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Cell Growth and Development

Protein Kinase C Phosphorylates Ribosomal Protein S6 Kinase βII and Regulates Its Subcellular Localization

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Pages 852-863 | Received 05 Jul 2002, Accepted 29 Oct 2002, Published online: 27 Mar 2023

REFERENCES

  • Akimoto, K., M. Nakaya, T. Yamanaka, J. Tanaka, S. Matsuda, Q. P. Weng, J. Avruch, and S. Ohno. 1998. Atypical protein kinase C lambda binds and regulates p70 S6 kinase. Biochem. J. 335: 417–424.
  • Avruch, J., C. Belham, Q. Weng, K. Hara, and K. Yonezawa. 2001. The p70 S6 kinase integrates nutrient and growth signals to control translational capacity. Prog. Mol. Subcell. Biol. 26: 115–154.
  • Brostrom, M. A., K. V. Chin, C. Cade, D. Gmitter, and C. O. Brostrom. 1987. Stimulation of protein synthesis in pituitary cells by phorbol esters and cyclic AMP. Evidence for rapid induction of a component of translational initiation. J. Biol. Chem. 262: 16515–16523.
  • Brown, E. J., P. A. Beal, C. T. Keith, J. Chen, T. B. Shin, and S. L. Schreiber. 1995. Control of p70 s6 kinase by kinase activity of FRAP in vivo. Nature 377: 441–446.
  • Brownawell, A. M., G. J. Kops, I. G. Macara, and B. M. Burgering. 2001. Inhibition of nuclear import by protein kinase B (Akt) regulates the subcellular distribution and activity of the forkhead transcription factor AFX. Mol. Cell. Biol. 21: 3534–3546.
  • Burgering, B. M., and P. J. Coffer. 1995. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376: 599–602.
  • Burnett, P. E., R. K. Barrow, N. A. Cohen, S. H. Snyder, and D. M. Sabatini. 1998. RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc. Natl. Acad. Sci. USA 95: 1432–1437.
  • Burnett, P. E., S. Blackshaw, M. M. Lai, I. A. Qureshi, A. F. Burnett, D. M. Sabatini, and S. H. Snyder. 1998. Neurabin is a synaptic protein linking p70 S6 kinase and the neuronal cytoskeleton. Proc. Natl. Acad. Sci. USA 95: 8351–8356.
  • Chou, M. M., and J. Blenis. 1996. The 70 kDa S6 kinase complexes with and is activated by the Rho family G proteins Cdc42 and Rac1. Cell. 85: 573–583.
  • Chou, M. M., and J. Blenis. 1995. The 70 kDa S6 kinase: regulation of a kinase with multiple roles in mitogenic signalling. Curr. Opin. Cell Biol. 7: 806–814.
  • Chung, J., T. C. Grammer, K. P. Lemon, A. Kazlauskas, and J. Blenis. 1994. PDGF- and insulin-dependent pp70S6k activation mediated by phosphatidylinositol-3-OH kinase. Nature 370: 71–75.
  • Cramer, R., W. J. Richter, E. Stimson, and A. L. Burlingame. 1998. Analysis of phospho- and glycopolypeptides with infrared matrix-assisted laser desorption and ionization. Anal. Chem. 70: 4939–4944.
  • de Groot, R. P., L. M. Ballou, and P. Sassone-Corsi. 1994. Positive regulation of the cAMP-responsive activator CREM by the p70 S6 kinase: an alternative route to mitogen-induced gene expression. Cell 79: 81–91.
  • Dennis, P. B., N. Pullen, R. B. Pearson, S. C. Kozma, and G. Thomas. 1998. Phosphorylation sites in the autoinhibitory domain participate in p70(s6k) activation loop phosphorylation. J. Biol. Chem. 273: 14845–14852.
  • Dufner, A., and G. Thomas. 1999. Ribosomal S6 kinase signaling and the control of translation. Exp. Cell Res. 253: 100–109.
  • Duncan, R., and E. H. McConkey. 1982. Preferential utilization of phosphorylated 40-S ribosomal subunits during initiation complex formation. Eur. J. Biochem. 123: 535–538.
  • Gorlich, D., and U. Kutay. 1999. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol. 15: 607–660.
  • Gorlich, D., and I. W. Mattaj. 1996. Nucleocytoplasmic transport. Science 271: 1513–1518.
  • Gout, I., T. Minami, K. Hara, Y. Tsujishita, V. Filonenko, M. D. Waterfield, and K. Yonezawa. 1998. Molecular cloning and characterization of a novel p70 S6 kinase, p70 S6 kinase beta containing a proline-rich region. J. Biol. Chem. 273: 30061–30064.
  • Han, J. W., R. B. Pearson, P. B. Dennis, and G. Thomas. 1995. Rapamycin, wortmannin, and the methylxanthine SQ20006 inactivate p70s6k by inducing dephosphorylation of the same subset of sites. J. Biol. Chem. 270: 21396–21403.
  • Hara, K., K. Yonezawa, Q. P. Weng, M. T. Kozlowski, C. Belham, and J. Avruch. 1998. Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4E BP1 through a common effector mechanism. J. Biol. Chem. 273: 14484–14494.
  • Harada, H., J. S. Andersen, M. Mann, N. Terada, and S. J. Korsmeyer. 2001. p70S6 kinase signals cell survival as well as growth, inactivating the pro-apoptotic molecule BAD. Proc. Natl. Acad. Sci. USA 98: 9666–9670.
  • Heist, E. K., M. Srinivasan, and H. Schulman. 1998. Phosphorylation at the nuclear localization signal of Ca2+/calmodulin-dependent protein kinase II blocks its nuclear targeting. J. Biol. Chem. 273: 19763–19771.
  • Jans, D. A., and S. Hubner. 1996. Regulation of protein transport to the nucleus: central role of phosphorylation. Physiol. Rev. 76: 651–685.
  • Jefferies, H. B., S. Fumagalli, P. B. Dennis, C. Reinhard, R. B. Pearson, and G. Thomas. 1997. Rapamycin suppresses 5′TOP mRNA translation through inhibition of p70s6k. EMBO J. 16: 3693–3704.
  • Kaffman, A., and E. K. O'Shea. 1999. Regulation of nuclear localization: a key to a door. Annu. Rev. Cell Dev. Biol. 15: 291–339.
  • Kim, J. E., and J. Chen. 2000. Cytoplasmic-nuclear shuttling of FKBP12-rapamycin-associated protein is involved in rapamycin-sensitive signaling and translation initiation. Proc. Natl. Acad. Sci. USA 97: 14340–14345.
  • Koh, H., K. Jee, B. Lee, J. Kim, D. Kim, Y. H. Yun, J. W. Kim, H. S. Choi, and J. Chung. 1999. Cloning and characterization of a nuclear S6 kinase, S6 kinase-related kinase (SRK); a novel nuclear target of Akt. Oncogene 18: 5115–5119.
  • Lane, H. A., A. Fernandez, N. J. Lamb, and G. Thomas. 1993. p70s6k function is essential for G1 progression. Nature 363: 170–172.
  • Lee-Fruman, K. K., C. J. Kuo, J. Lippincott, N. Terada, and J. Blenis. 1999. Characterization of S6K2, a novel kinase homologous to S6K1. Oncogene 18: 5108–5114.
  • Le Good, J. A., W. H. Ziegler, D. B. Parekh, D. R. Alessi, P. Cohen, and P. J. Parker. 1998. Protein kinase C isotypes controlled by phosphoinositide 3-kinase through the protein kinase PDK1. Science 281: 2042–2045.
  • Martin, K. A., S. S. Schalm, C. Richardson, A. Romanelli, K. L. Keon, and J. Blenis. 2001. Regulation of ribosomal S6 kinase 2 by effectors of the phosphoinositide 3-kinase pathway. J. Biol. Chem. 276: 7884–7891.
  • Martin, K. A., S. S. Schalm, A. Romanelli, K. L. Keon, and J. Blenis. 2001. Ribosomal S6 kinase 2 inhibition by a potent C-terminal repressor domain is relieved by mitogen-activated protein-extracellular signal-regulated kinase kinase-regulated phosphorylation. J. Biol. Chem. 276: 7892–7898.
  • Mellor, H., and P. J. Parker. 1998. The extended protein kinase C superfamily. Biochem. J. 332: 281–292.
  • Minami, T., K. Hara, N. Oshiro, S. Ueoku, K. Yoshino, C. Tokunaga, Y. Shirai, N. Saito, I. Gout, and K. Yonezawa. 2001. Distinct regulatory mechanism for p70 S6 kinase beta from that for p70 S6 kinase alpha. Genes Cells 6: 1003–1015.
  • Montagne, J., M. J. Stewart, H. Stocker, E. Hafen, S. C. Kozma, and G. Thomas. 1999. Drosophila S6 kinase: a regulator of cell size. Science 285: 2126–2129.
  • Morley, S. J., and J. A. Traugh. 1990. 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. 265: 10611–10616.
  • Newton, A. C. 1995. Protein kinase C: structure, function, and regulation. J. Biol. Chem. 270: 28495–28498.
  • Nigg, E. A. 1997. Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature 386: 779–787.
  • Nishizuka, Y. 1992. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258: 607–614.
  • Nishizuka, Y. 1984. The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature 308: 693–698.
  • Pardo, O. E., A. Arcaro, G. Salerno, T. D. Tetley, T. Valovka, I. Gout, and M. J. Seckl. 2001. Novel cross talk between MEK and S6K2 in FGF-2 induced proliferation of SCLC cells. Oncogene 20: 7658–7667.
  • Pellieux, C., T. Sauthier, A. Domenighetti, D. J. Marsh, R. D. Palmiter, H. R. Brunner, and T. Pedrazzini. 2000. Neuropeptide Y (NPY) potentiates phenylephrine-induced mitogen-activated protein kinase activation in primary cardiomyocytes via NPY Y5 receptors. Proc. Natl. Acad. Sci. USA 97: 1595–1600.
  • Pende, M., S. C. Kozma, M. Jaquet, V. Oorschot, R. Burcelin, Y. Le Marchand-Brustel, J. Klumperman, B. Thorens, and G. Thomas. 2000. Hypoinsulinaemia, glucose intolerance and diminished beta-cell size in S6K1-deficient mice. Nature 408: 994–997.
  • Petritsch, C., H. Beug, A. Balmain, and M. Oft. 2000. TGF-beta inhibits p70 S6 kinase via protein phosphatase 2A to induce G(1) arrest. Genes Dev. 14: 3093–3101.
  • Puceat, M., R. Hilal-Dandan, B. Strulovici, L. L. Brunton, and J. H. Brown. 1994. Differential regulation of protein kinase C isoforms in isolated neonatal and adult rat cardiomyocytes. J. Biol. Chem. 269: 16938–16944.
  • Pullen, N., P. B. Dennis, M. Andjelkovic, A. Dufner, S. C. Kozma, B. A. Hemmings, and G. Thomas. 1998. Phosphorylation and activation of p70s6k by PDK1. Science 279: 707–710.
  • Pullen, N., and G. Thomas. 1997. The modular phosphorylation and activation of p70s6k. FEBS Lett. 410: 78–82.
  • Reinhard, C., A. Fernandez, N. J. Lamb, and G. Thomas. 1994. Nuclear localization of p85s6k: functional requirement for entry into S phase. EMBO J. 13: 1557–1565.
  • Romanelli, A., K. A. Martin, A. Toker, and J. Blenis. 1999. p70 S6 kinase is regulated by protein kinase Cζ and participates in a phosphoinositide 3-kinase-regulated signalling complex. Mol. Cell Biol. 19: 2921–2928.
  • Rosenfeld, J., J. Capdevielle, J. C. Guillemot, and P. Ferrara. 1992. In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional gel electrophoresis. Anal. Biochem. 203: 173–179.
  • Shah, O. J., S. R. Kimball, and L. S. Jefferson. 2000. Among translational effectors, p70S6k is uniquely sensitive to inhibition by glucocorticoids. Biochem. J. 347: 389–397.
  • Shima, H., M. Pende, Y. Chen, S. Fumagalli, G. Thomas, and S. C. Kozma. 1998. Disruption of the p70(s6k)/p85(s6k) gene reveals a small mouse phenotype and a new functional S6 kinase. EMBO J. 17: 6649–6659.
  • Silver, P. A. 1991. How proteins enter the nucleus. Cell 64: 489–497.
  • Stewart, M. J., and G. Thomas. 1994. Mitogenesis and protein synthesis: a role for ribosomal protein S6 phosphorylation? Bioessays 16: 809–815.
  • Susa, M., A. R. Olivier, D. Fabbro, and G. Thomas. 1989. EGF induces biphasic S6 kinase activation: late phase is protein kinase C-dependent and contributes to mitogenicity. Cell 57: 817–824.
  • Susa, M., D. Vulevic, H. A. Lane, and G. Thomas. 1992. Inhibition or down-regulation of protein kinase C attenuates late phase p70s6k activation induced by epidermal growth factor but not by platelet-derived growth factor or insulin. J. Biol. Chem. 267: 6905–6909.
  • Tang, H., E. Hornstein, M. Stolovich, G. Levy, M. Livingstone, D. Templeton, J. Avruch, and O. Meyuhas. 2001. Amino acid-induced translation of TOP mRNAs is fully dependent on phosphatidylinositol 3-kinase-mediated signaling, is partially inhibited by rapamycin, and is independent of S6K1 and rpS6 phosphorylation. Mol. Cell. Biol. 21: 8671–8683.
  • Topham, M. K., M. Bunting, G. A. Zimmerman, T. M. McIntyre, P. J. Blackshear, and S. M. Prescott. 1998. Protein kinase C regulates the nuclear localization of diacylglycerol kinase-zeta. Nature 394: 697–700.
  • Valovka, T., V. Filonenko, S. Palchevsky, M. Velikiy, L. Drobot, M. D. Waterfield, G. Matsuka, and I. Gout. 1999. Functional and regulatory properties of p70S6 kinase β. Biopolym. Cell 15: 1–7.
  • Wang, L., I. Gout, and C. G. Proud. 2001. Cross-talk between the ERK and p70 S6 kinase (S6K) signaling pathways. MEK-dependent activation of S6K2 in cardiomyocytes. J. Biol. Chem. 276: 32670–32677.
  • Wang, L., X. Wang, and C. G. Proud. 2000. Activation of mRNA translation in rat cardiac myocytes by insulin involves multiple rapamycin-sensitive steps. Am. J. Physiol. Heart Circ. Physiol. 278: H1056–H1068.
  • Wang, X., W. Li, M. Williams, N. Terada, D. R. Alessi, and C. G. Proud. 2001. Regulation of elongation factor 2 kinase by p90(RSK1) and p70 S6 kinase. EMBO J. 20: 4370–4379.
  • Weng, Q. P., M. Kozlowski, C. Belham, A. Zhang, M. J. Comb, and J. Avruch. 1998. Regulation of the p70 S6 kinase by phosphorylation in vivo. Analysis using site-specific anti-phosphopeptide antibodies. J. Biol. Chem. 273: 16621–16629.

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