Activation of mRNA translation in rat cardiac myocytes by insulin involves multiple rapamycin-sensitive steps

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 278, Issue 4 47-4, 2000, Pages

  Wang, Lijun ^a   Wang, Xuemin ^a   Proud, Christopher G ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Heart; Initiation factor; Protein kinase; Protein synthesis

Indexed keywords

ELONGATION FACTOR 2; INITIATION FACTOR 4E; INSULIN; MESSENGER RNA; PROTEIN KINASE B; RAPAMYCIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HEART MUSCLE CELL; HORMONAL REGULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; TRANSLATION REGULATION;

EID: 0034107580     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.2000.278.4.h1056     Document Type: Article

References (88)

1. Alessi, D. R., M. Andjelkovic, B. Caudwell, P. Cron, N. Morrice, P. Cohen, and B. Hemmings. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15: 6541-6551, 1996.
2. Alessi, D. R., and P. Cohen. Mechanism of activation and function of protein kinase B. Curr. Opin. Genet. Dev. 8: 55-62, 1998.
3. Alessi, D. R., A. Cuenda, P. Cohen, D. T. Dudley, and A. R. Saltiel. PD-098059 is a specific inhibitor of the activation of mitogen-activated protein kinase in vitro and in vivo. J. Biol. Chem. 270: 27489-27494, 1995.
4. Andjelkovic, M., T. Jakubowicz, P. Cron, X. Ming, J. Han, and B. A. Hemmings. Activation and phosphorylation of a pleckstrin homology domain containing protein kinase (RAC-PK/ PKB) promoted by serum and protein phosphatase inhibitors. Proc. Natl. Acad. Sci. USA 93: 5699-5704, 1996.
5. Arcaro, A., and M. P. Wymann. Wortmannin is a potent phosphatidylinositol 3-kinase inhibitor: the role of phosphatidylinositol 3,4,5-trisphosphate in neutrophil responses. Biochem. J. 296: 297-301, 1993.
6. Azpiazu, I., A. R. Saltiel, A. A. DePaoli-Roach, and J. C. Lawrence. Regulation of both glycogen synthase and PHAS-I by insulin involves mitogen-activated protein kinase-independent and rapamycin-sensitive pathways. J. Biol. Chem. 271: 5033-5039, 1996.
7. Beretta, L., A.-C. Gingras, Y. V. Svitkin, M. N. Hall, and N. Sonenberg. Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent translation. EMBO J. 15: 658-664, 1996.
8. Borthwick, A. C., A. M. Wells, J. J. Rochford, S. J. Hurel, D. M. Turnbull, and S. J. Yeaman. Inhibition of glycogen synthase kinase-3 by insulin in cultured human skeletal-muscle myoblasts. Biochem. Biophys. Res. Commun. 210: 738-745, 1995.
9. Brunn, G. J., J. Williams, C. Sabers, G. Weiderrecht, J. C. Lawrence, and R. T. Abraham. Direct inhibition of the signaling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002. EMBOJ. 15: 5256-5267, 1996.
10. Burgering, B. M. T., and P. J. Coffer. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature (Lond.) 376: 599-602, 1995.
11. Carlberg, U., A. Nilsson, and O. Nygard. Functional properties of phosphorylated elongation factor 2. Eur. J. Biochem. 191: 639-645, 1990.
12. Cheatham, B., C. J. Vlahos, L. Cheatham, L. Wang, J. Blenis, and C. R. Kahn. 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, 1994.
13. Clemens, M. J., M. Bushell, and S. J. Morley. Degradation of eukaryotic polypeptide chain initiation factor (eIF) 4G in response to induction of apoptosis in human lymphoma cell lines. Oncogene 17: 2921-2931, 1998.
14. Cross, D. A. E., D. R. Alessi, P. Cohen, M. Andjelkovich, and B. A. Hemmings. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature (Lond.) 378: 785-789, 1995.
15. Cross, D. A. E., D. R. Alessi, J. R. Vandenheede, H. E. McDowell, H. S. Hundal, and P. Cohen. 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 anc Raf. Biochem. J. 303: 21-26, 1994.
16. Cross, D. A. E., P. W. Watt, M. Shaw, J. van der Kaay, C. P. Downes, J. C. Holder, and P. Cohen. Insulin activates protein kinase B, inhibits glycogen synthase kinase 3 and activates glycogen synthase by rapamycin-insensitive pathways in skeletal muscle and adipose tissue. FEBS Lett. 406: 211-215, 1997.
17. DeFronzo, R. A., and E. Ferrannini. International Textbook of Diabetes Mellitus, edited by K. G. M. M. Alberti, P. Zimmet, and R. A. DeFronzo. Chichester, UK: Wiley, 1992, p. 549-593.
18. Diggle, T. A., S. K. Moule, M B. Avison, A. Flynn, E. J. Foulstone, C. G. Proud, and R. M. Denton. Both rapamycin-sensitive and -insensitive pathways are involved in the phosphorylation of the initiation factor 4.5 binding protein (4E-BP1) in response to insulin in rat epididymal fat cells. Biochem. J. 316: 447-453, 1996.
19. Diggle, T. A., N. T. Redpath, K. J. Heesom, and R. M. Denton. Regulation of protein synthesis elongation factor-2 kinase by cAMP in adipocytes. Biochem. J. 336: 525-529, 1998.
20. Flynn, A., and C. G. Proud. TI e role of eIF4 in cell proliferation. Cancer Surveys 27: 293-310, 1996.
21. Flynn, A., and C. G. Proud. Insulin stimulation of the phosphorylation of initiation factor 4E is mediated by the MAP kinase pathway. FEBS Lett. 389: 162-166, 1996.
22. 1-adrenergic stimulation of cardiac protein synthesis may involve increased intracellular pH and protein kinase activity. Biochem. J. 273: 347-353, 1991.
23. 1-adrenoceptor. Biochem. J. 266: 727-736, 1990.
24. Fuller, S. J., and P. H. Sugden. Acute inhibition of rat heart protein synthesis in vitro during β-adrenergic stimulation or hypoxia. Am. J. Physiol. Endocrinol. Metab. 255: E537-E547, 1988.
25. Gilligan, M., G. I. Welsh, A. Flynn, I. Bujalska, C. G. Proud, and K. Docherty. Glucose stimulates the activity of the guanine nucleotide-exchange factor eIF-2B in isolated rat islets of Langerhans. J. Biol. Chem. 271: 2121-2125, 1996.
26. Gingras, A.-C., S. G. Kennedy, M. A. O'Leary, N. Sonenberg, and N. Hay. 4E-BP1, a repressor of mRNA translation, is phosphorylated and inactivated by the Akt(PKB) signaling pathway. Genes Dev. 12: 502-513, 1998.
27. Haghighat, A., S. Mader, A. Pause, and N. Sonenberg. 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, 1995.
28. Hughes, K., S. Ramakrishna, W. B. Benjamin, and J. R. Woodgett. Identification of multifunctional ATP-citrate lyase kinase as the alpha-isoform of glycogen synthase kinase-3. Biochem. J. 288: 309-314, 1992.
29. S6k. EMBO J. 16: 3693-3704, 1997.
30. Jefferies, H. B. J., G. Reinhard, S. C. Kozma, and G. Thomas. Rapamycin selectively represses translation of the "polypyrimidine tract" mRNA family. Proc. Natl. Acad. Sci. USA 91: 4441-4445, 1994.
31. Jefferson, L. S., E. B. Wolpert, K. E. Giger, and H. E. Morgan. Regulation of protein synthesis in heart muscle. III. Effect of anoxia on protein synthesis. Am. J. Physiol. 246: E2171-E2178, 1971.
32. Karinch, A. M., S. R. Kimball, T. C. Vary, and L. S. Jefferson. Regulation of eukaryotic initiation factor-2B activity in muscle of diabetic rats. Am. J. Physiol. Endocrinol. Metab. 264: E101-E108, 1993.
33. Kay, J. E., M. C. Smith, V. Frost, and G. Y. Morgan. Hypersensitivity to rapamycin of BJAB lymphoblastoid cells. Immunology 87: 390-395, 1996.
34. Kitamura, T., W. Ogawa, H. Sakaue, Y. Hino, S. Kuroda, M. Takata, M. Matsumoto, T. Maeda, H. Konishi, U. Kikkawa, and M. Kasuga. 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, 1998.
35. Kleijn, M., G. C. Scheper, H. O. Voorma, and A. A. M. Thomas. Regulation of translation initiation factors by signal transduction. Eur. J. Biochem. 253: 531-544, 1998.
36. Kleijn, M., G. I. Welsh, G. C. Scheper, H. O. Voorma, C. G. Proud, and A. A. M. Thomas. Nerve and epidermal growth factors induce protein synthesis and eIF2B activation in PC12 cells. J. Biol. Chem. 273: 5536-5541, 1998.
37. Kochel, P. J., Y. Kira, E. E. Gordon, and H. E. Morgan. Effects of anoxia and ischaemia on protein synthesis in perfused rat hearts. Circ. Res. 38, Suppl. I: I-124-I-130, 1995.
38. Koromilas, A. E., A. Lazaris-Karatzas, and N. Sonenberg. mRNAs containing extensive secondary structure in their 5′ non coding region translate efficiently in cells overexpressing initiation factor eIF-4E. EMBOJ. 11: 4153-4158, 1992.
39. Lavandero, S., R. Foncea, V. Perez, and M. Sapag-Hagar. Effect of inhibitors of signal transduction on IGF-1 induced protein synthesis associated with hypertrophy in cultured neonatal rat ventricular myocytes. FEBS Lett. 422: 193-196, 1998.
40. Lawrence, J. C., and R. T. Abraham. PHAS/4E-BPs as regulators of mRNA translation and cell proliferation. Trends Biochem. Sci. 22: 345-349, 1997.
41. Lin, T.-A., X. Kong, T. A. J. Haystead, A. Pause, G. J. Belsham, N. Sonenberg, and J. C. Lawrence. PHAS-I as a link between mitogen-activated protein kinase and translation initiation. Science 266: 653-656, 1994.
42. Mader, S., H. Lee, A. Pause, and N. Sonenberg. The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4gamma and the translational repressors 4E-binding proteins. Mol. Cell. Biol. 15: 4990-4997, 1995.
43. Makhlouf, A. A., and P. J. McDermott. Increased expression of eukaryotic initiation factor 4E during growth of neonatal rat cardiocytes in vitro. Am. J. Physiol. Heart Circ. Physiol. 274: H2133-H2142, 1998.
44. Mann, D. L., R. L. Kent, B. Parson, and G. Cooper. Load regulation of the properties of adult feline cardiocytes: growth induction by cellular deformation. Circ. Res. 64: 1079-1090, 1989.
45. Marin, P., K. L. Nastiuk, N. Daniel, J. Girault, A. J. Czernik, J. Glowinski, A. C. Nairn, and J. Premont. Glutamate dependent phosphorylation of elongation factor 2 and inhibition of protein synthesis in neurons. J. Neurosci. 17: 3445-3454, 1997.
46. McDowell, H. E., P. A. Eyers, and H. S. Hundal. Regulation of system A amino acid transport by insulin, chemical and hyperthermic stress. FEBS Lett. 441: 15-19, 1998.
47. McGivan, J. D., and M. Pastor-Anglada. Regulatory and molecular aspects of mammalian amino acid transport. Biochem. J. 299: 321-334, 1994.
48. 1-Adrenergic stimulation of rat myocardial cells increases protein synthesis. Am. J. Physiol. Heart Circ. Physiol. 251: H1076-H1084, 1986.
49. Meyuhas, O., D. Avni, and S. Shama. Translational control of ribosomal protein mRNAs in eukaryotes. In: Translational Control, edited by J. W. B. Hershey, M. B. Mathews, and N. Sonenberg. Cold Spring Harbor, NY: Cold Spring Harbor, 1996, p. 363-388.
50. Morley, S. J., and L. McKendrick. Involvement of stress-activated protein kinase and p38/RK mitogen-activated protein kinase signaling pathways in the enhanced phosphorylation of initiation factor eIF4E in NIH 3T3 cells. J. Biol. Chem. 272: 17887-17893, 1997.
51. Morley, S. J., and V. M. Pain. Translational regulation during activation of porcine peripheral blood lymphocytes: association and phosphorylation of the alpha and gamma subunits of the initiation factor complex eIF-4F. Biochem. J. 312: 627-635, 1995.
52. 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. Multiple signalling pathways involved in the stimulation of fatty acid and glycogen synthesis by insulin in rat epididymal fat pads. Biochem. J. 311: 595-601, 1995.
53. Nagai, R., R. B. Low, W. S. Stirewalt, N. R. Alpert, and R. Z. Litten. Efficiency and capacity of protein synthesis are increased in pressure overload cardiac hypertrophy. Am. J. Physiol. Heart Circ. Physiol. 255: H325-H328, 1988.
54. Nairn, A. C., and H. C. Palfrey. Regulation of protein synthesis by calcium. In: Translational Control, edited by J. W. B. Hershey, M. B. Mathews, and N. Sonenberg. Cold Spring Harbor, NY: Cold Spring Harbor, 1996, p. 295-318.
55. Oldfield, S., B. L. Jones, D. Tanton, and C. G. Proud. Use of monoclonal-antibodies to study the structure and function of eukaryotic protein synthesis initiation-factor-2B. Eur. J. Biochem. 221: 399-410, 1994.
56. Pain, V. M. Initiation of protein synthesis in eukaryotic cells. Eur. J. Biochem. 236: 747-771, 1996.
57. Pause, A., G. J. Belsham, A.-C. Gingras, O. Donzé, T. A. Lin, J. C. Lawrence, and N. Sonenberg. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature (Lond.) 371: 762-767, 1994.
58. Pedersen, S., J. E. Celis, J. Nielsen, J. Christiansen, and F. C. Nielsen. Distinct repression of translation by wortmannin and rapamycin. Eur. J. Biochem. 247: 449-456, 1997.
59. Peterson, R. T., and S. L. Schreiber. Translation Control: connecting mitogens and the ribosome. Curr. Biol. 8: R248-R250, 1998.
60. Poulin, F., A.-C. Gingras, H. Olsen, S. Chevalier, and N. Sonenberg. 4E-BP3, a new member of the eukaryotic initiation factor 4E-binding protein family. J. Biol. Chem. 273: 14002-14007, 1998.
61. Preedy, V. R., D. M. Smith, and P. H. Sugden. The effects of six hours of hypoxia on protein synthesis in rat tissues in vivo and in vitro. Biochem. J. 228: 179-185, 1985.
62. Price, N. T., and C. G. Proud. The guanine nucleotide-exchange factor, eIF-2B. Biochimie 76: 748-760, 1994.
63. Proud, C. G. p70 S6 kinase: an enigma with variations. Trends Biochem. Sci. 21: 181-185, 1996.
64. Proud, C. G., and R. M. Denton. Molecular mechanisms for the activation of protein synthesis by insulin. Biochem. J. 328: 329-341, 1997.
65. Redpath, N. T. High-resolution one-dimensional polyacrylamide gel isoelectric focusing of various forms of elongation factor-2. Anal. Biochem. 202: 340-343, 1992.
66. Redpath, N. T., E. J. Foulstone, and C. G. Proud. Regulation of translation elongation factor-2 by insulin via a rapamycin-sensitive signalling pathway. EMBO J. 15: 2291-2297, 1996.
67. Redpath, N. T., N. T. Price, K. V. Severinov, and C. G. Proud. Regulation of elongation factor-2 by multisite phosphorylation. Eur. J. Biochem. 213: 689-699, 1993.
68. Saito, Y., J. R. Vandenheede, and P. Cohen. The mechanism by which epidermal growth factor inhibits glycogen synthase kinase-3 in A431 cells. Biochem. J. 303: 27-31, 1994.
69. Shaw, M., P. Cohen, and D. R. Alessi. Further evidence that the inhibition of glycogen synthase kinase-3 β by IGF-1 is mediated by PDK1/PKB-induced phosphorylation of Ser-9 and not by dephosphorylation of Tyr-216. FEES Lett. 419: 307-311, 1997.
70. Sonenberg, N. mRNA 5′ cap binding protein eIF4E and control of cell growth. In: Translational Control, edited by J. W. B. Hershey, M. B. Mathews, and N. Sonenberg. Cold Spring Harbor NY: Cold Spring Harbor, 1996, p. 245-269.
71. Sugden, P. H., and S. J. Fuller. Regulation of protein turnover in skeletal and cardiac muscle. Biochem. J. 273: 21-37, 1991.
72. Sutherland, C., and P. Cohen. The alpha-isoform of glycogen synthase kinase-3 from rabbit skeletal muscle is inactivated by p70 S6 kinase or MAP kinase-activated protein kinase-1 in vitro. FEBS Lett. 338: 37-42, 1994.
73. Sutherland, C., I. A. Leighton, and P. Cohen. Inactivation of glycogen synthase kinase-3 beta by phosphorylation: new kinase connections in insulin and growth-factor signalling. Biochem. J. 296: 15-19, 1993.
74. Terada, N., H. R. Patel, K. Takase, K. Kohno, A. C. Nairn, and E. W. Gelfand. Rapamycin selectively inhibits translation of mRNAs encoding elongation factors and ribosomal proteins. Proc. Natl. Acad. Sci. USA 91: 11477-11481, 1994.
75. Thomas, G., and M. N. Hall. TOR signalling and the control of cell growth. Curr. Opin. Cell Biol. 9: 782-787, 1998.
76. Von Manteuffel, S. R., A. C. Gingras, X. F. Ming, N. Sonenberg, and G. Thomas. 4E-BP1 phosphorylation is mediated by the FRAP-p70(S6K) pathway and is independent of mitogen-activated protein kinase. Proc. Natl. Acad. Sci. USA 93: 4076-4080, 1996.
77. Vries, R. G. J., A. Flynn, J. C. Patel, X. Wang, R. M. Denton, and C. G. Proud. Heat shock increases the association of binding protein-1 with initiation factor 4E. J. Biol. Chem. 272: 32779-32784, 1997.
78. Wada, H., C. T. Ivester, B. A. Carabello, G. Cooper, and P. J. McDermott. Translational initiation factor eIF-4E: a link between cardiac load and protein synthesis. J. Biol. Chem. 271: 8359-8364, 1996.
79. Walker, K. S., M. Deak, A. Paterson, K. Hudson, P. Cohen, and D. R. Alessi. Activation of protein kinase B beta and gamma isoforms by insulin in vivo and by 3-phosphoinositide-dependent protein kinase-1 in vitro: comparison with protein kinase B alpha. Biochem. J. 331: 299-308, 1998.
80. Wang, X., and C. G. Proud. p70 S6 kinase is activated by sodium arsenite in adult rat cardiomyocytes: roles for phosphatidylinositol 3-kinase and p38 MAP kinase. Biochem. Biophys. Res. Commun. 238: 207-212, 1997.
81. i. Am. J. Physiol. Heart Circ. Physiol. 267: H1759-H1769, 1994.
82. Welsh, G. I., C. M. Miller, A. J. Loughlin, N. T. Price, and C. G. Proud. Regulation of eukaryotic initiation factor eIF2B: glycogen synthase kinase-3 phosphorylates a conserved serine which undergoes dephosphorylatiotion response to insulin. FEBS Lett. 421: 125-130, 1998.
83. Welsh, G. I., S. Miyamoto, C. G. Proud, and B. Safer. T-cell activation leads to rapid stimulation of translation initiation factor eIF-2B and inactivation of glycogen synthase kinase-3. J. Biol. Chem. 271: 11410-11413, 1996.
84. Welsh, G. I., J. C. Patel, and C. G. Proud. Peptide substrates suitable for assaying glycogen synthase kinase-3 (GSK-3) in crude cell extracts. Anal. Biochem. 244: 16-21, 1997.
85. Welsh, G. I., and C. G. Proud. Regulation of protein synthesis in Swiss 3T3 fibroblasts. Rapid activation of the guanine-nucleotide-exchange factor by insulin and growth factors. Biochem. J. 284: 19-23, 1992.
86. Welsh, G. I., and C. G. Proud. Glycogen synthase kinase-3 is rapidly inactivated in response to insulin and phosphorylates eukaryotic initiation factor eIF-2B. Biochem. J. 294: 625-629, 1993.
87. Welsh, G. I., C. M. Stokes, X. Wang, H. Sakaue, W. Ogawa, M. Kasuga, and C. G. Proud. Activation of translation initiation factor eIF2B by insulin requires phosphatidylinositol 3-kinase. FEBS Lett. 410: 418-422, 1997.
88. Welsh, G. I., C. Wilson, and C. G. Proud. GSK3: a shaggy frog story. Trends Cell Biol. 6: 274-279, 1996.