The mTOR pathway in the control of protein synthesis

Physiology

Volumn 21, Issue 5, 2006, Pages 362-369

  Wang, Xuemin ^a   Proud, Christopher G ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; MTOR PROTEIN, HUMAN; PROTEIN KINASE; TARGET OF RAPAMYCIN KINASE;

ANIMAL; CELL FUNCTION; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN SYNTHESIS; REVIEW; RIBOSOME; SIGNAL TRANSDUCTION;

ANIMALS; CELL PHYSIOLOGICAL PHENOMENA; CELL PHYSIOLOGY; HUMANS; PROTEIN BIOSYNTHESIS; PROTEIN KINASES; RIBOSOMES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 33749431713     PISSN: 15489213     EISSN: None     Source Type: Journal    
DOI: 10.1152/physiol.00024.2006     Document Type: Review

References (57)

1. Banko JL, Poulin F, Hou L, DeMaria CT, Sonenberg N, and Klann E. The translation repressor 4E-BP2 is critical for eIF4F complex formation, synaptic plasticity, and memory in the hippocampus. J Neurosci 25: 9581-9590, 2005.
2. Beugnet A, Tee AR, Taylor PM, and Proud CG. Evidence that intracellular amino acids regulate translation factor function in mammalian cells. Biochem J 372: 566, 2002.
3. Browne GJ, Finn SG, and Proud CG. Stimulation of the AMPactivated protein kinase leads to activation of eukaryotic elongation factor 2 kinase and to its phosphorylation at a novel site, serine 398. J Biol Chem 279: 12220-12231, 2004.
4. Browne GJ, Proud CG. A novel mTOR-regulated phosphorylation site in elongation factor 2 kinase modulates the activity of the kinase and its binding to calmodulin. Mol Cell Biol 24: 2986-2997, 2004.
5. Byfield MP, Murray JT, and Backer JM. hVps34 is a nutrientregulated lipid kinase required for activation of p70 S6 kinase. J Biol Chem 280: 33076-33082, 2005.
6. Carlberg U, Nilsson A, and Nygard O. Functional properties of phosphorylated elongation factor 2. Eur J Biochem 191: 639-645, 1990.
7. Dennis PB, Jaeschke A, Saitoh M, Fowler B, Kozma SC, and Thomas G. Mammalian TOR: a homeostatic ATP sensor. Science 294: 1102-1105, 2001.
8. Fattori R and Piva T. Drug-eluting stents in vascular intervention. Lancet 361: 247-249, 2003.
9. Fumagalli S and Thomas G. S6 phosphorylation, and signal transduction. In: Translational Control of Gene Expression, edited by Sonenberg N, Hershey JWB, and Mathews MB. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2000, p. 695-717.
10. Gangloff YG, Mueller M, Dann SG, Svoboda P, Sticker M, Spetz JF, Um SH, Brown EJ, Cereghini S, Thomas G, and Kozma SC. Disruption of the mouse mTOR gene leads to early postimplantation lethality and prohibits embryonic stem cell development. Mol Cell Biol 24: 9508-9516, 2004.
11. Gingras AC, Raught B, Gygi SP, Niedzwieka A, Miron M, Burley SK, Polakiewicz RD, Wyslouch-Cieczyska A, Aebersold R, and Sonenberg N. Hierarchical phosphorylation of the translation inhibitor 4E-BP1. Genes Dev 15: 2852-2864, 2001.
12. Gingras AC, Raught B, and Sonenberg N. eIF4 translation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68: 913-963, 1999.
13. Hannan KM, Brandenburger Y, Jenkins A, Sharkey K, Cavanaugh A, Rothblum L, Moss T, Poortinga G, McArthur GA, Pearson RB, and Hannan RD. mTOR-dependent regulation of ribosomal gene transcription requires S6K1 and is mediated by phosphorylation of the carboxy-terminal activation domain of the nucleolar transcription factor UBF. Mol Cell Biol 23: 8862-8877, 2003.
14. Hannan RD, Jenkins A, Jenkins AK, and Brandenburger Y. Cardiac hypertrophy: a matter of translation. Clin Exp Pharmacol Physiol 30: 517-527, 2003.
15. Hara K, Yonezawa K, Weng QP, Kozlowski MT, Belham C, and Avruch J. Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF4E BP1 through a common effector mechanism. J Biol Chem 273: 14484-14494, 1998.
16. Harrington LS, Findlay GM, Gray A, Tolkacheva T, Wigfield S, Rebholz H, Barnett J, Leslie NR, Cheng S, Shepherd PR, Gout I, Downes CP, and Lamb RF. The TSC1-2 tumor suppressor controls insulin-PI3K signaling via regulation of IRS proteins. J Cell Biol 166: 213-223, 2004.
17. Harris TE and Lawrence JC. TOR signaling. Science STKE 212: re15, 2003.
18. Herbert TP, Kilhams GR, Batty IH, and Proud CG. Distinct signalling pathways mediate insulin and phorbol ester-stimulated eIF4F assembly and protein synthesis in HEK 293 cells. J Biol Chem 275: 11249-11256, 2000.
19. Holz MK, Ballif BA, Gygi SP, and Blenis J. mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123: 569-580, 2005.
20. Horman S, Browne GJ, Krause U, Patel JV, Vertommen D, Bertrand L, Lavoinne A, Hue L, Proud CG, and Rider MH. Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Curr Biol 12: 1419-1423, 2002.
21. Inoki K, Zhu T, and Guan KL. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115: 577-590, 2003.
22. Jefferies HBJ, Fumagalli S, Dennis PB, Reinhard C, Pearson RB, and Thomas G. Rapamycin suppresses 5'TOP mRNA translation through inhibition of p70S6k. EMBO J 16: 3693-3704, 1997.
23. Jefferies HBJ, Reinhard G, Kozma SC, and Thomas G. Rapamycin selectively represses translation of the 'polypyrimidine tract' mRNA family. Proc Natl Acad Sci USA 91: 4441-4445, 1994.
24. Kimball SR and Jefferson LS. Signaling pathways and molecular mechanisms through which branched-chain amino acids mediate translational control of protein synthesis. J Nutr 136: 227-231, 2006.
25. Koritzinsky M, Magagnin MG, van den BT, Seigneuric R, Savelkouls K, Dostie J, Pyronnet S, Kaufman RJ, Weppler SA, Voncken JW, Lambin P, Koumenis C, Sonenberg N, and Wouters BG. Gene expression during acute and prolonged hypoxia is regulated by distinct mechanisms of translational control. EMBO J 25: 1114-1125, 2006.
26. Lawson TG, Lee KA, Maimone MM, Abramson RD, Dever TE, Merrick WC, and Thach RE. Dissociation of double-stranded polynucleotide helical structures by eukaryotic initiation factors, as revealed by a novel assay. Biochemistry 28: 4729-4734, 1989.
27. Liu L, Cash TP, Jones RG, Keith B, Thompson CB, and Simon MC. Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol Cell 21: 521-531, 2006.
28. Long X, Lin Y, Ortiz-Vega S, Yonezawa K, and Avruch J. Rheb binds and regulates the mTOR kinase. Curr Biol 15: 702-713, 2005.
29. Ma L, Chen Z, Erdjument-Bromage H, Tempst P, and Pandolfi PP. Phosphorylation and functional inactivation of TSC2 by Erk implications for tuberous sclerosis and cancer pathogenesis. Cell 121: 179-193, 2005.
30. Manning BD and Cantley LC. Rheb fills a GAP between TSC and TOR. Trends Biochem Sci 28: 573-576, 2003.
31. Mayer C, Zhao J, Yuan X, and Grummt I. mTORdependent activation of the transcription factor TIF-IA links rRNA synthesis to nutrient availability. Genes Dev 18: 423-434, 2004.
32. McMullen JR, Sherwood MC, Tarnavski O, Zhang L, Dorfman AL, Shioi T, and Izumo S. Inhibition of mTOR signaling with rapamycin regresses established cardiac hypertrophy induced by pressure overload. Circulation 109: 3050-3055, 2004.
33. McMullen JR, Shioi T, Zhang L, Tarnavski O, Sherwood MC, Dorfman AL, Longnus S, Pende M, Martin KA, Blenis J, Thomas G, and Izumo S. Deletion of ribosomal S6 kinases does not attenuate pathological, physiological, or insulin-like growth factor 1 receptor-phosphoinositide 3-kinase-induced cardiac hypertrophy. Mol Cell Biol 24: 6231-6240, 2004.
34. Meyuhas O and Hornstein E. Translational control of T.O.P. mRNAs. In: Translational Control of Gene Expression, edited by Sonenberg N, Hershey JWB, and Mathews MB. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2000, p. 671-693.
35. Montagne J, Stewart MJ, Stocker H, Hafen E, Kozma SC, and Thomas G. Drosophila S6 kinase: a regulator of cell size. Science 285: 2126-2129, 1999.
36. Murakami M, Ichisaka T, Maeda M, Oshiro N, Hara K, Edenhofer F, Kiyama H, Yonezawa K, and Yamanaka S. mTOR is essential for growth and proliferation in early mouse embryos and embryonic stem cells. Mol Cell Biol 24: 6710-6718, 2004.
37. Nobukuni T, Joaquin M, Roccio M, Dann SG, Kim SY, Gulati P, Byfield MP, Backer JM, Natt F, Bos JL, Zwartkruis FJ, and Thomas G. Amino acids mediate mTOR/raptor signaling through activation of class 3 phosphatidylinositol 3OH-kinase. Proc Natl Acad Sci USA 102: 14238-14243, 2005.
38. Pende M, Kozma SC, Jaquet M, Oorschot V, Burcelin R, Le Marchand-Brustel Y, Klumperman J, Thorens B, and Thomas G. Hypoinsulinaemia, glucose intolerance and diminished beta-cell size in S6K1-deficient mice. Nature 408: 994-997, 2000.
39. Pende M, Um SH, Mieulet V, Sticker M, Goss VL, Mestan J, Mueller M, Fumagalli S, Kozma SC, and Thomas G. S6K1(-/-)/S6K2(-/-) mice exhibit perinatal lethality and rapamycin-sensitive 5'-terminal oligopyrimidine mRNA translation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway. Mol Cell Biol 24: 3112-3124, 2004.
40. Proud CG. The eukaryotic initiation factor 4Ebinding proteins and apoptosis. Cell Death Differ 12: 541-546, 2005.
41. Proud CG. Control of the elongation phase of protein synthesis. In: Translational Control of Gene Expression, edited by Sonenberg N, Hershey JWB, Mathews MB. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2000, p. 719-739.
42. Raught B, Peiretti F, Gingras AC, Livingstone M, Shahbazian D, Mayeur GL, Polakiewicz RD, Sonenberg N, and Hershey JW. Phosphorylation of eucaryotic translation initiation factor 4B Ser422 is modulated by S6 kinases. EMBO J 23: 1761-1769, 2004.
43. Redpath NT, Foulstone EJ, and Proud CG. Regulation of translation elongation factor-2 by insulin via a rapamycin-sensitive signaling pathway. EMBO J 15: 2291-2297, 1996.
44. Roccio M, Bos JL, and Zwartkruis FJ. Regulation of the small GTPase Rheb by amino acids. Oncogene 25: 657-664, 2006.
45. Roux PP, Ballif BA, Anjum R, Gygi SP, and Blenis J. Tumor-promoting phorbol esters and activated Ras inactivate the tuberous sclerosis tumor suppressor complex via p90 ribosomal S6 kinase. Proc Natl Acad Sci USA 101: 13489-13494, 2004.
46. Roux PP and Blenis J. ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 68: 320-344, 2004.
47. Ruvinsky I, Sharon N, Lerer T, Cohen H, Stolovich-Rain M, Nir T, Dor Y, Zisman P, and Meyuhas O. Ribosomal protein S6 phosphorylation is a determinant of cell size and glucose homeostasis. Genes Dev 19: 2199-2211, 2005.
48. Ryazanov AG, Ward MD, Mendola CE, Pavur KS, Dorovkov MV, Wiedmann M, Erdjument-Bromage H, Tempst P, Parmer TG, Prostko CR, Germino FJ, and Hait WN. Identification of a new class of protein kinases represented by eukaryotic elongation factor-2 kinase. Proc Natl Acad Sci USA 94: 4884-4889, 1997.
49. Sarbassov dD, Ali SM, and Sabatini DM. Growing roles for the mTOR pathway. Curr Opin Cell Biol 17: 596-603, 2005.
50. Smith EM, Finn SG, Tee AR, Browne GJ, and Proud CG. The tuberous sclerosis protein TSC2 is not required for the regulation of the mammalian target of rapamycin by amino acids and certain cellular stresses. J Biol Chem 280: 18717-18727, 2005.
51. Tsukiyama-Kohara K, Poulin F, Kohara M, DeMaria CT, Cheng A, Wu Z, Gingras AC, Katsume A, Elchebly M, Spiegelman BM, Harper ME, Tremblay ML, and Sonenberg N. Adipose tissue reduction in mice lacking the translational inhibitor 4E-BP1. Nat Med 7: 1128-1132, 2001.
52. Um SH, Frigerio F, Watanabe M, Picard F, Joaquin M, Sticker M, Fumagalli S, Allegrini PR, Kozma SC, Auwerx J, and Thomas G. Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 431: 200-205, 2004.
53. Wang L and Proud CG. Ras/Erk signaling is essential for activation of protein synthesis by Gq protein-coupled receptor agonists in adult cardiomyocytes. Circ Res 91: 821-829, 2002.
54. Wang L, Wang X, and Proud CG. Activation of mRNA translation by insulin in rat cardiomyocytes involves multiple rapamycin-sensitive steps. Am J Physiol Heart Circ Physiol 278: H1056-H1068, 2000.
55. Wang X, Beugnet A, Murakami M, Yamanaka S, and Proud CG. Distinct signaling events downstream of mTOR cooperate to mediate the effects of amino acids and insulin on initiation factor 4Ebinding proteins. Mol Cell Biol 25: 2558-2572, 2005.
56. Wang X, Campbell LE, Miller CM, and Proud CG. Amino acid availability regulates p70 S6 kinase and multiple translation factors. Biochem J 334: 261-267, 1998.
57. Wang X, Li W, Williams M, Terada N, Alessi DR, and Proud CG. Regulation of elongation factor 2 kinase by p90RSK1 and p70 S6 kinase. EMBO J 20: 4370-4379, 2001.