A conserved loop in the catalytic domain of eukaryotic elongation factor 2 kinase plays a key role in its substrate specificity

Molecular and Cellular Biology

Volumn 34, Issue 12, 2014, Pages 2294-2307

  Moore, Claire E ^a   Da Mota, Sergio Regufe ^a   Mikolajek, Halina ^a   Proud, Christopher G ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR 2 KINASE; MYOSIN HEAVY CHAIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL M7;

ARTICLE; AUTOPHOSPHORYLATION; CELL PROTECTION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; EMBRYO; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; GENE MUTATION; HUMAN; HUMAN CELL; HYDROGEN BOND; IN VITRO STUDY; MOLECULAR DOCKING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; WESTERN BLOTTING;

AMINO ACID SEQUENCE; AMINO ACIDS; BINDING SITES; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASES; CATALYTIC DOMAIN; CONSERVED SEQUENCE; ELONGATION FACTOR 2 KINASE; HEK293 CELLS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NEOPLASMS; PHOSPHORYLATION; PHOSPHOTHREONINE; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTOZOAN PROTEINS; STRUCTURAL HOMOLOGY, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 84901318578     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00388-14     Document Type: Article

References (29)

1. Middelbeek J, Clark K, Venselaar H, Huynen MA, van Leeuwen FN. 2010. The alpha-kinase family: an exceptional branch on the protein kinase tree. Cell Mol. Life Sci. 67:875-890. http://dx.doi.org/10.1007/s00018-009-0215-z.
2. 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.
3. Yamaguchi H, Matsushita M, Nairn AC, Kuriyan J. 2001. Crystal structure of the atypical protein kinase domain of a TRP channel with phosphotransferase activity. Mol. Cell 7:1047-1057. http://dx.doi.org/10.1016/S1097-2765(01)00256-8.
4. Ye Q, Crawley SW, Yang Y, Cote GP, Jia Z. 2010. Crystal structure of the alpha-kinase domain of Dictyostelium myosin heavy chain kinase A. Sci. Signal. 3:ra17. http://dx.doi.org/10.1126/scisignal.2000525.
5. Proud CG. 2007. Signalling to translation: how signal transduction pathways control the protein synthetic machinery. Biochem. J. 403:217-234. http://dx.doi.org/10.1042/BJ20070024.
6. Drennan D, Ryazanov AG. 2004. Alpha-kinases: analysis of the family and comparison with conventional protein kinases. Prog. Biophys. Mol. Biol. 85:1-32. http://dx.doi.org/10.1016/S0079-6107(03)00060-9.
7. 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.
8. 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.
9. Pigott CR, Mikolajek H, Moore CE, Finn SJ, Phippen CW, Werner JM, Proud CG. 2012. 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.
10. Clark K, Middelbeek J, Morrice NA, Figdor CG, Lasonder E, van Leeuwen FN. 2008. Massive autophosphorylation of the Ser/Thr-rich domain controls protein kinase activity of TRPM6 and TRPM7. PLoS One. 3(3):e1876. http://dx.doi.org/10.1371/journal.pone.0001876.
11. Crawley SW, Gharaei MS, Ye Q, Yang Y, Raveh B, London N, Schueler-Furman O, Jia Z, Cote GP. 2011. Autophosphorylation activates Dictyostelium myosin II heavy chain kinase A by providing a ligand for an allosteric binding site in the alpha-kinase domain. J. Biol. Chem. 286:2607-2616. http://dx.doi.org/10.1074/jbc.M110.177014.
12. 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.
13. Pyr Dit Ruys S, 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.
14. 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.
15. Tavares CD, O'Brien JP, Abramczyk O, Devkota AK, Shores KS, Ferguson SB, Kaoud TS, Warthaka M, Marshall KD, Keller KM, Zhang Y, Brodbelt JS, Ozpolat B, Dalby KN. 2012. Calcium/calmodulin stimulates the autophosphorylation of elongation factor 2 kinase on Thr-348 and Ser-500 to regulate its activity and calcium dependence. Biochemistry 51: 2232-2245. http://dx.doi.org/10.1021/bi201788e.
16. Crawley SW, Cote GP. 2008. Determinants for substrate phosphorylation by Dictyostelium myosin II heavy chain kinases A and B and eukaryotic elongation factor-2 kinase. Biochim. Biophys. Acta 1784:908-915. http://dx.doi.org/10.1016/j.bbapap.2008.03.001.
17. 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.
18. Eswar N, John B, Mirkovic N, Fiser A, Ilyin VA, Pieper U, Stuart AC, Marti-Renom MA, Madhusudhan MS, Yerkovich B, Sali A. 2003. Tools for comparative protein structure modeling and analysis. Nucleic Acids Res. 31:3375-3380. http://dx.doi.org/10.1093/nar/gkg543.
19. Pieper U, Webb BM, Barkan DT, Schneidman-Duhovny D, Schlessinger A, Braberg H, Yang Z, Meng EC, Pettersen EF, Huang CC, Datta RS, Sampathkumar P, Madhusudhan MS, Sjolander K, Ferrin TE, Burley SK, Sali A. 2011. ModBase, a database of annotated comparative protein structure models, and associated resources. Nucleic Acids Res. 39:D465-D474. http://dx.doi.org/10.1093/nar/gkt1091.
20. Eswar N, Eramian D, Webb B, Shen MY, Sali A. 2008. Protein structure modeling with MODELLER. Methods Mol. Biol. 426:145-159. http://dx.doi.org/10.1007/978-1-60327-058-8_8.
21. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612. http://dx.doi.org/10.1002/jcc.20084.
22. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
23. Hall-Jackson CA, Cross DA, Morrice N, Smythe C. 1999. ATR is a caffeine-sensitive, DNA-activated protein kinase with a substrate specificity distinct from DNA-PK. Oncogene 18:6707-6713.
24. 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.
25. Schmidt EK, Clavarino G, Ceppi M, Pierre P. 2009. SUnSET, a nonradioactive method to monitor protein synthesis. Nat. Methods 6:275-277. http://dx.doi.org/10.1038/nmeth.1314.
26. Matsushita M, Kozak JA, Shimizu Y, McLachlin DT, Yamaguchi H, Wei FY, Tomizawa K, Matsui H, Chait BT, Cahalan MD, Nairn AC. 2005. Channel function is dissociated from the intrinsic kinase activity and autophosphorylation of TRPM7/ChaK1. J. Biol. Chem. 280:20793-20803. http://dx.doi.org/10.1074/jbc.M413671200.
27. Kruiswijk F, Yuniati L, Magliozzi R, Low TY, Lim R, Bolder R, Mohammed S, Proud CG, Heck AJ, Pagano M, Guardavaccaro D. 2012. Coupled activation and degradation of eEF2K regulates protein synthesis in response to genotoxic stress. Sci. Signal. 5:ra40. http://dx.doi.org/10.1126/scisignal.2002718.
28. 2+/calmodulin-independent activity. Biochem. J. 353:621- 626.
29. Price NT, Redpath NT, Severinov KV, Campbell DG, Russell JM, Proud CG. 1991. Identification of the phosphorylation sites in elongation factor-2 from rabbit reticulocytes. FEBS Lett. 282:253-258. http://dx.doi.org/10.1016/0014-5793(91)80489-P.