Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 30 April 2004:
Vol. 304. no. 5671, pp. 730 - 734
DOI: 10.1126/science.1095596
Prev | Table of Contents | Next

Reports

Protein Displacement by DExH/D "RNA Helicases" Without Duplex Unwinding

Margaret E. Fairman,1* Patricia A. Maroney,2* Wen Wang,1 Heath A. Bowers,1 Paul Gollnick,3 Timothy W. Nilsen,2{dagger} Eckhard Jankowsky1,2{dagger}

Members of the DExH/D superfamily of nucleic acid–activated nucleotide triphosphatases are essential for virtually all aspects of RNA metabolism, including pre–messenger RNA splicing, RNA interference, translation, and nucleocytoplasmic trafficking. Physiological substrates for these enzymes are thought to be regions of double-stranded RNA, because several DExH/D proteins catalyze strand separation in vitro. These "RNA helicases" can also disrupt RNA-protein interactions, but it is unclear whether this activity is coupled to duplex unwinding. Here we demonstrate that two unrelated DExH/D proteins catalyze protein displacement independently of duplex unwinding. Therefore, the essential functions of DExH/D proteins are not confined to RNA duplexes but can be exerted on a wide range of ribonucleoprotein substrates.

1 Department of Biochemistry, School of Medicine, Case Western Reserve University, Cleveland, OH 44106, USA.
2 The Center for RNA Molecular Biology, School of Medicine, Case Western Reserve University, Cleveland, OH 44106, USA.
3 Department of Biological Sciences, State University of New York at Buffalo, Buffalo, NY 14260, USA.


* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: exj13{at}po.cwru.edu (E.J.); twn{at}po.cwru.edu (T.W.N.)

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Human DDX3 functions in translation and interacts with the translation initiation factor eIF3.
C.-S. Lee, A. P. Dias, M. Jedrychowski, A. H. Patel, J. L. Hsu, and R. Reed (2008)
Nucleic Acids Res. 36, 4708-4718
   Abstract »    Full Text »    PDF »
Distinct activities of the DExD/H-box splicing factor hUAP56 facilitate stepwise assembly of the spliceosome.
H. Shen, X. Zheng, J. Shen, L. Zhang, R. Zhao, and M. R. Green (2008)
Genes & Dev. 22, 1796-1803
   Abstract »    Full Text »    PDF »
Cylindrical inclusion protein of potato virus A is associated with a subpopulation of particles isolated from infected plants.
R. Gabrenaite-Verkhovskaya, I. A. Andreev, N. O. Kalinina, L. Torrance, M. E. Taliansky, and K. Makinen (2008)
J. Gen. Virol. 89, 829-838
   Abstract »    Full Text »    PDF »
The MLE Subunit of the Drosophila MSL Complex Uses Its ATPase Activity for Dosage Compensation and Its Helicase Activity for Targeting.
R. Morra, E. R. Smith, R. Yokoyama, and J. C. Lucchesi (2008)
Mol. Cell. Biol. 28, 958-966
   Abstract »    Full Text »    PDF »
Cooperative binding of ATP and RNA induces a closed conformation in a DEAD box RNA helicase.
B. Theissen, A. R. Karow, J. Kohler, A. Gubaev, and D. Klostermeier (2008)
PNAS 105, 548-553
   Abstract »    Full Text »    PDF »
Biochemical Characterization of the ATPase and Helicase Activity of UAP56, an Essential Pre-mRNA Splicing and mRNA Export Factor.
J. Shen, L. Zhang, and R. Zhao (2007)
J. Biol. Chem. 282, 22544-22550
   Abstract »    Full Text »    PDF »
Distinct Induction Patterns and Functions of Two Closely Related Interferon-inducible Human Genes, ISG54 and ISG56.
F. Terenzi, D. J. Hui, W. C. Merrick, and G. C. Sen (2006)
J. Biol. Chem. 281, 34064-34071
   Abstract »    Full Text »    PDF »
Nonspecific binding to structured RNA and preferential unwinding of an exposed helix by the CYT-19 protein, a DEAD-box RNA chaperone.
P. Tijerina, H. Bhaskaran, and R. Russell (2006)
PNAS 103, 16698-16703
   Abstract »    Full Text »    PDF »
Structure of the Exon Junction Core Complex with a Trapped DEAD-Box ATPase Bound to RNA.
C. B. F. Andersen, L. Ballut, J. S. Johansen, H. Chamieh, K. H. Nielsen, C. L. P. Oliveira, J. S. Pedersen, B. Seraphin, H. L. Hir, and G. R. Andersen (2006)
Science 313, 1968-1972
   Abstract »    Full Text »    PDF »
Remodeling of ribonucleoprotein complexes with DExH/D RNA helicases.
E. Jankowsky and H. Bowers (2006)
Nucleic Acids Res. 34, 4181-4188
   Abstract »    Full Text »    PDF »
DExD/H box RNA helicases: multifunctional proteins with important roles in transcriptional regulation.
F. V. Fuller-Pace (2006)
Nucleic Acids Res. 34, 4206-4215
   Abstract »    Full Text »    PDF »
DEAD-box RNA helicases in Escherichia coli.
I. Iost and M. Dreyfus (2006)
Nucleic Acids Res. 34, 4189-4197
   Abstract »    Full Text »    PDF »
DNA unwinding and protein displacement by superfamily 1 and superfamily 2 helicases.
S. G. Mackintosh and K. D. Raney (2006)
Nucleic Acids Res. 34, 4154-4159
   Abstract »    Full Text »    PDF »
The network of protein-protein interactions within the human U4/U6.U5 tri-snRNP.
S. Liu, R. Rauhut, H.-P. Vornlocher, and R. Luhrmann (2006)
RNA 12, 1418-1430
   Abstract »    Full Text »    PDF »
Genomic localization of RNA binding proteins reveals links between pre-mRNA processing and transcription.
I. A. Swinburne, C. A. Meyer, X. S. Liu, P. A. Silver, and A. S. Brodsky (2006)
Genome Res. 16, 912-921
   Abstract »    Full Text »    PDF »
RNA helicases and abiotic stress.
G. W. Owttrim (2006)
Nucleic Acids Res. 34, 3220-3230
   Abstract »    Full Text »    PDF »
Xp54 and related (DDX6-like) RNA helicases: roles in messenger RNP assembly, translation regulation and RNA degradation.
A. Weston and J. Sommerville (2006)
Nucleic Acids Res. 34, 3082-3094
   Abstract »    Full Text »    PDF »
The nucleolar protein Esf2 interacts directly with the DExD/H box RNA helicase, Dbp8, to stimulate ATP hydrolysis.
S. Granneman, C. Lin, E. A. Champion, M. R. Nandineni, C. Zorca, and S. J. Baserga (2006)
Nucleic Acids Res. 34, 3189-3199
   Abstract »    Full Text »    PDF »
Salt Stress in Desulfovibrio vulgaris Hildenborough: an Integrated Genomics Approach.
A. Mukhopadhyay, Z. He, E. J. Alm, A. P. Arkin, E. E. Baidoo, S. C. Borglin, W. Chen, T. C. Hazen, Q. He, H.-Y. Holman, et al. (2006)
J. Bacteriol. 188, 4068-4078
   Abstract »    Full Text »    PDF »
Displacement of a DNA binding protein by Dda helicase.
A. K. Byrd and K. D. Raney (2006)
Nucleic Acids Res. 34, 3020-3029
   Abstract »    Full Text »    PDF »
Double-stranded RNA Is Internalized by Scavenger Receptor-mediated Endocytosis in Drosophila S2 Cells.
J. Ulvila, M. Parikka, A. Kleino, R. Sormunen, R. A. Ezekowitz, C. Kocks, and M. Ramet (2006)
J. Biol. Chem. 281, 14370-14375
   Abstract »    Full Text »    PDF »
A Novel Ded1-like RNA Helicase Interacts with the Y-box Protein ctYB-1 in Nuclear mRNP Particles and in Polysomes.
D. Nashchekin, J. Zhao, N. Visa, and B. Daneholt (2006)
J. Biol. Chem. 281, 14263-14272
   Abstract »    Full Text »    PDF »
Discriminatory RNP remodeling by the DEAD-box protein DED1.
H. A. Bowers, P. A. Maroney, M. E. Fairman, B. Kastner, R. Luhrmann, T. W. Nilsen, and E. Jankowsky (2006)
RNA 12, 903-912
   Abstract »    Full Text »    PDF »
Mutational analysis of human eIF4AIII identifies regions necessary for exon junction complex formation and nonsense-mediated mRNA decay..
T. SHIBUYA, T. O. TANGE, M. E. STROUPE, and M. J. MOORE (2006)
RNA 12, 360-374
   Abstract »    Full Text »    PDF »
Comprehensive Mutational Analysis of Yeast DEXD/H Box RNA Helicases Involved in Large Ribosomal Subunit Biogenesis.
K. A. Bernstein, S. Granneman, A. V. Lee, S. Manickam, and S. J. Baserga (2006)
Mol. Cell. Biol. 26, 1195-1208
   Abstract »    Full Text »    PDF »
Prp43p Is a DEAH-Box Spliceosome Disassembly Factor Essential for Ribosome Biogenesis.
D. J. Combs, R. J. Nagel, M. Ares Jr., and S. W. Stevens (2006)
Mol. Cell. Biol. 26, 523-534
   Abstract »    Full Text »    PDF »
Ddx42p--a human DEAD box protein with RNA chaperone activities.
H. Uhlmann-Schiffler, C. Jalal, and H. Stahl (2006)
Nucleic Acids Res. 34, 10-22
   Abstract »    Full Text »    PDF »
Structure of Dicer and Mechanistic Implications for RNAi.
I.J. MacRAE, F. LI, K. ZHOU, W.Z. CANDE, and J.A. DOUDNA (2006)
Cold Spring Harb Symp Quant Biol 71, 73-80
   Abstract »    PDF »
An obligate intermediate along the slow folding pathway of a group II intron ribozyme.
L. J. Su, C. Waldsich, and A. M. Pyle (2005)
Nucleic Acids Res. 33, 6674-6687
   Abstract »    Full Text »    PDF »
Brome Mosaic Virus 1a Nucleoside Triphosphatase/Helicase Domain Plays Crucial Roles in Recruiting RNA Replication Templates.
X. Wang, W.-M. Lee, T. Watanabe, M. Schwartz, M. Janda, and P. Ahlquist (2005)
J. Virol. 79, 13747-13758
   Abstract »    Full Text »    PDF »
YxiN Is a Modular Protein Combining a DExD/H Core and a Specific RNA-binding Domain.
F. V. Karginov, J. M. Caruthers, Y. Hu, D. B. McKay, and O. C. Uhlenbeck (2005)
J. Biol. Chem. 280, 35499-35505
   Abstract »    Full Text »    PDF »
Crystal structure and functional analysis of DEAD-box protein Dhh1p.
Z. CHENG, J. COLLER, R. PARKER, and H. SONG (2005)
RNA 11, 1258-1270
   Abstract »    Full Text »    PDF »
Stimulation of mammalian translation initiation factor eIF4A activity by a small molecule inhibitor of eukaryotic translation.
M.-E. Bordeleau, J. Matthews, J. M. Wojnar, L. Lindqvist, O. Novac, E. Jankowsky, N. Sonenberg, P. Northcote, P. Teesdale-Spittle, and J. Pelletier (2005)
PNAS 102, 10460-10465
   Abstract »    Full Text »    PDF »
Physical and Genetic Interactions Link the Yeast Protein Zds1p with mRNA Nuclear Export.
F. Estruch, C. A. Hodge, S. Rodriguez-Navarro, and C. N. Cole (2005)
J. Biol. Chem. 280, 9691-9697
   Abstract »    Full Text »    PDF »
Choosing between DNA and RNA: the polymer specificity of RNA helicase NPH-II.
J. Kawaoka and A. M. Pyle (2005)
Nucleic Acids Res. 33, 644-649
   Abstract »    Full Text »    PDF »
The splicing of yeast mitochondrial group I and group II introns requires a DEAD-box protein with RNA chaperone function.
H.-R. Huang, C. E. Rowe, S. Mohr, Y. Jiang, A. M. Lambowitz, and P. S. Perlman (2005)
PNAS 102, 163-168
   Abstract »    Full Text »    PDF »
Effects of the U1C L13 mutation and temperature regulation of yeast commitment complex formation.
H. Du, D. F. Tardiff, M. J. Moore, and M. Rosbash (2004)
PNAS 101, 14841-14846
   Abstract »    Full Text »    PDF »
Complex cis-elements determine an RNA editing site in pea mitochondria.
M. Takenaka, J. Neuwirt, and A. Brennicke (2004)
Nucleic Acids Res. 32, 4137-4144
   Abstract »    Full Text »    PDF »


ADVERTISEMENT
Click Me!

ADVERTISEMENT
Click Me!

To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)