DOI: 10.1002/jcb.240590405. Phosphorylation of elF‐4E and initiation of protein synthesis in P19 embryonal carcinoma cells

Phosphorylation of elF‐4E and initiation of protein synthesis in P19 embryonal carcinoma cells

10.1002/jcb.240590405

Crossref journal-article

Wiley

Journal of Cellular Biochemistry (311)

Abstract

AbstractMitogenic stimulation of protein synthesis is accompanied by an increase in elF‐4E phosphorylation. The effect on protein synthesis by induction of differentiation is less well known. We treated P19 embryonal carcinoma cells with the differentiating agent retinoic acid and found that protein synthesis increased during the first hour of addition. However, the phosphorylation state, as well as the turnover of phosphate on elF‐4E, remained unchanged. Apparently, the change in protein synthesis after RA addition is regulated by another mechanism than elF‐4E phosphorylation.By using P19 cells overexpressing the EGF receptor, we show that the signal transduction pathway that leads to phosphorylation of elF‐4E is present in P19 cells; the EGF‐induced change in phosphorylation of elF‐4E in these cells is likely to be regulated by a change in elF‐4E phosphatase activity.These results suggest that the onset of retinoic acid‐induced differentiation is triggered by a signal transduction pathway which involves changes in protein synthesis, but not elF‐4E phosphorylation. © 1995 Wiley‐Liss, Inc.

Bibliography

Kleijn, M., Voorma, H. O., & Thomas, A. A. M. (1995). Phosphorylation of elFâ4E and initiation of protein synthesis in P19 embryonal carcinoma cells. Journal of Cellular Biochemistry, 59(4), 443â452. Portico.

Authors 3

Miranda Kleijn (first)
Harry O. Voorma (additional)
Adri A. M. Thomas (additional)

References 58 Referenced 16

10.1016/S0021-9258(18)60935-4 / J Biol Chem / Involvement of the 24–kDa cap‐binding protein in regulation of protein synthesis in mitosis by Bonneau A (1987)
10.1083/jcb.97.1.92
10.1016/0014-5793(91)80592-Q
10.1073/pnas.87.21.8212
{'key': 'e_1_2_1_6_1', 'first-page': '155', 'article-title': 'Neuronal differentiation in response to epidermal growth factor of transfected murine P19 embryonal carcinoma cells expressing human epidermal growth factor receptors', 'volume': '2', 'author': 'den Hertog J', 'year': '1991', 'journal-title': 'Cell Growth Differ'} / Cell Growth Differ / Neuronal differentiation in response to epidermal growth factor of transfected murine P19 embryonal carcinoma cells expressing human epidermal growth factor receptors by den Hertog J (1991)
10.1016/0014-4827(91)90255-S
10.1073/pnas.85.1.51
10.1016/S0021-9258(18)49968-1 / J Biol Chem / Epidermal growth factor or okadaic acid stimulates phosphorylation of eukaryotic initiation factor 4F by Donaldson RW (1991)
10.1016/S0021-9258(18)89049-4 / J Biol Chem / Regulation of initiation factors during translational repression caused by serum depletion by Duncan R (1985)
10.1016/S0021-9258(19)75938-9 / J Biol Chem / Regulated phosphorylation and low abundance of HeLa cell initiation factor elF‐4F suggest a role in translational control by Duncan R (1987)
10.1128/MCB.11.5.2896
10.1128/MCB.12.3.1239
10.1038/330624a0
10.1016/0014-4827(79)90445-2
10.1016/S0021-9258(17)39529-7 / J Biol Chem / Immunological detection of the messenger RNA cap‐binding protein by Hiremath LS (1985)
10.1016/0092-8674(91)90161-Q
10.1016/S0021-9258(18)99245-8 / J Biol Chem / Multiple mRNAs encode the murine translation initiation factor elF‐4E by Jaramillo M (1991)
{'key': 'e_1_2_1_19_1', 'first-page': '315', 'article-title': 'Regulation of the epidermal growth factor receptor gene in murine embryonal carcinoma cells', 'volume': '3', 'author': 'Joh T', 'year': '1992', 'journal-title': 'Cell Growth Differ'} / Cell Growth Differ / Regulation of the epidermal growth factor receptor gene in murine embryonal carcinoma cells by Joh T (1992)
10.1083/jcb.94.2.253
10.1016/S0021-9258(19)39897-7 / J Biol Chem / Alteration of the major phosphorylation site of eukaryotic protein synthesis initiation factor 4E prevents its association with the 48 S initiation complex by Joshi‐Barve S (1990)
10.1016/S0021-9258(19)39637-1 / J Biol Chem / Simultaneous cytoplasmic redistribution of ribosomal protein L32 mRNA and phosphorylation of eukaryotic initiation factor 4E after mitogenic stimulation of Swiss 3T3 cells by Kaspar RL (1990)
10.1016/S0021-9258(18)32875-8
10.1002/j.1460-2075.1992.tb05508.x
10.1093/nar/15.20.8125
10.1016/0167-4889(93)90142-C
10.1016/S0021-9258(19)39358-5 / J Biol Chem / Cap binding protein complex that restores protein synthesis in heat‐shocked Ehrlich cell lysates contains highly phosphorylated elF‐4E by Lamphear BJ (1990)
10.1016/S0021-9258(18)49916-4 / J Biol Chem / Heat shock impairs the interaction of cap‐binding protein comples with 5′ mRNA cap by Lamphear BJ (1991)
10.1021/bi00437a033
10.1038/345544a0
10.1101/gad.6.9.1631
10.1038/295672a0
10.1016/S0021-9258(18)52255-9 / J Biol Chem / Insulin induction of ornithine decarboxylase: Importance of mRNA secondary structure and phosphorylation of eucaryotic initiation factors elF‐4B and elF‐4E by Manzella JM (1991)
10.1016/S0021-9258(18)49896-1 / J Biol Chem / Phosphorylation of the proto‐oncogene product eukaryotic initiation factor 4E is a common cellular response to tumor necrosis factor by Marino MW (1991)
10.1126/science.6250214
10.1016/0003-2697(89)90182-6
10.1038/299165a0
10.1073/pnas.91.16.7668
10.1016/S0021-9258(19)81626-5 / J Biol Chem / Phorbol esters stimulate phosphrylation of eukaryotic initiation factors 3, 4B, and 4F by Morley SJ (1989)
10.1016/S0021-9258(18)86990-3 / J Biol Chem / Differential stimulation of phosphorylation of initiation factors elF‐4E, elF‐4B, elF‐3, and ribosomal protein S6 by insulin and phorbol esters by Morley SJ (1990)
10.1038/371762a0
10.1038/330444a0
10.1016/0167-4889(94)90130-9
10.1016/0968-0004(88)90028-X
10.1016/S0021-9258(19)50068-0 / J Biol Chem / ras transformation of cloned rat embryo fibroblasts results in increased rates of protein synthesis and phosphorylation of eukaryotic initiation factor 4E by Rinker‐Schaeffer CW (1992)
10.1128/MCB.10.3.1134
10.1016/S0021-9258(17)45396-8 / J Biol Chem / Increased rate of phosphorylation‐dephosphorylation of the translational initiation factor elF‐4E correlates with the induction of protein and glycoprotein biosynthesis in activated B lymphocytes by Rychlik W (1990)
10.1111/j.1432-1033.1984.tb08526.x
10.1073/pnas.79.8.2537
10.1021/bi00197a018
10.1073/pnas.75.10.4843
10.1073/pnas.83.19.7330
{'key': 'e_1_2_1_53_1', 'first-page': '3034', 'article-title': 'Role of retinoids in differentiation and carcinogenesis', 'volume': '43', 'author': 'Sporn MB', 'year': '1983', 'journal-title': 'Cancer research'} / Cancer research / Role of retinoids in differentiation and carcinogenesis by Sporn MB (1983)
10.1093/jn/105.10.1299 / J Nutr / Vitamin A deficiency and fetal growth and development in the rat by Takahashi YI (1975)
10.1016/0012-1606(85)90348-3
10.1042/bj2840019
10.1016/0167-4889(93)90035-N
10.1006/dbio.1993.1234
10.1128/jvi.68.11.7040-7050.1994 / J Virol / A late adenovirus factor induces elF‐4E dephosphorylation and inhibition of cell protein synthesis by Zhang Y (1994)

Dates

Type	When
Created	20 years, 2 months ago (May 28, 2005, 6:14 p.m.)
Deposited	1 year, 9 months ago (Oct. 25, 2023, 10:34 p.m.)
Indexed	11 months, 1 week ago (Sept. 13, 2024, 1:44 p.m.)
Issued	29 years, 8 months ago (Dec. 1, 1995)
Published	29 years, 8 months ago (Dec. 1, 1995)
Published Online	21 years, 6 months ago (Feb. 19, 2004)
Published Print	29 years, 8 months ago (Dec. 1, 1995)

Funders 0

None

BibTeX

@article{Kleijn_1995, title={Phosphorylation of elF‐4E and initiation of protein synthesis in P19 embryonal carcinoma cells}, volume={59}, ISSN={1097-4644}, url={http://dx.doi.org/10.1002/jcb.240590405}, DOI={10.1002/jcb.240590405}, number={4}, journal={Journal of Cellular Biochemistry}, publisher={Wiley}, author={Kleijn, Miranda and Voorma, Harry O. and Thomas, Adri A. M.}, year={1995}, month=dec, pages={443–452} }

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