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Research Article

The Principal Rapamycin-Sensitive p70s6k Phosphorylation Sites, T-229 and T-389, Are Differentially Regulated by Rapamycin-Insensitive Kinase Kinases

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Pages 6242-6251 | Received 13 Jun 1996, Accepted 06 Aug 1996, Published online: 29 Mar 2023

REFERENCES

  • Ballou, L. M., H. Luther, and G. Thomas. 1991. MAP2 kinase and 70 kDa S6 kinase lie on distinct signalling pathways. Nature (London) 349:348–350.
  • Bandi, H. R., S. Ferrari, J. Krieg, H. E. Meyer, and G. Thomas. 1993. Identification of 40S ribosomal protein S6 phosphorylation sites in Swiss mouse 3T3 fibroblasts stimulated with serum. J. Biol. Chem. 268:4530–4533.
  • Banerjee, P., M. F. Ahmad, J. R. Grove, C. Kozlosky, D. J. Price, and J. Avruch. 1990. Molecular structure of a major insulin/mitogen-activated 70 kDa S6 protein kinase. Proc. Natl. Acad. Sci. USA 87:8550–8554.
  • Blenis, J., J. Chung, E. Erikson, D. A. Alcorta, and R. L. Erikson. 1991. Distinct mechanisms for the activation of the RSK kinase/MAP2kinase/ pp90rsk and pp70-S6 kinase signaling systems are indicated by inhibition of protein synthesis. Cell Growth Differentiation 2:279–285.
  • Bos, J. L. 1995. A target for phosphoinositide 3-kinase: Akt/PKB. Trends Biochem. Sci. 20:441–442.
  • Boyle, W. J., P. van der Geer, and T. Hunter. 1991. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 201:110–149.
  • Brown, E. J., M. A. Albers, T. B. Shin, K. Ichikawa, C. T. Keith, W. S. Lane, and S. L. Schreiber. 1994. A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature (London) 369:756–758.
  • 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 (London) 377:441–446.
  • Burgering, B. M. T., and P. J. Coffer. 1995. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature (London) 376:599–602.
  • Cano, E., C. A. Hazzalin, and L. C. Mahadevan. 1994. Anisomycin-activated protein kinases p45 and p55 but not mitogen-activated protein kinases ERK-1 and -2 are implicated in the induction of c-fos and c-jun. Mol. Cell. Biol. 14:7352–7362.
  • Cheatham, L., M. Monfar, M. M. Chou, and J. Blenis. 1995. Structural and functional analysis of pp70s6k. Proc. Natl. Acad. Sci. USA 92:11696–11700.
  • 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.
  • Chung, J., T. C. Grammer, K. P. Lemon, A. Kazlauskas, and J. Blenis. 1994. PDGF- and insulin-dependent pp70s6k activation mediated by phosphatidyl-inositol-3-OH kinase. Nature (London) 370:71–75.
  • Chung, J., C. J. Kuo, G. R. Crabtree, and J. Blenis. 1992. Rapamycin-FKBP specifically blocks growth-dependent activation of and signaling by the 70 kDa S6 protein kinases. Cell 69:1227–1236.
  • Cross, M. J., A. Stewart, M. N. Hodgkin, D. J. Kerr, and M. J. O. Wakelam. 1995. Wortmannin and its structural analogue demethoxyviridin inhibit stimulated phospholipase A2 activity in Swiss 3T3 cells. J. Biol. Chem. 270:25352–25355.
  • Deng, T., and M. Karin. 1994. c-Fos transcriptional activity stimulated by H-Ras-activated protein kinase distinct from JNK and ERK. Nature (London) 371:171–175.
  • Downward, J. 1994. Regulating S6 kinase. Nature (London) 371:378–379.
  • Downward, J. 1995. A target for PI(3) kinase. Nature (London) 376:553–554.
  • Ferrari, S., H. R. Bandi, B. M. Bussian, and G. Thomas. 1991. Mitogen-activated 70 K S6 kinase. J. Biol. Chem. 266:22770–22775.
  • Ferrari, S., W. Bannwarth, S. J. Morley, N. F. Totty, and G. Thomas. 1992. Activation of p70s6k is associated with phosphorylation of four clustered sites displaying Ser/Thr-Pro motifs. Proc. Natl. Acad. Sci. USA 89:7282–7285.
  • Ferrari, S., R. B. Pearson, M. Siegmann, S. C. Kozma, and G. Thomas. 1993. The immunosuppressant rapamycin induces inactivation of p70s6k through dephosphorylation of a novel set of sites. J. Biol. Chem. 268:16091–16094.
  • Ferrari, S., and G. Thomas. 1994. S6 phosphorylation and the p70s6k/p85s6k. Crit. Rev. Biochem. Mol. Biol. 29:385–413.
  • Flotow, H., and G. Thomas. 1992. Substrate recognition determinants of the mitogen-activated 70 K S6 kinase from rat liver. J. Biol. Chem. 267:3074–3078.
  • Franke, T. F., S. I. Yang, T. O. Chan, K. Datta, A. Kazlauskas, D. K. Morrison, D. R. Kaplan, and P. N. Tsichlis. 1995. The protein kinase encoded by the Akt protooncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81:727–736.
  • 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.
  • Hanks, S. K., and T. Hunter. 1995. The eukaryotic protein kinase superfamily, p. 7–47. In G. Hardie and S. K. Hanks (ed.), The protein kinase facts book. Protein-serine kinases. Academic Press, London.
  • Hara, K., K. Yonezawa, H. Sakaue, A. Ando, K. Kotani, T. Kitamura, Y. Kitamura, H. Ueda, L. Stephens, T. R. Jackson, M. D. Waterfield, and M. Kasuga. 1994. 1-Phosphatidylinositol 3-kinase activity is required for insulin-stimulated glucose transport but not for ras activation in CHO cells. Proc. Natl. Acad. Sci. USA 91:7415–7419.
  • Hara, K., K. Yonezawa, H. Sakaue, K. Kotani, A. Kojima, M. D. Waterfield, and M. Kasuga. 1995. Normal activation of p70 S6 kinase by insulin in cells overexpressing dominant negative 85 kDa subunit of phosphoinositide 3-kinase. Biochem. Biophys. Res. Commun. 208:735–741.
  • Hibi, M., A. Lin, T. Smeal, A. Minden, and M. Karin. 1993. Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-jun activation domain. Genes Dev. 7:2135–2148.
  • Hunter, T. 1995. When is a lipid kinase not a lipid kinase? When it is a protein kinase. Cell 83:1–4.
  • Jakubowicz, T., and D. P. Leader. 1987. Activation of a ribosomal protein S6 kinase in mouse fibroblasts during infection with herpesvirus. Eur. J. Biochem. 168:371–376.
  • Jefferies, H. B. J., and G. Thomas. 1995. Ribosomal protein S6 phosphorylation and signal transduction, p. 389–410. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
  • Kazlauskas, A., and J. A. Cooper. 1989. Autophosphorylation of the PDGF receptor in the kinase insert region regulates interactions with cell proteins. Cell 58:1121–1133.
  • Kunz, J., R. Henriquez, U. Scheider, M. Deuter-Reinhard, N. R. Movva, and M. N. Hall. 1993. Target of rapamycin in yeast, TOR2 is an essential phosphatidylinositol kinase homologue required for G1 progression. Cell 73:585–596.
  • Kuo, C. J., J. Chung, D. F. Fiorentino, W. M. Flanagan, J. Blenis, and G. R. Crabtree. 1992. Rapamycin selectively inhibits interleukin-2 activation of p70 S6 kinase. Nature (London) 358:70–73.
  • Loreni, F. Personal communication.
  • Mahalingam, M., and D. J. Templeton. 1996. Constitutive activation of S6 kinase by deletion of amino-terminal autoinhibitory and rapamycin sensitivity domains. Mol. Cell. Biol. 16:405–413.
  • Meyuhas, O., D. Avni, and S. Shama. 1996. Translational control of ribosomal protein mRNAs in eukaryotes, p. 363–388. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
  • Ming, X.-F., B. M. T. Burgering, S. Wennström, L. Claesson-Welsh, C. H. Heldin, J. L. Bos, S. C. Kozma, and G. Thomas. 1994. Activation of p70/p85 S6 kinase by a pathway independent of p21ras. Nature (London) 371:426–429.
  • Mukhopadhyay, N. K., D. J. Price, J. M. Kyriakis, S. L. Pelech, J. Sanghera, and J. Avruch. 1992. An array of insulin-activated, proline-directed serine/ threonine protein kinases phosphorylate the p70 S6 kinase. J. Biol. Chem. 267:3325–3335.
  • Pause, A., G. J. Belsham, A. C. Gingras, O. Donze, T. A. Lin, J. C. Lawrence Jr., and N. Sonenberg. 1994. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature (London) 371:762–767.
  • Pearson, R. B., P. B. Dennis, J.-W. Han, N. A. Williamson, S. C. Kozma, R. E. H. Wettenhall, and G. Thomas. 1995. The principal target of rapamycin-induced p70s6k inactivation is a novel phosphorylation site within a conserved hydrophobic domain. EMBO J. 21:5279–5287.
  • Price, D. J., J. R. Grove, V. Calvo, J. Avruch, and B. E. Bierer. 1992. Rapamycin-induced inhibition of the 70-kilodalton S6 protein kinase. Science 257:973–977.
  • Price, D. J., N. K. Mukhopadhyay, and J. Avruch. 1991. Insulin-activated kinases phosphorylate a pseudo-substrate inhibitor of the p70 S6 kinase. J. Biol. Chem. 266:16281–16284.
  • Reinhard, C., A. Fernandez, N. J. C. Lamb, and G. Thomas. 1994. Nuclear localization of p85s6k: functional requirement for entry into S phase. EMBO J. 13:1557–1565.
  • Reinhard, C., G. Thomas, and S. C. Kozma. 1992. A single gene encodes two isoforms of the p70 S6 kinase: activation upon mitogenic stimulation. Proc. Natl. Acad. Sci. USA 89:4052–4056.
  • Stewart, M. J., and G. Thomas. 1994. Mitogenesis and protein synthesis: a role for ribosomal protein S6 phosphorylation? Bioessays 16:1–7.
  • Vazquez, D., and A. Jimenez. 1980. Antibiotic inhibitors of translation in eukaryotes, p. 847–870. In G. Chambliss, G. R. Craven, J. Davis, K. Davis, L. Kahan, and M. Nomura (ed.), Ribosomes. Structure, function and genetics. University Park Press, Baltimore.
  • Von Manteuffel, S. R., A.-C. Gingras, X.-F. Ming, N. Sonenberg, and G. Thomas. 1996. 4E-BP1 phosphorylation is mediated by the FRAP-p70s6k pathway and is independent of mitogen-activated protein kinase. Proc. Natl. Acad. Sci. USA 93:4076–4080.
  • Weng, Q.-P., K. Andrabi, A. Klippel, M. T. Kozlowski, L. T. Williams, and J. Avruch. 1995. Phosphatidylinositol 3-kinase signals activation of p70 S6 kinase in situ through site specific p70 phosphorylation. Proc. Natl. Acad. Sci. USA 92:5744–5748.
  • Weng, Q.-P., K. Andrabi, M. T. Kozlowski, J. R. Grove, and J. Avruch. 1995. Multiple independent inputs are required for activation of the p70 S6 kinase. Mol. Cell. Biol. 15:2333–2340.

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