The mRNA 5' cap-binding protein eIF4E and control of cell growth.

Control of gene expression at the translational level is important in cell growth and proliferation. Recent work has identified pathways that transmit signals from extracellular stimuli to several translation components. A key participant in regulation of translation is eIF4E, the mRNA 5' cap-binding protein. Several signalling pathways impact on the activity of eIF4E. This review will summarise recent findings on the MAP kinase signalling pathway that leads to phosphorylation of eIF4E and on pathways that regulate repression of eIF4E function. A major unresolved question is how the changes in translation modulate cell growth rate, and a working model will be discussed.

[1]  N. Sonenberg,et al.  Translation initiation of ornithine decarboxylase and nucleocytoplasmic transport of cyclin D1 mRNA are increased in cells overexpressing eukaryotic initiation factor 4E. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Andrius Kazlauskas,et al.  The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase , 1995, Cell.

[3]  N. Sonenberg,et al.  Angiotensin II induces phosphorylation of eukaryotic protein synthesis initiation factor 4E in vascular smooth muscle cells. , 1994, The Journal of biological chemistry.

[4]  A. Geballe 6 Translational Control Mediated by Upstream AUG Codons , 1996 .

[5]  M. Polymenis,et al.  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 , 1996, Molecular and cellular biology.

[6]  Benjamin D. L. Li,et al.  Elevated expression of eIF4E and FGF-2 isoforms during vascularization of breast carcinomas , 1997, Oncogene.

[7]  B. Carabello,et al.  Translational Initiation Factor eIF-4E , 1996, The Journal of Biological Chemistry.

[8]  C. Berset,et al.  A novel inhibitor of cap‐dependent translation initiation in yeast: p20 competes with eIF4G for binding to eIF4E , 1997, The EMBO journal.

[9]  V. M. Pain Initiation of protein synthesis in eukaryotic cells. , 1996, European journal of biochemistry.

[10]  N. Sonenberg 8 mRNA 5′ Cap-binding Protein elF4E and Control of Cell Growth , 1996 .

[11]  N. Sonenberg,et al.  The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4 gamma and the translational repressors 4E-binding proteins , 1995, Molecular and cellular biology.

[12]  L. McKendrick,et al.  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* , 1997, The Journal of Biological Chemistry.

[13]  P. Blackshear,et al.  Control of PHAS-I by Insulin in 3T3-L1 Adipocytes , 1995, The Journal of Biological Chemistry.

[14]  S. Schreiber,et al.  PIK-Related Kinases: DNA Repair, Recombination, and Cell Cycle Checkpoints , 1995, Science.

[15]  G. Panayotou,et al.  Phosphoinositide 3-kinases: a conserved family of signal transducers. , 1997, Trends in biochemical sciences.

[16]  A. Gingras,et al.  Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5'-cap function , 1994, Nature.

[17]  L. Shantz,et al.  Expression of an ornithine decarboxylase dominant-negative mutant reverses eukaryotic initiation factor 4E-induced cell transformation. , 1996, Cancer research.

[18]  S. Moriya,et al.  EGF or PDGF receptors activate atypical PKClambda through phosphatidylinositol 3‐kinase. , 1996, The EMBO journal.

[19]  N. Sonenberg,et al.  PHAS-I as a link between mitogen-activated protein kinase and translation initiation. , 1994, Science.

[20]  J. Hershey,et al.  Translational control in mammalian cells. , 1991, Annual review of biochemistry.

[21]  A. Gingras,et al.  Rapamycin blocks the phosphorylation of 4E‐BP1 and inhibits cap‐dependent initiation of translation. , 1996, The EMBO journal.

[22]  R. Rhoads,et al.  Phosphorylation of Eukaryotic Protein Synthesis Initiation Factor 4E at Ser-209 (*) , 1995, The Journal of Biological Chemistry.

[23]  N. Sonenberg,et al.  Translational control of programmed cell death: eukaryotic translation initiation factor 4E blocks apoptosis in growth-factor-restricted fibroblasts with physiologically expressed or deregulated Myc , 1996, Molecular and cellular biology.

[24]  N. Sonenberg,et al.  Involvement of the 24-kDa cap-binding protein in regulation of protein synthesis in mitosis. , 1987, The Journal of biological chemistry.

[25]  J. Hershey,et al.  Heat shock-induced translational alterations in HeLa cells. Initiation factor modifications and the inhibition of translation. , 1984, The Journal of biological chemistry.

[26]  N. Sonenberg,et al.  1 Origins and Targets of Translational Control , 1996 .

[27]  A. De Benedetti,et al.  The proto‐oncogene/translation factor eIF4E: A survey of its expression in breast carcinomas , 1995, International journal of cancer.

[28]  A. Gingras,et al.  The eIF4E-binding proteins 1 and 2 are negative regulators of cell growth. , 1996, Oncogene.

[29]  E. Krebs,et al.  cAMP- and rapamycin-sensitive regulation of the association of eukaryotic initiation factor 4E and the translational regulator PHAS-I in aortic smooth muscle cells. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Jonathan A. Cooper,et al.  Mitogen‐activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2 , 1997, The EMBO journal.

[31]  S. Schreiber,et al.  Control of p70 S6 kinase by kinase activity of FRAP in vivo , 1995, Nature.

[32]  C. Proud,et al.  Insulin‐stimulated phosphorylation of initiation factor 4E is mediated by the MAP kinase pathway , 1996, FEBS letters.

[33]  A. Gingras,et al.  Structure of translation factor elF4E bound to m7GDP and interaction with 4E-binding protein , 1997, Nature Structural Biology.

[34]  A. Gingras,et al.  4E binding proteins inhibit the translation factor eIF4E without folded structure. , 1998, Biochemistry.

[35]  X Wang,et al.  Activation of translation initiation factor eIF2B by insulin requires phosphatidyl inositol 3‐kinase , 1997, FEBS letters.

[36]  T. Haystead,et al.  Identification of Phosphorylation Sites in the Translational Regulator, PHAS-I, That Are Controlled by Insulin and Rapamycin in Rat Adipocytes* , 1997, The Journal of Biological Chemistry.

[37]  J. Celis,et al.  Distinct repression of translation by wortmannin and rapamycin. , 1997, European journal of biochemistry.

[38]  R. Panniers,et al.  Cap binding protein complex that restores protein synthesis in heat-shocked Ehrlich cell lysates contains highly phosphorylated eIF-4E. , 1990, The Journal of biological chemistry.

[39]  S. Snyder,et al.  RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[40]  H. O. Voorma,et al.  Phosphorylation of the eIF4E‐binding protein PHAS‐I after exposure of PC12 cells to EGF and NGF , 1996, FEBS letters.

[41]  Stuart L. Schreiber,et al.  A mammalian protein targeted by G1-arresting rapamycin–receptor complex , 1994, Nature.

[42]  K. Arndt,et al.  Nutrients, via the Tor proteins, stimulate the association of Tap42 with type 2A phosphatases. , 1996, Genes & development.

[43]  A. Nairn,et al.  Inhibition of Tumor Necrosis Factor Signal Transduction in Endothelial Cells by Dimethylaminopurine* , 1996, The Journal of Biological Chemistry.

[44]  B. Burgering,et al.  Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction , 1995, Nature.

[45]  V. M. Pain,et al.  A Reevaluation of the Cap-binding Protein, eIF4E, as a Rate-limiting Factor for Initiation of Translation in Reticulocyte Lysate (*) , 1996, The Journal of Biological Chemistry.

[46]  N. Sonenberg,et al.  A Novel Functional Human Eukaryotic Translation Initiation Factor 4G , 1998, Molecular and Cellular Biology.

[47]  J Downward,et al.  PKB/Akt: connecting phosphoinositide 3-kinase to cell survival and beyond. , 1997, Trends in biochemical sciences.

[48]  J. Lawrence,et al.  Molecular cloning and tissue distribution of PHAS-I, an intracellular target for insulin and growth factors. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Christine C. Hudson,et al.  Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. , 1997, Science.

[50]  Tony Hunter,et al.  MNK1, a new MAP kinase‐activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates , 1997, The EMBO journal.

[51]  M. Kasuga,et al.  Regulation of eIF-4E BP1 Phosphorylation by mTOR* , 1997, The Journal of Biological Chemistry.

[52]  D. Melton,et al.  Induction of mesoderm in Xenopus laevis embryos by translation initiation factor 4E. , 1994, Science.

[53]  A. Gingras,et al.  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 p70s6k , 1997, Molecular and cellular biology.

[54]  M. White,et al.  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 , 1996, Molecular and cellular biology.

[55]  J. Heitman,et al.  Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast , 1991, Science.

[56]  P. Blackshear,et al.  Insulin induction of ornithine decarboxylase. Importance of mRNA secondary structure and phosphorylation of eucaryotic initiation factors eIF-4B and eIF-4E. , 1991, The Journal of biological chemistry.

[57]  L. Shantz,et al.  Overproduction of ornithine decarboxylase caused by relief of translational repression is associated with neoplastic transformation. , 1994, Cancer research.

[58]  A. Gingras,et al.  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 , 1997 .

[59]  G. Thomas,et al.  14 Ribosomal Protein S6 Phosphorylation and Signal Transduction , 1996 .

[60]  T. Haystead,et al.  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. , 1994, The Journal of biological chemistry.

[61]  Y. Miyagi,et al.  Elevated levels of eukaryotic translation initiation factor eIF-4E, mRNA in a broad spectrum of transformed cell lines. , 1995, Cancer letters.

[62]  T. Haystead,et al.  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 , 1997, The Journal of Biological Chemistry.

[63]  Benjamin D. L. Li,et al.  Detection of the proto-oncogene eIF4E in surgical margins may predict recurrence in head and neck cancer , 1997, Oncogene.

[64]  R. Abraham,et al.  PHAS/4E-BPs as regulators of mRNA translation and cell proliferation. , 1997, Trends in biochemical sciences.

[65]  M. White,et al.  Requirement of protein kinase C zeta for stimulation of protein synthesis by insulin , 1997, Molecular and cellular biology.

[66]  R. Rhoads,et al.  Chromatographic resolution of in vivo phosphorylated and nonphosphorylated eukaryotic translation initiation factor eIF-4E: increased cap affinity of the phosphorylated form. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[67]  Lewis C Cantley,et al.  PI3K: Downstream AKTion Blocks Apoptosis , 1997, Cell.

[68]  J. N. Dholakia,et al.  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. , 1993, Developmental genetics.

[69]  Jun Wu,et al.  B cell receptor-associated protein α4 displays rapamycin-sensitive binding directly to the catalytic subunit of protein phosphatase 2A , 1997 .

[70]  A. Gingras,et al.  Angiotensin II Stimulates Phosphorylation of the Translational Repressor 4E-binding Protein 1 by a Mitogen-activated Protein Kinase-independent Mechanism* , 1997, The Journal of Biological Chemistry.

[71]  A. Gingras,et al.  4E-BP1 phosphorylation is mediated by the FRAP-p70s6k pathway and is independent of mitogen-activated protein kinase. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[72]  A. Gingras,et al.  Cocrystal Structure of the Messenger RNA 5′ Cap-Binding Protein (eIF4E) Bound to 7-methyl-GDP , 1997, Cell.

[73]  N. Sonenberg,et al.  Repression of cap‐dependent translation by 4E‐binding protein 1: competition with p220 for binding to eukaryotic initiation factor‐4E. , 1995, The EMBO journal.