Requirement for activation of the serine-threonine kinase Akt (Protein kinase B) in insulin stimulation of protein synthesis but not of glucose transport

Molecular and Cellular Biology

Volumn 18, Issue 7, 1998, Pages 3708-3717

  Kitamura, Tadahiro ^a   Ogawa, Wataru ^a   Sakaue, Hiroshi ^a   Hino, Yasuhisa ^a   Kuroda, Shoji ^a   Takata, Masafumi ^a   Matsumoto, Michihiro ^a   Maeda, Tetsuo ^a   Konishi, Hiroaki ^a   Kikkawa, Ushio ^a   Kasuga, Masato ^a  

^a KOBE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN SERINE THREONINE KINASE;

AMINO ACID TRANSPORT; ANIMAL CELL; ARTICLE; EFFECTOR CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GENE TARGETING; GLUCOSE TRANSPORT; INSULIN SYNTHESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN SYNTHESIS REGULATION;

ADENOVIRIDAE; ANIMALIA;

EID: 0031806103     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.7.3708     Document Type: Article

References (62)

1. 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.
2. 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.
3. 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.
4. 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.
5. Carpenter, L. C., and L. C. Cantley. 1996. Phosphoinositide kinases. Curr. Opin. Cell Biol. 8:153-158.
6. 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.
7. 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.
8. Cowley, S., H. Paterson, P. Kemp, and C. J. Marshall. 1994. Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and tranformation of NIH 3T3 cells. Cell 77:841-852.
9. 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.
10. 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.
11. phox by a membrane-targeted phosphoinositide 3-kinase. Curr. Biol. 6:1271-1278.
12. Dorrestijn, J., D. M. Ouwens, N. Van den Berghe, J. L. Bos, and J. A. Massen. 1996. Expression of a dominant negative Ras mutant does not affect stimulation of glucose uptake and glycogen synthesis by insulin. Diabelogia 39:558-563.
13. 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.
14. 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.
15. 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.
16. 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.
17. ras in insulin-stimulated glucose transport in 3T3-L1 adipocytes. J. Biol. Chem. 269:21391-21394.
18. Holman, G. H., and M. Kasuga. 1997. From receptor to transporter: insulin signaling to glucose transport. Diabetologia 40:991-1003.
19. 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: 4171-1175.
20. 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.
21. Kimball, S. R., T. C. Vary, and L. S. Jefferson. 1994. Regulation of protein synthesis by insulin. Annu. Rev. Physiol. 56:321-348.
22. 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 Nek-associated protein 1 with activated GTP-binding protein Rac. Biochem. J. 322:873-878.
23. 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.
24. 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.
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. mapk are required for fibroblast proliferation. Proc. Natl. Acad. Sci. USA 90:8319-8323.
41. 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.
42. Proud, C. G. 1996. p70 S6 kinase: an enigma with variations. Trends Biochem. Sci. 21:181-185.
43. s6k. FEBS Lett. 410:78-82.
44. s6k by PDK1. Science 279:707-710.
45. 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.
46. 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.
47. 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.
48. 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.
49. 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.
50. 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.
51. 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.
52. 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.
53. 52a. Takata, M., W. Ogawa, and M. Kasuga. Unpublished data.
54. 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.
55. 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.
56. 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.
57. 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.
58. 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.
59. 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.
60. White, M. F., and C. R. Kahn. 1994. The insulin signaling system. J. Biol. Chem. 269:1-4.
61. Wu, X., S. J. Non, 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.
62. 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.