rapamycin-sensitive pathway. Nature 377: 358-362.
47. Pause, A., G.J. Belsham, A.C. Gingras, O. Donze, T.A. Lin, H.C.J. Lawrence, and N. Sonenberg. 1994. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′ cap function. Nature 371: 762-767.
48. Polunovsky, V.A., I.B. Rosenwald, A.T. Tan, J. White, L. Chiang, N. Sonenberg, and P.B. Bitterman. 1996. Translational control of programmed cell death: Eukaryotic translation initiation factor 4E blocks apoptosis in growth-factor-restricted fibroblasts with physiologically expressed or deregulated Myc. Mol. Cell. Biol. 16: 6573-6581.
49. Polunovsky, V.A., C.H. Wendt, D.H. Ingbar, M.S. Peterson, and P.B. Bitterman. 1994. Induction of endothelial cell apoptosis by TNF alpha: Modulation by inhibitors of protein synthesis. Exper. Cell Res. 214: 584-594.
50. Price, D.J., J.R. Grove, V. Calvo, J. Avruch, and B.E. Bierer. 1992. Rapamycin-induced inhibition of the 70-kilodalton S6 protein kinase. Science 257: 973-977.
51. Proud, C.G. 1996. p70 S6 kinase: An enigma with variations. Trends Biochem. Sci. 21: 181-185.
52. Reif, K., B. Burgering, and D. Cantrell. 1997. Phosphatidylinositol 3-kinase links the interleukin-2 receptor to protein kinase B and p70 S6 kinase. J. Biol. Chem. 272: 14426-14433.
53. Reinartz, J., M.J. Bechtel, and M.D. Kramer. 1996. Tumor necrosis factor-alpha-induced apoptosis in a human keratinocyte cell line (HaCaT) is counteracted by transforming growth factor-alpha. Exper. Cell Res. 228: 334-340.
54. Rousseau, D., A.C. Gingras, A. Pause, and N. Sonenberg. 1996. The eIF4E-binding proteins 1 and 2 are negative regulators of cell growth. Oncogene 13: 2415-2420.
55. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular cloning: A laboratory manual, 2nd ed., pp. 16.33-16.35. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
56. Shi, Y., A. Frankel, L.G. Radvanyi, L.Z. Penn, R.G. Miller, and G.B. Mills. 1995. Rapamycin enhances apoptosis and increases sensitivity to cisplatin in vitro. Cancer Res. 55: 1982-1988.
57. Sonenberg, N. 1996. Translational control. (ed. J.W.B. Hershey, M.B. Mathews, and N. Sonenberg), pp. 245-269. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
58. Stokoe, D., L.R. Stephens, T. Copeland, P.R.J. Gaffney, C.B. Reese, G.F. Painter, A.B. Holmes, F. McCormick, and P.T. Hawkins. 1997. Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science 277: 567-570.
59. Ueda, K. and D. Ganem. 1996. Apoptosis is induced by N-myc expression in hepatocytes, a frequent event in hepadnavirus oncogenesis, and is blocked by insulin-like growth factor II. J. Virol. 70: 1375-1383.
60. van der Geer, P. and T. Hunter. 1994. Phosphopeptide mapping and phosphoamino acid analysis by electrophoresis and chromatography on thin-layer cellulose plates. Electrophoresis 15: 544-554.
61. Vanhaesebroeck, B., S.J. Leevers, G. Panayotou, and M.D. Waterfield. 1997. Phosphoinositide 3-kinases: A conserved family of signal transducers. Trends Biochem. Sci. 22: 267-272.
62. von Manteuffel, S.R., A.C. Gingras, X.F. Ming, N. Sonenberg, and G. Thomas. 1996. 4EBP-I phosphorylation is mediated by the FRAP-p70S6K pathway and is independent of mitogen-activated protein kinase. Proc. Natl. Acad. Sci. 93: 4076-4080.
63. s6k. Mol. Cell. Biol. 1997: 5426-5436.
64. waf1/cip1. Genes & Dev. 8: 2817-2830.
65. Waterston, R., C. Martin, M. Craxton, C. Huynh, A. Coulson, L. Hillier, R. Durbin, P. Green, R. Shownkeen, N. Halloran, et al. 1992. A survey of expressed genes in Caenorhabditis elegans. Nature Genet. 1: 114-123.
66. Whalen, S.G., A.C. Gingras, L. Amankwa, S. Mader, P.E. Branton, R. Aebersold, and N. Sonenberg. 1996. Phosphorylation of eIF-4E on serine 209 by protein kinase C is inhibited by the translational repressors, 4E-binding proteins. J. Biol. Chem. 271: 11831-11837.
67. S6K activity. Oncogene 13: 343-351.