Identification of eukaryotic elongation factor-2 as a novel cellular target of lithium and glycogen synthase kinase-3

Molecular and Cellular Neuroscience

Volumn 45, Issue 4, 2010, Pages 449-455

  Karyo, Racheli ^a   Eskira, Yael ^b   Pinhasov, Albert ^c   Belmaker, R H ^b   Agam, Galila ^b   Eldar Finkelman Hagit, H ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^c ARIEL UNIVERSITY   (Israel)

Author keywords

EEF 2; GSK 3; Lithium; Phosphorylation; Protein synthesis

Indexed keywords

ELONGATION FACTOR 2; EUKARYOTIC ELONGATION FACTOR 2; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; LITHIUM SALT; THREONINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG PROTEIN BINDING; ENZYME INHIBITION; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; PROTEOMICS; STRESS;

ANIMALS; ANTIDEPRESSIVE AGENTS; CELL LINE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ELONGATION FACTOR 2 KINASE; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; HUMANS; LITHIUM COMPOUNDS; MICE; MICE, INBRED ICR; PHOSPHORYLATION;

ANIMALIA; EUKARYOTA;

EID: 77957963266     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2010.08.004     Document Type: Article

References (75)

1. Althausen S., Mengesdorf T., Mies G., Olah L., Nairn A.C., Proud C.G., Paschen W. Changes in the phosphorylation of initiation factor eIF-2alpha, elongation factor eEF-2 and p70 S6 kinase after transient focal cerebral ischaemia in mice. J. Neurochem. 2001, 78:779-787.
2. Aronson P.S. Properties of the renal Na+ -H+exchanger. Ann. NY Acad. Sci. 1985, 456:220-228.
3. Bassell G.J., Warren S.T. Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron 2008, 60:201-214.
4. Beaulieu J.M., Marion S., Rodriguiz R.M., Medvedev I.O., Sotnikova T.D., Ghisi V., Wetsel W.C., Lefkowitz R.J., Gainetdinov R.R., Caron M.G. A beta-arrestin 2 signaling complex mediates lithium action on behavior. Cell 2008, 132:125-136.
5. Berridge M.J., Downes C.P., Hanley M.R. Neural and developmental actions of lithium: a unifying hypothesis. Cell 1989, 59:411-419.
6. Bersudsky Y., Shaldubina A., Kozlovsky N., Woodgett J.R., Agam G., Belmaker R.H. Glycogen synthase kinase-3beta heterozygote knockout mice as a model of findings in postmortem schizophrenia brain or as a model of behaviors mimicking lithium action: negative results. Behav. Pharmacol. 2008, 19:217-224.
7. Beyer J.L., Kuchibhatla M., Payne M.E., Moo-Young M., Cassidy F., Macfall J., Krishnan K.R. Hippocampal volume measurement in older adults with bipolar disorder. Am. J. Geriatr. Psychiatry 2004, 12:613-620.
8. Boyce M., Py B.F., Ryazanov A.G., Minden J.S., Long K., Ma D., Yuan J. A pharmacoproteomic approach implicates eukaryotic elongation factor 2 kinase in ER stress-induced cell death. Cell Death Differ. 2008, 15:589-599.
9. Browne G.J., Finn S.G., Proud C.G. Stimulation of the AMP-activated protein kinase leads to activation of eukaryotic elongation factor 2 kinase and to its phosphorylation at a novel site, serine 398. J. Biol. Chem. 2004, 279:12220-12231.
10. Chen G., Bower K.A., Ma C., Fang S., Thiele C.J., Luo J. Glycogen synthase kinase 3beta (GSK3beta) mediates 6-hydroxydopamine-induced neuronal death. FASEB J. 2004, 18:1162-1164.
11. Cheng K., Creacy S., Larner J. 'Insulin-like' effects of lithium ion on isolated rat adipocytes. I. Stimulation of glycogenesis beyond glucose transport. Mol. Cell. Biochem. 1983, 56:177-182.
12. Chepenik L.G., Fredericks C., Papademetris X., Spencer L., Lacadie C., Wang F., Pittman B., Duncan J.S., Staib L.H., Duman R.S., Gelernter J., Blumberg H.P. Effects of the brain-derived neurotrophic growth factor val66met variation on hippocampus morphology in bipolar disorder. Neuropsychopharmacology 2009, 34:944-951.
13. Coghlan M.P., Culbert A.A., Cross D.A., Corcoran S.L., Yates J.W., Pearce N.J., Rausch O.L., Murphy G.J., Carter P.S., Roxbee Cox L., Mills D., Brown M.J., Haigh D., Ward R.W., Smith D.G., Murray K.J., Reith A.D., Holder J.C. Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen metabolism and gene transcription. Chem. Biol. 2000, 7:793-803.
14. De Sarno P., Li X., Jope R.S. Regulation of Akt and glycogen synthase kinase-3bet phosphorylation by sodium valproate and lithium. Neuropharmacology 2001, 43:1158-1164.
15. Dorovkov M.V., Pavur K.S., Petrov A.N., Ryazanov A.G. Regulation of elongation factor-2 kinase by pH. Biochemistry 2002, 41:13444-13450.
16. Gould T.D., Chen G., Manji H.K. In vivo evidence in the brain for lithium inhibition of glycogen synthase kinase-3. Neuropsychopharmacology 2004, 29:32-38.
17. Gould T.D., Einat H., Bhat R., Manji H.K. AR-A014418, a selective GSK-3 inhibitor, produces antidepressant-like effects in the forced swim test. Int. J. Neuropsychopharmacol. 2004, 7:387-390.
18. Hay N., Sonenberg N. Upstream and downstream of mTOR. Genes Dev. 2004, 18:1926-1945.
19. Hennion J.P., el-Masri M.A., Huff M.O., el-Mailakh R.S. Evaluation of neuroprotection by lithium and valproic acid against ouabain-induced cell damage. Bipolar Disord. 2002, 4:201-206.
20. Hiroi T., Wei H., Hough C., Leeds P., Chuang D.M. Protracted lithium treatment protects against the ER stress elicited by thapsigargin in rat PC12 cells: roles of intracellular calcium, GRP78 and Bcl-2. Pharmacogenomics J. 2005, 5:102-111.
21. Huang H.C., Klein P.S. Multiple roles for glycogen synthase kinase-3 as a drug target in Alzheimer's disease. Curr. Drug Targets 2006, 7:1389-1397.
22. Johnson G., Gotlib J., Haroutunian V., Bierer L., Nairn A.C., Merril C., Wallace W. Increased phosphorylation of elongation factor 2 in Alzheimer's disease. Brain Res. Mol. Brain Res. 1992, 15:319-326.
23. Kaidanovich-beilin O., Milman A., Weizman A., Pick C., Eldar-Finkelman H. Rapid anti-depressive like activity of specific GSK-3 inhibitor, and its effect on -catenin in the mouse hippocampus. Biol. Psychiatry 2004.
24. Kaidanovich-Beilin O., Lipina T.V., Takao K., van Eede M., Hattori S., Laliberte C., Khan M., Okamoto K., Chambers J.W., Fletcher P.J., Macaulay K., Doble B.W., Henkelman M., Miyakawa T., Roder J., Woodgett J.R. Abnormalities in brain structure and behavior in GSK-3alpha mutant mice. Mol. Brain 2009, 2:35.
25. Kelleher R.J., Bear M.F. The autistic neuron: troubled translation?. Cell 2008, 135:401-406.
26. Kim H.J., Thayer S.A. Lithium increases synapse formation between hippocampal neurons by depleting phosphoinositides. Mol. Pharmacol. 2009, 75:1021-1030.
27. Kim W.Y., Zhou F.Q., Zhou J., Yokota Y., Wang Y.M., Yoshimura T., Kaibuchi K., Woodgett J.R., Anton E.S., Snider W.D. Essential roles for GSK-3 s and GSK-3-primed substrates in neurotrophin-induced and hippocampal axon growth. Neuron 2006, 52:981-996.
28. Kirshennboim N., Plotkin B., Ben Shlomo S., Kaidanovich-Beilin O., Eldar-Finkelman H. Lithium-mediated phosphorylation of glycogen synthase kinase-3 involves PI3 Kinase-dependent activation of protein kinase C-alpha. J. Mol. Neurosci. 2004, 24:199-207.
29. Klein P.S., Melton D.A. A molecular mechanism for the effect of lithium on development. Proc. Nat. Acad. Sci. U.S.A. 1996, 93:8455-8459.
30. Knebel A., Morrice N., Cohen P. A novel method to identify protein kinase substrates: eEF2 kinase is phosphorylated and inhibited by SAPK4/p38delta. EMBO J. 2001, 20:4360-4369.
31. Lahne H.U., Kloster M.M., Lefdal S., Blomhoff H.K., Naderi S. Degradation of cyclin D3 independent of Thr-283 phosphorylation. Oncogene 2006, 25:2468-2476.
32. Laitusis A.L., Brostrom C.O., Ryazanov A.G., Brostrom M.A. An examination of the role of increased cytosolic free Ca2+ concentrations in the inhibition of mRNA translation. Arch. Biochem. Biophys. 1998, 354:270-280.
33. Leazer T.M., Klaassen C.D. The presence of xenobiotic transporters in rat placenta. Drug Metab. Dispos. 2003, 31:153-167.
34. Liu C., Li Y., Semenov M., Han C., Baeg G.H., Tan Y., Zhang Z., Lin X., He X. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 2002, 108:837-847.
35. Lucas J.J., Hernandez F., Gomez-Ramos P., Moran M.A., Hen R., Avila J. Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J. 2001, 20:27-39.
36. Macdonald A., Briggs K., Poppe M., Higgins A., Velayudhan L., Lovestone S. A feasibility and tolerability study of lithium in Alzheimer's disease. Int. J. Geriatr. Psychiatry 2008.
37. MacQueen G.M., Campbell S., McEwen B.S., Macdonald K., Amano S., Joffe R.T., Nahmias C., Young L.T. Course of illness, hippocampal function, and hippocampal volume in major depression. Proc. Nat. Acad. Sci. U.S.A. 2003, 100:1387-1392.
38. Manji H.K., Moore G.J., Chen G. Lithium at 50: have the neuroprotective effects of this unique cation been overlooked?. Biol. Psychiatry 1999, 46:929-940.
39. Mariappan M.M., Shetty M., Sataranatarajan K., Choudhury G.G., Kasinath B.S. Glycogen synthase kinase 3beta is a novel regulator of high glucose- and high insulin-induced extracellular matrix protein synthesis in renal proximal tubular epithelial cells. J. Biol. Chem. 2008, 283:30566-30575.
40. Marin P., Nastiuk K.L., Daniel N., Girault J.A., Czernik A.J., Glowinski J., Nairn A.C., Premont J. Glutamate-dependent phosphorylation of elongation factor-2 and inhibition of protein synthesis in neurons. J. Neurosci. 1997, 17:3445-3454.
41. Martinek S., Inonog S., Manoukian A.S., Young M.W. A role for the segment polarity gene shaggy/GSK-3 in the Drosophila circadian clock. Cell 2001, 105:769-779.
42. Martinez A., Alonso M., Castro A., Perez C., Moreno F.J. First non-ATP competitive glycogen synthase kinase 3 beta (GSK-3beta) inhibitors: thiadiazolidinones (TDZD) as potential drugs for the treatment of Alzheimer's disease. J. Med. Chem. 2002, 45:1292-1299.
43. Meijer A., Flajolet M., Greengard P. Pharmacological inhibitors of glycogen synthase kinase 3. Trends Pharmacol. Sci. 2004, 25:471-480.
44. Mora A., Sabio G., Risco A.M., Cuenda A., Alonso J.C., Soler G., Centeno F. Lithium blocks the PKB and GSK3 dephosphorylation induced by ceramide through protein phosphatase-2A. Cell. Signal. 2002, 14:557-562.
45. Nairn A.C., Palfrey H.C. Identification of the major Mr 100, 000 substrate for calmodulin-dependent protein kinase III in mammalian cells as elongation factor-2. J. Biol. Chem. 1987, 262:17299-17303.
46. Narayanan U., Nalavadi V., Nakamoto M., Thomas G., Ceman S., Bassell G.J., Warren S.T. S6K1 phosphorylates and regulates fragile X mental retardation protein (FMRP) with the neuronal protein synthesis-dependent mammalian target of rapamycin (mTOR) signaling cascade. J. Biol. Chem. 2008, 283:18478-18482.
47. Nemeth Z.H., Deitch E.A., Szabo C., Hauser C.J., Hasko G. Lithium induces NF-kappa B activation and interleukin-8 production in human intestinal epithelial cells. J. Bio. Chem. 2002, 277:7713-7719.
48. O'Brien W.T., Harper A.D., Jove F., Woodgett J.R., Maretto S., Piccolo S., Klein P.S. Glycogen synthase kinase-3beta haploinsufficiency mimics the behavioral and molecular effects of lithium. J. Neurosci. 2004, 24:6791-6798.
49. Pachet A.K., Wisniewski A.M. The effects of lithium on cognition: an updated review. Psychopharmacology (Berl) 2003, 170:225-234.
50. Patel J., McLeod L.E., Vries R.G., Flynn A., Wang X., Proud C.G. Cellular stresses profoundly inhibit protein synthesis and modulate the states of phosphorylation of multiple translation factors. Eur. J. Biochem. 2002, 269:3076-3085.
51. Pavur K.S., Petrov A.N., Ryazanov A.G. Mapping the functional domains of elongation factor-2 kinase. Biochemistry 2000, 39:12216-12224.
52. Peterson R.T., Schreiber S.L. Translation control: connecting mitogens and the ribosome. Curr. Biol. 1998, 8:R248-R250.
53. Phiel C.J., Klein P.S. Molecular targets of lithium action. Ann. Rev. Pharm. Toxicol. 2001, 41:789-813.
54. Picking W.D., Kudlicki W., Kramer G., Hardesty B., Vandenheede J.R., Merlevede W., Park I.K., DePaoli-Roach A. Fluorescence studies on the interaction of inhibitor 2 and okadaic acid with the catalytic subunit of type 1 phosphoprotein phosphatases. Biochemistry 1991, 30:10280-10287.
55. Plotkin B., Kaidanovich O., Talior I., Eldar-Finkelman H. Insulin mimetic action of synthetic phosphorylated peptide inhibitors of glycogen synthase kinase-3. J. Pharmacol. Exp. Ther. 2003, 974-980.
56. Proud C.G. Regulation of protein synthesis by insulin. Biochem. Soc. Trans. 2006, 34:213-216.
57. Proud C.G., Wang X., Patel J.V., Campbell L.E., Kleijn M., Li W., Browne G.J. Interplay between insulin and nutrients in the regulation of translation factors. Biochem. Soc. Trans. 2001, 29:541-547.
58. Redpath N.T., Price N.T., Severinov K.V., Proud C.G. Regulation of elongation factor-2 by multisite phosphorylation. Eur. J. Biochem. 1993, 213:689-699.
59. Rockenstein E., Torrance M., Adame A., Mante M., Bar-on P., Rose J.B., Crews L., Masliah E. Neuroprotective effects of regulators of the glycogen synthase kinase-3beta signaling pathway in a transgenic model of Alzheimer's disease are associated with reduced amyloid precursor protein phosphorylation. J. Neurosci. 2007, 27:1981-1991.
60. Ryazanov A.G. Ca2+/calmodulin-dependent phosphorylation of elongation factor 2. FEBS Lett. 1987, 214:331-334.
61. Ryazanov A.G., Shestakova E.A., Natapov P.G. Phosphorylation of elongation factor 2 by EF-2 kinase affects rate of translation. Nature 1988, 334:170-173.
62. Scherk H., Backens M., Schneider-Axmann T., Kemmer C., Usher J., Reith W., Falkai P., Gruber O. Neurochemical pathology in hippocampus in euthymic patients with bipolar I disorder. Acta Psychiatr. Scand. 2008, 117:283-288.
63. Sheline Y.I., Gado M.H., Kraemer H.C. Untreated depression and hippocampal volume loss. Am. J. Psychiatry 2003, 160:1516-1518.
64. Stambolic V., Ruel L., Woodgett J.R. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr. Biol. 1996, 6:1664-1668.
65. Stolovich M., Lerer T., Bolkier Y., Cohen H., Meyuhas O. Lithium can relieve translational repression of TOP mRNAs elicited by various blocks along the cell cycle in a glycogen synthase kinase-3- and S6-kinase-independent manner. J. Biol. Chem. 2005, 280:5336-5342.
66. Strakowski S.M., Adler C.M., Holland S.K., Mills N.P., DelBello M.P., Eliassen J.C. Abnormal FMRI brain activation in euthymic bipolar disorder patients during a counting Stroop interference task. Am. J. Psychiatry 2005, 162:1697-1705.
67. Terwel D., Muyllaert D., Dewachter I., Borghgraef P., Croes S., Devijver H., Van Leuven F. Amyloid activates GSK-3beta to aggravate neuronal tauopathy in bigenic mice. Am. J. Pathol. 2008, 172:786-798.
68. Vandenheede J.R., Yang S.D., Merlevede W., Jurgensen S., Chock P.B. Kinase FA-mediated regulation of rabbit skeletal muscle protein phosphatase. Reversible phosphorylation of the modulator subunit. J. Biol. Chem. 1985, 260:10512-10516.
69. Vasconcellos A.P., Tabajara A.S., Ferrari C., Rocha E., Dalmaz C. Effect of chronic stress on spatial memory in rats is attenuated by lithium treatment. Physiol. Behav. 2003, 79:143-149.
70. Wang X., Campbell L.E., Miller C.M., Proud C.G. Amino acid availability regulates p70 S6 kinase and multiple translation factors. Biochem. J. 1998, 334(Pt 1):261-267.
71. Wang X., Li W., Williams M., Terada N., Alessi D.R., Proud C.G. Regulation of elongation factor 2 kinase by p90(RSK1) and p70 S6 kinase. EMBO J. 2001, 20:4370-4379.
72. Watase K., Gatchel J.R., Sun Y., Emamian E., Atkinson R., Richman R., Mizusawa H., Orr H.T., Shaw C., Zoghbi H.Y. Lithium therapy improves neurological function and hippocampal dendritic arborization in a spinocerebellar ataxia type 1 mouse model. PLoS Med. 2007, 4:e182.
73. Welsh G.I., Proud C.G. Glycogen synthase kinase-3 is rapidly inactivated in response to insulin and phosphorylates eukaryotic initiation factor eIF-2B. Biochem. J. 1993, 294:625-629.
74. Yan L., Nairn A.C., Palfrey H.C., Brady M.J. Glucose regulates EF-2 phosphorylation and protein translation by a protein phosphatase-2A-dependent mechanism in INS-1-derived 832/13 cells. J. Biol. Chem. 2003, 278:18177-18183.
75. Zhang F., Phiel C.J., Spece L., Gurvich N., Klein P.S. Inhibitory phosphorylation of glycogen synthase kinase-3 (GSK-3) in response to lithium. Evidence for autoregulation of GSK-3. J. Biol. Chem. 2003, 278:33067-33077.