Insulin and IGF-I stimulate the formation of the eukaryotic initiation factor 4F complex and protein synthesis in C2C12 myotubes independent of availability of external amino acids

Journal of Endocrinology

Volumn 185, Issue 2, 2005, Pages 275-289

  Shen, Wei Hua ^a   Boyle, David W ^a   Wisniowski, Paul ^a   Bade, Aashia ^a   Liechty, Edward A ^a,b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; AMINO ACID; GLYCOGEN SYNTHASE KINASE 3BETA; INITIATION FACTOR 4E; INITIATION FACTOR 4E BINDING PROTEIN 1; INITIATION FACTOR 4F; INITIATION FACTOR 4G; INSULIN; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATE BUFFERED SALINE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAPAMYCIN; SOMATOMEDIN C;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; MOUSE; MYOTUBE; NONHUMAN; NUTRIENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; TRANSLATION INITIATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AMINO ACIDS; ANIMALS; BLOTTING, WESTERN; CARRIER PROTEINS; CELL LINE; CHROMONES; DOSE-RESPONSE RELATIONSHIP, DRUG; EUKARYOTIC INITIATION FACTOR-4F; GLYCOGEN SYNTHASE KINASE 3; HYPOGLYCEMIC AGENTS; IMMUNOSUPPRESSIVE AGENTS; INSULIN; INSULIN-LIKE GROWTH FACTOR I; MICE; MORPHOLINES; MUSCLE FIBERS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; PROTEINS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SIROLIMUS; STIMULATION, CHEMICAL;

EID: 18844390423     PISSN: 00220795     EISSN: None     Source Type: Journal    
DOI: 10.1677/joe.1.06080     Document Type: Article

References (43)

1. Beugnet A, Tee AR, Taylor PM & Proud CG 2003 Regulation of targets of mTOR (mammalian target of rapamycin) signaling by intracellular amino acid availability. Biochemical Journal 372 555-566.
2. Bu X, Haas DW & Hagedorn CH 1993 Novel phosphorylation sites of eukaryotic initiation factor-4F and evidence that phosphorylation stabilizes interactions of the p25 and p220 subunits. Journal of Biological Chemistry 268 4975-4978.
3. Campbell LE, Wang X & Proud CG 1999 Nutrients differentially regulate multiple translation factors and their control by insulin. Biochemical Journal 344 433-441.
4. Choi KM, McMahon LP & Lawrence JC Jr 2003 Two motifs in the translational repressor PHAS-I required for efficient phosphorylation by mTOR and recognition by raptor. Journal of Biological Chemistry 278 19667-19673.
5. Cross DA, Alessi DR, Cohen P, Andjelkovich M & Hemmings BA 1995 Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378 785-789.
6. Dardevet D, Sornet C, Vary T & Grizard J 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.
7. Dennis PB, Jaeschke A, Saitoh M, Fowler B, Kozma SC & Thomas G 2001 Mammalian TOR: a homeostatic ATP sensor. Science 294 1102-1105.
8. Diggle TA, Moule SK, Avison MB, Flynn A, Foulstone EJ, Proud CG & Denton RM 1996 Both rapamycin-sensitive and -insensitive pathways are involved in the phosphorylation of the initiation factor-4E-binding protein (4E-BP1) in response to insulin in rat epididymal fat-cells. Biochemical Journal 316 447-453.
9. Gingras AC, Raught B & Sonenberg N 2001 Regulation of translation initiation by FRAP/mTOR. Genes and Development 15 807-826.
10. Graves LM, Bornfeldt KE, Argast GM, Krebs EG, Kong X, Lin TA & Lawrence JC 1995 cAMP- and rapamycin-sensitive regulation of the association of eukaryotic factor 4E and the translational regulator PHAS-I in aortic smooth muscle cells. PNAS 92 7222-7226.
11. Haghihat A, Maderr S, Pause A & Sonenberg N 1995 Repression of cap-dependent translation by 4E binding protein I: competition with p220 for binding to eukaryotic initiation factor 4E. EMBO Journal 14 5701-5709.
12. Hara K, Yonezawa K, Weng QP, Kozlowski MT, Belham C & Avruch J 1998 Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4EBP1 through a common effector mechanism. Journal of Biological Chemistry 273 14484-14494.
13. Herbert TP, Kilhams GR, Batty IH & Proud CG 2000 Distinct signalling pathways mediate insulin and phorbol ester-stimulated eukaryotic initiation factor 4F assembly and protein synthesis in HEK 293 cells. Journal of Biological Chemistry 275 11249-11256.
14. Herbert TP, Tee AR & Proud CG 2002 The extracellular signal-regulated kinase pathway regulates the phosphorylation of 4E-BP1 at multiple sites. Journal of Biological Chemistry 277 11591-11596.
15. Kimball SR, Jefferson LS, Fadden P, Haystead TA & Lawrence JC Jr 1996 Insulin and diabetes cause reciprocal changes in the association of eIF-4E and PHAS-1 in rat skeletal muscle. American Journal of Physiology - Cell Physiology 270 C705-C709.
16. Kimball SR, Horetsky RL & Jefferson LS 1998a Implication of eIF2B rather than eIF4E in the regulation of global protein synthesis by amino acids in L6 myoblasts. Journal of Biological Chemistry 273 30945-30953.
17. Kimball SR, Horetsky RL & Jefferson LS 1998b Signal transduction pathways involved in the regulation of protein synthesis by insulin in L6 myoblasts. American Journal of Physiology - Cell Physiology 274 C221-C228.
18. Kimball SR, Shantz LM, Horetsky RL & Jefferson LS 1999 Leucine regulates translation of specific mRNAs in L6 myoblasts through mTOR-mediated changes in availability of eIF4E and phosphorylation of ribosomal protein S6. Journal of Biological Chemistry 274 11647-11652.
19. Kitamura T, Ogawa W, Sakaue H, Hino Y, Kuroda S, Takata M, Matsumoto M, Maeda T, Konishi H, Kikkawa U & Kasuga M 1998 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 18 3708-3717.
20. Kleijn M & Proud CG 2000 Glucose and amino acids modulate translation factor activation by growth factors in PC12 cells. Biochemical Journal 347 399-406.
21. Lin TA, Kong X, Saltiel AR, Blackshear PJ & Lawrence JC Jr 1995 Control of PHAS-I by insulin in 3T3-L1 adipocytes. Journal of Biological Chemistry 270 18531-18538.
22. Lowry OH, Rosebrough NJ, Farr AL & Randall RJ 1951 Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193 265-275.
23. Mendez R, Myers MG Jr, White MF & Rhoads RE 1996 Stimulation of protein synthesis, eukaryotic translation initiation factor 4E phosphorylation, and PHAS-1 phosphorylation by insulin requires insulin receptor substrate 1 and phosphatidylinositol 3-kinase. Molecular and Cellular Biology 16 2857-2864.
24. Minich WB, Balasta ML, Goss DJ & Rhoads RE 1994 Chromatographic resolution of in vivo phosphorylated and nonphosphorylated eukaryotic translation initiation factor eIF-4E: increased cap affinity of the phosphorylated form. PNAS 91 7668-7672.
25. Morley SJ & McKendrick L 1997 Involvement of stress-activated protein kinase signaling pathways in the enhanced phosphorylation of initiation factor 4E in NIH 3T3 cells. Journal of Biological Chemistry 272 17887-17893.
26. Morley SJ & Naegele S 2002 Phosphorylation of eukaryotic initiation factor (eIF) 4E is not required for de novo protein synthesis following recovery from hypertonic stress in human kidney cells. Journal of Biological Chemistry 277 32855-32859.
27. Mothe-Satney I, Brunn GJ, McMahon LP, Capaldo CT, Abraham RT & Lawrence JC Jr 2000 Mammalian target of rapamycin-dependent phosphorylation of PHAS-I in four (S/T)P sites detected by phospho-specific antibodies. Journal of Biological Chemistry 275 33836-33843.
28. Nave BT, Ouwens M, Withers DJ, Alessi DR & Shepherd PR 1999 Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochemical Journal 344 427-431.
29. Pain VM 1996 Initiation of protein synthesis in eukaryotic cells. European Journal of Biochemistry 236 747-771.
30. Patti ME, Brambilla E, Luzi L, Landaker EJ & Kahn CR 1998 Bidirectional modulation of insulin action by amino acids. Journal of Clinical Investigation 101 1519-1529.
31. Pause A, Belsham GJ, Gingras AC, Donze O, Lin TA, Lawrence JC Jr & Sonenberg N 1994 Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature 371 762-767.
32. Peterson RT, Beal PA, Comb MJ & Schreiber S 2000 FKBP12-rapamycin-associated protein (FRAP) autophosphorylates at serine 2481 under translationally repressive conditions. Journal of Biological Chemistry 275 7416-7423.
33. Poulin F, Gingras AC, Olsen H, Chevalier S & Sonenberg N 1998 4E-BP3, a new member of the eukaryotic initiation factor 4E-binding protein family. Journal of Biological Chemistry 273 14002-14007.
34. Rommel C, Clarke BA, Zimmermann S, Nunez L, Rossman R, Reid K, Moelling K, Yancopoulos GD & Glass DJ 1999 Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt. Science 286 1738-1741.
35. Scott PH, Brunn GJ, Kohn AD, Roth RA & Lawrence JC Jr 1998 Evidence of insulin-stimulated phosphorylation and activation of the mammalian target of rapamycin mediated by a protein kinase B signaling pathway. PNAS 95 7772-7777.
36. Shah OJ, Anthony JC, Kimball SR & Jefferson LS 2000a 4EBP1 and S6K1: translational integration sites for nutritional and hormonal information in muscle. American Journal of Physiology - Endocrinology and Metabolism 279 E715-E729.
37. Shah OJ, Kimball SR & Jefferson LS 2000b Glucocorticoids abate p70(S6K) and eIF4E function in L6 skeletal myoblasts. American Journal of Physiology - Endocrinology and Metabolism 279 E74-E82.
38. Shen W, Mallon D, Boyle DW & Liechty EA 2002 IGF-I and insulin regulate eIF4F formation by different mechanisms in muscle and liver in the ovine fetus. American Journal of Physiology - Endocrinology and Metabolism 283 E593-E603.
39. Svegliati-Baroni G, Ridolfi F, Di Sario A, Casini A, Marucci L, Gaggiotti G, Orlandoni P, Macarri G, Perego L, Benedetti A & Folli F 1999 Insulin and insulin-like growth factor-I stimulate proliferation and type I collagen accumulation by human hepatic stellate cells: differential effects on signal transduction pathways. Hepatology 29 1743-1751.
40. Tee AR, Fingar DC, Manning BD, Kwiatkowski DJ, Cantley LC & Blenis J 2002 Tuberous sclerosis complex-1 and -2 gene products function together to inhibit mammalian target of rapamycin (mTOR)-mediated downstream signaling. PNAS 99 13571-13576.
41. Vary TC, Jefferson LS & Kimball SR 2000 Role of eIF4E in stimulation of protein synthesis by IGF-I in perfused rat skeletal muscle. American Journal of Physiology - Endocrinology and Metabolism 278 E58-E64.
42. Wang X, Campbell LE, Miller CM & Proud CG 1998 Amino acid availability regulates p70 S6 kinase and multiple translation factors. Biochemical Journal 334 261-267.
43. Xu G, Kwon G, Marshall CA, Lin TA, Lawrence JC Jr & McDaniel ML 1998 Branched-chain amino acids are essential in the regulation of PHAS-I and p70 S6 kinase by pancreatic beta-cells. A possible role in protein translation and mitogenic signaling. Journal of Biological Chemistry 273 28178-28184.