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RAS/ERK Signaling Promotes Site-specific Ribosomal Protein S6 Phosphorylation via RSK and Stimulates Cap-dependent Translation
Abstract
Converging signals from the mammalian target of rapamycin (mTOR) and phosphoinositide 3-kinase (PI3K) pathways are well established to modulate translation initiation. Less is known regarding the molecular basis of protein synthesis regulated by other inputs, such as agonists of the Ras/extracellular signal-regulated kinase (ERK) signaling cascade. Ribosomal protein (rp) S6 is a component of the 40S ribosomal subunit that becomes phosphorylated at several serine residues upon mitogen stimulation, but the exact molecular mechanisms regulating its phosphorylation and the function of phosphorylated rpS6 is poorly understood. Here, we provide evidence that activation of the p90 ribosomal S6 kinases (RSKs) by serum, growth factors, tumor promoting phorbol esters, and oncogenic Ras is required for rpS6 phosphorylation downstream of the Ras/ERK signaling cascade. We demonstrate that while ribosomal S6 kinase 1 (S6K1) phosphorylates rpS6 at all sites, RSK exclusively phosphorylates rpS6 at Ser(235/236) in vitro and in vivo using an mTOR-independent mechanism. Mutation of rpS6 at Ser(235/236) reveals that phosphorylation of these sites promotes its recruitment to the 7-methylguanosine cap complex, suggesting that Ras/ERK signaling regulates assembly of the translation preinitiation complex. These data demonstrate that RSK provides an mTOR-independent pathway linking the Ras/ERK signaling cascade to the translational machinery.
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In yeast, dephosphorylation of Atg13 is associated with activation/assembly of the core complex that reflects the reduction of TORC1 and PKA activities.
“In yeast, dephosphorylation of Atg13 is associated with activation/assembly of the core complex that reflects the reduction of TORC1 and PKA activities.”
From Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition) 1 (2021) · cites this paper as [740]
Mutants such as vac8∆ and tlg2∆ accumulate prApe1 under nutrient-rich conditions, but not during autophagy.
“In addition, mutants such as vac8∆ and tlg2∆ accumulate prApe1 under nutrient-rich conditions, but not during autophagy [740, 1081].”
From Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition) 1 (2021) · cites this paper as [740]
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Research works printed but not linked: 39
- Dever, 2002, Cell, 108, 545, 10.1016/S0092-8674(02)00642-6 · DOI
- Clemens, 2004, Oncogene, 23, 3180, 10.1038/sj.onc.1207544 · DOI
- Richter, 2005, Nature, 433, 477, 10.1038/nature03205 · DOI
- Hay, 2004, Genes Dev., 18, 1926, 10.1101/gad.1212704 · DOI · Paper page
- Fingar, 2004, Oncogene, 23, 3151, 10.1038/sj.onc.1207542 · DOI
- Richardson, 2004, Semin. Cell Dev. Biol., 15, 147, 10.1016/j.semcdb.2003.12.023 · DOI
- Gingras, 2004, Curr. Top Microbiol. Immunol., 279, 169
- Averous, 2006, Oncogene, 25, 6423, 10.1038/sj.onc.1209887 · DOI
- Ruvinsky, 2006, Trends Biochem. Sci., 31, 342, 10.1016/j.tibs.2006.04.003 · DOI
- Thomas, 1979, Proc. Natl. Acad. Sci. U. S. A., 76, 3952, 10.1073/pnas.76.8.3952 · DOI
- Gressner, 1974, J. Biol. Chem., 249, 6917, 10.1016/S0021-9258(19)42145-5 · DOI
- Bandi, 1993, J. Biol. Chem., 268, 4530, 10.1016/S0021-9258(18)53642-5 · DOI
- Krieg, 1988, J. Biol. Chem., 263, 11473, 10.1016/S0021-9258(18)37981-X · DOI
- Roux, 2004, Microbiol. Mol. Biol. Rev., 68, 320, 10.1128/MMBR.68.2.320-344.2004 · DOI
- Hauge, 2006, J. Cell Sci., 119, 3021, 10.1242/jcs.02950 · DOI
- Chung, 1992, Cell, 69, 1227, 10.1016/0092-8674(92)90643-Q · DOI
- Blenis, 1991, Cell Growth Differ., 2, 279
- Lee-Fruman, 1999, Oncogene, 18, 5108, 10.1038/sj.onc.1202894 · DOI
- Pende, 2004, Mol. Cell Biol., 24, 3112, 10.1128/MCB.24.8.3112-3124.2004 · DOI
- Volarevic, 2000, Science, 288, 2045, 10.1126/science.288.5473.2045 · DOI
- Nygard, 1990, J. Biol. Chem., 265, 6030, 10.1016/S0021-9258(19)39286-5 · DOI
- Burkhard, 1983, J. Biol. Chem., 258, 14003, 10.1016/S0021-9258(17)44016-6 · DOI
- Ruvinsky, 2005, Genes Dev., 19, 2199, 10.1101/gad.351605 · DOI
- Roux, 2004, Proc. Natl. Acad. Sci. U. S. A., 101, 13489, 10.1073/pnas.0405659101 · DOI
- Kruger, 2001, Mol. Cell Biol., 21, 8357, 10.1128/MCB.21.24.8357-8364.2001 · DOI
- Roux, 2003, Mol. Cell Biol., 23, 4796, 10.1128/MCB.23.14.4796-4804.2003 · DOI
- Cohen, 2005, Science, 308, 1318, 10.1126/science1108367 · DOI
- Anjum, 2005, Curr. Biol., 15, 1762, 10.1016/j.cub.2005.08.050 · DOI
- Shahbazian, 2006, EMBO J., 25, 2781, 10.1038/sj.emboj.7601166 · DOI
- Tee, 2003, Curr. Biol., 13, 1259, 10.1016/S0960-9822(03)00506-2 · DOI · Paper page
- Romanelli, 1999, Mol. Cell Biol., 19, 2921, 10.1128/MCB.19.4.2921 · DOI
- Leighton, 1995, FEBS Lett., 375, 289, 10.1016/0014-5793(95)01170-J · DOI
- Richards, 2001, Mol. Cell Biol., 21, 7470, 10.1128/MCB.21.21.7470-7480.2001 · DOI
- Holz, 2005, Cell, 123, 569, 10.1016/j.cell.2005.10.024 · DOI · Paper page
- Erikson, 1985, Proc. Natl. Acad. Sci. U. S. A., 82, 742, 10.1073/pnas.82.3.742 · DOI
- Ballou, 1991, Nature, 349, 348, 10.1038/349348a0 · DOI
- Ma, 2005, Cell, 121, 179, 10.1016/j.cell.2005.02.031 · DOI · Paper page
- Rajasekhar, 2003, Mol. Cell, 12, 889, 10.1016/S1097-2765(03)00395-2 · DOI · Paper page
- Kelleher, 2004, Neuron, 44, 59, 10.1016/j.neuron.2004.09.013 · DOI · Paper page
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Elkabets, M., Vora, S., Juric, D., Morse, N., Mino-Kenudson, M., Muranen, T., Tao, J., Campos, A. B., Rodon, J., Ibrahim, Y. H., et al. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3005747 · Cited by 332
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Metadata
- Authors
- Roux, P. P., Shahbazian, D., Vu, H., Holz, M. K., Cohen, M. S., Taunton, J., Sonenberg, N., & Blenis, J.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2007-05
- Volume
- 282
- Issue
- 19
- Pages
- 14056-14064
- ISSN
- 0021-9258
- Cited by
- 702
- References
- 0
- Language
- en
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