Structure of the Yeast DEAD Box Protein Mss116p Reveals Two Wedges that Crimp RNA

Molecular Cell

Volumn 35, Issue 5, 2009, Pages 598-609

  Del Campo, Mark ^a   Lambowitz, Alan M ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

PROTEINS; RNA

Indexed keywords

ADENOSINE TRIPHOSPHATE DERIVATIVE; DEAD BOX PROTEIN; FUNGAL PROTEIN; HELICASE; NUCLEOTIDE; OLIGODEOXYRIBONUCLEOTIDE; RNA; SINGLE STRANDED RNA; TERNARY COMPLEX FACTOR;

ALPHA HELIX; ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; ENZYME CONFORMATION; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NONHUMAN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RNA BINDING; RNA STRUCTURE; X RAY CRYSTALLOGRAPHY; YEAST;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ADENYLYL IMIDODIPHOSPHATE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DEAD-BOX RNA HELICASES; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; ORGANOMETALLIC COMPOUNDS; POLY U; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RNA; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 69749126977     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2009.07.032     Document Type: Article

References (47)

1. Andersen C.B., Ballut L., Johansen J.S., Chamieh H., Nielsen K.H., Oliveira C.L., Pedersen J.S., Séraphin B., Le Hir H., and Andersen G.R. Structure of the exon junction core complex with a trapped DEAD-box ATPase bound to RNA. Science 313 (2006) 1968-1972
2. Baker N.A., Sept D., Joseph S., Holst M.J., and McCammon J.A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. USA 98 (2001) 10037-10041
3. Bhaskaran H., and Russell R. Kinetic redistribution of native and misfolded RNAs by a DEAD-box chaperone. Nature 449 (2007) 1014-1018
4. Bono F., Ebert J., Lorentzen E., and Conti E. The crystal structure of the exon junction complex reveals how it maintains a stable grip on mRNA. Cell 126 (2006) 713-725
5. Chen B., Doucleff M., Wemmer D.E., De Carlo S., Huang H.H., Nogales E., Hoover T.R., Kondrashkina E., Guo L., and Nixon B.T. ATP ground and transition states of bacterial enhancer binding AAA+ ATPases support complex formation with their target protein, sigma54. Structure 15 (2007) 429-440
6. Chen Y., Potratz J.P., Tijerina P., Del Campo M., Lambowitz A.M., and Russell R. DEAD-box proteins can completely separate an RNA duplex using a single ATP. Proc. Natl. Acad. Sci. USA 105 (2008) 20203-20208
7. Collaborative Computational Project, Number 4 (CCP4). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50 (1994) 760-763
8. Collins R., Karlberg T., Lehtiö L., Schütz P., van den Berg S., Dahlgren L.G., Hammarström M., Weigelt J., and Schüler H. The DExD/H-box RNA helicase DDX19 is regulated by an α-helical switch. J. Biol. Chem. 284 (2009) 10296-10300
9. Cordin O., Tanner N.K., Doére M., Linder P., and Banroques J. The newly discovered Q motif of DEAD-box RNA helicases regulates RNA-binding and helicase activity. EMBO J. 23 (2004) 2478-2487
10. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., Wang X., Murray L.W., Arendall III W.B., Snoeyink J., Richardson J.S., et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35 (2007) W375-W383
11. Del Campo M., and Lambowitz A.M. Crystallization and preliminary X-ray diffraction of the DEAD-box protein Mss116p complexed with an RNA oligonucleotide and AMP-PNP. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 65 (2009) 832-835
12. Del Campo M., Tijerina P., Bhaskaran H., Mohr S., Yang Q., Jankowsky E., Russell R., and Lambowitz A.M. Do DEAD-box proteins promote group II intron splicing without unwinding RNA?. Mol. Cell 28 (2007) 159-166
13. Del Campo M., Mohr S., Jiang Y., Jia H., Jankowsky E., and Lambowitz A.M. Unwinding by local strand separation is critical for the function of DEAD-box proteins as RNA chaperones. J. Mol. Biol. 389 (2009) 674-693
14. Dittrich M., and Schulten K. Zooming in on ATP hydrolysis in F1. J. Bioenerg. Biomembr. 37 (2005) 441-444
15. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2126-2132
16. Grohman J.K., Del Campo M., Bhaskaran H., Tijerina P., Lambowitz A.M., and Russell R. Probing the mechanisms of DEAD-box proteins as general RNA chaperones: the C-terminal domain of CYT-19 mediates general recognition of RNA. Biochemistry 46 (2007) 3013-3022
17. Halls C., Mohr S., Del Campo M., Yang Q., Jankowsky E., and Lambowitz A.M. Involvement of DEAD-box proteins in group I and II intron splicing. Biochemical characterization of MSS116p, ATP-hydrolysis-dependent and -independent mechanisms, and general RNA chaperone activity. J. Mol. Biol. 365 (2007) 835-855
18. Holm L., Kääriäinen S., Rosenström P., and Schenkel A. Searching protein structure databases with DaliLite v.3. Bioinformatics 24 (2008) 2780-2781
19. Huang, H.-R. (2004). Functional studies of intron- and nuclear-encoded splicing factors in the mitochondria of Saccharomyces cerevisiae. Ph.D. thesis, University of Texas Southwestern Medical Center, Dallas, Texas.
20. Huang H.-R., Rowe C.E., Mohr S., Jiang Y., Lambowitz A.M., and Perlman P.S. The splicing of yeast mitochondrial group I and group II introns requires a DEAD-box protein with RNA chaperone function. Proc. Natl. Acad. Sci. USA 102 (2005) 163-168
21. Jankowsky E., and Fairman M.E. RNA helicases-one fold for many functions. Curr. Opin. Struct. Biol. 17 (2007) 316-324
22. Krissinel E., and Henrick K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372 (2007) 774-797
23. Langer G., Cohen S.X., Lamzin V.S., and Perrakis A. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protocols 3 (2008) 1171-1179
24. Linder P. Dead-box proteins: a family affair-active and passive players in RNP-remodeling. Nucleic Acids Res. 34 (2006) 4168-4180
25. Liu F., Putnam A., and Jankowsky E. ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding. Proc. Natl. Acad. Sci. USA 105 (2008) 20209-20214
26. Lorsch J.R., and Herschlag D. The DEAD box protein eIF4A. 1. A minimal kinetic and thermodynamic framework reveals coupled binding of RNA and nucleotide. Biochemistry 37 (1998) 2180-2193
27. Lorsch J.R., and Herschlag D. The DEAD box protein eIF4A. 2. A cycle of nucleotide and RNA-dependent conformational changes. Biochemistry 37 (1998) 2194-2206
28. Luo D., Xu T., Watson R.P., Scherer-Becker D., Sampath A., Jahnke W., Yeong S.S., Wang C.H., Lim S.P., Strongin A., et al. Insights into RNA unwinding and ATP hydrolysis by the flavivirus NS3 protein. EMBO J. 27 (2008) 3209-3219
29. Mohr S., Stryker J.M., and Lambowitz A.M. A DEAD-box protein functions as an ATP-dependent RNA chaperone in group I intron splicing. Cell 109 (2002) 769-779
30. Mohr S., Matsuura M., Perlman P.S., and Lambowitz A.M. A DEAD-box protein alone promotes group II intron splicing and reverse splicing by acting as an RNA chaperone. Proc. Natl. Acad. Sci. USA 103 (2006) 3569-3574
31. Mohr G., Del Campo M., Mohr S., Yang Q., Jia H., Jankowsky E., and Lambowitz A.M. Function of the C-terminal domain of the DEAD-box protein Mss116p analyzed in vivo and in vitro. J. Mol. Biol. 375 (2008) 1344-1364
32. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53 (1997) 240-255
33. Nielsen K.H., Chamieh H., Andersen C.B., Fredslund F., Hamborg K., Le Hir H., and Andersen G.R. Mechanism of ATP turnover inhibition in the EJC. RNA 15 (2009) 67-75
34. Noble C.G., and Song H. MLN51 stimulates the RNA-helicase activity of eIF4AIII. PLoS ONE 2 (2007) e303 10.1371/journal.pone.0000303
35. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
36. Polach K.J., and Uhlenbeck O.C. Cooperative binding of ATP and RNA substrates to the DEAD/H protein DbpA. Biochemistry 41 (2002) 3693-3702
37. Schütz P., Bumann M., Oberholzer A.E., Bieniossek C., Trachsel H., Altmann M., and Baumann U. Crystal structure of the yeast eIF4A-eIF4G complex: an RNA-helicase controlled by protein-protein interactions. Proc. Natl. Acad. Sci. USA 105 (2008) 9564-9569
38. Sengoku T., Nureki O., Nakamura A., Kobayashi S., and Yokoyama S. Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 125 (2006) 287-300
39. Silverman E., Edwalds-Gilbert G., and Lin R.J. DExD/H-box proteins and their partners: helping RNA helicases unwind. Gene 312 (2003) 1-16
40. Solem A., Zingler N., and Pyle A.M. A DEAD protein that activates intron self-splicing without unwinding RNA. Mol. Cell 24 (2006) 611-617
41. Studier F.W. Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41 (2005) 207-234
42. Theissen B., Karow A.R., Kohler J., Gubaev A., and Klostermeier D. Cooperative binding of ATP and RNA induces a closed conformation in a DEAD box RNA helicase. Proc. Natl. Acad. Sci. USA 105 (2008) 548-553
43. Tijerina P., Bhaskaran H., and Russell R. Nonspecific binding to structured RNA and preferential unwinding of an exposed helix by the CYT-19 protein, a DEAD-box RNA chaperone. Proc. Natl. Acad. Sci. USA 103 (2006) 16698-16703
44. von Moeller H., Basquin C., and Conti E. The mRNA export protein DBP5 binds RNA and the cytoplasmic nucleoporin NUP214 in a mutually exclusive manner. Nat. Struct. Mol. Biol. 16 (2009) 247-254
45. Vonrhein C., Blanc E., Roversi P., and Bricogne G. Automated structure solution with autoSHARP. Methods Mol. Biol. 364 (2007) 215-230
46. Yang Q., and Jankowsky E. The DEAD-box protein Ded1 unwinds RNA duplexes by a mode distinct from translocating helicases. Nat. Struct. Mol. Biol. 13 (2006) 981-986
47. Yang Q., Del Campo M., Lambowitz A.M., and Jankowsky E. DEAD-box proteins unwind duplexes by local strand separation. Mol. Cell 28 (2007) 253-263