Eukaryotic elongation factor 2 kinase activity is controlled by multiple inputs from oncogenic signaling

Molecular and Cellular Biology

Volumn 34, Issue 22, 2014, Pages 4088-4103

  Wang, Xuemin ^a   da Mota, Sergio Regufe ^a   Liu, Rui ^a   Moore, Claire E ^a   Xie, Jianling ^a   Lanucara, Francesco ^b   Agarwala, Usha ^a   Ruys, Sébastien Pyr dit ^c   Vertommen, Didier ^c   Rider, Mark H ^c   Eyers, Claire E ^b   Proud, Christopher G ^a,d  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^d SOUTH AUSTRALIAN HEALTH AND MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AZD 8055; CALMODULIN BINDING PROTEIN; ELONGATION FACTOR 2 KINASE; GLYCOGEN SYNTHASE KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE; RAPAMYCIN; SELUMETINIB; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; RAF PROTEIN; RAS PROTEIN; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ARTICLE; CANCER CELL; CELL ONCOGENE; CONTROLLED STUDY; ENZYME ACTIVITY; HEK293 CELL LINE; HUMAN; HUMAN CELL; KB CELL LINE; MOUSE; NONHUMAN; ONCOGENE RAS; PROTEIN PHOSPHORYLATION; RAT; ANIMAL; CELL LINE; ENZYME ACTIVATION; GENETICS; METABOLISM; NEOPLASM; PHOSPHORYLATION; POINT MUTATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; CELL LINE; CELL LINE, TUMOR; ELONGATION FACTOR 2 KINASE; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MULTIPROTEIN COMPLEXES; NEOPLASMS; PHOSPHORYLATION; POINT MUTATION; RAF KINASES; RAS PROTEINS; RATS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84908879570     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01035-14     Document Type: Article

References (50)

1. Ryazanov AG, Shestakova EA, Natapov PG. 1988. Phosphorylation of elongation factor 2 by EF-2 kinase affects rate of translation. Nature 334: 170-173. http://dx.doi.org/10.1038/334170a0.
2. Carlberg U, Nilsson A, Nygard O. 1990. Functional properties of phosphorylated elongation factor 2. Eur. J. Biochem. 191:639-645. http://dx.doi.org/10.1111/j.1432-1033.1990.tb19169.x.
3. Redpath NT, Proud CG. 1989. The tumour promoter okadaic acid inhibits reticulocyte-lysate protein synthesis by increasing the net phosphorylation of elongation factor 2. Biochem. J. 262:69-75.
4. Ryazanov AG, Davydova EK. 1989. Mechanism of elongation factor 2 (EF-2) inactivation upon phosphorylation: phosphorylated EF-2 is unable to catalyze translocation. FEBS Lett. 251:187-190. http://dx.doi.org/10.1016/0014-5793(89)81452-8.
5. Mitsui K, Brady M, Palfrey HC, Nairn AC. 1993. Purification and characterization of calmodulin-dependent protein kinase III from rabbit reticulocytes and rat pancreas. J. Biol. Chem. 268:13422-13433.
6. Nairn AC, Palfrey HC. 1987. Identification of the major Mr 100,000 substrate for calmodulin-dependent protein kinase III in mammalian cells as elongation factor-2. J. Biol. Chem. 262:17299-17303.
7. Redpath NT, Proud CG. 1993. Purification and phosphorylation of elongation factor-2 kinase from rabbit reticulocytes. Eur. J. Biochem. 212:511-520. http://dx.doi.org/10.1111/j.1432-1033.1993.tb17688.x.
8. Ryazanov AG, Ward MD, Mendola CE, Pavur KS, Dorovkov MV, Wiedmann M, Erdjument-Bromage H, Tempst P, Parmer TG, Prostko CR, Germino FJ, Hait WN. 1997. Identification of a new class of protein kinases represented by eukaryotic elongation factor-2 kinase. Proc. Natl. Acad. Sci. U. S. A. 94:4884-4889. http://dx.doi.org/10.1073/pnas.94.10.4884.
9. 2+/calmodulin-dependent system of protein phosphorylation. Biochimie 70: 619-626. http://dx.doi.org/10.1016/0300-9084(88)90245-3.
10. Redpath NT, Foulstone EJ, Proud CG. 1996. Regulation of translation elongation factor-2 by insulin via a rapamycin-sensitive signaling pathway. EMBO J. 15:2291-2297.
11. Wang X, Proud CG. 2006. The mTOR pathway in the control of protein synthesis. Physiology (Bethesda) 21:362-369. http://dx.doi.org/10.1152/physiol.00024.2006.
12. Feldman ME, Apsel B, Uotila A, Loewith R, Knight ZA, Ruggero D, Shokat KM. 2009. Active-site inhibitors of mTOR target rapamycinresistant outputs of mTORC1 and mTORC2. PLoS Biol. 7:e38. http://dx.doi.org/10.1371/journal.pbio.1000038.
13. Thoreen CC, Kang SA, Chang JW, Liu Q, Zhang J, Gao Y, Reichling LJ, Sim T, Sabatini DM, Gray NS. 2009. An ATP-competitive mTOR inhibitor reveals rapamycin-insensitive functions of mTORC1. J. Biol. Chem. 284:8023-8032. http://dx.doi.org/10.1074/jbc.M900301200.
14. Chresta CM, Davies BR, Hickson I, Harding T, Cosulich S, Critchlow SE, Vincent JP, Ellston R, Jones D, Sini P, James D, Howard Z, Dudley P, Hughes G, Smith L, Maguire S, Hummersone M, Malagu K, Menear K, Jenkins R, Jacobsen M, Smith GC, Guichard S, Pass M. 2010. AZD8055 is a potent, selective, and orally bioavailable ATP-competitive mammalian target of rapamycin kinase inhibitor with in vitro and in vivo antitumor activity. Cancer Res. 70:288-298. http://dx.doi.org/10.1158/0008-5472.CAN-09-1751.
15. RSK1 and p70 S6 kinase. EMBO J. 20:4370-4379. http://dx.doi.org/10.1093/emboj/20.16.4370.
16. Browne GJ, Proud CG. 2004. 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. http://dx.doi.org/10.1128/MCB.24.7.2986-2997.2004.
17. Knebel A, Morrice N, Cohen P. 2001. A novel method to identify protein kinase substrates: eEF2 kinase is phosphorylated and inhibited by SAPK4/p38delta. EMBO J. 20:4360-4369. http://dx.doi.org/10.1093/emboj/20.16.4360.
18. Smith EM, Proud CG. 2008. cdc2-cyclin B regulates eEF2 kinase activity in a cell cycle-and amino acid-dependent manner. EMBO J. 27:1005-1016. http://dx.doi.org/10.1038/emboj.2008.39.
19. Roux PP, Blenis J. 2004. ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev. 68:320-344. http://dx.doi.org/10.1128/MMBR.68.2.320-344.2004.
20. Wang L, Proud CG. 2002. Regulation of the phosphorylation of elongation factor 2 by MEK-dependent signaling in adult rat cardiomyocytes. FEBS Lett. 531:285-289. http://dx.doi.org/10.1016/S0014-5793(02)03536-6.
21. Wang L, Proud CG. 2002. Ras/Erk signaling is essential for activation of protein synthesis by Gq protein-coupled receptor agonists in adult cardiomyocytes. Circ. Res. 91:821-829. http://dx.doi.org/10.1161/01.RES.0000041029.97988.E9.
22. Knebel A, Haydon CE, Morrice N, Cohen P. 2002. Stress-induced regulation of eEF2 kinase by SB203580-sensitive and-insensitive pathways. Biochem. J. 367:525-532. http://dx.doi.org/10.1042/BJ20020916.
23. Leprivier G, Remke M, Rotblat B, Dubuc A, Mateo AR, Kool M, Agnihotri S, El-Naggar A, Yu B, Prakash SS, Faubert B, Bridon G, Tognon CE, Mathers J, Thomas R, Li A, Barokas A, Kwok B, Bowden M, Smith S, Wu X, Korshunov A, Hielscher T, Northcott PA, Galpin JD, Ahern CA, Wang Y, McCabe MG, Collins VP, Jones RG, Pollak M, Delattre O, Gleave ME, Jan E, Pfister SM, Proud CG, Derry WB, Taylor MD, Sorensen PH. 2013. The eEF2 Kinase confers resistance to nutrient deprivation by blocking translation elongation. Cell 153:1064-1079. http://dx.doi.org/10.1016/j.cell.2013.04.055.
24. Bagaglio DM, Cheng EH, Gorelick FS, Mitsui K, Nairn AC, Hait WN. 1993. Phosphorylation of elongation factor 2 in normal and malignant rat glial cells. Cancer Res. 53:2260-2264.
25. Parmer TG, Ward MD, Yurkow EJ, Vyas VH, Kearney TJ, Hait WN. 1999. Activity and regulation by growth factors of calmodulin-dependent protein kinase III (elongation factor 2-kinase) in human breast cancer. Br. J. Cancer 79:59-64. http://dx.doi.org/10.1038/sj.bjc.6690012.
26. Beauchamp EM, Platanias LC. 2013. The evolution of the TOR pathway and its role in cancer. Oncogene 32:3923-3932. http://dx.doi.org/10.1038/onc.2012.567.
27. Diggle TA, Seehra CK, Hase S, Redpath NT. 1999. Analysis of the domain structure of elongation factor-2 kinase by mutagenesis. FEBS Lett. 457:189-192. http://dx.doi.org/10.1016/S0014-5793(99)01034-0.
28. Pavur KS, Petrov AN, Ryazanov AG. 2000. Mapping the functional domains of elongation factor-2 kinase. Biochemistry 39:12216-12224. http://dx.doi.org/10.1021/bi0007270.
29. Pigott CR, Mikolajek H, Moore CE, Finn SJ, Phippen CW, Werner JM, Proud CG. 2011. Insights into the regulation of eukaryotic elongation factor 2 kinase and the interplay between its domains. Biochem. J. 442: 105-118. http://dx.doi.org/10.1042/BJ20111536.
30. Mittl PR, Schneider-Brachert W. 2007. Sel1-like repeat proteins in signal transduction. Cell Signal. 19:20-31. http://dx.doi.org/10.1016/j.cellsig.2006.05.034.
31. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 77:248-254.
32. Pyr Dit RS, Wang X, Smith EM, Herinckx G, Hussain N, Rider MH, Vertommen D, Proud CG. 2012. Identification of autophosphorylation sites in eukaryotic elongation factor-2 kinase. Biochem. J. 442:681-692. http://dx.doi.org/10.1042/BJ20111530.
33. Fonseca BD, Smith EM, Lee VH, MacKintosh C, Proud CG. 2007. PRAS40 is a target for mammalian target of rapamycin complex 1 and is required for signaling downstream of this complex. J. Biol. Chem. 282: 24514-24524. http://dx.doi.org/10.1074/jbc.M704406200.
34. Yeh TC, Marsh V, Bernat BA, Ballard J, Colwell H, Evans RJ, Parry J, Smith D, Brandhuber BJ, Gross S, Marlow A, Hurley B, Lyssikatos J, Lee PA, Winkler JD, Koch K, Wallace E. 2007. Biological characterization of ARRY-142886 (AZD6244), a potent, highly selective mitogenactivated protein kinase kinase 1/2 inhibitor. Clin. Cancer Res. 13:1576-1583. http://dx.doi.org/10.1158/1078-0432.CCR-06-1150.
35. Pearce LR, Alton GR, Richter DT, Kath JC, Lingardo L, Chapman J, Hwang C, Alessi DR. 2010. Characterization of PF-4708671, a novel and highly specific inhibitor of p70 ribosomal S6 kinase (S6K1). Biochem. J. 431:245-255. http://dx.doi.org/10.1042/BJ20101024.
36. - 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. 2:3112-3124. http://dx.doi.org/10.1128/MCB.24.8.3112-3124.2004.
37. Inoki K, Ouyang H, Zhu T, Lindvall C, Wang Y, Zhang X, Yang Q, Bennett C, Harada Y, Stankunas K, Wang CY, He X, MacDougald OA, You M, Williams BO, Guan KL. 2006. TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell 126:955-968. http://dx.doi.org/10.1016/j.cell.2006.06.055.
38. McManus EJ, Sakamoto K, Armit LJ, Ronaldson L, Shpiro N, Marquez R, Alessi DR. 2005. Role that phosphorylation of GSK3 plays in insulin and Wnt signaling defined by knockin analysis. EMBO J. 24:1571-1583. http://dx.doi.org/10.1038/sj.emboj.7600633.
39. Williams DD, Marin O, Pinna LA, Proud CG. 1999. Phosphorylated seryl and threonyl, but not tyrosyl, residues are efficient specificity determinants for GSK-3b and Shaggy. FEBS Lett. 448:86-90. http://dx.doi.org/10.1016/S0014-5793(99)00342-7.
40. Marin O, Meggio F, Draetta G, Pinna LA. 1992. The consensus sequences for cdc2 kinase and for casein kinase-2 are mutually incompatible. A study with peptides derived from the beta-subunit of casein kinase-2 FEBS Lett. 301:111-114.
41. Bennett CN, Ross SE, Longo KA, Bajnok L, Hemati N, Johnson KW, Harrison SD, MacDougald OA. 2002. Regulation of Wnt signaling during adipogenesis. J. Biol. Chem. 277:30998-31004. http://dx.doi.org/10.1074/jbc.M204527200.
42. Fonseca BD, Alain T, Finestone LK, Huang BP, Rolfe M, Jiang T, Yao Z, Hernandez G, Bennett CF, Proud CG. 2011. Pharmacological and genetic evaluation of proposed roles of mitogen-activated protein kinase/extracellular signal-regulated kinase kinase (MEK), extracellular signalregulated kinase (ERK), and p90RSK in the control of mTORC1 protein signaling by phorbol esters. J. Biol. Chem. 286:27111-27122. http://dx.doi.org/10.1074/jbc.M111.260794.
43. Hayashi AA, Proud CG. 2007. The rapid activation of protein synthesis by growth hormone requires signaling through mTOR. Am. J. Physiol. Endocrinol. Metab. 292:E1647-E1655. http://dx.doi.org/10.1152/ajpendo.00674.2006.
44. Jewell JL, Guan KL. 2013. Nutrient signaling to mTOR and cell growth. Trends Biochem. Sci. 38:233-242. http://dx.doi.org/10.1016/j.tibs.2013.01.004.
45. Tekedereli I, Alpay SN, Tavares CD, Cobanoglu ZE, Kaoud TS, Sahin I, Sood AK, Lopez-Berestein G, Dalby KN, Ozpolat B. 2012. Targeted silencing of elongation factor 2 kinase suppresses growth and sensitizes tumors to doxorubicin in an orthotopic model of breast cancer. PLoS One 7:e41171. http://dx.doi.org/10.1371/journal.pone.0041171.
46. Hardie DG, Ross FA, Hawley SA. 2012. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell. Biol. 13: 251-262. http://dx.doi.org/10.1038/nrm3311.
47. Wang L, Wang X, Proud CG. 2000. Activation of mRNA translation by insulin in rat cardiac myocytes by insulin involves multiple rapamycinsensitive steps. Am. J. Physiol. Heart Circ. Physiol. 278:H1056-H1068.
48. Kang SA, Pacold ME, Cervantes CL, Lim D, Lou HJ, Ottina K, Gray NS, Turk BE, Yaffe MB, Sabatini DM. 2013. mTORC1 phosphorylation sites encode their sensitivity to starvation and rapamycin. Science 341:1236566. http://dx.doi.org/10.1126/science.1236566.
49. Schalm SS, Blenis J. 2002. Identification of a conserved motif required for mTOR signaling. Curr. Biol. 12:632-639. http://dx.doi.org/10.1016/S0960-9822(02)00762-5.
50. Taha E, Gildish I, Gal-Ben-Ari S, Rosenblum K. 2013. The role of eEF2 pathway in learning and synaptic plasticity. Neurobiol. Learn. Mem. 105: 100-106. http://dx.doi.org/10.1016/j.nlm.2013.04.015.