Requirement for Activation of the Serine-Threonine Kinase Akt (Protein Kinase B) in Insulin Stimulation of Protein Synthesis but Not of Glucose Transport

REFERENCES

• Alessi, D. R., M. Andjelkovic, B. Caudwell, P. Cron, N. Morrice, P. Cohen, and B. A. Hemmings 1996. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15: 6541–6551.
   PubMed Web of Science ®Google Scholar
• Alessi, D. R., S. R. James, C. P. Downes, A. B. Holmes, P. R. Gaffney, C. B. Reese, and P. Cohen 1997. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Bα. Curr. Biol. 7: 261–269.
   PubMed Web of Science ®Google Scholar
• Bellacosa, A., J. R. Testa, S. P. Staal, and P. N. Tsichlis 1991. A retroviral oncogene, AKT, encoding a serine-threonine kinase containing an SH2-like region. Science 254: 244–247.
   Google Scholar
• Burgering, B. M. T., and P. J. Coffer 1995. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376: 599–602.
   PubMed Web of Science ®Google Scholar
• Carpenter, L. C., and L. C. Cantley 1996. Phosphoinositide kinases. Curr. Opin. Cell Biol. 8: 153–158.
   PubMed Web of Science ®Google Scholar
• Cheatham, B., C. J. Vlahos, L. Cheatham, L. Wang, J. Blenis, and C. R. Kahn 1994. Phosphatidylinositol 3-kinase activation is required for insulin stimulation of pp70 S6 kinase, DNA synthesis, and glucose transporter translocation. Mol. Cell. Biol. 14: 4902–4911.
   PubMed Web of Science ®Google Scholar
• Coffer, P. J., and J. R. Woodgett 1991. Molecular cloning and characterization of a novel putative protein-serine kinase related to the cAMP-dependent and protein kinase-C families. Eur. J. Biochem. 201: 475–481.
   PubMedGoogle Scholar
• Cowley, S., H. Paterson, P. Kemp, and C. J. Marshall 1994. Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and transformation of NIH 3T3 cells. Cell 77: 841–852.
   PubMed Web of Science ®Google Scholar
• Cross, D. A. E., D. R. Alessi, P. Cohen, M. Andjelkovich, and B. A. Hemmings 1995. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378: 785–789.
   PubMed Web of Science ®Google Scholar
• Dardevet, D., C. Sornet, T. Vary, and J. Grizard 1996. Phosphatidylinositol 3-kinase and p70 S6 kinase participate in the regulation of protein turnover in skeletal muscle by insulin and insulin-like growth factor I. Endocrinology 137: 4087–4094.
   PubMed Web of Science ®Google Scholar
• Didchenko, S. A., B. Tlton, B. A. Hemmings, K. Ballmer-Hofer, and M. Thelen 1996. Constitutive activation of protein kinase B and phosphorylation of p47phox by a membrane-targeted phosphoinositide 3-kinase. Curr. Biol. 6: 1271–1278.
   PubMedGoogle Scholar
• Dorrestijn, J., D. M. Ouwens, N. Van den Berghe, J. L. Bos, and J. A. Maassen 1996. Expression of a dominant negative Ras mutant does not affect stimulation of glucose uptake and glycogen synthesis by insulin. Diabetologia 39: 558–563.
   PubMed Web of Science ®Google Scholar
• Dudek, H., S. R. Datta, T. F. Franke, M. J. Birnbaum, R. Yao, G. M. Cooper, R. A. Segal, D. R. Kaplan, and M. E. Greenberg 1997. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275: 661–665.
   PubMed Web of Science ®Google Scholar
• Franke, T. F., S. I. Yang, T. O. Chan, K. Datta, A. Kazluskas, 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.
   PubMed Web of Science ®Google Scholar
• Franke, T. F., D. R. Kaplan, L. C. Cantley, and A. Toker 1997. Direct binding of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science 275: 665–667.
   PubMed Web of Science ®Google Scholar
• Hara, K., K. Yonezawa, H. Sakaue, A. Ando, K. Kotani, T. Kitamura, Y. Kitamura, H. Ueda, L. Stephens, T. R. Jackson, P. T. Hawkins, R. Dhand, A. E. Clark, G. D. Holman, M. D. Waterfield, and M. Kasuga 1994. 1-Phosphatidylinositol 3-kinase activity is required for insulin stimulated glucose transport but not for activation in CHO cells. Proc. Natl. Acad. Sci. USA 91: 7415–7419.
   PubMed Web of Science ®Google Scholar
• Hausdroff, S. F., J. V. Frangioni, and M. J. Birnbaum 1994. Role of p21ras in insulin-stimulated glucose transport in 3T3-L1 adipocytes. J. Biol. Chem. 269: 21391–21394.
   PubMedGoogle Scholar
• Holman, G. H., and M. Kasuga 1997. From receptor to transporter: insulin signaling to glucose transport. Diabetologia 40: 991–1003.
   PubMed Web of Science ®Google Scholar
• Jones, P. F., T. Jakubowicz, F. J. Pitossi, F. Maurer, and B. A. Hemmings 1991. Molecular cloning and identification of a serine/threonine protein kinase of the second-messenger subfamily. Proc. Natl. Acad. Sci. USA 88: 4171–4175.
   PubMed Web of Science ®Google Scholar
• Khwaja, A., P. Rodriguez-Viciana, S. Wennstrom, P. H. Warne, and J. Downward 1997. Matrix adhesion and Ras transformation both activate a phosphoinositide 3-OH kinase and protein kinase B/Akt cellular survival pathway. EMBO J. 16: 2783–2793.
   PubMed Web of Science ®Google Scholar
• Kimball, S. R., T. C. Vary, and L. S. Jefferson 1994. Regulation of protein synthesis by insulin. Annu. Rev. Physiol. 56: 321–348.
   PubMedGoogle Scholar
• Kitamura, Y., T. Kitamura, H. Sakaue, T. Maeda, H. Ueno, S. Nishio, S. Ohno, S.-I. Osada, M. Sakaue, W. Ogawa, and M. Kasuga 1997. Interaction of Nck-associated protein 1 with activated GTP-binding protein Rac. Biochem. J. 322: 873–878.
   PubMedGoogle Scholar
• Klippel, A., C. Reinhard, M. Kavanaugh, G. Apell, M. A. Escobedo, and L. T. Williams 1996. Membrane localization of phosphatidylinositol 3-kinase is sufficient to activate multiple signal-transducing kinase pathways. Mol. Cell. Biol. 16: 4117–4127.
   PubMed Web of Science ®Google Scholar
• Klippel, A., W. M. Kavanaugh, D. Pot, and L. T. Williams 1997. A specific product of phosphatidylinositol 3-kinase directly activates the protein kinase Akt through its pleckstrin homology domain. Mol. Cell. Biol. 17: 338–344.
   PubMed Web of Science ®Google Scholar
• Kohn, A. D., K. S. Kovacina, and R. A. Roth 1995. Insulin stimulates the kinase-activity of RAC-PK, a pleckstrin homology domain-containing Ser/Thr kinase. EMBO J. 14: 4288–4295.
   PubMedGoogle Scholar
• Kohn, A. D., F. Takeuchi, and R. A. Roth 1996. Akt, a pleckstrin homology domain containing kinase, is activated primarily by phosphorylation. J. Biol. Chem. 271: 21920–21926.
   PubMed Web of Science ®Google Scholar
• Kohn, A. D., S. A. Summers, M. J. Birnbaum, and R. A. Roth 1996. Expression of constitutively active Akt Ser/Thr kinase in 3T3-L1 adipocytes stimulates glucose uptake and glucose transporter 4 translocation. J. Biol. Chem. 271: 31372–31378.
   PubMed Web of Science ®Google Scholar
• Konishi, H., T. Shinomura, S.-I. Kuroda, Y. Ono, and U. Kikkawa 1994. Molecular cloning of rat RAC protein kinase α and β and their association with protein kinase C ζ. Biochem. Biophys. Res. Commun. 205: 817–825.
   PubMedGoogle Scholar
• Konishi, H., S. Kuroda, M. Tanaka, H. Matsuzaki, Y. Ono, K. Kameyama, T. Haga, and U. Kikkawa 1995. Molecular cloning and characterization of a new member of the RAC protein kinase family: association of the pleckstrin homology domain of three types of RAC protein kinase with protein kinase C subspecies and beta gamma subunits of G proteins. Biochem. Biophys. Res. Commun. 216: 526–534.
   PubMedGoogle Scholar
• Konishi, H., H. Matsuzaki, M. Tanaka, Y. Ono, C. Tokunaga, S. Kuroda, and U. Kikkawa 1996. Activation of RAC-protein kinase by heat shock and hyperosmolarity stress through a pathway independent of phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 93: 7639–7643.
   PubMed Web of Science ®Google Scholar
• Kotani, K., K. Yonezawa, K. Hara, H. Ueda, Y. Kitamura, H. Sakaue, A. Ando, A. Chavanieu, B. Calas, F. Grigorescu, M. Nishiyama, M. D. Waterfield, and M. Kasuga 1994. Involvement of phosphoinositide 3-kinase in insulin- or IGF-1-induced membrane ruffling. EMBO J. 13: 2313–2321.
   PubMedGoogle Scholar
• Kozma, L., K. Baltensperger, J. Klarlund, A. Porras, E. Santos, and M. P. Czech 1993. The ras signaling pathway mimics insulin action on glucose transporter translocation. Proc. Natl. Acad. Sci. USA 90: 4460–4464.
   PubMedGoogle Scholar
• Kozma, S. C., S. Ferrari, P. Bassand, M. Siegmann, N. Totty, and G. Thomas 1990. Cloning of the mitogen-activated S6 kinase from rat liver reveals an enzyme of the second messenger subfamily. Proc. Natl. Acad. Sci. USA 87: 7365–7369.
   PubMed Web of Science ®Google Scholar
• Mendez, R., M. G. Myers, M. F. White, and R. E. Rhoads 1996. Stimulation of protein synthesis, eukaryotic translation initiation factor 4E phosphorylation, and PHAS-I phosphorylation by insulin requires insulin receptor substrate 1 and phosphatidylinositol 3-kinase. Mol. Cell. Biol. 16: 2857–2864.
   PubMed Web of Science ®Google Scholar
• Mendez, R., G. Kollmorgen, M. F. White, and R. E. Rhoads 1997. Requirement of protein kinase Cζ for stimulation of protein synthesis by insulin. Mol. Cell. Biol. 17: 5184–5192.
   PubMedGoogle Scholar
• Miyake, S., M. Makimura, Y. Kanegae, S. Harada, Y. Sato, K. Takamori, C. Tokuda, and I. Saito 1996. Efficient generation of recombinant adenoviruses using adenovirus DNA terminal protein complex and a cosmid bearing the full length virus genome. Proc. Natl. Acad. Sci. USA 93: 1320–1324.
   PubMedGoogle Scholar
• Moule, S. K., N. J. Edgell, G. I. Welsh, T. A. Diggle, E. J. Foulstone, K. J. Heesom, C. G. Proud, and R. M. Denton 1995. Multiple signalling pathways involved in the stimulation of fatty acid and glycogen synthesis by insulin in rat epididymal fat cells. Biochem. J. 311: 595–601.
   PubMedGoogle Scholar
• Nakanishi, H., K. A. Brewer, and J. H. Exton 1993. Activation of the ζ isoenzyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 268: 13–16.
   PubMed Web of Science ®Google Scholar
• Okada, T., Y. Kawano, T. Sakakibara, O. Hazeki, and M. Ui 1994. Essential role of phosphatidylinositol 3-kinase in insulin-induced glucose transport and antilipolysis in rat adipocytes. J. Biol. Chem. 269: 3568–3573.
   PubMed Web of Science ®Google Scholar
• Pagés, G., P. Lenormand, G. L’Allemain, J.-C. Chambard, S. Meloche, and J. Pouysségur 1993. Mitogen-activated protein kinases p42mapk and p44mapk are required for fibroblast proliferation. Proc. Natl. Acad. Sci. USA 90: 8319–8323.
   PubMed Web of Science ®Google Scholar
• Price, D. 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.
   PubMed Web of Science ®Google Scholar
• Proud, C. G. 1996. p70 S6 kinase: an enigma with variations. Trends Biochem. Sci. 21: 181–185.
   PubMedGoogle Scholar
• Pullen, N., and G. Thomas 1997. The modular phosphorylation and activation of p70s6k. FEBS Lett. 410: 78–82.
   PubMed Web of Science ®Google Scholar
• Pullen, N., P. B. Dennis, M. Andjelkovic, A. Dafner, S. C. Kozma, B. A. Hemmings, and G. Thomas 1998. Phosphorylation and activation of p70s6k by PDK1. Science 279: 707–710.
   PubMed Web of Science ®Google Scholar
• Quon, M. J., H. Chen, B. R. Ing, M.-L. Liu, M. J. Zarnowski, K. Yonezawa, M. Kasuga, S. W. Cushman, and S. I. Taylor 1995. Roles of 1-phosphatidylinositol 3-kinase and Ras in regulating translocation of GLUT4 in transfected rat adipose cells. Mol. Cell. Biol. 15: 5403–5411.
   PubMed Web of Science ®Google Scholar
• Redpath, N. T., and C. G. Proud 1994. Molecular mechanisms in the control of translation by hormones and growth factors. Biochim. Biophys. Acta 1220: 147–162.
   PubMed Web of Science ®Google Scholar
• Sakaue, H., K. Hara, T. Noguchi, T. Matozaki, K. Kotani, W. Ogawa, K. Yonezawa, M. D. Waterfield, and M. Kasuga 1995. Ras-independent and wortmannin-sensitive activation of glycogen synthase by insulin in Chinese hamster ovary cells. J. Biol. Chem. 270: 11304–11309.
   PubMedGoogle Scholar
• Sakaue, H., W. Ogawa, M. Takata, S. Kuroda, K. Kotani, M. Matsumoto, M. Sakaue, S. Nishio, H. Ueno, and M. Kasuga 1997. Phosphoinositide 3-kinase is required for insulin-induced but not for growth hormone- or hyperosmolarity-induced glucose uptake in 3T3-L1 adipocytes. Mol. Endocrinol. 11: 1552–1562.
   PubMedGoogle Scholar
• Sakaue, M., D. Bowtell, and M. Kasuga 1995. A dominant-negative mutant of mSOS1 inhibits insulin-induced Ras activation and reveals Ras-dependent and -independent insulin signaling pathways. Mol. Cell. Biol. 15: 379–388.
   PubMedGoogle Scholar
• Stephens, L., K. Anderson, D. Stokes, H. Erdjumrnt-Bromega, G. F. Painter, A. B. Holmes, P. R. J. Gaffney, C. B. Reese, F. McCormick, P. Tempst, J. Coadwell, and P. T. Hawkins 1998. Protein kinase B kinases that mediate phosphatidylinositol 3,4,5-triphosphate-dependent activation of protein kinase B. Science 279: 710–714.
   PubMed Web of Science ®Google Scholar
• Stokes, D., L. R. Stephens, T. Copeland, P. J. Gaffney, C. Reese, G. F. Painter, A. B. Holmes, F. McCormick, and P. T. Hawkins 1997. Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science 277: 567–570.
   PubMedGoogle Scholar
• Sutherland, C., R. M. O’Brien, and D. K. Granner 1995. Phosphatidylinositol 3-kinase, but not p70/p85 ribosomal S6 protein kinase, is required for the regulation of phosphoenolpyruvate carboxykinase (PEPCK) gene expression by insulin. Dissociation of signaling pathways for insulin and phorbol ester regulation of PEPCK gene expression. J. Biol. Chem. 270: 15501–15506.
   PubMedGoogle Scholar
• Takata, M., W. Ogawa, and M. Kasuga. Unpublished data.
   Google Scholar
• Tanti, J. F., S. Grillo, T. Gremeaux, P. J. Coffer, E. Van-Obberghen, and Y. Le-Marchand-Brustel 1997. Potential role of protein kinase B in glucose transporter 4 translocation in adipocytes. Endocrinology 138: 2005–2010.
   PubMed Web of Science ®Google Scholar
• Tsakiridis, T., H. E. McDowell, T. Walker, C. P. Downes, H. S. Hundal, M. Vranic, and A. Klip 1995. Multiple roles of phosphatidylinositol 3-kinase in regulation of glucose transport, amino acid transport, and glucose transporters in L6 skeletal muscle cells. Endocrinology 136: 4315–4322.
   PubMed Web of Science ®Google Scholar
• Ui, M., T. Okada, K. Hazeki, and O. Hazeki 1994. Wortmannin as a unique probe for an intracellular signalling protein, phosphoinositide 3-kinase. Trends Biochem. Sci. 20: 303–307.
   Google Scholar
• Welsh, G. I., and C. G. Proud 1993. Glycogen synthase kinase-3 is rapidly inactivated in response to insulin and phosphorylates eukaryotic initiation factor eIF-2B. Biochem. J. 294: 625–629.
   PubMed Web of Science ®Google Scholar
• Welsh, G. I., C. M. Stokes, X. Wang, H. Sakaue, W. Ogawa, M. Kasuga, and C. G. Proud 1997. Activation of translation initiation factor eIF2B by insulin requires phosphatidylinositol 3-kinase. FEBS Lett. 410: 418–422.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• White, M. F., and C. R. Kahn 1994. The insulin signaling system. J. Biol. Chem. 269: 1–4.
   PubMed Web of Science ®Google Scholar
• Wu, X., S. J. Noh, G. Zhou, J. E. Dixon, and K.-L. Guan 1996. Selective activation of MEK1 but not MEK2 by A-Raf from epidermal growth factor-stimulated Hela cells. J. Biol. Chem. 271: 3265–3271.
   PubMed Web of Science ®Google Scholar
• Yano, H., S. Nakanishi, K. Kimura, N. Hanai, Y. Saitoh, Y. Fukui, Y. Nonomura, and Y. Matsuda 1993. Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBL-2H3 cells. J. Biol. Chem. 268: 25846–25856.
   PubMed Web of Science ®Google Scholar