Mechanism of ATP turnover inhibition in the EJC

RNA

Volumn 15, Issue 1, 2009, Pages 67-75

  Nielsen, Klaus H ^a   Chamieh, Hala ^b   Andersen, Christian B F ^a   Fredslund, Folmer ^a   Hamborg, Kristiane ^a   Le Hir, Hervé ^b   Andersen, Gregers R ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b CENTRE DE GÉNÉTIQUE MOLÉCULAIRE   (France)

Author keywords

AlF; DEAD box ATPase; EJC; mRNP; Transition state

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; DEAD BOX PROTEIN; EXON JUNCTION COMPLEX; INITIATION FACTOR 4A; MESSENGER RNA; RNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; NONHUMAN; PRIORITY JOURNAL; RNA BINDING;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DEAD-BOX RNA HELICASES; EUKARYOTIC INITIATION FACTOR-4A; EXONS; HYDROLYSIS; MODELS, MOLECULAR; NUCLEAR PROTEINS; PROTEIN CONFORMATION; RIBONUCLEOPROTEINS; RNA HELICASES;

EID: 58149092125     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1283109     Document Type: Article

References (47)

1. Adams, P.D., Grosse-Kunstleve, R.W., Hung, L.W., Ioerger, T.R., McCoy, A.J., Moriarty, N.W., Read, R.J., Sacchettini, J.C., Sauter, N.K., and Terwilliger, T.C. 2002. PHENIX: Building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58: 1948-1954.
2. Andersen, C.B.F., Ballut, L., Johansen, J.S., Chamieh, H., Nielsen, K.H., Oliveira, C., Pedersen, J.S., Seraphin, B., Le Hir, H., and Andersen, G.R. 2006. Structure of the exon junction core complex with a trapped DEAD-box ATPase bound to RNA. Science 313: 1968-1972.
3. Ballut, L., Marchadier, B., Baguet, A., Tomasetto, C., Seraphin, B., and Le Hir, H. 2005. The exon junction core complex is locked onto RNA by inhibition of eIF4AIII ATPase activity. Nat. Struct. Mol. Biol. 12: 861-869.
4. Bizebard, T., Ferlenghi, I., Iost, I., and Dreyfus, M. 2004. Studies on three E. coli DEAD-box helicases point to an unwinding mechanism different from that of model DNA helicases. Biochemistry 43: 7857-7866.
5. Bono, F., Ebert, J., Lorentzen, E., and Conti, E. 2006. The crystal structure of the exon junction complex reveals how it maintains a stable grip on mRNA. Cell 126: 713-725.
6. 2+ ADP and aluminium fluoride. Structure 8: 567-573.
7. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.-S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. 1998. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54: 905-921.
8. Caruthers, J.M. and McKay, D.B. 2002. Helicase structure and mechanism. Curr. Opin. Struct. Biol. 12: 123-133.
9. Coleman, D.E., Berghuis, A.M., Lee, E., Linder, M.E., Gilman, A.G., and Sprang, S.R. 1994. Structures of active conformations of Gi α 1 and the mechanism of GTP hydrolysis. Science 265: 1405-1412.
10. Cordin, O., Banroques, J., Tanner, N.K., and Linder, P. 2006. The DEAD-box protein family of RNA helicases. Gene 367: 17-37.
11. DeLano, W.L. 2002. The PyMOL user's manual. DeLano Scientific, San Carlos, CA.
12. Fairman, M.E., Maroney, P.A., Wang, W., Bowers, H.A., Gollnick, P., Nilsen, T.W., and Jankowsky, E. 2004. Protein displacement by DExH/D "RNA helicases" without duplex unwinding. Science 304: 730-734.
13. - as a transition state analog of phosphoryl transfer. Chem. Biol. 9: 375-381.
14. Henn, A., Cao, W., Hackney, D.D., and De La Cruz, E.M. 2008. The ATPase cycle mechanism of the DEAD-box rRNA helicase, DbpA. J. Mol. Biol. 377: 193-205.
15. Jankowsky, E., Gross, C.H., Shuman, S., and Pyle, A.M. 2001. Active disruption of an RNA-protein interaction by a DExH/D RNA helicase. Science 291: 121-125.
16. Jones, T.A., Cowan, S., Zou, J.-Y., and Kjeldgaard, M. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47: 110-119.
17. Kabsch, W. 2001. XDS. In International tables for crystallography (eds. M.G. Rossmann and E. Arnold), chap. 25.22.29. Kluwer Academic Publishers, Dordrecht, The Netherlands.
18. Kagawa, R., Montgomery, M.G., Braig, K., Leslie, A.G., and Walker, J.E. 2004. The structure of bovine F1-ATPase inhibited by ADP and beryllium fluoride. EMBO J. 23: 2734-2744.
19. Lee, J.Y. and Yang, W. 2006. UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke. Cell 127: 1349-1360.
20. Le Hir, H. and Andersen, G.R. 2008. Structural insights into the exon junction complex. Curr. Opin. Struct. Biol. 18: 112-119.
21. Le Hir, H., Izaurralde, E., Maquat, L.E., and Moore, M.J. 2000. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 19: 6860-6869.
22. Lund, M.K. and Guthrie, C. 2005. The DEAD-box protein Dbp5p is required to dissociate Mex67p from exported mRNPs at the nuclear rim. Mol. Cell 20: 645-651.
23. Menz, R.I., Walker, J.E., and Leslie, A.G. 2001. Structure of bovine mitochondrial F(1)-ATPase with nucleotide bound to all three catalytic sites: Implications for the mechanism of rotary catalysis. Cell 106: 331-341.
24. Nassar, N., Hoffman, G.R., Manor, D., Clardy, J.C., and Cerione, R.A. 1998. Structures of Cdc42 bound to the active and catalytically compromised forms of Cdc42GAP. Nat. Struct. Biol. 5: 1047-1052.
25. Noble, C.G. and Song, H. 2007. MLN51 stimulates the RNA-helicase activity of eIF4AIII. PLoS One 2: e303. doi: 10.1371/journal.pone.0000303.
26. Pan, X., Eathiraj, S., Munson, M., and Lambright, D.G. 2006. TBC-domain GAPs for Rab GTPases accelerate GTP hydrolysis by a dual-finger mechanism. Nature 442: 303-306.
27. Ray, B.K., Lawson, T.G., Kramer, J.C., Cladaras, M.H., Grifo, J.A., Abramson, R.D., Merrick, W.C., and Thach, R.E. 1985. ATP-dependent unwinding of messenger RNA structure by eukaryotic initiation factors. J. Biol. Chem. 260: 7651-7658.
28. Rogers Jr., G.W., Richter, N.J., and Merrick, W.C. 1999. Biochemical and kinetic characterization of the RNA helicase activity of eukaryotic initiation factor 4A. J. Biol. Chem. 274: 12236-12244.
29. Rozen, F., Edery, I., Meerovitch, K., Dever, T.E., Merrick, W.C., and Sonenberg, N. 1990. Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F. Mol. Cell. Biol. 10: 1134-1144.
30. Scheffzek, K., Ahmadian, M.R., Kabsch, W., Wiesmuller, L., Lautwein, A., Schmitz, F., and Wittinghofer, A. 1997. The Ras-RasGAP complex: Structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 277: 333-338.
31. Scrima, A. and Wittinghofer, A. 2006. Dimerization-dependent GTPase reaction of MnmE: How potassium acts as GTPase-activating element. EMBO J. 25: 2940-2951.
32. Sengoku, T., Noreki, O., Nakamura, A., Kobayashi, S., and Shigeyuki, Y. 2006. Structural basis for RNA unwinding by the DEAD-box protein Drosophila vasa. Cell 125: 287-300.
33. Shu, Z., Vijayakumar, S., Chen, C.F., Chen, P.L., and Lee, W.H. 2004. Purified human SUV3p exhibits multiple-substrate unwinding activity upon conformational change. Biochemistry 43: 4781-4790.
34. Singleton, M.R. and Wigley, D.B. 2002. Modularity and specialization in superfamily 1 and 2 helicases. J. Bacteriol. 184: 1819-1826.
35. Snay-Hodge, C., Colot, H., Goldstein, A., and Cole, C. 1998. Dbp5p/Rat8p is a yeast nuclear pore-associated DEAD-box protein essential for RNA export. EMBO J. 17: 2663-2676.
36. Stebbins, C.E. and Galan, J.E. 2000. Modulation of host signaling by a bacterial mimic: Structure of the Salmonella effector SptP bound to Rac1. Mol. Cell 6: 1449-1460.
37. Storoni, L.C., McCoy, A.J., and Read, R.J. 2004. Likelihood-enhanced fast rotation functions. Acta Crystallogr. D Biol. Crystallogr. 60: 432-438.
38. Svitkin, Y.V., Pause, A., Haghighat, A., Pyronnet, S., Witherell, G., Belsham, G.J., and Sonenberg, N. 2001. The requirement for eukaryotic initiation factor 4A (elF4A) in translation is in direct proportion to the degree of mRNA 5′ secondary structure. RNA 7: 382-394.
39. Tange, T.O., Nott, A., and Moore, M.J. 2004. The ever-increasing complexities of the exon junction complex. Curr. Opin. Cell Biol. 16: 279-284.
40. Tran, E.J., Zhou, Y., Corbett, A.H., and Wente, S.R. 2007. The DEAD-box protein Dbp5 controls mRNA export by triggering specific RNA:protein remodeling events. Mol. Cell 28: 850-859.
41. Velankar, S.S., Soultanas, P., Dillingham, M.S., Subramanya, H.S., and Wigley, D.B. 1999. Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell 97: 75-84.
42. Wagner, J.D., Jankowsky, E., Company, M., Pyle, A.M., and Abelson, J.N. 1998. The DEAH-box protein PRP22 is an ATPase that mediates ATP-dependent mRNA release from the spliceosome and unwinds RNA duplexes. EMBO J. 17: 2926-2937.
43. Weirich, C.S., Erzberger, J.P., Flick, J.S., Berger, J.M., Thorner, J., and Weis, K. 2006. Activation of the DExD/H-box protein Dbp5 by the nuclear-pore protein Gle1 and its coactivator InsP6 is required for mRNA export. Nat. Cell Biol. 8: 668-676.
44. Wittinghofer, A. 2006. Phosphoryl transfer in Ras proteins, conclusive or elusive? Trends Biochem. Sci. 31: 20-23.
45. Wurtele, M., Wolf, E., Pederson, K.J., Buchwald, G., Ahmadian, M.R., Barbieri, J.T., and Wittinghofer, A. 2001. How the Pseudomonas aeruginosa ExoS toxin downregulates Rac. Nat. Struct. Biol. 8: 23-26.
46. Yang, Q. and Jankowsky, E. 2005. ATP- and ADP-dependent modulation of RNA unwinding and strand annealing activities by the DEAD-box protein DED1. Biochemistry 44: 13591-13601.
47. Yang, Q. and Jankowsky, E. 2006. The DEAD-box protein Ded1 unwinds RNA duplexes by a mode distinct from translocating helicases. Nat. Struct. Mol. Biol. 13: 981-986.