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

Molecular and Cellular Biology

Volumn 16, Issue 6, 1996, Pages 2857-2864

  Mendez, Raul ^a   Myers Jr , Martin G ^b   White, Morris F ^b   Rhoads, Robert E ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; RAPAMYCIN; WORTMANNIN;

ARTICLE; ENZYME INACTIVATION; PRIORITY JOURNAL; PROMYELOCYTE; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; PROTEIN SYNTHESIS INHIBITION; PROTEIN SYNTHESIS REGULATION; TRANSLATION INITIATION; TRANSLATION REGULATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CARRIER PROTEINS; CELL LINE; EUKARYOTIC INITIATION FACTOR-4E; GRB2 ADAPTOR PROTEIN; HUMANS; INSULIN; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PEPTIDE INITIATION FACTORS; PHOSPHOPROTEINS; PHOSPHORYLATION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN BIOSYNTHESIS; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE-PHOSPHATASE; PROTEINS; RECEPTOR, INSULIN; RIBOSOMAL PROTEIN S6 KINASES; RNA, MESSENGER; SHP1 PROTEIN TYROSINE PHOSPHATASE;

EUKARYOTA;

EID: 0030013326     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.6.2857     Document Type: Article

References (63)

1. Barve, S. S., D. A. Cohen, A. DeBenedetti, R. E. Rhoads, and A. M. Kaplan. 1994. Mechanism of differential regulation of IL-2 murine Th1 and Th2 cell subsets. J. Immunol. 152:1171-1181.
2. Baserga, R. 1990. The cell cycle: myths and realities. Cancer Res. 50:6769-6771.
3. Bommer, U.-A., A. Lazaris-Karatzas, A. DeBenedetti, P. Nurnberg, R. Benndorf, H. Bielka, and N. Sonenberg. 1994. Translational regulation of the mammalian growth-related protein P23: involvement of eIF-4E. Cell. Mol. Biol. Res. 40:633-641.
4. 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.
5. S6K activation mediated by phosphatidylinositol-3-OH kinase. Nature (London) 370:71-75.
6. Chung, J., C. J. Kuo, G. R. Crabtree, and J. Blenis. 1992. Rapamycin-FKBP specifically blocks growth-dependent activation of signaling by the 70 kd S6 protein kinase. Cell 69:1227-1236.
7. Cross, D. A., D. R. Alessi, J. R. Vandenheede, H. E. McDowell, H. S. Hundal, and P. Cohen. 1994. The inhibition of glycogen synthase kinase-3 by insulin or insulin-like growth factor 1 in the rat skeletal muscle cell line L6 is blocked by wortmannin, but not by rapamycin: evidence that wortmannin blocks activation of the mitogen-activated protein kinase pathway in L6 cells between Ras and Raf. Biochem. J. 303:21-26.
8. 2 activity in Swiss 3T3 cells. J. Biol. Chem. 270:25352-25355.
9. DeBenedetti, A., B. Joshi, J. R. Graff, and S. G. Zimmer. 1994. CHO cells transformed by the translation factor eIF4E display increased c-myc expression, but require overexpression of Max for tumorigenicity. Mol. Cell. Differ. 2:347-371.
10. DeBenedetti, A., and R. E. Rhoads. 1990. Overexpression of eukaryotic protein synthesis initiation factor 4E in HeLa cells results in aberrant growth and morphology. Proc. Natl. Acad. Sci. USA 87:8212-8216.
11. Pagan, R. J., A. Lazaris-Karatzas, N. Sonenberg, and R. D. Rozen. 1991. Translational control of ornithine aminotransferase. Modulation by initiation factor eIF-4E. J. Biol. Chem. 266:16518-16523.
12. Fantl, W. J., J. A. Escobedo, and L. T. Williams. 1989. Mutations of the platelet-derived growth factor receptor that cause a loss of ligand-induced conformational change, subtle changes in kinase activity, and impaired ability to stimulate DNA synthesis. Mol. Cell. Biol. 9:4473-4478.
13. Farese, R. V., M. L. Standaert, A. J. Francois, K. Ways, T. P. Arnold, H. Hernandez, and D. R. Cooper. 1992. Effects of insulin and phorbol esters on subcellular distribution of protein kinase C isoforms in rat adipocytes. Biochem. J. 288:319-323.
14. Fingar, D. C., S. F. Hausdorff, J. Blenis, and M. J. Birnbaum. 1993. Dissociation of pp70 ribosomal protein S6 kinase from insulin-stimulated glucose transport in 3T3-L1 adipocytes. J. Biol. Chem. 268:3004-3008.
15. Franke, T. F., S. 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.
16. Graves, L. M., K. E. Bornfeldt, G. M. Argast, E. G. Krebs, X. Kong, T. A. Lin, and J. C. Lawrence, Jr. 1995. cAMP- and rapamycin-sensitive regulation of the association of eukaryotic initiation factor 4E and the translational regulator PHAS-I in aortic smooth muscle cells. Proc. Natl. Acad. Sci. USA 92:7222-7226.
17. Haghighat, A., S. Mader, A. Pause, and N. Sonenberg. 1995. Repression of cap-dependent translation by 4E-binding protein 1: competition with p220 for binding to eukaryotic initiation factor-4E. EMBO J. 14:5701-5709.
18. Hara, K., K. Yonezawa, H. Sakaue, A. Ando, K. Kotani, T. Kitamura, Y. Kitamura, H. Ueda, L. Stephens, T. Jackson, M. D. Waterfield, and M. Kasuga. 1994. 1-Phosphatidylinositol 3-kinase activity is required for insulin-stimulated glucose transport hut not for RAS activation in CHO cells. Proc. Natl. Acad. Sci. USA 91:7415-7419.
19. Haystead, T. A., C. Haystead, C. Hu, T. Lin, and J. C. Lawrence. 1994. Phosphorylation of PHAS-I by mitogen-activated protein (MAP) kinase. J. Biol. Chem. 269:23185-23191.
20. Jefferies, H. B. J., C. Reinhard, S. C. Kozma, and G. Thomas. 1994. Rapamycin selectively represses translation of the "polypyrimidine tract" mRNA family. Proc. Natl. Acad. Sci. USA 91:4441-4445.
21. Joshi, B., A.-L. Cai, B. D. Keiper, W. B. Minich, R. Mendez, C. M. Beach, J. Stepinski, R. Stolarski, E. Darzynkiewicz, and R. E. Rhoads. 1995. Phosphorylation of eukaryotic protein synthesis initiation factor 4E at Ser-209. J. Biol. Chem. 270:14597-14603.
22. Kimball, S. R., T. C. Vary, and L. S. Jefferson. 1994. Regulation of protein synthesis by insulin. Annu. Rev. Physiol. 56:321-348.
23. 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.
24. Kuhne, M. R., Z. Zhizhuang, J. Rowles, B. E. Lavan, S. Shen, E. H. Fischer, and G. E. Lienhard. 1994. Dephosphorylation of insulin receptor substrate 1 by the tyrosine phosphatse PTP2C. J. Biol. Chem. 269:15833-15837.
25. Kulas, D. T., W. R. Zhang, B. J. Goldstein, R. W. Furlanetto, and A. Mooney. 1995. Insulin receptor signaling is augmented by antisense inhibition of the protein tyrosine phosphatase LAR. J. Biol. Chem. 270:2435-2438.
26. Lamphear, B. J., R. Kirchweger, T. Skern, and R. E. Rhoads. 1995. Mapping of functional domains in eIF4G with picornaviral proteases. Implications for cap-dependent and cap-independent translational initiation. J. Biol. Chem. 270:21975-21983.
27. Lazaris-Karatzas, A., K. S. Montine, and N. Sonenberg. 1990. Malignant transformation by a eukaryotic initiation factor subunit that hinds to mRNA 5′ cap. Nature (London) 345:544-547.
28. Lee, C. H., L. W. Li, R. Nishimura, M. Zhou, A. G. Batzer, M. G. Myers, M. F. White, J. Schlessinger, and E. Y. Skolnik. 1993. Nek associates with the SH2 domain-docking protein IRS-1 in insulin-stimulated cells. Proc. Natl. Acad. Sci. USA 90:11713-11717.
29. Lin, T., X. Kong, T. A. J. Haystead, A. Pause, G. Belsham, N. Sonenberg, and J. C. Lawrence. 1994. PHAS-I as a link between mitogen-activated protein kinase and translation initiation. Science 266:653-656.
30. Lin, T. A., X. Kong, A. R. Saltiel, P. J. Blackshear, and J. C. Lawrence, Jr. 1995. Control of PHAS-I by insulin in 3T3-L1 adipocytes. Synthesis, degradation, und phosphorylation by a rapamycin-sensitive and mitogen-activated protein kinase-independent pathway. J. Biol. Chem. 270:18531-18538.
31. Mader, S., H. Lee, A. Pause, and N. Sonenberg. 1995. The translation initiation factor eIF-4E hinds to a common motif shared by the translation factor eIF-4-γ and the translational repressors 4E-binding proteins. Mol. Cell. Biol. 15:4990-4997.
32. Manzella, J. M., W. Rychlik, R. E. Rhoads, J. W. B. Hershey, and P. J. Blackshear. 1991. Insulin induction of ornithine decarboxylase. Importance of mRNA secondary structure and phosphorylation of eucaryotic initiation factors eIF-4B and eIF-4E. J. Biol. Chem. 266:2383-2389.
33. Mendez, R., and C. De Haro. 1994. Casein kinase II is implicated in the regulation of heme-controlled translational inhibitor of reticulocyte lysates. J. Biol. Chem. 269:6170-6176.
34. Milarski, K. L., and A. R. Saltiel. 1994. Expression of catalytically inactive Syp phosphatase in 3T3 cells blocks stimulation of mitogen-activated protein kinase by insulin. J. Biol. Chem. 269:21239-21243.
35. Minich, W. B., M. L. Balasta, D. J. Goss, and R. E. Rhoads. 1994. Chromatographic resolution of in vivo-phosphorylated and nonphosphorylated translation initiation factor eIF-4E. Demonstration of increased cap affinity of the phosphorylated form. Proc. Natl. Acad. Sci. USA 91:7668-7672.
36. 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.
37. Morris, D. R., T. Kakegawa, R. L. Kaspar, and M. W. While. 1993. Polypyrimidine tracts and their binding proteins: regulatory sites for posttranscriptional modulation of gene expression. Biochemistry 32:2931-2937.
38. Myers, M. G., T. C. Grammer, L. Wang, X. J. Sun, J. H. Pierce, J. Blenis, and M. F. White. 1994. Insulin receptor substrate-1 mediates phosphatidylinositol 3′-kinase and p70S6K signaling during insulin, insulin-like growth factor-1, and interleukin-4 stimulation. J. Biol. Chem. 269:28783-28789.
39. Myers, M. G., and M. W. White. Unpublished data.
40. Myers, M. G., Jr., L.-M. Wang, X. J. Sun, Y. Zhang, L. Yenush, J. Schlessinger, J. H. Pierce, and M. F. White. 1994. Role of IRS-1-GRB-2 complexes in insulin signaling. Mol. Cell. Biol. 14:3577-3587.
41. Myers, M. G., Jr., Y. Zhang, E. Glasheen, T. Grammer, L. Yenush, L. M. Wang, X. J. Sun, J. Blenis, J. H. Pierce, and M. F. White. YMXM-motifs and signaling by an IRS-1 molecule without tyrosine phosphorylation sites. Submitted for publication.
42. Nakanishi, H., K. A. Brewer, and J. H. Exton. 1993. Activation of the zeta isozyme of protein kinase C by phosphatidylinositol 3,4,5-triphosphate. J. Biol. Chem. 258:13-16.
43. Nakanishi, S., K. J. Catt, and T. Balla. 1995. A wortmannin-sensitive phosphatidylinositol 4-kinase that regulates hormone-sensitive pools of inositol-phospholipids. Proc. Natl. Acad. Sci. USA 92:5317-5321.
44. Nishimura, K., W. Li, A. Kashishian, A. Mondino, M. Zhou, J. Cooper, and J. Schlessinger. 1993. Two signaling molecules share a phosphotyrosine-containing binding site in the platelet-derived growth factor receptor. Mol. Cell. Biol. 13:6889-6896.
45. Noguchi, T., T. Matozaki, K. Horita, Y. Fujioka, and M. Kasuga. 1994. Role of SH-PTP2, a protein-tyrosine phosphatase with Src homology 2 domains, in insulin-stimulated Ras activation. Mol. Cell. Biol. 14:6674-6682.
46. 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.
47. Pause, A., G. J. Belsham, A. Gingras, O. Donze. T. Lin, J. C. Lawrence, and N. Sonenberg. 1994. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature (London) 371:762-767.
48. Rhoads, R. E. 1993. Regulation of eukaryotic protein synthesis by initiation factors. J. Biol. Chem. 268:3017-3020.
49. Rosenwald, I. B., R. Kaspar, D. Rousseau, L. Gehrke, P. Leboulch, J. J. Chenn, E. V. Schmidt, N. Sonenberg, and I. M. London. 1995. Eukaryotic translation initiation factor 4E regulates expression of cyclin D1 at transcriptional and posttranscriptional levels. J. Biol. Chem. 270:21176-21180.
50. Ruderman, N. B., R. Kapeller, M. F. White, and L. C. Cantley. 1990. Activation of phosphatidylinositol 3-kinase by insulin. Proc. Natl. Acad. Sci. USA 87:1411-1415.
51. Saito, Y., J. R. Vandenheede, and P. Cohen. 1994. The mechanism by which epidermal growth factor inhibits glycogen synthase kinase 3 in A431 cells. Biochem. J. 303:27-31.
52. Sakanaka, C., I. Ferby, I. Waga, H. Bito, and T. Shimizu. 1994. On the mechanism of cytosolic phospholipase A2 activation in CHO cells carrying somatostatin receptor: wortmannin-sensitive pathway to activate mitogen-activated protein kinase. Biochem. Biophys. Res. Commun. 205:18-23.
53. Saltiel, A. R. 1994. The paradoxical regulation of protein phosphorylation in insulin action. FASEB J 8:1034-1040.
54. Shantz, L. M., and A. E. Pegg. 1994. Overproduction of ornithine decarboxylase caused by relief of translational repression is associated with neoplastic transformation. Cancer Res. 54:2313-2316.
55. Sun, X. J., L. M. Wang, Y. Zhang, L. Yenush, M. G. Myers, E. Glasheen, W. S. Lane, J. H. Pierce, and M. F. White. 1995. Role of IRS-2 in insulin and cytokine signalling. Nature (London) 377:173-177.
56. Tamemoto, H., T. Kadowaki, K. Tobe, T. Yagi, H. Sakura, T. Hayakawa, Y. Terauchi, K. Ueki, Y. Kaburagi, S. Satoh, H. Sekihara, S. Yoshioka, H. Horikoshi, Y. Furuta, Y. Ikawa, M. Kasauga, Y. Yazaki, and S. Aizawa. 1994. Insulin resistance and growth retardation in mice lacking insulin receptor substrate-1. Nature (London) 372:182-186.
57. Terada, N., H. R. Patel, K. Takase, K. Kohno, and A. C. Nairn. 1994. Rapamycin selectively inhibits translation of mRNAs encoding elongation factors and ribosomal proteins. Proc. Natl. Acad. Sci. USA 91:11477-11481.
58. Toker, A., M. Meyer, K. K. Reddy, J. R. Falck, R. Aneja, S. Aneja, A. Parra, D. J. Burns, L. M. Ballas, and L. C. Cantley. 1994. Activation of protein kinase C family members by the novel polyphosphoinositides PtdIns-3,4-P2 and PtdIns-3,4,5-P3. J. Biol. Chem. 269:32358-32367.
59. Wang, L., M. G. Myers, X. J. Sun, S. A. Aaronson, M. White, and J. H. Pierce. 1993. IRS-1: essential for insulin- and IL-4-stimulated mitogenesis in hematopoietic cells. Science 261:1591-1594.
60. White, M. F., and C. R. Kahn. 1994. The insulin signaling system. J. Biol. Chem. 269:1-4.
61. Xiao, S., D. W. Rose, T. Sasaoka, H. Maegawa, T. R. Burke, P. P. Roller, S. E. Shoelson, and J. M. Olefsky. 1994. Syp (SH-PTP2) is a positive mediator of growth factor-stimulated mitogenic signal transduction. J. Biol. Chem. 269:21244-21248.
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.
63. Yao, R., and G. M. Cooper. 1995. Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 267:2003-2006.