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. 1992 Mar;12(3):1234–1238. doi: 10.1128/mcb.12.3.1234

The mRNA 5' cap-binding protein, eIF-4E, cooperates with v-myc or E1A in the transformation of primary rodent fibroblasts.

A Lazaris-Karatzas 1, N Sonenberg 1
PMCID: PMC369555  PMID: 1532049

Abstract

We present evidence that eIF-4E, the mRNA 5' cap-binding protein, cooperates with two immortalizing oncogenes, v-myc and E1A, to cause transformation of rat embryo fibroblasts. eIF-4E alone can transform rat embryo fibroblasts when selection is applied. The pattern of transformation by eIF-4E is similar to that of p21 Ras, raising the possibility that eIF-4E shares a common signal transduction pathway with p21 Ras.

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Selected References

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  1. Asselin C., Bastin M. Sequences from polyomavirus and simian virus 40 large T genes capable of immortalizing primary rat embryo fibroblasts. J Virol. 1985 Dec;56(3):958–968. doi: 10.1128/jvi.56.3.958-968.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bonneau A. M., Sonenberg N. Involvement of the 24-kDa cap-binding protein in regulation of protein synthesis in mitosis. J Biol Chem. 1987 Aug 15;262(23):11134–11139. [PubMed] [Google Scholar]
  3. Darveau A., Pelletier J., Sonenberg N. Differential efficiencies of in vitro translation of mouse c-myc transcripts differing in the 5' untranslated region. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2315–2319. doi: 10.1073/pnas.82.8.2315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. De Benedetti A., Rhoads R. E. 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):8212–8216. doi: 10.1073/pnas.87.21.8212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Duncan R., Milburn S. C., Hershey J. W. Regulated phosphorylation and low abundance of HeLa cell initiation factor eIF-4F suggest a role in translational control. Heat shock effects on eIF-4F. J Biol Chem. 1987 Jan 5;262(1):380–388. [PubMed] [Google Scholar]
  6. Fagan R. J., Lazaris-Karatzas A., Sonenberg N., Rozen R. Translational control of ornithine aminotransferase. Modulation by initiation factor eIF-4E. J Biol Chem. 1991 Sep 5;266(25):16518–16523. [PubMed] [Google Scholar]
  7. Frederickson R. M., Montine K. S., Sonenberg N. Phosphorylation of eukaryotic translation initiation factor 4E is increased in Src-transformed cell lines. Mol Cell Biol. 1991 May;11(5):2896–2900. doi: 10.1128/mcb.11.5.2896. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hershey J. W. Protein phosphorylation controls translation rates. J Biol Chem. 1989 Dec 15;264(35):20823–20826. [PubMed] [Google Scholar]
  9. Hiremath L. S., Webb N. R., Rhoads R. E. Immunological detection of the messenger RNA cap-binding protein. J Biol Chem. 1985 Jul 5;260(13):7843–7849. [PubMed] [Google Scholar]
  10. Huang J. T., Schneider R. J. Adenovirus inhibition of cellular protein synthesis involves inactivation of cap-binding protein. Cell. 1991 Apr 19;65(2):271–280. doi: 10.1016/0092-8674(91)90161-q. [DOI] [PubMed] [Google Scholar]
  11. Hunter T. Cooperation between oncogenes. Cell. 1991 Jan 25;64(2):249–270. doi: 10.1016/0092-8674(91)90637-e. [DOI] [PubMed] [Google Scholar]
  12. Jagus R., Anderson W. F., Safer B. The regulation of initiation of mammalian protein synthesis. Prog Nucleic Acid Res Mol Biol. 1981;25:127–185. doi: 10.1016/s0079-6603(08)60484-5. [DOI] [PubMed] [Google Scholar]
  13. Joshi-Barve S., Rychlik W., Rhoads R. E. Alteration of the major phosphorylation site of eukaryotic protein synthesis initiation factor 4E prevents its association with the 48 S initiation complex. J Biol Chem. 1990 Feb 15;265(5):2979–2983. [PubMed] [Google Scholar]
  14. Kirschmeier P. T., Housey G. M., Johnson M. D., Perkins A. S., Weinstein I. B. Construction and characterization of a retroviral vector demonstrating efficient expression of cloned cDNA sequences. DNA. 1988 Apr;7(3):219–225. doi: 10.1089/dna.1988.7.219. [DOI] [PubMed] [Google Scholar]
  15. Land H., Chen A. C., Morgenstern J. P., Parada L. F., Weinberg R. A. Behavior of myc and ras oncogenes in transformation of rat embryo fibroblasts. Mol Cell Biol. 1986 Jun;6(6):1917–1925. doi: 10.1128/mcb.6.6.1917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Land H., Parada L. F., Weinberg R. A. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature. 1983 Aug 18;304(5927):596–602. doi: 10.1038/304596a0. [DOI] [PubMed] [Google Scholar]
  17. Lazaris-Karatzas A., Montine K. S., Sonenberg N. Malignant transformation by a eukaryotic initiation factor subunit that binds to mRNA 5' cap. Nature. 1990 Jun 7;345(6275):544–547. doi: 10.1038/345544a0. [DOI] [PubMed] [Google Scholar]
  18. Lee W. M., Schwab M., Westaway D., Varmus H. E. Augmented expression of normal c-myc is sufficient for cotransformation of rat embryo cells with a mutant ras gene. Mol Cell Biol. 1985 Dec;5(12):3345–3356. doi: 10.1128/mcb.5.12.3345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Manzella J. M., Blackshear P. J. Regulation of rat ornithine decarboxylase mRNA translation by its 5'-untranslated region. J Biol Chem. 1990 Jul 15;265(20):11817–11822. [PubMed] [Google Scholar]
  20. Marino M. W., Feld L. J., Jaffe E. A., Pfeffer L. M., Han H. M., Donner D. B. Phosphorylation of the proto-oncogene product eukaryotic initiation factor 4E is a common cellular response to tumor necrosis factor. J Biol Chem. 1991 Feb 15;266(5):2685–2688. [PubMed] [Google Scholar]
  21. Marth J. D., Overell R. W., Meier K. E., Krebs E. G., Perlmutter R. M. Translational activation of the lck proto-oncogene. Nature. 1988 Mar 10;332(6160):171–173. doi: 10.1038/332171a0. [DOI] [PubMed] [Google Scholar]
  22. Matlashewski G., Schneider J., Banks L., Jones N., Murray A., Crawford L. Human papillomavirus type 16 DNA cooperates with activated ras in transforming primary cells. EMBO J. 1987 Jun;6(6):1741–1746. doi: 10.1002/j.1460-2075.1987.tb02426.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Morley S. J., Dever T. E., Etchison D., Traugh J. A. Phosphorylation of eIF-4F by protein kinase C or multipotential S6 kinase stimulates protein synthesis at initiation. J Biol Chem. 1991 Mar 15;266(8):4669–4672. [PubMed] [Google Scholar]
  24. Morley S. J., Traugh J. A. 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. 1990 Jun 25;265(18):10611–10616. [PubMed] [Google Scholar]
  25. Rao C. D., Pech M., Robbins K. C., Aaronson S. A. 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):284–292. doi: 10.1128/mcb.8.1.284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rassoulzadegan M., Naghashfar Z., Cowie A., Carr A., Grisoni M., Kamen R., Cuzin F. Expression of the large T protein of polyoma virus promotes the establishment in culture of "normal" rodent fibroblast cell lines. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4354–4358. doi: 10.1073/pnas.80.14.4354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Reed J. C., Haldar S., Croce C. M., Cuddy M. P. Complementation by BCL2 and C-HA-RAS oncogenes in malignant transformation of rat embryo fibroblasts. Mol Cell Biol. 1990 Aug;10(8):4370–4374. doi: 10.1128/mcb.10.8.4370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rhoads R. E. Cap recognition and the entry of mRNA into the protein synthesis initiation cycle. Trends Biochem Sci. 1988 Feb;13(2):52–56. doi: 10.1016/0968-0004(88)90028-x. [DOI] [PubMed] [Google Scholar]
  29. Rozen F., Edery I., Meerovitch K., Dever T. E., Merrick W. C., Sonenberg N. Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F. Mol Cell Biol. 1990 Mar;10(3):1134–1144. doi: 10.1128/mcb.10.3.1134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ruley H. E. Adenovirus early region 1A enables viral and cellular transforming genes to transform primary cells in culture. Nature. 1983 Aug 18;304(5927):602–606. doi: 10.1038/304602a0. [DOI] [PubMed] [Google Scholar]
  31. Ruppert J. M., Vogelstein B., Kinzler K. W. The zinc finger protein GLI transforms primary cells in cooperation with adenovirus E1A. Mol Cell Biol. 1991 Mar;11(3):1724–1728. doi: 10.1128/mcb.11.3.1724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rychlik W., Russ M. A., Rhoads R. E. Phosphorylation site of eukaryotic initiation factor 4E. J Biol Chem. 1987 Aug 5;262(22):10434–10437. [PubMed] [Google Scholar]
  33. Shih C., Weinberg R. A. Isolation of a transforming sequence from a human bladder carcinoma cell line. Cell. 1982 May;29(1):161–169. doi: 10.1016/0092-8674(82)90100-3. [DOI] [PubMed] [Google Scholar]
  34. Smith M. R., Jaramillo M., Liu Y. L., Dever T. E., Merrick W. C., Kung H. F., Sonenberg N. Translation initiation factors induce DNA synthesis and transform NIH 3T3 cells. New Biol. 1990 Jul;2(7):648–654. [PubMed] [Google Scholar]
  35. Sonenberg N. Cap-binding proteins of eukaryotic messenger RNA: functions in initiation and control of translation. Prog Nucleic Acid Res Mol Biol. 1988;35:173–207. doi: 10.1016/s0079-6603(08)60614-5. [DOI] [PubMed] [Google Scholar]
  36. Spandidos D. A., Wilkie N. M. Malignant transformation of early passage rodent cells by a single mutated human oncogene. Nature. 1984 Aug 9;310(5977):469–475. doi: 10.1038/310469a0. [DOI] [PubMed] [Google Scholar]
  37. Weinberg R. A. Oncogenes, antioncogenes, and the molecular bases of multistep carcinogenesis. Cancer Res. 1989 Jul 15;49(14):3713–3721. [PubMed] [Google Scholar]
  38. Weinberg R. A. The action of oncogenes in the cytoplasm and nucleus. Science. 1985 Nov 15;230(4727):770–776. doi: 10.1126/science.2997917. [DOI] [PubMed] [Google Scholar]
  39. Wigler M., Pellicer A., Silverstein S., Axel R., Urlaub G., Chasin L. DNA-mediated transfer of the adenine phosphoribosyltransferase locus into mammalian cells. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1373–1376. doi: 10.1073/pnas.76.3.1373. [DOI] [PMC free article] [PubMed] [Google Scholar]

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