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PMID: 12215171 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Oxidative stress increases eukaryotic initiation factor 4E phosphorylation in vascular cells.

The Biochemical journal ·Vol. 369 ·No. Pt 2 ·2003-01-15 ·Pages 213-25

Duncan RF, Peterson H, Hagedorn CH, Sevanian A

Abstract

Dysregulated cell growth can be caused by increased activity of protein synthesis eukaryotic initiation factor (eIF) 4E. Dysregulated cell growth is also characteristic of atherosclerosis. It is postulated that exposure of vascular cells, such as endothelial cells, smooth muscle cells and monocytes/macrophages, to oxidants, such as oxidized low-density lipoprotein (oxLDL), leads to the elaboration of growth factors and cytokines, which in turn results in smooth muscle cell hyperproliferation. To investigate whether activation of eIF4E might play a role in this hyperproliferative response, vascular cells were treated with oxLDL, oxidized lipid components of oxLDL and several model oxidants, including H(2)O(2) and dimethyl naphthoquinone. Exposure to each of these compounds led to a dose- and time-dependent increase in eIF4E phosphorylation in all three types of vascular cells, correlated with a modest increase in overall translation rate. No changes in eIF4EBP, eIF2 or eIF4B modification state were observed. Increased eIF4E phosphorylation was paralleled by increased presence of eIF4E in high-molecular-mass protein complexes characteristic of its most active form. Anti-oxidants at concentrations typically employed to block oxidant-induced cell signalling likewise promoted eIF4E phosphorylation. The results of this study indicate that increased eIF4E activity may contribute to the pathophysiological events in early atherogenesis by increasing the expression of translationally inefficient mRNAs encoding growth-promoting proteins.

MeSH Terms
Animals Antioxidants/pharmacology Cells, Cultured DNA/biosynthesis Endothelium, Vascular/cytology,drug effects,metabolism Eukaryotic Initiation Factor-4E/metabolism Humans Hydrogen Peroxide/pharmacology Linoleic Acids/pharmacology Lipid Peroxides/pharmacology Lipoproteins, LDL/pharmacology Macromolecular Substances Macrophages/cytology,drug effects,metabolism Myocytes, Smooth Muscle/cytology,drug effects,metabolism Naphthoquinones/pharmacology Oxidants/pharmacology Oxidative Stress Phosphorylation Protein Biosynthesis Rabbits Reactive Oxygen Species
Chemicals
Antioxidants Eukaryotic Initiation Factor-4E Linoleic Acids Lipid Peroxides Lipoproteins, LDL Macromolecular Substances Naphthoquinones Oxidants Reactive Oxygen Species oxidized low density lipoprotein linoleic acid hydroperoxide 2,3-dimethoxy-1,4-naphthoquinone DNA Hydrogen Peroxide
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Duncan Roger F
Department of Molecular Pharmacology and Toxicology, School of Pharmacy, University of Southern California, 1985 Zonal Avenue, Los Angeles, CA 90033, U.S.A. rduncan@hsc.usc.edu
Peterson Hazel
Hagedorn Curt H
Sevanian Alex
References (54)
54 references, click to expand
  1. Inactivation of eIF2B and phosphorylation of PHAS-I in heat-shocked rat hepatoma cells.
    J Biol Chem. 1997 Oct 24;272(43):26850-6 PMID: 9341116
  2. Phosphorylation of eukaryotic initiation factor 4E markedly reduces its affinity for capped mRNA.
    J Biol Chem. 2002 Feb 1;277(5):3303-9 PMID: 11723111
  3. Oxygen radicals and signaling.
    Curr Opin Cell Biol. 1998 Apr;10(2):248-53 PMID: 9561849
  4. Regulation of translation initiation factors by signal transduction.
    Eur J Biochem. 1998 May 1;253(3):531-44 PMID: 9654048
  5. Atherosclerosis--an inflammatory disease.
    N Engl J Med. 1999 Jan 14;340(2):115-26 PMID: 9887164
  6. Phosphorylation of eukaryotic translation initiation factor 4E is critical for growth.
    Mol Cell Biol. 2002 Mar;22(6):1656-63 PMID: 11865045
  7. Heat shock causes diverse changes in the phosphorylation of the ribosomal proteins of mammalian cells.
    FEBS Lett. 1984 Apr 24;169(2):267-73 PMID: 6714428
  8. Evaluation of isoelectric focusing running conditions during two-dimensional isoelectric focusing/sodium dodecyl sulfate-polyacrylamide gel electrophoresis: variation of gel patterns with changing conditions and optimized isoelectric focusing conditions.
    Anal Biochem. 1984 Apr;138(1):144-55 PMID: 6731839
  9. The 5' untranslated sequence of the c-sis/platelet-derived growth factor 2 transcript is a potent translational inhibitor.
    Mol Cell Biol. 1988 Jan;8(1):284-92 PMID: 3275870
  10. cis-acting translational effects of the 5' noncoding region of c-myc mRNA.
    Mol Cell Biol. 1988 Jul;8(7):2875-83 PMID: 3043198
  11. Oxidants induce phosphorylation of ribosomal protein S6.
    J Biol Chem. 1988 Nov 25;263(33):17452-8 PMID: 3141421
  12. Cap-binding proteins of eukaryotic messenger RNA: functions in initiation and control of translation.
    Prog Nucleic Acid Res Mol Biol. 1988;35:173-207 PMID: 3065823
  13. Inhibition by linoleic acid hydroperoxide of alveolar macrophage superoxide production: effects upon mitochondrial and plasma membrane potentials.
    Arch Biochem Biophys. 1989 Nov 1;274(2):443-52 PMID: 2552924
  14. Cap binding protein complex that restores protein synthesis in heat-shocked Ehrlich cell lysates contains highly phosphorylated eIF-4E.
    J Biol Chem. 1990 Apr 5;265(10):5333-6 PMID: 2318815
  15. Malignant transformation by a eukaryotic initiation factor subunit that binds to mRNA 5' cap.
    Nature. 1990 Jun 7;345(6275):544-7 PMID: 2348862
  16. Overexpression of eukaryotic protein synthesis initiation factor 4E in HeLa cells results in aberrant growth and morphology.
    Proc Natl Acad Sci U S A. 1990 Nov;87(21):8212-6 PMID: 2122455
  17. 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. 1990 Nov 15;265(32):19467-71 PMID: 2246237
  18. Heat shock induces two distinct S6 protein kinase activities in quiescent mammalian fibroblasts.
    J Cell Physiol. 1991 Aug;148(2):252-9 PMID: 1880153
  19. Expression of antisense RNA against initiation factor eIF-4E mRNA in HeLa cells results in lengthened cell division times, diminished translation rates, and reduced levels of both eIF-4E and the p220 component of eIF-4F.
    Mol Cell Biol. 1991 Nov;11(11):5435-45 PMID: 1922056
  20. Active oxygen species stimulate vascular smooth muscle cell growth and proto-oncogene expression.
    Circ Res. 1992 Mar;70(3):593-9 PMID: 1371430
  21. The mRNA 5' cap-binding protein, eIF-4E, cooperates with v-myc or E1A in the transformation of primary rodent fibroblasts.
    Mol Cell Biol. 1992 Mar;12(3):1234-8 PMID: 1532049
  22. mRNAs containing extensive secondary structure in their 5' non-coding region translate efficiently in cells overexpressing initiation factor eIF-4E.
    EMBO J. 1992 Nov;11(11):4153-8 PMID: 1396596
  23. Preferential translation of heat shock mRNAs in HeLa cells deficient in protein synthesis initiation factors eIF-4E and eIF-4 gamma.
    J Biol Chem. 1992 Oct 15;267(29):21038-43 PMID: 1400417
  24. cis-acting elements involved in the alternative translation initiation process of human basic fibroblast growth factor mRNA.
    Mol Cell Biol. 1992 Oct;12(10):4796-805 PMID: 1406661
  25. Nuclear factor kappa B: an oxidative stress-responsive transcription factor of eukaryotic cells (a review).
    Free Radic Res Commun. 1992;17(4):221-37 PMID: 1473734
  26. The pathogenesis of atherosclerosis: a perspective for the 1990s.
    Nature. 1993 Apr 29;362(6423):801-9 PMID: 8479518
  27. The role of oxygen radicals in human disease, with particular reference to the vascular system.
    Haemostasis. 1993 Mar;23 Suppl 1:118-26 PMID: 8495863
  28. Oxidants, antioxidants, and the degenerative diseases of aging.
    Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):7915-22 PMID: 8367443
  29. Increased phosphorylation of eukaryotic initiation factor 4 alpha during early activation of T lymphocytes correlates with increased initiation factor 4F complex formation.
    Eur J Biochem. 1993 Nov 15;218(1):39-48 PMID: 8243475
  30. Decreasing the level of translation initiation factor 4E with antisense RNA causes reversal of ras-mediated transformation and tumorigenesis of cloned rat embryo fibroblasts.
    Int J Cancer. 1993 Nov 11;55(5):841-7 PMID: 8244582
  31. Elevated levels of cyclin D1 protein in response to increased expression of eukaryotic initiation factor 4E.
    Mol Cell Biol. 1993 Dec;13(12):7358-63 PMID: 8246956
  32. In vitro synthesis of human protein synthesis initiation factor 4 gamma and its localization on 43 and 48 S initiation complexes.
    J Biol Chem. 1994 Jan 21;269(3):2048-55 PMID: 8294456
  33. Overproduction of ornithine decarboxylase caused by relief of translational repression is associated with neoplastic transformation.
    Cancer Res. 1994 May 1;54(9):2313-6 PMID: 8162572
  34. Biochemical and cytotoxic characteristics of an in vivo circulating oxidized low density lipoprotein (LDL-).
    J Lipid Res. 1994 Apr;35(4):669-77 PMID: 8006522
  35. 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 U S A. 1994 Aug 2;91(16):7668-72 PMID: 8052640
  36. Linoleic acid hydroperoxide-induced peroxidation of endothelial cell phospholipids and cytotoxicity.
    Free Radic Biol Med. 1994 Oct;17(4):285-95 PMID: 8001833
  37. Theodore Cooper Memorial Lecture. Hypertension and the pathogenesis of atherosclerosis. Oxidative stress and the mediation of arterial inflammatory response: a new perspective.
    Hypertension. 1995 Feb;25(2):155-61 PMID: 7843763
  38. Transient adaptation of oxidative stress in mammalian cells.
    Arch Biochem Biophys. 1995 Apr 1;318(1):231-40 PMID: 7726566
  39. 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. 1995 Sep 15;270(37):21684-8 PMID: 7665584
  40. Repression of cap-dependent translation by 4E-binding protein 1: competition with p220 for binding to eukaryotic initiation factor-4E.
    EMBO J. 1995 Nov 15;14(22):5701-9 PMID: 8521827
  41. Translational enhancement of FGF-2 by eIF-4 factors, and alternate utilization of CUG and AUG codons for translation initiation.
    Oncogene. 1995 Dec 7;11(11):2339-48 PMID: 8570185
  42. A reevaluation of the cap-binding protein, eIF4E, as a rate-limiting factor for initiation of translation in reticulocyte lysate.
    J Biol Chem. 1996 Apr 12;271(15):8983-90 PMID: 8621544
  43. The role of oxidized lipoproteins in atherogenesis.
    Free Radic Biol Med. 1996;20(5):707-27 PMID: 8721615
  44. Mitogen-activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2.
    EMBO J. 1997 Apr 15;16(8):1909-20 PMID: 9155017
  45. MNK1, a new MAP kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates.
    EMBO J. 1997 Apr 15;16(8):1921-33 PMID: 9155018
  46. Cocrystal structure of the messenger RNA 5' cap-binding protein (eIF4E) bound to 7-methyl-GDP.
    Cell. 1997 Jun 13;89(6):951-61 PMID: 9200613
  47. eIF4G dramatically enhances the binding of eIF4E to the mRNA 5'-cap structure.
    J Biol Chem. 1997 Aug 29;272(35):21677-80 PMID: 9268293
  48. Striking multiplicity of eIF4E-BP1 phosphorylated isoforms identified by 2D gel electrophoresis regulation by heat shock.
    Eur J Biochem. 1999 Oct;265(2):728-43 PMID: 10504405
  49. Oxidant stress stimulates phosphorylation of eIF4E without an effect on global protein synthesis in smooth muscle cells. Lack of evidence for a role of H202 in angiotensin II-induced hypertrophy.
    J Biol Chem. 2000 Jun 2;275(22):16993-9 PMID: 10828072
  50. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation.
    Annu Rev Biochem. 1999;68:913-63 PMID: 10872469
  51. Negative regulation of protein translation by mitogen-activated protein kinase-interacting kinases 1 and 2.
    Mol Cell Biol. 2001 Aug;21(16):5500-11 PMID: 11463832
  52. Phosphorylation of eukaryotic initiation factor 4E (eIF4E) at Ser209 is not required for protein synthesis in vitro and in vivo.
    Eur J Biochem. 2001 Oct;268(20):5375-85 PMID: 11606200
  53. Hierarchical phosphorylation of the translation inhibitor 4E-BP1.
    Genes Dev. 2001 Nov 1;15(21):2852-64 PMID: 11691836
  54. The phosphorylation of eukaryotic initiation factor eIF4E in response to phorbol esters, cell stresses, and cytokines is mediated by distinct MAP kinase pathways.
    J Biol Chem. 1998 Apr 17;273(16):9373-7 PMID: 9545260
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
0264-6021
Published
2003-01-15
Pages
213-25
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1223074
Subset
IM
Grants
NHLBI NIH HHS · HL 50350 · United States
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