Recognition of two distinct elements in the RNA substrate by the RNA-binding domain of the T. thermophilus DEAD box helicase Hera

Nucleic Acids Research

Volumn 41, Issue 12, 2013, Pages 6259-6272

  Steimer, Lenz ^a   Wurm, Jan Philip ^b   Linden, Martin H ^c,e   Rudolph, Markus G ^d   Wöhnert, Jens ^b   Klostermeier, Dagmar ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY OF BASEL   (Switzerland)

^d F HOFFMANN LA ROCHE LTD   (Switzerland)

^e German Institute of Food Technologies   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DEAD BOX PROTEIN; DOUBLE STRANDED RNA; HEAT RESISTANT RNA DEPENDENT ATPASE; SINGLE STRANDED RNA; UNCLASSIFIED DRUG;

ALPHA HELIX; ANISOTROPY; ARTICLE; BACILLUS SUBTILIS; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; FLUORESCENCE ANALYSIS; GENE DUPLICATION; GENE MAPPING; MOLECULAR RECOGNITION; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN RNA BINDING; PROTON NUCLEAR MAGNETIC RESONANCE; RNA ANALYSIS; RNA BINDING DOMAIN; SEQUENCE ANALYSIS; STRUCTURAL HOMOLOGY; THERMUS THERMOPHILUS; X RAY CRYSTALLOGRAPHY;

BACTERIAL PROTEINS; BINDING SITES; DEAD-BOX RNA HELICASES; MODELS, MOLECULAR; MUTATION; PROTEIN STRUCTURE, TERTIARY; RNA; THERMUS THERMOPHILUS;

EID: 84880247736     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt323     Document Type: Article

References (42)

1. Hilbert, M., Karow, A.R. and Klostermeier, D. (2009) The mechanism of ATP-dependent RNA unwinding by DEAD box proteins. Biol. Chem., 390, 1237-1250.
2. Linder, P. and Jankowsky, E. (2011) From unwinding to clamping-the DEAD box RNA helicase family. Nat. Rev. Mol. Cell Biol., 12, 505-516.
3. Collins, R., Karlberg, T., Lehtio, L., Schutz, P., van den Berg, S., Dahlgren, L.G., Hammarstrom, M., Weigelt, J. and Schuler, H. (2009) The DExD/H-box RNA helicase DDX19 is regulated by an alpha-helical switch. J. Biol. Chem., 284, 10296-10300.
4. Fan, J.S., Cheng, Z., Zhang, J., Noble, C., Zhou, Z., Song, H. and Yang, D. (2009) Solution and crystal structures of mRNA exporter Dbp5p and its interaction with nucleotides. J. Mol. Biol., 388, 1-10.
5. Napetschnig, J., Kassube, S.A., Debler, E.W., Wong, R.W., Blobel, G. and Hoelz, A. (2009) Structural and functional analysis of the interaction between the nucleoporin Nup214 and the DEAD-box helicase Ddx19. Proc. Natl Acad. Sci. USA, 106, 3089-3094.
6. von Moeller, H., Basquin, C. and Conti, E. (2009) The mRNA export protein DBP5 binds RNA and the cytoplasmic nucleoporin NUP214 in a mutually exclusive manner. Nat. Struct. Mol. Biol., 16, 247-254.
7. Linden, M.H., Hartmann, R.K. and Klostermeier, D. (2008) The putative RNase P motif in the DEAD box helicase Hera is dispensable for efficient interaction with RNA and helicase activity. Nucleic Acids Res., 36, 5800-5811.
8. Yan, X., Mouillet, J.F., Ou, Q. and Sadovsky, Y. (2003) A novel domain within the DEAD-box protein DP103 is essential for transcriptional repression and helicase activity. Mol. Cell. Biol., 23, 414-423.
9. Pugh, G.E., Nicol, S.M. and Fuller-Pace, F.V. (1999) Interaction of the Escherichia coli DEAD box protein DbpA with 23 S ribosomal RNA. J. Mol. Biol., 292, 771-778.
10. Karginov, F.V., Caruthers, J.M., Hu, Y., McKay, D.B. and Uhlenbeck, O.C. (2005) YxiN is a modular protein combining a DEx(D/H) core and a specific RNA-binding domain. J. Biol. Chem., 280, 35499-35505.
11. Kossen, K., Karginov, F.V. and Uhlenbeck, O.C. (2002) The carboxy-terminal domain of the DExDH protein YxiN is sufficient to confer specificity for 23S rRNA. J. Mol. Biol., 324, 625-636.
12. Tijerina, P., Bhaskaran, H. and Russell, R. (2006) 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, 16698-16703.
13. Del Campo, M. and Lambowitz, A.M. (2009) Structure of the Yeast DEAD-Box Protein Mss116p Reveals Two Wedges that Crimp RNA. Mol. Cell, 35, 598-609.
14. Morlang, S., Weglohner, W. and Franceschi, F. (1999) Hera from Thermus thermophilus: the first thermostable DEAD-box helicase with an RNase P protein motif. J. Mol. Biol., 294, 795-805.
15. Rudolph, M.G. and Klostermeier, D. (2009) The Thermus thermophilus DEAD box helicase Hera contains a modified RNA recognition motif domain loosely connected to the helicase core. RNA (NY), 15, 1993-2001.
16. Rudolph, M.G., Wittmann, J.G. and Klostermeier, D. (2009) Crystallization and preliminary characterization of the Thermus thermophilus RNA helicase Hera C-terminal domain. Acta Crystallogr. Sect. F, 65, 248-252.
17. Klostermeier, D. and Rudolph, M.G. (2009) A novel dimerization motif in the C-terminal domain of the Thermus thermophilus DEAD box helicase Hera confers substantial flexibility. Nucleic Acids Res., 37, 421-430.
18. Rudolph, M.G., Heissmann, R., Wittmann, J.G. and Klostermeier, D. (2006) Crystal structure and nucleotide binding of the thermus thermophilus RNA helicase hera N-terminal domain. J. Mol. Biol., 361, 731-743.
19. Sengoku, T., Nureki, O., Nakamura, A., Kobayashi, S. and Yokoyama, S. (2006) Structural basis for RNA unwinding by the DEAD-box protein drosophila vasa. Cell, 125, 287-300.
20. Oubridge, C., Ito, N., Evans, P.R., Teo, C.H. and Nagai, K. (1994) Crystal structure at 1.92 A resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature, 372, 432-438.
21. Hargous, Y., Hautbergue, G.M., Tintaru, A.M., Skrisovska, L., Golovanov, A.P., Stevenin, J., Lian, L.Y., Wilson, S.A. and Allain, F.H. (2006) Molecular basis of RNA recognition and TAP binding by the SR proteins SRp20 and 9G8. EMBO J., 25, 5126-5137.
22. Eghbalnia, H.R., Wang, L., Bahrami, A., Assadi, A. and Markley, J.L. (2005) Protein energetic conformational analysis from NMR chemical shifts (PECAN) and its use in determining secondary structural elements. J. Biomol. NMR, 32, 71-81.
23. Daubner, G.M., Clery, A. and Allain, F.H. (2013) RRM-RNA recognition: NMR or crystallography.and new findings. Curr. Opin. Struct. Biol., 23, 100-108.
24. Hardin, J.W., Hu, Y.X. and McKay, D.B. (2010) Structure of the RNA binding domain of a DEAD-box helicase bound to its ribosomal RNA target reveals a novel mode of recognition by an RNA recognition motif. J. Mol. Biol., 402, 412-427.
25. Studier, F.W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif., 41, 207-234.
26. Sambrook, J. and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York, A2.2.
27. Duchardt-Ferner, E., Weigand, J.E., Ohlenschlager, O., Schmidtke, S.R., Suess, B. and Wohnert, J. (2010) Highly modular structure and ligand binding by conformational capture in a minimalistic riboswitch. Angew. Chem. Int. Ed. Engl., 49, 6216-6219.
28. Sattler, M., Schleucher, J. and Griesinger, C. (1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients Prog. Nucl. Magn. Res. Spectr., 34, 93-158.
29. Keller, R. (2004) The Computer Aided Resonance Tutorial. CANTINA Verlag, Goldau, Switzerland.
30. Warkentin, M. and Thorne, R.E. (2007) A general method for hyperquenching protein crystals. J. Struct. Funct. Genomics, 8, 141-144.
31. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr., 66, 125-132.
32. CCP4. (1994) The Collaborative Computational Project Number 4, suite programs for protein crystallography. Acta Cryst., D50, 760-763.
33. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C. and Read, R.J. (2007) Phaser crystallographic software. J. Appl. Crystallogr., 40, 658-674.
34. Emsley, P., Lohkamp, B., Scott, W.G. and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr., D66, 486-501.
35. Zwart, P.H., Afonine, P.V., Grosse-Kunstleve, R.W., Hung, L.W., Ioerger, T.R., McCoy, A.J., McKee, E., Moriarty, N.W., Read, R.J., Sacchettini, J.C. et al. (2008) Automated structure solution with the PHENIX suite. Methods Mol. Biol., 426, 419-435.
36. Einspahr, H.M. and Weiss, M.S. (2011) Quality Indicators in Macromolecular Crystallography: Definitions and Applications. International Tables for Crystallography Vol. F, Crystallography of Biological Macromolecules, 2nd edn, Kluwer Academic Publishers, Dordrecht/Boston/London, 64-74.
37. Brunger, A.T. (1997) The free R value: A more objective statistic for crystallography. Meth Enzymol, 277, 366-396.
38. Maris, C., Dominguez, C. and Allain, F.H. (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J., 272, 2118-1231.
39. Dominguez, C., Fisette, J.F., Chabot, B. and Allain, F.H. (2010) Structural basis of G-tract recognition and encaging by hnRNP F quasi-RRMs. Nat. Struct. Mol. Biol., 17, 853-861.
40. Kossen, K. and Uhlenbeck, O.C. (1999) Cloning and biochemical characterization of Bacillus subtilis YxiN, a DEAD protein specifically activated by 23S rRNA: delineation of a novel subfamily of bacterial DEAD proteins. Nucleic Acids Res., 27, 3811-3820.
41. Mohr, S., Stryker, J.M. and Lambowitz, A.M. (2002) A DEAD-box protein functions as an ATP-dependent RNA chaperone in group I intron splicing. Cell, 109, 769-779.
42. Grohman, J.K., Campo, M.D., Bhaskaran, H., Tijerina, P., Lambowitz, A.M. and Russell, R. (2007) 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, 3013-3022.