Regulation of translation initiation factors by signal transduction

European Journal of Biochemistry

Volumn 253, Issue 3, 1998, Pages 531-544

  Kleijn, Miranda ^a   Scheper, Gert C ^a   Voorma, Harry O ^a   Thomas, Adri A M ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Eukaryotic initiation factor 2B; Eukaryotic initiation factor 4E; FK506 binding protein rapamycin associated protein; Initiation factor 4E binding protein; Inositolphospholipid 3 kinase; Mammalian target of rapamycin; Mitogen activated protein kinase; Signal transduction; Translation initiation

Indexed keywords

BINDING PROTEIN; FK 506 BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INITIATION FACTOR 4E; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; RAPAMYCIN;

ANIMAL CELL; CELL COMMUNICATION; EUKARYOTE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; TRANSLATION INITIATION; TRANSLATION REGULATION;

ANIMALS; EUKARYOTIC INITIATION FACTOR-2B; EUKARYOTIC INITIATION FACTOR-4E; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; PEPTIDE INITIATION FACTORS; PROTEIN BIOSYNTHESIS; PROTEINS; SIGNAL TRANSDUCTION;

ANIMALIA; EUKARYOTA; MAMMALIA;

EID: 0032079873     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1998.2530531.x     Document Type: Review

References (175)

1. Hershey, J. W. B. (1990) Overview: phosphorylation and translation control, Enzyme 44, 17-27.
2. Pain, V. M. (1996) Initiation of protein synthesis in eukaryotic cells, Eur. J. Biochem. 236, 747-771.
3. Sonenberg, N., Morgan, M. A., Merrick, W. C. & Shatkin, A. J. (1978) A polypeptide in eukaryotic initiation factors that cross-links specifically to the 5′-terminal cap in mRNA, Proc. Natl Acad. Sci. USA 75, 4843-4847.
4. Rhoads, R. E. (1988) Cap recognition and the entry of mRNA into the protein synthesis initiation cycle, Trends Biochem. Sci. 13, 52-56.
5. Abramson, R. D., Dever, T. E., Lawson, T. G., Ray, B. K., Thach, R. E. & Merrick, W. C. (1987) The ATP-dependent interaction of eukaryotic initiation factors with mRNA, J. Biol. Chem. 262, 3826-3832.
6. Rozen, F., Edery, I., Meerovitch, K., Dever, T. E., Merrick, W. C. & Sonenberg, N. (1990) Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F, Mol. Cell. Biol. 10, 1134-1144.
7. Pause, A. & Sonenberg, N. (1992) Mutational analysis of a DEAD box RNA helicase: the mammalian translation initiation factor eIF-4A, EMBO J. 11, 2643-2654.
8. Haghighat, A. & Sonenberg, N. (1997) eIF4G dramatically enhances the binding of eIF4E to the mRNA 5′-cap structure, J. Biol. Chem. 272, 21 677-21 680.
9. Lamphear, B. J., Kirchweger, R., Skern, T. & Rhoads, R. E. (1995) Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF4G) with picornaviral proteases. J. Biol. Chem. 270, 21 975-21 983.
10. Mader, S., Lee, H., Pause, A. & Sonenberg, N. (1995) The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4γ and the translational repressors 4E-binding proteins, Mol. Cell. Biol. 15, 4990-4997.
11. Lawson, T. G., Lee, K. A., Maimone, M. M., Abramson, R. D., Dever, T. E., Merrick, W. C. & Thach, R. E. (1989) Dissociation of double-stranded polynucleotide helical structures by eukaryotic initiation factors, as revealed by a novel assay, Biochemistry 28, 4729-4734.
12. Trachsel, H. & Staehelin, T. (1979) Initiation of mammalian protein synthesis. The multiple functions of the initiation factor eIF-3, Biochim. Biophys. Acta 565, 305-314.
13. Schreier, M. H. & Staehelin, T. (1973) Functional characterization of five initiation factors for mammalian protein synthesis, in Mosbach Colloquia (Bautz, E. K. F., Karlson, P. & Kersten, H., eds) pp. 335-348, Springer, Heidelberg.
14. Benne, R. & Hershey, J. W. B. (1976) Purification and characterization of initiation factor IF-E3 from rabbit reticulocytes, Proc. Natl Acad. Sci. USA 73, 3005-3009.
15. Thomas, A., Goumans, H., Voorma, H. O. & Benne, R. (1980) The mechanism of action of eukaryotic initiation factor 4C in protein synthesis, Eur. J. Biochem. 107, 39-45.
16. Thompson, H. A., Sadnik, I., Scheinbuks, J. & Moldave, K. (1977) Studies on native ribosomal subunits from rat liver. Purification and characterization of a ribosome dissociating factor, Biochemistry 16, 2221-2230.
17. Chakrabarti, A. & Maitra, U. (1991) Function of eukaryotic initiation factor 5 in the formation of an 80S ribosomal polypeptide chain initiation complex, J. Biol. Chem. 266, 14 039-14 045.
18. De Benedetti, A. & Rhoads, R. E. (1990) Overexpression of eukaryotic protein synthesis initiation factor 4E in HeLa cells results in aberrant growth and morphology, Proc. Natl Acad. Sci. USA 87, 8212-8216.
19. Lazaris-Karatzas, A., Montine, K. S. & Sonenberg, N. (1990) Malignant transformation by a eukaryotic initiation factor subunit that binds to mRNA 5′ cap, Nature 345, 544-547.
20. Koromilas, A. E., Lazaris-Karatzas, A. & Sonenberg, N. (1992) mRNAs encoding extensive secondary structure in their 5′ noncoding region translate efficiently in cells overexpressing initiation factor eIF-4E, EMBO J. 11, 4153-4158.
21. Rousseau, D., Kaspar, R., Rosenwald, I., Gehrke, L. & Sonenberg, N. (1996) Translation initiation of ornithine decarboxylase and nucleocytoplasmic transport of cyclin D1 mRNA are increased in cells overexpressing eukaryotic initiation factor 4E, Proc. Natl Acad. Sci. USA 93, 1065-1070.
22. Rosenwald, I. B., Kaspar, R., Rousseau, D., Gehrke, L., Leboulch, P., Chen, J.-J., Schmidt, E. V., Sonenberg, N. & London, I. M. (1995) Eukaryotic translation initiation factor 4E regulates expression of cyclin D1 at transcriptional and post-transcriptional levels, J. Biol. Chem. 270, 21 176-21 180.
23. Fagan, R. J., Lazaris-Karatzas, A., Sonenberg, N. & Rozen, R. (1991) Translational control of ornithine aminotransferase, J. Biol. Chem. 266, 16 518-16 523.
24. De Benedetti, A., Joshi, B., Graff, J. R. & Zimmer, S. G. (1994) CHO cells transformed by the translation factor eIF-4E display increased c-myc expression, but require overexpression of Max for tumorigenicity, Mol. Cell. Diff. 2, 309-334.
25. Bommer, U.-A., Lazaris-Karatzas, A., De Bennedetti, A., Nürnberg, P., Benndorf, R., Bielka, H. & Sonenberg, N. (1994) Translational regulation of the mammalian growth-related protein p23: involvement of eIF4E, Cell. Mol. Biol. Res. 40, 633-641.
26. Barve, S. S., Cohen, D. A., De Benedetti, A., Rhoads, R. E. & Kaplan, A. M. (1994) Mechanism of differential regulation of IL-2 in murine Th1 and Th2 T cell subsets. 1. Induction of IL-2 transcription in Th2 cells by up-regulation of transcription factors with the protein synthesis initiation factor 4E, J. Immunol. 152, 1171-1181.
27. Klein, P. S. & Melton, D. A. (1994) Induction of mesoderm in Xenopus leavis embryos by translation initiation factor 4E, Science 265, 803-806.
28. Manzella, J. M., Rychlik, W., Rhoads, R. E., Hershey, J. W. B. & Blackshear, P. J. (1991) Insulin induction of ornithine decarboxylase: importance of mRNA secondary structure and phosphorylation of eucaryotic initiation factors eIF-4B and eIF-4E, J. Biol. Chem. 266, 2383-2389.
29. Joshi, B., Cai, A. L., Keiper, B. D., Minich, W. B., Mendez, R., Beach, C. M., Stepinski, J., Stolarski, R., Darzynkiewicz, E. & Rhoads, R. E. (1995) Phosphorylation of eukaryotic protein synthesis initiation factor 4E at Ser-209, J. Biol. Chem. 270, 14 597-14 603.
30. Flynn, A. & Proud, C. G. (1995) Serine 209, not serine 53, is the major site of phosphorylation in initiation factor eIF-4E in serum-treated Chinese hamster ovary cells, J. Biol. Chem. 270, 21 684-21 688.
31. Marcotrigiano, I., Gingras, A.-C., Sonenberg, N. & Burley, S. K. (1997) Cocrystal structure of the messenger RNA 5′ cap binding protein (eIF4E) bound to 7-methyl-GDP, Cell 89, 951-961.
32. Whalen, S. G., Gingras, A.-C., Amankwa, L., Mader, S., Branton, P. E., Aebersold, R. & Sonenberg, N. (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, 11 831-11 837.
33. Hiremath, L. S., Webb, N. R. & Rhoads, R. E. (1985) Immunological detection of the messenger RNA cap binding protein, J. Biol. Chem. 260, 7843-7849.
34. Duncan, R., Milburn, S. C. & Hershey, J. W. B. (1987) Regulated phosphorylation and low abundance of HeLa cell initiation factor eIF-4F suggest a role in translational control, J. Biol. Chem. 262, 380-388.
35. Rau, M., Ohlmann, T., Morley, S. J. & Pain, V. M. (1996) A reevaluation of the cap-binding protein, eIF4E, as a rate-limiting factor for initiation of translation in reticulocyte lysate, J. Biol. Chem. 271, 8983-8990.
36. Joshi-Barve, S., Rychlik, W. & Rhoads, R. E. (1990) Alteration of the major phosphorylation site of eukaryotic protein synthesis initiation factor 4E prevents its association with the 48S initiation complex, J. Biol. Chem. 265, 2979-2983.
37. Lamphear, B. J. & Panniers, R. (1990) Cap binding protein complex that restores protein synthesis in heat-shocked Ehrlich cell lysates contains highly phosphorylated eIF-4E, J. Biol. Chem. 265, 5333-5336.
38. Minich, W. B., Balasta, M. L., Goss, D. J. & Rhoads, R. E. (1994) Chromatographic resolution of in vivo phosphorylated and non-phosphorylated eukaryotic translation factor eIF-4E: increased cap affinity of the phosphorylated form, Proc. Natl Acad. Sci. USA 91, 7668-7672.
39. Proud, C. G. (1992) Protein phosphorylation in translational control, Curr. Top. Cell. Reg. 32, 243-369.
40. Rhoads, R. E. (1993) Regulation of eukaryotic protein synthesis by initiation factors, J. Biol. Chem. 268, 3017-3020.
41. Kimball, S. R., Jurasinski, C. V., Lawrence, J. C. Jr & Jefferson, L. S. (1997) Insulin stimulates protein synthesis in skeletal muscle by enhancing the association of eIF-4E and eIF-4G, Am. J. Physiol. 272, C754-C759.
42. Morley, S. J. & McKendrick, L. (1997) Involvement of stress-activated protein kinase and p38/RK mitogen-activated protein kinase signaling pathways in the enhanced phosphorylation of initiation factor 4E in NIH 3T3 cells, J. Biol. Chem. 272, 17 887-17 893.
43. Feigenblum, D. & Schneider, R. J. (1993) Modification of eukaryotic initiation factor 4F during infection by influenza virus, J. Virol. 67, 3027-3035.
44. Kleijn, M., Vrins, C. L. J., Voorma, H. O. & Thomas, A. A. M. (1996) Phosphorylation state of the cap binding protein eIF4E during viral infection, Virology 217, 486-494.
45. Gingras, A.-C., Svitkin, Y., Belsham, G. J., Pause, A. & Sonenberg, N. (1996) Activation of the translational suppressor 4E-BP1 following infection with encephalomyocarditis virus and poliovirus, Proc. Natl Acad. Sci. USA 93, 5578-5583.
46. Etchison, D., Hansen, J., Ehrenfeld, E., Edery, I., Sonenberg, N., Milburn, S. & Hershey, J. W. B. (1984) Demonstration in vitro that eukaryotic initiation factor 3 is active but that cap binding protein complex is inactive in poliovirus-infected HeLa cells, J. Virol. 51, 832-837.
47. Frederickson, R. M., Mushynski, W. & Sonenberg, N. (1992) Phosphorylation of translation initiation factor eIF-4E is induced in a ras-dependent manner during nerve growth factor-mediated PC12 cell differentiation, Mol. Cell. Biol. 12, 1239-1247.
48. Kleijn, M., Voorma, H. O. & Thomas, A. A. M. (1995) Phosphorylation of eIF4E and initiation of protein synthesis in P19 embryonal carcinoma cells, J. Cell. Biochem. 59, 443-452.
49. Lazaris-Karatzas, A., Smith, M. R., Frederickson, R. M., Jaramillo, M. L., Liu, Y. L., Kung, H. F. & Sonenberg, N. (1992) Ras mediates translation initiation factor-4E-induced malignant transformation, Genes Dev. 6, 1631-1642.
50. 53 mutant eukaryotic initiation factor 4E overexpression in mammalian cells, J. Biol. Chem. 268, 11 902-11 909.
51. Kozak, M. (1987) An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs, Nucleic Acids Res. 15, 8125-8148.
52. Pause, A., Belsham, G. J., Gingras, A.-C., Donzé, O., Lin, T.-A., Lawrence, J. C. Jr & Sonenberg, N. (1994) Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function, Nature 371, 762-767.
53. Hu, C., Pang, S., Kong, X., Velleca, M. & Lawrence, J. C. Jr (1994) Molecular cloning and tissue distribution of PHAS-I, an intracellular target for insulin and growth factors, Proc. Natl Acad. Sci. USA 91, 3730-3734.
54. Lin, T.-A., Kong, X., Haystead, T. A. J., Pause, A., Belsham, G., Sonenberg, N. & Lawrence, J. C. Jr (1994) PHAS-I as a link between mitogen-activated protein kinase and translation initiation, Science 266, 653-656.
55. Haghighat, A., Mader, S., Pause, A. & Sonenberg, N. (1995) Repression of cap-dependent translation by 4E-binding protein 1: competition with p220 for binding to eukaryotic initiation factor-4E, EMBO J. 14, 5701-5709.
56. Flynn, A. & Proud, C. G. (1996) Insulin-stimulated phosphorylation of initiation factor 4E is mediated by the MAP kinase pathway, FEBS Lett. 389, 162-166.
57. Lawrence, J. C. Jr & Abraham, R. T. (1997) PHAS/4E-BPs as regulators of mRNA translation and cell proliferation, Trends Biochem. Sci. 22, 345-349.
58. Mendez, R., Myers, M. G. Jr, White, M. F. & Rhoads, R. E. (1996) Stimulation of protein synthesis, eukaryotic translation initiation factor 4E phosphorylation, and PHAS-I phosphorylation by insulin requires insulin receptor substrate 1 and phosphatidylinositol 3-kinase, Mol. Cell. Biol. 16, 2857-2864.
59. Feigenblum, D. & Schneider, R. J. (1996) Cap-binding protein (eukaryotic initiation factor 4E) and 4E-inactivating protein BP-1 independently regulate cap-dependent translation, Mol. Cell. Biol. 16, 5450-5457.
60. Scheper, G. C., Mulder, J., Kleijn, M., Voorma, H. O. & Thomas, A. A. M. (1997) Inactivation of eIF2B and phosphorylation of PHAS-I in heat-shocked rat hepatoma cells, J. Biol. Chem. 272, 26 850-26 856.
61. Vries, R. G. J., Flynn, A., Patel, J. C., Wang, X., Denton, R. M. & Proud, C. G. (1998) Heat shock increases the association of binding protein-1 with initiation factor 4E, J. Biol. Chem. 272, 32 779-32 784.
62. Beretta, L., Gingras, A.-C., Svitkin, Y. V., Hall, M. N. & Sonenberg, N. (1996) Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation, EMBO J. 15, 658-664.
63. Rowlands, A. G., Montine, K. S., Henshaw, E. C. & Panniers, R. (1988) Physiological stresses inhibit guanine-nucleotide-exchange factor in Ehrlich cells, Eur. J. Biochem. 175, 93-99.
64. Oldfield, S., Jones, B. L., Tanton, D. & Proud, C. G. (1994) Use of monoclonal antibodies to study the structure and function of eukaryotic protein synthesis initiation factor eIF-2B, Eur. J. Biochem. 221, 399-410.
65. Price, N. & Proud, C. G. (1994) The guanine nucleotide-exchange factor, eIF-2B, Biochimie (Paris) 76, 748-760.
66. Yang, W. & Hinnebusch, A. G. (1996) Identification of a regulatory subcomplex in the guanine nucleotide exchange factor eIF2B that mediates inhibition by phosphorylated eIF2, Mol. Cell. Biol. 16, 6603-6616.
67. Fabian, J. R., Kimball, S. R., Heinzinger, N. K. & Jefferson, L. S. (1997) Subunit assembly and guanine nucleotide exchange activity of eukaryotic initiation factor-2B expressed in Sf9 cells, J. Biol. Chem. 272, 12 359-12 365.
68. Dholakia, J. N., Mueser, T. C., Woodley, C. L., Parkhurst, L. J. & Wahba, A. J. (1986) The association of NADPH with the guanine nucleotide exchange factor from rabbit reticulocytes: a role of pyridine dinucleotides in eukaryotic polypeptide chain initiation, Proc. Natl Acad. Sci. USA 83, 6746-6750.
69. Kimball, S. R., Mellor, H., Flowers, K. M. & Jefferson, L. S. (1996) Role of translation initiation factor eIF-2B in the regulation of protein synthesis in mammalian cells, Prog. Nucleic Acid. Res. Mol. Biol. 54, 165-196.
70. Rowlands, A. G., Panniers, R. & Henshaw, E. C. (1988) The catalytic mechanism of guanine nucleotide exchange factor action and competitive inhibition by phosphorylated eukaryotic initiation factor 2, J. Biol. Chem. 263, 5526-5533.
71. Gross, M. & Rubino, M. S. (1989) Regulation of eukaryotic initiation factor-2B activity by polyamines and amino acid starvation in rabbit reticulocyte lysate, J. Biol. Chem. 264, 21 879-21 884.
72. Gross, M., Rubino, M. S. & Starn, T. K. (1988) Regulation of protein synthesis in rabbit reticulocyte lysate. Glucose 6-phosphate is required to maintain the activity of eukaryotic initiation factor (eIF)-2B by a mechanism that is independent of the phosphorylation of eIF-2α, J. Biol. Chem. 263, 12 486-12 492.
73. Dholakia, J. N. & Wahba, A. J. (1988) Phosphorylation of the guanine nucleotide exchange factor from rabbit reticulocytes regulates its activity in polypeptide chain initiation, Proc. Natl Acad. Sci. USA 85, 51-54.
74. Welsh, G. I. & Proud, C. G. (1993) Glycogen synthase kinase-3 is rapidly inactivated in response to insulin and phosphorylates eukaryotic initiation factor eIF-2B, Biochem. J. 294, 625-629.
75. Kimball, S. R. & Jefferson, L. S. (1988) Effect of diabetes on guanine nucleotide exchange factor activity in skeletal muscle and heart, Biochem. Biophys. Res. Commun. 156, 706-711.
76. Cox, S., Redpath, N. T. & Proud, C. G. (1988) Regulation of polypeptide-chain initiation in rat skeletal muscle. Starvation does not alter the activity or phosphorylation state of initiation factor eIF-2, FEBS Lett. 239, 333-338.
77. Jeffrey, I. W., Kelly, F. J., Duncan, R., Hershey, J. W. B. & Pain, V. M. (1990) Effect of starvation and diabetes on the activity of the eukaryotic initiation factor eIF-2 in rat skeletal muscle, Biochimie (Paris) 72, 751-757.
78. Duncan, R. F. & Hershey, J. W. B. (1989) Protein synthesis and protein phosphorylation during heat stress, recovery, and adaptation, J. Cell. Biol. 109, 1467-1481.
79. Kaspar, R. L., Rychlik, W., White, M. W., Rhoads, R. E. & Morris, D. R. (1990) Simultaneous cytoplasmic redistribution of ribosomal protein L32 mRNA and phosphorylation of eukaryotic initiation factor 4E after mitogenic stimulation of Swiss 3T3 cells, J. Biol. Chem. 265, 3619-3622.
80. Welsh, G. I. & Proud, C. G. (1992) Regulation of protein synthesis in Swiss 3T3 fibroblasts - rapid activation of the guanine-nucleotide-exchange factor by insulin and growth factors, Biochem. J. 284, 19-23.
81. Kleijn, M., Welsh, G. I., Scheper, G. C., Voorma, H. O., Proud, C. G. & Thomas, A. A. M. (1998) Nerve and epidermal growth factor induce protein synthesis and eIF2B activation in PC12 cells, J. Biol. Chem. 273, 5536-5541.
82. S6K pathway and is independent of mitogen-activated protein kinase, Proc. Natl Acad. Sci. USA 93, 4076-4080.
83. Kimball, S. R., Jefferson, L. S., Fadden, P., Haystead, T. A. J. & Lawrence, J. C. Jr (1996) Insulin and diabetes cause reciprocal changes in the association of eIF-4E and PHAS-I in rat skeletal muscle, Am. J. Physiol. 270, C705-C709.
84. Samuel, C. E. (1993) The eIF-2-α protein kinases, regulators of translation in eukaryotes from yeasts to humans, J. Biol. Chem. 268, 7603-7606.
85. De Haro, C., Méndez, R. & Santoyo, J. (1996) The eIF-2α kinases and the control of protein synthesis, FASEB J. 10, 1378-1387.
86. Sonenberg, N. (1990) Measures and countermeasures in the modulation of initiation factor activities by viruses, New Biol. 2, 402-409.
87. Katze, M. G. (1995) Regulation of the interferon-induced PKR: can viruses cope? Trends Microbiol. 3, 75-78.
88. Hinnebusch A. G. (1997) Translational regulation of yeast GCN4. A window on factors that control initiator-trna binding to the ribosome, J. Biol. Chem. 272, 21 661-21 664.
89. Duncan, R. & Hershey, J. W. B. (1985) Regulation of initiation factors during translational repression caused by serum depletion, J. Biol. Chem. 260, 5493-5497.
90. Webster, C., Gaut, R. L., Browning, K. S., Ravel, J. M. & Roberts, J. K. M. (1991) Hypoxia enhances phosphorylation of eukaryotic initiation factor 4A in maize root tips, J. Biol. Chem. 266, 23 341-23 346.
91. Wolthuis, R. M. F., Cremers, A. F. M., Kasperaitis, M. A. M., van der Mast, C. A., Voorma, H. O. & Boonstra, J. (1993) Epidermal growth factor stimulates phosphorylation of eukaryotic initiation factor 4B, independently of protein kinase C, Biochim. Biophys. Acta 1177, 160-166.
92. Morley, S. J. & Traugh, J. A. (1989) Phorbol esters stimulate phosphorylation of eukaryotic initiation factors 3, 4B, and 4F, J. Biol. Chem. 264, 2401-2404.
93. Morley, S. J. & Traugh, J. A. (1990) Differential stimulation of phosphorylation of initiation factors eIF-4F, eIF-4B, eIF-3, and ribosomal protein S6 by insulin and phorbol esters, J. Biol. Chem. 265, 10 611-10 616.
94. Donaldson, R. W., Hagedorn, C. H. & Cohen, S. (1991) Epidermal growth factor or okadaic acid stimulates phosphorylation of eukaryotic initiation factor 4F, J. Biol. Chem. 266, 3162-3166.
95. Bu, X., Haas, D. W. & Hagedorn, C. H. (1993) Novel phosphorylation sites of eukaryotic initiation factor-4F and evidence that phosphorylation stabilizes interactions of the p25 and p220 subunits, J. Biol. Chem. 268, 4975-4978.
96. Morley, S. J., Dever, T. E., Etchison, D. & Traugh, J. A. (1991) Phosphorylation of eIF-4F by protein kinase C or multipotential S6 kinase stimulates protein synthesis at initiation, J. Biol. Chem. 266, 4669-4672.
97. s6k, Crit. Rev. Biochem. Mol. 29, 385-413.
98. Bandi, H. R., Ferrari, S., Krieg, J., Meyer, H. E. & Thomas, G. (1993) Identification of 40S ribosomal protein S6 phosphorylation sites in Swiss mouse 3T3 fibroblasts stimulated with serum, J. Biol. Chem. 268, 4530-4533.
99. Duncan, R. & McConkey, E. H. (1982) Preferential utilization of phosphorylated 40-S ribosomal subunits during initiation complex formation, Eur. J. Biochem. 123, 535-538.
100. Jefferies, H. B. J., Reinhard, C., Kozma, S. C. & Thomas, G. (1994) Rapamycin selectively represses translation of the 'polypyrimidine tract' mRNA family, Proc. Natl Acad. Sci. USA 91, 4441-4445.
101. Kaspar, R. L., Kakegawa, T., Cranston, H., Morris, D. R. & White, M. W. (1992) A regulatory cis element and a specific binding factor involved in the mitogenic control of murine ribosomal protein L32 translation, J. Biol. Chem. 267, 508-514.
102. Jefferies, H. B. J. & Thomas, G. (1996). Ribosomal protein S6 phosphorylation and signal-transduction. In Translational control (Hershey, J. W. B., Mathews, M. B. & Sonenberg, N., eds) pp. 389-409, Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
103. Terada, N., Patel, H. R., Takase, K., Kohno, K., Nairn, A. C. & Gelfand, E. W. (1994) Rapamycin selectively inhibits translation of mRNAs encoding elongation factors and ribosomal proteins, Proc. Natl Acad. Sci. USA 91, 11 477-11 481.
104. S6K, EMBO J. 16, 3693-3704.
105. s6k inactivation is a novel phosphorylation site within a conserved hydrophobic domain, EMBO J. 14, 5279-5287.
106. Chung, J., Kuo, C. J., Crabtree, G. R. & Blenis, J. (1992) Rapamycin-FKBP specifically blocks growth-dependent activation of and signalling by the 70 kd S6 protein kinases, Cell 69, 1227-1236.
107. Burgering, B. M. T. & Coffer, P. J. (1995) Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal-transduction. Nature 376, 599-602.
108. ras, Nature 371, 426-429.
109. Kuo, C. J., Chung, J., Fiorentino, D. F., Flanagan, W. M., Blenis, J. & Crabtree, G. R. (1992) Rapamycin selectively inhibits interleukin-2 activation of p70 S6 kinase, Nature 358, 70-73.
110. Price, D. J., Grove, J. R., Calvo, V., Avruch, J. & Bierer, B. E. (1992) Rapamycin-induced inhibition of the 70-kilodalton S6 protein kinase, Science 257, 973-977.
111. Tuazon, P. T., Morley, S. J., Dever, T. E., Merrick, W. C., Rhoads, R. E. & Traugh, J. A. (1990) Association of initiation factor eIF-4E in a cap binding protein complex (eIF-4F) is critical for and enhances phosphorylation by protein kinase C, J. Biol. Chem. 265, 10 617-10 621.
112. Haas, D. W. & Hagedorn, C. H. (1991) Casein kinase 1 phosphorylates the 25-kDa mRNA cap binding protein, Arch. Biochem. Biophys. 284, 84-89.
113. Amick, G. D. & Damuni, Z. (1992) Protamine kinase phosphorylates eukaryotic protein synthesis initiation factor 4E, Biochem. Biophys. Res. Commun. 183, 431-437.
114. Waskiewicz, A. J., Flynn, A., Proud, C. G. & Cooper, J. A. (1997) Mitogen-activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2, EMBO J. 16, 1909-1920.
115. Makkinje, A., Xiong, H., Li, M. & Damuni, Z. (1995) Phosphorylation of eukaryotic initiation factor 4E by insulin-stimulated protein kinase, J. Biol. Chem. 270, 14 824-14 828.
116. Flynn, A. & Proud, C. G. (1996) Insulin and phorbol ester stimulate initiation factor eIF-4E phosphorylation by distinct pathways in Chinese hamster ovary cells overexpressing the insulin receptor, Eur. J. Biochem. 236, 40-47.
117. Rychlik, W., Rush, J. S., Rhoads, R. E. & Waechter, C. J. (1990) Increased rate of phosphorylation-dephosphorylation of the translational initiation factor eIF-4E correlates with the induction of protein and glycoprotein biosynthesis in activated B lymphocytes, J. Biol. Chem. 265, 19 467-19 471.
118. Smith, M. R., Jaramillo, M., Tuazon, P. T., Traugh, J. A., Liu, Y.-L., Sonenberg, N. & Kung, H. (1991) Modulation of the mitogenic activity of eukaryotic translation initiation factor-4E by protein kinase C, New Biol. 3, 601-607.
119. Bialojan, C. & Takai, A. (1988) Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases, Biochem. J. 256, 283-290.
120. Cohen, P., Holmes, C. F. B. & Tsukitani, Y. (1990) Okadaic acid: a new probe for the study of cellular regulation, Trends Biochem. Sci. 15, 98-102.
121. Bu, X. & Hagedorn, C. H. (1992) Phosphoprotein phosphatase 2A dephosphorylates eIF-4E and does not alter binding to the mRNA cap, FEBS Lett. 301, 15-18.
122. Guy, G. R., Cao, X., Chua, S. P. & Tan, Y. H. (1992) Okadaic acid mimics multiple changes in early protein phosphorylation and gene expression induced by tumor necrosis factor or interleukin-1, J. Biol. Chem. 267, 1846-1852.
123. Haystead, T. A. J., Haystead, C. M. M., Hu, C., Lin, T.-A. & Lawrence J. C. Jr (1994) Phosphorylation of PHAS-I by mitogen-activated protein (MAP) kinase, J. Biol. Chem. 269, 23 185-23 191.
124. Aronica, S. M., Gingras, A.-C., Sonenberg, N., Cooper, S., Hague, N. & Broxmeyer, H. E. (1997) Macrophage inflammatory protein-1α and interferon-inducible protein 10 inhibit synergistically induced growth-factor stimulation of MAP kinase activity and suppress phosphorylation of eukaryotic initiation factor 4E and 4E binding protein 1, Blood 89, 3582-3595.
125. Lin, T.-A., Kong, X., Saltiel, A. R., Blackshear, P. J. & Lawrence J. C. Jr (1995) Control of PHAS-I by insulin in 3T3-L1 adipocytes, J. Biol. Chem. 270, 18 531-18 538.
126. Azpiazu, I., Saltiel, A. R., DePaoli-Roach, A. A. & Lawrence, J. C. Jr (1996) Regulation of both glycogen synthase and PHAS-I by insulin in rat skeletal muscle involves mitogen-activated protein kinase-independent and rapamycin-sensitive pathways, J. Biol. Chem. 271, 5033-5039.
127. Graves, L. M., Bornfeldt, K. E., Argast, G. M., Krebs, E. G., Kong, X., Lin, T. A. & Lawrence, J. C. Jr (1995) cAMP- and rapamycin-sensitive regulation of the association of eukaryotic initiation factor 4E and the translational regulator PHAS-I in aortic smooth muscle cells, Proc. Natl Acad. Sci. USA 92, 7222-7226.
128. Kleijn, M., Korthout, M. M. R., Voorma, H. O. & Thomas, A. A. M. (1996) Phosphorylation of the eIF4E-binding protein PHAS-I after exposure of PC12 cells to EGF and NGF, FEBS Lett. 396, 165-171.
129. Arnott, C. H., Atkinson, P. G., Sale, E. M. & Sale, G. J. (1997) PHAS-I phosphorylation in response to foetal bovine serum (FBS) is regulated by an ERK1/ERK2-independent and rapamycin-sensitive pathway in 3T3-L1 adipocytes, FEBS Lett. 406, 179-183.
130. Saito, Y., Vanderheede, J. R. & Cohen, P. (1994) The mechanism by which epidermal growth factor inhibits glycogen synthase kinase 3 in A431 cells, Biochem. J. 303, 27-31.
131. Cross, D. A. E., Alessi, D. R., Vandenheede, J. R., McDowell, H. E., Hundal, H. S. & Cohen, P. (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.
132. Welsh, G. I., Foulstone, E. J., Young, S. W., Tavare, J. M. & Proud, C. G. (1994) Wortmannin inhibits the effects of insulin and serum on the activities of glycogen synthase kinase-3 and mitogen-activated protein kinase, Biochem. J. 303, 15-20.
133. Brunn, G. J., Williams, J., Sabers, C., Wiederrecht, G., Lawrence, J. C. Jr & Abraham, R. T. (1996) Direct inhibition of the signalling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002, EMBO J. 15, 5256-5267.
134. Yamauchi, T., Tobe, K., Tamemoto, H., Ueki, K., Kaburagi, Y., Yamamoto-Honda, R., Takahashi, Y. Yoshizawa, F., Aizawa, S., Akanuma, Y., Sonenberg, N., Yazaki, Y. & Kadowaki, T. (1996) Insulin sigballing and insulin actions in the muscles and livers of insulin-resistant, insulin receptor substrate 1-deficient mice, Mol. Cell. Biol. 16, 3074-3084.
135. Brunn, G. J., Hudson, C. C., Sekulic, A., Williams, J. M., Hosoi, H., Houghton, P. J., Lawrence, J. C. Jr & Abraham, R. T. (1997) Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin, Science 277, 99-101.
136. Diggle, T. A., Moule, S. K., Avison, M. B., Flynn, A., Foulstone, E. J., Proud, C. G. & Denton, R. M. (1996) Both rapamycin-sensitive and -insensitive pathways are involved in the phosphorylation of the initiation factor-4E-binding protein (4E-BP1) in response to insulin in rat epididymal fat-cells, Biochem. J. 316, 447-453.
137. Fadden, P., Haystead, T. A. & Lawrence, J. C. Jr (1997) Identification of phosphorylation sites in the translational regulator, PHAS-I, that are controlled by insulin and rapamycin in rat adipocytes, J. Biol. Chem. 272, 10 240-10 247.
138. Fiol, C. J., Mahrenholz, A. M., Wang, Y., Roeske, R. W. & Roach, P. J. (1987) Formation of protein kinase recognition sites by covalent modification of the substrate, J. Biol. Chem. 262, 14 042-14 048.
139. Welsh, G. I., Wilson, C. & Proud, C. G. (1996) GSK3: a shaggy frog story, Trends Cell Biol. 6, 274-279.
140. Singh, L. P., Denslow, N. D. & Wahba, A. J. (1996) Modulation of rabbit reticulocyte guanine nucleotide exchange factor activity by casein kinase 1 and 2 and glycogen synthase kinase 3, Biochemistry 35, 3206-3212.
141. Welsh, G. I., Miyamoto, S., Price, N. T., Safer, B. & Proud, C. G. (1996) T-cell activation leads to rapid stimulation of translation initiation factor eIF2B and inactivation of glycogen synthase kinase-3, J. Biol. Chem. 271, 11 410-11 413.
142. Welsh, G. I., Stokes, C. M., Wang, X., Sakaue, H., Ogawa, W., Kasuga, M. & Proud, C. G. (1997) Activation of translation initiation factor eIF2B by insulin requires phosphatidyl inositol 3-kinase, FEBS Lett. 410, 418-422.
143. Sommercorn, J., Mulligan, J. A., Lozeman, F. J. & Krebs, E. G. (1987) Activation of casein kinase II in response to insulin and to epidermal growth factor. Proc. Natl Acad. Sci. USA 84, 8834-8838.
144. Klarlund, J. K. & Czech, M. P. (1988) Insulin-like growth factor I and insulin rapidly increase casein kinase II activity in BALB/c 3T3 fibroblasts, J. Biol. Chem. 263, 15 872-15 875.
145. Ackerman, P. & Osheroff, N. (1989) Regulation of casein kinase II activity by epidermal growth factor in human A-431 carcinoma cells, J. Biol. Chem. 264, 11 958-11 965.
146. Carroll, D. & Marshak, D. R. (1989) Serum-stimulated cell growth causes oscillations in casein kinase II activity, J. Biol. Chem. 264, 7345-7348.
147. Sutherland, C., Leighton, I. A. & Cohen, P. (1993) Inactivation of glycogen synthase kinase-3β by phosphorylation: new kinase connections in insulin and growth-factor signalling, Biochem. J. 296, 15-19.
148. Sutherland, C. & Cohen, P. (1994) The α-isoform of glycogen synthase kinase-3 from rabbit skeletal muscle is inactivated by p70 S6 kinase or MAP kinase-activated protein kinase-1 in vitro, FEBS Lett. 338, 37-42.
149. Cross, D. A. E., Alessi, D. R., Cohen, P., Andjelković, M. & Hemmings, B. A. (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B, Nature 378, 785-789.
150. Moule, S. K., Edgell, N. J., Welsh, G. I., Diggle, T. A., Foulstone, E. J., Heesom, K. J., Proud, C. G. & Denton, R. M. (1995) Multiple signalling pathways involved in the stimulation of fatty acid and glycogen synthesis by insulin in rat epididymal fat cells, Biochem. J. 311, 595-601.
151. Moule, S. K., Welsh, G. I., Edgell, N. J., Foulstone, E. J., Proud, C. G. & Denton, R. M. (1997) Regulation of protein kinase B and glycogen synthase kinase-3 by insulin and ß-adrenergic agonists in rat epididymal fat cells, J. Biol. Chem. 272, 7713-7719.
152. Morley, S. J. & Pain, V. M. (1995) Translational regulation during activation of porcine peripheral blood lymphocytes: association and phosphorylation of the α and the γ subunits of the initiation factor complex eIF-4F, Biochem. J. 312, 627-635.
153. Huang, J. & Schneider, R. J. (1991) Adenovirus inhibition of cellular protein synthesis involves inactivation of cap binding protein, Cell 65, 271-280.
154. Lamphear, B. J. & Panniers, R. (1991) Heat shock impairs the interaction of cap binding protein complex with 5′ mRNA cap, J. Biol. Chem. 266, 2789-2794.
155. Bonneau, A. & Sonenberg, N. (1987) Involvement of the 24-kDa cap binding protein in regulation of protein synthesis in mitosis, J. Biol. Chem. 262, 11 134-11 139.
156. Frederickson, R. M., Montine, K. S. & Sonenberg, N. (1991) Phosphorylation of eukaryotic translation initiation factor 4E is increased in Src-transformed cell lines, Mol. Cell. Biol. 11, 2896-2900.
157. Marino, M. W., Feld, L. J., Jaffe, E. A., Pfeffer, L. M., Han, H.-M. & Donner, D. B. (1991) Phosphorylation of the proto-oncogene product eukaryotic initiation factor 4E is a common cellular response to tumor necrosis factor, J. Biol. Chem. 266, 2685-2688.
158. Bu, X. & Hagedorn, C. H. (1991) Platelet-derived growth factor stimulates phosphorylation of the 25 kDa mRNA cap binding protein (eIF-4E) in human lung fibroblasts, FEBS Lett. 283, 219-222.
159. Rinker-Schaeffer, C. W., Austin, V., Zimmer, S. & Rhoads, R. E. (1992) ras Transformation of cloned rat embryo fibroblasts results in increased rates of protein synthesis and phosphorylation of eukaryotic initiation factor 4E, J. Biol. Chem. 267, 10 659-10 664.
160. Rao, G. N., Griendling, K. K., Frederickson, R. M., Sonenberg, N. & Alexander, R. W. (1994) Angiotensin II induces phosphorylation of eukaryotic protein synthesis initiation factor 4E in vascular smooth muscle cells, J. Biol. Chem. 269, 7180-7184.
161. Morley, S. J., Rau, M., Kay, J. E. & Pain, V. M. (1993) Increased phosphorylation of eukaryotic initiation factor 4α during early activation of T lymphocytes correlates with increased initiation factor 4F complex formation, Eur. J. Biochem. 218, 39-48.
162. Boal, T. R., Chiorini, J. A., Cohen, R. B., Miyamoto, S., Frederickson, R. M., Sonenberg, N. & Safer, B. (1993) Regulation of eukaryotic translation initiation factor expression during T-cell activation, Biochim. Biophys. Acta 1176, 257-264.
163. Mick, S. J., Abramson, R. D., Ray, B. K., Merrick, W. C., Thach, R. E. & Hagedorn, C. H. (1988) Induction of eIF-4E phosphorylation by the addition of 1-pyrroline-5-carboxylic acid to rabbit reticulocyte lysate, FEBS Lett. 236, 484-488.
164. Gierman, T. D., Frederickson, R. M., Sonenberg, N. & Pickup, D. J. (1992) The eukaryotic initiation factor 4E is not modified during the course of vaccinia virus replication, Virology 188, 934-937.
165. Schnierle, B. S. & Moss, B. (1992) Vaccinia virus-mediated inhibition of protein synthesis involved neither degradation nor underphosphorylation of components of the cap binding eukaryotic translation initiation factor complex eIF-4F, Virology 188, 931-933.
166. Buckley, B. & Ehrenfeld, E. (1986) Two-dimensional gel analyses of the 24-kDa cap binding protein from poliovirus-infected and uninfected HeLa cells, Virology 152, 497-501.
167. r-22000 protein in 3T3-L1 adipocytes, Biochem. J. 214, 11-19.
168. Jedlicka, P. & Panniers, R. (1991) Mechanism of activation of protein synthesis initiation in mitogen-stimulated T lymphocytes, J. Biol. Chem. 266, 15 663-15 669.
169. Gilligan, M., Welsh, G. I., Flynn, A., Bujalska, I., Diggle, T. A., Denton, R. M., Proud, C. G. & Docherty, K. (1996) Glucose stimulates the activity of the guanine nucleotide-exchange factor eIF-2B in isolated rat islets of langerhans, J. Biol. Chem. 271, 2121-2125.
170. Akkaraju, G. R., Hansen, L. J. & Jagus, R. (1991) Increase in eukaryotic initiation factor 2B activity following fertilization reflects changes in redox potential, J. Biol. Chem. 266, 24 451-24 459.
171. Clemens, M. J., Galpine, A., Austin, S. A., Panniers, R., Henshaw, E. C., Duncan, R. F., Hershey, J. W. B. & Pollard, J. W. (1987) Regulation of polypeptide chain initiation in Chinese hamster ovary cells with a temperature-sensitive leucyl-tRNA synthetase. Changes in phosphorylation of initiation factor eIF-2 and in the activity of the guanine nucleotide exchange factor GEF, J. Biol. Chem. 262, 767-771.
172. Kimball, S. R. & Jefferson, L. S. (1990) Mechanism of the inhibition of protein synthesis by vasopressin in rat liver, J. Biol. Chem. 265, 16 794-16 798.
173. Kimball, S. R. & Jefferson, L. S. (1991) Inhibition of microsomal calcium sequestration causes an impairment of initiation of protein synthesis in perfused rat liver, Biochem. Biophys. Res. Commun. 177, 1082-1086.
174. Kimball, S. R., Antonetti, D. A., Brawley, R. M. & Jefferson, L. S. (1991) Mechanism of inhibition of peptide chain initiation by amino acid deprivation in perfused rat liver. Regulation involving inhibition of eukaryotic initiation factor 2α phosphatase activity, J. Biol. Chem. 266, 1969-1976.
175. Prostko, C. R., Brostrom, M. A., Malara, E. M. & Brostrom, C. O. (1992) Phosphorylation of eukaryotic initiation factor (eIF) 2α and inhibition of eIF-2B in GH3 pituitary cells by perturbants of early protein processing that induce GRP78, J. Biol. Chem. 267, 16 751-16 754.