The mRNA 5' cap-binding protein elF4E and control of cell growth

Current Opinion in Cell Biology

Volumn 10, Issue 2, 1998, Pages 268-275

  Sonenberg, Nahum ^a   Gingras, Anne Claude ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 4E; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE;

CELL GROWTH; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GROWTH REGULATION; PRIORITY JOURNAL; REVIEW;

EID: 0032054816     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(98)80150-6     Document Type: Article

References (75)

1. Sonenberg N. mRNA 5′ cap-binding protein eIF4E and control of cell growth. Hershey JWB, Mathews MB, Sonenberg N. Translational Control. 1996;245-269 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
2. Hershey JWB, Mathews MB, Sonenberg N. Translational control. 1996;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
3. Hershey JWB. Translational control in mammalian cells. Annu Rev Biochem. 60:1991;715-755.
4. Mathews MB, Sonenberg N, Hershey JWB. Origins and targets of translational control. Hershey JWB, Mathews MB, Sonenbeg N. Translational Control. 1996;1-30 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
5. Rau M, Ohlmann T, Morley SJ, Pain VM. A reevaluation of the cap-binding protein, eIF4E, as a rate-limiting factor for initiation of translation in reticulocyte lysate. J Biol Chem. 271:1996;8983-8990.
6. Pain VM. Initiation of protein synthesis in eukaryotic cells. Eur J Biochem. 236:1996;747-771.
7. Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK. Cocrystal structure of the messenger RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDP. of outstanding interest Cell. 89:1997;951-961 A 2.2 Å resolution of murine eIF4E-m7GDP co-crystals provides important information on the cap-binding properties of eIF4E. It also suggests a mechanism whereby phosphorylation of eIF4E could increase its affinity for mRNA caps.
8. Matsuo H, Li HJ, McGuire AM, Fletcher CM, Gingras AC, Sonenberg N, Wagner G. Structure of translation factor eIF4E bound to m7GDP and interaction with 4E-binding protein. of outstanding interest Nature Struct Biol. 4:1997;717-724 The structure of yeast eIF4E as determined by NMR provides important information about the cap-binding site and 4E-BP1 binding. The structure underscores the conservation between yeast and mammalian eIF4E.
9. Lamphear BJ, Panniers R. Cap binding protein complex that restores protein synthesis in heat-shocked Ehrlich cell lysates contains highly phosphorylated eIF-4E. J Biol Chem. 265:1990;5333-5336.
10. Minich WB, Balasta ML, Goss DJ, Rhoads RE. Chromatographic resolution of in vivo phosphorylated and nonphosphorylated eukaryotic translation initiation factor eIF-4E: increased cap affinity of the phosphorylated form. Proc Natl Acad Sci USA. 91:1994;7668-7672.
11. Bonneau AM, Sonenberg N. Involvement of the 24-kDa cap-binding protein in regulation of protein synthesis in mitosis. J Biol Chem. 262:1987;11134-11139.
12. Haas DW, Shepherd VL, Hagedorn CH. Lipopolysaccharide stimulates phosphorylation of eukaryotic initiation factor-4F in macrophages and tumor necrosis factor participates in this event. Second Messengers Phosphoproteins. 14:1992;163-171.
13. Marino MW, Dunbar JD, Wu LW, Ngaiza JR, Han HM, Guo D, Matsushita M, Nairn AC, Zhang Y, Kolesnick R, et al. Inhibition of tumor necrosis factor signal transduction in endothelial cells by dimethylaminopurine. J Biol Chem. 271:1996;28624-28629.
14. Duncan R, Hershey JW. Heat shock-induced translational alterations in HeLa cells. Initiation factor modifications and the inhibition of translation. J Biol Chem. 259:1984;11882-11889.
15. Wada H, Ivester CT, Carabello BA, Cooper GT, McDermott PJ. Translational initiation factor eIF-4E. A link between cardiac load and protein synthesis. J Biol Chem. 271:1996;8359-8364.
16. Rao GN, Griendling KK, Frederickson RM, Sonenberg N, Alexander RW. Angiotensin II induces phosphorylation of eukaryotic protein synthesis initiation factor 4E in vascular smooth muscle cells. J Biol Chem. 269:1994;7180-7184.
17. Joshi B, Cai AL, Keiper BD, Minich WB, Mendez R, Beach CM, Stepinski J, Stolarski R, Darzynkiewicz E, Rhoads RE. Phosphorylation of eukaryotic protein synthesis initiation factor 4E at Ser-209. J Biol Chem. 270:1995;14597-14603.
18. Waskiewicz AJ, Flynn A, Proud CG, Cooper JA. Mitogen-activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2. of special interest EMBO J. 16:1997;1909-1920 The authors isolated two cDNAs termed MNK1 and MNK2 using ERK2 as bait. These are two related kinases that bind to ERK2 and p38, but not to JNK1. MNK1 phosphorylates eIF4E in vitro on Ser209.
19. Fukunaga R, Hunter T. MNK1, a new MAP-kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates. of special interest EMBO J. 16:1997;1921-1933 The cloning of MNK1 as a substrate for ERK1 using a novel expression screening technique to identify kinase substrates. MNK1 was phosphorylated and activated in vitro by ERK1 and p38 MAPK, but not by JNK/SAPK, and in vivo by growth factors and stresses.
20. Flynn A, Proud G. Insulin-stimulated phosphorylation of initiation factor 4E is mediated by the MAP kinase pathway. FEBS Lett. 389:1996;162-166.
21. Morley SJ, McKendrick L. 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. 272:1997;17887-17893.
22. Lawrence JC, Abraham RT. PHAS/4E-BPs as regulators of mRNA translation and cell proliferation. Trends Biochem Sci. 22:1997;345-349.
23. Altmann M, Schmitz N, Berset C, Trachsel H. A novel inhibitor of cap-dependent translation initiation in yeast - p20 competes with eIF4G for binding to eIF4E. of special interest EMBO J. 16:1997;1114-1121 The yeast protein p20 is a functional homologue of mammalian 4E-BPs, implying a common mechanism for translational regulation from yeast to mammals.
24. Pause A, Belsham GJ, Gingras AC, Donze O, Lin TA, Lawrence J Jr, Sonenberg N. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature. 371:1994;762-767.
25. Hu C, Pang S, Kong X, Velleca M, Lawrence J Jr. Molecular cloning and tissue distribution of PHAS-I, an intracellular target for insulin and growth factors. Proc Natl Acad Sci USA. 91:1994;3730-3734.
26. Mader S, Lee H, Pause A, Sonenberg N. 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. 15:1995;4990-4997.
27. Lin TA, Kong X, Haystead TA, Pause A, Belsham G, Sonenberg N, Lawrence J Jr. PHAS-I as a link between mitogen-activated protein kinase and translation initiation. Science. 266:1994;653-656.
28. Haghighat A, Mader S, Pause A, Sonenberg N. Repression of cap-dependent translation by 4E-binding protein 1: competition with p220 for binding to eukaryotic initiation factor-4E. EMBO J. 14:1995;5701-5709.
29. Fleurent M, Gingras AC, Sonenberg N, Meloche S. Angiotensin II stimulates phosphorylation of the translational repressor 4E-binding protein 1 by a mitogen-activated protein kinase-independent mechanism. J Biol Chem. 272:1997;4006-4012.
30. Aronica SM, Gingras AC, Sonenberg N, Cooper S, Hague N, Broxmeyer HE. Macrophage inflammatory protein-1-alpha 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. 89:1997;3582-3595.
31. Kleijn M, Korthout MMR, Voorma HO, Thomas AAM. Phosphorylation of the eIF4E-binding protein PHAS-I after exposure of PC12 cells to EGF and NGF. FEBS Lett. 396:1996;165-171.
32. Graves LM, Bornfeldt KE, Argast GM, Krebs EG, Kong X, Lin TA, Lawrence JC Jr. 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. 92:1995;7222-7226.
33. Fadden P, Haystead TAJ, Lawrence JC. Identification of phosphorylation sites in the translational regulator, PHAS-I, that are controlled by insulin and rapamycin in rat adipocytes. J Biol Chem. 272:1997;10240-10247.
34. von Manteuffel SR, Gingras A-C, Ming XF, Sonenberg N, Thomas G. 4E-BP1 phosphorylation is mediated by the FRAP-p70s6k pathway and is independent of mitogen-activated protein kinase. Proc Natl Acad Sci USA. 93:1996;4076-4080.
35. Hara K, Yonezawa K, Kozlowski MT, Sugimoto T, Andrabi K, Weng QP, Kasuga M, Nishimoto I, Avruch J. Regulation of eIF-4E BP1 phosphorylation by mTOR. J Biol Chem. 272:1997;26457-26463.
36. Vanhaeserbroek B, Leevers SJ, Panayotou G, Waterfield MD. Phosphoinositide 3-kinases: a conserved family of signal transducers. Trends Biochem Sci. 22:1997;267-272.
37. Akimoto K, Takahashi R, Moriya S, Nishioka N, Takayanagi J, Kimura K, Fukui Y, Osada S, Mizuno K, Hirai A, et al. EGF or PDGF receptors activate atypical PKClambda through phosphatidylinositol 3-kinase. EMBO J. 15:1996;788-798.
38. Burgering BM, Coffer PJ. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature. 376:1995;599-602.
39. Franke TF, Yang S, Chan TO, Datta D, Kazlauskas A, Morrison DK, Kaplan DR, Tsichlis PN. The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell. 81:1995;727-736.
40. Mendez R, Kollmorgen G, White MF, Rhoads RE. Requirement of protein kinase C-ζ for stimulation of protein synthesis by insulin. Mol Cell Biol. 17:1997;5184-5192.
41. Franke TF, Kaplan DR, Cantley LC. PI3K: Downstream AKTion blocks apoptosis. Cell. 88:1997;435-437.
42. Marte BM, Downward J. PKB/AKT - connecting phosphoinositide 3-kinase to cell survival and beyond. Trends Biochem Sci. 22:1997;355-358.
43. Jefferies HBJ, Thomas G. Ribosomal protein S6 phosphorylation and signal transduction. Hershey JWB, Mathews MB, Sonenberg N. Translational Control. 1996;389-409 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
44. Heitman J, Movva NR, Hall MN. Targets for cell cycle arrest by the immunopressant rapamycin in yeast. Science. 253:1991;905-909.
45. Brown EJ, Albers MW, Shin TB, Ichikawa K, Keith CT, Lane WS, Schreiber SL. A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature. 369:1994;756-759.
46. Keith CT, Schreiber SL. PIK-related kinases: DNA repair, recombination, and cell cycle checkpoints. Science. 270:1995;50-51.
47. Brown EJ, Beal PA, Keith CT, Chen J, Shin TB, Schreiber SL. Regulation of p70 S6 kinase by the kinase activity of FRAP in vivo. Nature. 377:1995;441-446.
48. Beretta L, Gingras AC, Svitkin YV, Hall MN, Sonenberg N. Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation. EMBO J. 15:1996;658-664.
49. Lin TA, Kong XM, Saltiel AR, Blackshear PJ, Lawrence JC. 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. 270:1995;18531-18538.
50. von Manteuffel SR, Dennis PB, Pullen N, Gingras AC, Sonenberg N, Thomas G. The insulin-induced signalling pathway leading to S6 and initiation factor 4E Binding Protein 1 phosphorylation bifurcates at a rapamycin-sensitive point immediately upstream of p70(s6k). of special interest Mol Cell Biol. 17:1997;5426-5436 p70S6k does not mediate 4E-BP1 phosphorylation. The bifurcation point in the signalling pathway leading to 4E-BP1 and p70S6k phosphorylation is immediately upstream of these two proteins.
51. Haystead TA, Haystead CM, Hu C, Lin TA, Lawrence J Jr. Phosphorylation of PHAS-I by mitogen-activated protein (MAP) kinase. Identification of a site phosphorylated by MAP kinase in vitro and in response to insulin in rat adipocytes. J Biol Chem. 269:1994;23185-23191.
52. Brunn GJ, Hudson CC, Sekulic A, Williams JM, Hosoi H, Houghton PJ, Lawrence JC, Abraham RT. Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. of special interest Science. 277:1997;99-101 The authors show that FRAP/mTOR is involved in PHAS-I (4E-BP1) phosphorylation in vivo and that it can phosphorylate 4E-BP1 in an in vitro immune-kinase assay.
53. Burnett PE, Barrow RK, Cohen NA, Snyder SH, Sabatini DM. RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc Natl Acad Sci USA. 95:1998;1432-1437.
54. Di Como CJ, Arndt KT. Nutrients, via the Tor proteins, stimulate the association of Tap42 with type 2A phosphatases. Genes Dev. 10:1996;1904-1916.
55. Murata K, Wu J, Brautigan DL. B cell receptor-associated protein α4 displays repamycin-sensitive binding directly to the catalytic subunit of protein phosphatase 2A. Proc Natl Acad Sci USA. 94:1997;10624-10629.
56. Manzella JM, Rychlik W, Rhoads RE, Hershey JW, Blackshear PJ. Insulin induction of ornithine decarboxylase. Importance of mRNA secondary structure and phosphorylation of eucaryotic initiation factor eIF-4B and eIF-4E. J Biol Chem. 266:1991;2383-2389.
57. Geballe AP. Translational control mediated by upstream AUG codons. Hershey JWB, Mathews MB, Sonenberg N. Translational Control. 1996;173-197 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
58. Mendez R, Myers MG Jr, White MF, Rhoads RE. 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. of special interest Mol Cell Biol. 16:1996;2857-2864 Phosphorylation of p70S6k and of 4E-BP1 in response to insulin stimulation is dependent on IRS-1. Wortmannin treatment prevents stimulation of general protein synthesis, but rapamycin only affects translation of some mRNAs (here c-myc).
59. Pedersen S, Celis JE, Nielsen J, Christiansen J, Nielsen FC. Distinct repression of translation by wortmannin and rapamycin. Eur J Biochem. 247:1997;449-456.
60. Welsh GI, Stokes CM, Wang XM, Sakaue H, Ogawa W, Kasuga M, Proud CG. Activation of translation initiation factor eIF2B by insulin requires phosphatidyl inositol 3-kinase. FEBS Lett. 410:1997;418-422.
61. Shantz LM, Pegg AE. Overproduction of ornithine decarboxylase caused by relief of translational repression is associated with neoplastic transformation. Cancer Res. 54:1994;2313-2316.
62. Rousseau D, Kaspar R, Rosenwald I, Gehrke L, Sonenberg N. 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. 93:1996;1065-1070.
63. Shantz LM, Coleman CS, Pegg AE. Expression of an ornithine decarboxylase dominant-negative mutant reverses eukaryotic initiation factor 4E-induced cell transformation. Cancer Res. 56:1996;5136-5140.
64. Rousseau D, Gingras A-C, Pause A, Sonenberg N. The eIF4E-binding proteins 1 and 2 are negative regulators of cell growth. of special interest Oncogene. 13:1996;2415-2420 The translational inhibitors 4E-BP1 and 4E-BP2 were stably transfected in cells transformed by eIF4E, SRC or RAS. This resulted in a partial reversion of the transformed phenotype, suggesting that the 4E-BPs could function as tumour suppressors.
65. Miyagi Y, Sugiyama A, Asai A, Okazaki T, Kuchino Y, Kerr SJ. Elevated levels of eukaryotic translation initiation factor eIF-4E mRNA in a broad spectrum of transformed cell lines. Cancer Lett. 91:1995;247-252.
66. Kerekatte V, Smiley K, Hu B, Smith A, Gelder F, De Benedetti A. The proto-oncogene/translation factor eIF4E: a survey of its expression in breast carcinomas. Int J Cancer. 64:1995;27-31.
67. Nathan CA, Carter P, Liu L, Li BD, Abreo F, Tudor A, Zimmer SG, Debenedetti A. Elevated expression of eIF4E and FGF-2 isoforms during vascularization of breast carcinomas. Oncogene. 15:1997;1087-1094.
68. Nathan CAO, Liu L, Li BD, Abreo FW, Nandy I, Debenedetti A. Detection of the proto-oncogene eIF4E in surgical margins may predict recurrence in head and neck cancer. Oncogene. 15:1997;579-584.
69. Jones RM, Branda J, Johnston KA, Polymenis M, Gadd M, Rustgi A, Callanan L, Schmidt EV. An essential E box in the promoter of the gene encoding the mRNA cap-binding protein (eukaryotic initiation factor 4E) is a target for activation by c-myc. of special interest Mol Cell Biol. 16:1996;4754-4764 This paper identifies an E-box in the promoter of eIF4E, which is the target for transcriptional activation by c-Myc, consistent with the elevation of eIF4E mRNA levels in c-myc-overexpressing cells.
70. Polunovsky VA, Rosenwald IB, Tan AT, White J, Chiang L, Sonenberg N, Bitterman PB. 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. 16:1996;6573-6581.
71. Xu Z, Dholakia JN, Hille MB. Maturation hormone induced an increase in the translational activity of starfish oocytes coincident with the phosphorylation of the mRNA cap binding protein, eIF-4E, and the activation of several kinases. Dev Gen. 14:1993;424-439.
72. Klein PS, Melton DA. Induction of mesoderm in Xenopus laevis embryos by translation initiation factor 4E. Science. 265:1994;803-806.
73. Gradi A, Imataka H, Svitkin YV, Rom E, Raught B, Morino S, Sonenberg N. A novel functional human eukaryotic translation initiation factor 4G. Mol Cell Biol. 18:1998;334-342.
74. Brunn GJ, Fadden P, Haystead TAJ, Lawrence JC Jr. The mammalian target of rapamycin phosphorylates sites having a (Ser/Thr)-Pro motif and is activated by antibodies to a region near its COOH terminus. J Biol Chem. 272:1997;32547-32550.
75. Fletcher CM, McGuire AM, Gingras A-C, Li H, Matsuo H, Sonenberg N, Wagner G. 4E binding proteins inhibit the translation factor of eIF4F without folded structure. Biochem. 37:1998;9-15.