A role for protein kinase Bβ/Akt2 in insulin-stimulated GLUT4 translocation in adipocytes

Molecular and Cellular Biology

Volumn 19, Issue 11, 1999, Pages 7771-7781

  Hill, Michelle M ^a   Clark, Sharon F ^a   Tucker, David F ^b   Birnbaum, Morris J ^c   James, David E ^a   Macaulay, S Lance ^b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b CSIRO   (Australia)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE TRANSPORTER; INSULIN; PROTEIN KINASE B;

ADIPOCYTE; ANIMAL CELL; ARTICLE; ENZYME ACTIVITY; GLUCOSE TRANSPORT; HORMONAL REGULATION; INTRACELLULAR TRANSPORT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; PROTEIN TRANSPORT;

ANIMALIA;

EID: 0032695529     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.19.11.7771     Document Type: Article

References (60)

1. Alessi, D. R., F. B. Caudwell, M. Andjelkovic, B. A. Hemmings, and P. Cohen. 1996. Molecular basis for the substrate specificity of protein kinase B; comparison with MAPKAP kinase-1 and p70 S6 kinase. FEBS Lett. 399: 333-338.
2. Alessi, D. R., and P. Cohen. 1998. Mechanism of activation and function of protein kinase B. Curr. Opin. Genet. Dev. 8:55-62.
3. Altomare, D. A., G. E. Lyons, Y. Mitsuuchi, J. Q. Cheng, and J. R. Testa. 1998. Akt2 mRNA is highly expressed in embryonic brown fat and the AKT2 kinase is activated by insulin. Oncogene 16:2407-2411.
4. Anderson, K. E., J. Coadwell, L. R. Stephens, and P. T. Hawkins. 1998. Translocation of PDK-1 to the plasma membrane is important in allowing PDK-1 to activate protein kinase B. Curr. Biol. 8:684-691.
5. Andjelkovic, M., D. R. Alessi, R. Meier, A. Fernandez, N. J. Lamb, M. Frech, P. Cron, P. Cohen, J. M. Lucocq, and B. A. Hemmings. 1997. Role of translocation in the activation and function of protein kinase B. J. Biol. Chem. 272:31515-31524.
6. Araki, E., M. A. Lipes, M. E. Patti, J. C. Bruning, B. Haag 3rd, R. S. Johnson, and C. R. Kahn. 1994. Alternative pathway of insulin signalling in mice with targeted disruption of the IRS-1 gene. Nature 372:186-190.
7. Arand, M., T. Friedberg, and F. Oesch. 1994. Monitoring sodium dodecyl sulfate contamination, p. 276-278. In J. E. Celis (ed.), Cell biology: a laboratory handbook, vol. 3. Academic Press, London, United Kingdom.
8. Bandyopadhyay, G., M. L. Standaert, L. Zhao, B. Yu, A. Avignon, L. Galloway, P. Karnam, J. Moscat, and R. V. Farese. 1997. Activation of protein kinase C (α, β, and ζ) by insulin in 3T3/L1 cells. Transfection studies suggest a role for PKC-ζ in glucose transport. J. Biol. Chem. 272:2551-2558.
9. Bellacosa, A., T. O. Chan, N. N. Ahmed, K. Datta, S. Malstrom, D. Stokoe, F. McCormick, J. Feng, and P. Tsichlis. 1998. Akt activation by growth factors is a multiple-step process: the role of the PH domain. Oncogene 17:313-325.
10. Brady, M. J., F. J. Bourbonais, and A. R. Saltiel. 1998. The activation of glycogen synthase by insulin switches from kinase inhibition to phosphatase activation during adipogenesis in 3T3-L1 cells. J. Biol. Chem. 273:14063-14066.
11. Burgering, B. M., and P. J. Coffer. 1995. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376:599-602.
12. Calera, M. R., C. Martinez, H. Liu, A. K. Jack, M. J. Birnbaum, and P. F. Pilch. 1998. Insulin increases the association of Akt-2 with Glut4-containing vesicles. J. Biol. Chem. 273:7201-7204.
13. Calera, M. R., and P. F. Pilch. 1998. Induction of akt-2 correlates with differentiation in so18 muscle cells. Biochem. Biophys. Res. Commun. 251: 835-841.
14. 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.
15. Cheng, J. Q., D. A. Altomare, M. A. Klein, W. C. Lee, G. D. Kruh, N. A. Lissy, and J. R. Testa. 1997. Transforming activity and mitosis-related expression of the AKT2 oncogene: evidence suggesting a link between cell cycle regulation and oncogenesis. Oncogene 14:2793-2801.
16. Clark, S. F., S. Martin, A. J. Carozzi, M. M. Hill and D. E. James. 1998. Intracellular localization of phosphatidylinositide 3-kinase and insulin receptor substrate-1 in adipocytes: potential involvement of a membrane skeleton. J. Cell Biol. 140:1211-1225.
17. Clarke, J. F., P. W. Young, K. Yonezawa, M. Kasuga, and G. D. Holman. 1994. Inhibition of the translocation of GLUT1 and GLUT4 in 3T3-L1 cells by the phosphatidylinositol 3-kinase inhibitor, wortmannin. Biochem. J. 300: 631-635.
18. Cong, L. N., H. Chen, Y. Li, L. Zhou, M. A. McGibbon, S. I. Taylor, and M. J. Quon. 1997. Physiological role of Akt in insulin-stimulated translocation of GLUT4 in transfected rat adipose cells. Mol. Endocrinol. 11:1881-1890.
19. Conricode, K. M. 1995. Involvement of phosphatidylinositol 3-kinase in stimulation of glucose transport by growth factors in 3T3-L1 adipocytes. Biochem. Mol. Biol. Int. 36:835-843.
20. Cross, D. A., 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.
21. Datta, K., T. F. Franke, T. O. Chan, A. Makris, S. I. Yang, D. R. Kaplan, D. K. Morrison, E. A. Golemis, and P. N. Tsichlis. 1995. AH/PH domain-mediated interaction between Akt molecules and its potential role in Akt regulation. Mol. Cell. Biol. 15:2304-2310.
22. 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 proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81:727-736.
23. Hajduch, E., D. R. Alessi, B. A. Hemmings, and H. S. Hundal. 1998. Constitutive activation of protein kinase Ba by membrane targeting promotes glucose and system A amino acid transport, protein synthesis, and inactivation of glycogen synthase kinase 3 in L6 muscle cells. Diabetes 47:1005-1013.
24. Hill, M. M., S. F. Clark, and D. E. James. 1997. Insulin-regulatable phosphoproteins in 3T3-L1 adipocytes form detergent-insoluble complexes not associated with caveolin. Electrophoresis 18:2629-2637.
25. Hunter, S. J., and W. T. Garvey. 1998. Insulin action and insulin resistance: diseases involving defects in insulin receptors, signal transduction, and the glucose transport effector system. Am. J. Med. 105:331-345.
26. James, D. E., M. Strube, and M. Mueckler. 1989. Molecular cloning and characterization of an insulin-regulatable glucose transporter. Nature 338: 83-87.
27. Kelada, A. S., S. L. Macaulay, and J. Proietto. 1992. Cyclic AMP acutely stimulates translocation of the major insulin-regulatable glucose transporter GLUT4. J. Biol. Chem. 267:7021-7025.
28. Kellerer, M., R. Lammers, and H. U. Haring. 1999. Insulin signal transduction: possible mechanisms for insulin resistance. Exp. Clin. Endocrinol. Diabetes 107:97-106.
29. Kitamura, T., W. Ogawa, H. Sakaue, Y. Hino, S. Kuroda, M. Takata, M. Matsumoto, T. Maeda, H. Konishi, V. Kikkawa, and M. Kasuga. 1998. Requirement for activation of the serine-threonine kinase Akt (protein kinase B) in insulin stimulation of protein synthesis but not of glucose transport. Mol. Cell. Biol. 18:3708-3717.
30. Kohn, A. D., S. A. Summers, M. J. Birnbaum, and R. A. Roth. 1996. Expression of a constitutively active Akt Ser/Thr kinase in 3T3-L1 adipocytes stimulates glucose uptake and glucose transporter 4 translocation. J. Biol. Chem. 271:31372-31378.
31. Kotani, K., A. J. Carozzi, H. Sakaue, K. Kara, L. J. Robinson, S. F. Clark, K. Yonezawa, D. E. James, and M. Kasuga. 1995. Requirement for phosphoinositide 3-kinase in insulin-stimulated GLUT4 translocation in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 209:343-348.
32. Kotani, K., W. Ogawa, M. Matsumoto, T. Kitamura, H. Sakaue, Y. Hino, K. Miyake, W. Sano, K. Akimoto, S. Ohno, and M. Kasuga. 1998. Requirement of atypical protein kinase Cλ for insulin stimulation of glucose uptake but not for Akt activation in 3T3-L1 adipocytes. Mol. Cell. Biol. 18:6971-6982.
33. Kupriyanova, T. A., and K. V. Kandror. 1999. Akt-2 binds to Glut4-containing vesicles and phosphorylates their component proteins in response to insulin. J. Biol. Chem. 274:1458-1464.
34. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
35. Macaulay, S. L., D. R. Hewish, K. H. Gough, V. Stoichevska, S. F. MacPherson, M. Jagadish, and C. W. Ward. 1997. Functional studies in 3T3L1 cells support a role for SNARE proteins in insulin stimulation of GLUT4 translocation. Biochem. J. 324:217-224.
36. Magun, R., B. M. Burgering, P. J. Coffer, D. Pardasani, Y. Lin, J. Chabot, and A. Sorisky. 1996. Expression of a constitutively activated form of protein kinase B (c-Akt) in 3T3-L1 preadipose cells causes spontaneous differentiation. Endocrinology 137:3590-3593.
37. Marsh, B. J., R. A. Alm, S. R. McIntosh, and D. E. James. 1995. Molecular regulation of GLUT4 targeting in 3T3-L1 adipocytes. J. Cell Biol. 130:1081-1091.
38. Martin, S. S., T. Haruta, A. J. Morris, A. Klippel, L. T. Williams, and J. M. Olefsky. 1996. Activated phosphatidylinositol 3-kinase is sufficient to mediate actin rearrangement and GLUT4 translocation in 3T3-L1 adipocytes. J. Biol. Chem. 271:17605-17608.
39. Meier, R., D. R. Alessi, P. Cron, M. Andjelkovic, and B. A. Hemmings. 1997. Mitogenic activation, phosphorylalion, and nuclear translocation of protein kinase Bβ. J. Biol. Chem. 272:30491-30497.
40. Meier, R., and B. A. Hemmings. 1999. Regulation of protein kinase B. J. Recept. Signal Transduct. Res. 19:121-128.
41. Nave, B. T., R. J. Haigh, A. C. Hayward, K. Siddle, and P. R. Shepherd. 1996. Compartment-specific regulation of phosphoinositide 3-kinase by platelet-derived growth factor and insulin in 3T3-L1 adipocytes. Biochem. J. 318:55-60.
42. 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. Studies with a selective inhibitor wortmannin. J. Biol. Chem. 269:3568-3573.
43. Quon, M. J., A. J. Butte, M. J. Zarnowski, G. Sesti, S. W. Cushman, and S. I. Taylor. 1994. Insulin receptor substrate 1 mediates the stimulatory effect of insulin on GLUT4 translocation in transfected rat adipose cells. J. Biol. Chem. 269:27920-27924.
44. Rice, K. M., and C. W. Garner. 1994. Correlation of the insulin receptor substrate-1 with insulin-responsive deoxyglucose transport in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 198:523-530.
45. Ricort, J. M., J. F. Tanti, E. Van Obberghen, and Y. Le Marchand-Brustel. 1996. Different effects of insulin and platelet-derived growth factor on phosphatidylinositol 3-kinase at the subcellular level in 3T3-L1 adipocytes. A possible explanation for their specific effects on glucose transport. Eur. J. Biochem. 239:17-22.
46. Robinson, L. J., and D. E. James. 1992. Insulin-regulated sorting of glucose transporters in 3T3-L1 adipocytes. Am. J. Physiol. 263:E383-393.
47. Sharma, P. M., K. Egawa, Y. Huang, J. L. Martin, I. Huvar, G. R. Boss, and J. M. Olefsky. 1998. Inhibition of phosphatidylinositol 3-kinase activity by adenovirus-mediated gene transfer and its effect on insulin action. J. Biol. Chem. 273:18528-18537.
48. 2 or heat shock is mediated by phosphoinositide 3-kinase and not by mitogen-activated protein kinase-activated protein kinase-2. Biochem. J. 336:241-246.
49. Simpson, I. A., D. R. Yver, P. J. Hissin, L. J. Wardzala, E. Karnieli, L. B. Salans, and S. W. Cushman. 1983. Insulin-stimulated translocation of glucose transporters in the isolated rat adipose cells: characterization of sub-cellular fractions. Biochim. Biophys. Acta 763:393-407.
50. Standaert, M. L., L. Galloway, P. Karnam, G. Bandvopadhyay, J. Moscat, and R. V. Farese. 1997. Protein kinase C-ζ as a downstream effector of phosphatidylinositol 3-kinase during insulin stimulation in rat adipocytes. Potential role in glucose transport. J. Biol. Chem. 272:30075-30082.
51. Staubs, P. A., J. G. Nelson, D. R Reichart, and J. M. Olefsky. 1998. Platelet-derived growth factor inhibits insulin stimulation of insulin receptor sub-strate-1-associated phosphatidylinositol 3-kinase in 3T3-L1 adipocytes without affecting glucose transport. J. Biol. Chem. 273:25139-25147.
52. Summers, S. A., E. L. Whiteman, H. Cho, L. Lipfert and M. J. Birnbaum. 1999. Differentiation-dependent suppression of platelet-derived growth factor signaling in cultured adipocytes. J. Biol. Chem. 274:23858-23867.
53. Tanti, J. F., T. Gremeaux, S. Grillo, V. Calleja, A. Klippel, L. T. Williams, E. Van Obberghen, and Y. Le Marchand-Brustel. 1996. Overexpression of a constitutively active form of phosphatidylinositol 3-kinase is sufficient to promote Glut 4 translocalion in adipocytes. J. Biol. Chem. 271:25227-25232.
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. Tordjman, K. M., K. A. Leingang, D. E. James, and M. M. Mueckler. 1989 Differential regulation of two distinct glucose transporter species expressed in 3T3-L1 adipocytes: effect of chronic insulin and tolbutamide treatment. Proc. Natl. Acad. Sci. USA 86:7761-7765.
56. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
57. Ueki, K., R. Yamamoto-Honda, Y. Kaburagi, T. Yamauchi, K. Tobe, B. M. Burgering, P. J. Coffer, I. Komuro, Y. Akanuma, Y. Yazaki, and T. Kadowaki. 1998. Potential role of protein kinase B in insulin-induced glucose transport, glycogen synthesis, and protein synthesis. J. Biol. Chem. 273:5315-5322.
58. Walker, K. S., M. Deak, A. Paterson, K. Hudson, P. Cohen, and D. R. Alessi. 1998. Activation of protein kinase B β and γ isoforms by insulin in vivo and by 3-phosphoinositide-dependent protein kinase-1 in vitro: comparison with protein kinase B α. Biochem. J. 331:299-308.
59. Wang, Q., R. Somwar, P. J. Bilan, Z. Liu, J. Jin, J. R. Woodgett, and A. Klip. 1999. Protein kinase B/Akt participates in GLUT4 translocation by insulin in L6 myoblasts. Mol. Cell. Biol. 19:4008-4018.
60. Withers, D. J., J. S. Gutierrez, H. Towery, D. J. Burks, J. M. Ren, S. Previs, Y. Zhang, D. Bernal, S. Pons, G. I. Shulman, S. Bonner-Weir, and M. F. White. 1998. Disruption of 1RS-2 causes type 2 diabetes in mice. Nature 391:900-904.