When core competence is not enough: Functional interplay of the DEAD-box helicase core with ancillary domains and auxiliary factors in RNA binding and unwinding

Biological Chemistry

Volumn 396, Issue 8, 2015, Pages 849-865

  Rudolph, Markus G ^a   Klostermeier, Dagmar ^b  

^a F HOFFMANN LA ROCHE LTD   (Switzerland)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

basic domain; conformational dynamics; helicase; RNA recognition motif; RNA unwinding

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; DEAD BOX PROTEIN; HELICASE; INITIATION FACTOR 4A; INITIATION FACTOR 4B; INITIATION FACTOR 4G; RNA; RNA 23S; SINGLE STRANDED RNA; PROTEIN BINDING;

AMINO TERMINAL SEQUENCE; BASE PAIRING; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DISSOCIATION; DNA FLANKING REGION; HYDROGEN BOND; HYDROLYSIS; MITOCHONDRIAL TARGETING SIGNAL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; RNA BINDING; RNA CONFORMATION; RNA SPLICING; RNA TRANSPORT; STEREOSPECIFICITY; TRANSLATION INITIATION; CHEMISTRY; CONFORMATION; METABOLISM; PROTEIN TERTIARY STRUCTURE;

ADENOSINE TRIPHOSPHATE; BINDING SITES; DEAD-BOX RNA HELICASES; HYDROLYSIS; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA;

EID: 84936803147     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2014-0277     Document Type: Review

References (75)

1. Ahmadian, M.R., Stege, P., Scheffzek, K., and Wittinghofer, A. (1997). Confirmation of the arginine-finger hypothesis for the GAP-stimulated GTP-hydrolysis reaction of Ras. Nat. Struct. Biol. 4, 686-689.
2. Andersen, C.B., Ballut, L., Johansen, J.S., Chamieh, H., Nielsen, K.H., Oliveira, C.L., 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. Andreou, A.Z. and Klostermeier, D. (2012a). Conformational changes of DEAD-box helicases monitored by single molecule fluorescence resonance energy transfer. Methods Enzymol. 511, 75-109.
4. Andreou, A.Z. and Klostermeier, D. (2012b). The DEAD-box helicase eIF4A: paradigm or the odd one out? RNA Biol. 1, 19-32.
5. Andreou, A.Z. and Klostermeier, D. (2014). eIF4B and eIF4G jointly stimulate eIF4A ATPase and unwinding activities by modulation of the eIF4A conformational cycle. J. Mol. Biol. 426, 51-61.
6. Aregger, R. and Klostermeier, D. (2009). The DEAD-box helicase YxiN maintains a closed conformation during ATP hydrolysis. Biochemistry 48, 10679-10681.
7. Banroques, J., Doere, M., Dreyfus, M., Linder, P., and Tanner, N.K. (2009). Motif III in superfamily 2 "helicases" helps convert the binding energy of ATP into a high-affinity RNA binding site in the yeast DEAD-box protein Ded1. J. Mol. Biol. 396, 949-966.
8. Banroques, J., Cordin, O., Doere, M., Linder, P., and Tanner, N.K. (2011). Analyses of the functional regions of DEAD-box RNA "helicases" with deletion and chimera constructs tested in vivo and in vitro. J. Mol. Biol. 413, 451-472.
9. 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.
10. Büchwald, G., Ebert, J., Basquin, C., Sauliere, J., Jayachandran, U., Bono, F., Le Hir, H., and Conti, E. (2010). Insights into the recruitment of the NMD machinery from the crystal structure of a core EJC-UPF3b complex. Proc. Natl. Acad. Sci. USA 107, 10050-10055.
11. Buchwald, G., Schussler, S., Basquin, C., Le Hir, H., and Conti, E. (2013). Crystal structure of the human eIF4AIII-CWC22 complex shows how a DEAD-box protein is inhibited by a MIF4G domain. Proc. Natl. Acad. Sci. USA 110, E4611-E4608.
12. Caruthers, J.M., Johnson, E.R., and McKay, D.B. (2000). Crystal structure of yeast initiation factor 4A, a DEAD-box RNA helicase. Proc. Natl. Acad. Sci. USA 97, 13080-13085.
13. Caruthers, J.M., Hu, Y., and McKay, D.B. (2006). Structure of the second domain of the Bacillus subtilis DEAD-box RNA helicase YxiN. Acta Crystallogr. Sect. F 62, 1191-1195.
14. Cheng, Z., Coller, J., Parker, R., and Song, H. (2005). Crystal structure and functional analysis of DEAD-box protein Dhh1p. RNA 11, 1258-1270.
15. 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 α-helical switch. J. Biol. Chem. 284, 10296-10300.
16. Del Campo, M. and Lambowitz, A.M. (2009). Structure of theyeast DEAD-box protein Mss116p reveals two wedges that crimp RNA. Mol. Cell 35, 598-609.
17. Diges, C.M. and Uhlenbeck, O.C. (2001). Escherichia coli DbpA is an RNA helicase that requires hairpin 92 of 23S rRNA. EMBO J. 20, 5503-5512.
18. Elles, L.M. and Uhlenbeck, O.C. (2008). Mutation of the arginine finger in the active site of Escherichia coli DbpA abolishes ATPase and helicase activity and confers a dominant slow growth phenotype. Nucleic Acids Res. 36, 41-50.
19. 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.
20. 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.
21. Harms, U., Andreou, A.Z., Gubaev, A., and Klostermeier, D. (2014). eIF4B, eIF4G and RNA regulate eIF4A activity in translation initiation by modulating the eIF4A conformational cycle. Nucleic Acids Res. 42, 7911-7922.
22. Henn, A., Bradley, M.J., and De La Cruz, E.M. (2012). ATP Utilization and RNA Conformational Rearrangement by DEAD-Box Proteins. Annu. Rev. Biophys. 41, 247-267.
23. 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.
24. Hilbert, M., Kebbel, F., Gubaev, A., and Klostermeier, D. (2011). eIF4G stimulates the activity of the DEAD box protein eIF4A by a conformational guidance mechanism. Nucleic Acids Res. 39, 2260-2270.
25. Hogbom, M., Collins, R., van den Berg, S., Jenvert, R.M., Karlberg, T., Kotenyova, T., Flores, A., Hedestam, G.B., and Schiavone, L.H. (2007). Crystal Structure of Conserved Domains 1 and 2 of the Human DEAD-box Helicase DDX3X in Complex with the Mononucleotide AMP. J. Mol. Biol. 372, 150-159.
26. Jacewicz, A., Schwer, B., Smith, P., and Shuman, S. (2014). Crystal structure, mutational analysis and RNA-dependent ATPase activity of the yeast DEAD-box pre-mRNA splicing factor Prp28. Nucleic Acids Res. 42, 12885-12898.
27. Jarmoskaite, I., Bhaskaran, H., Seifert, S., and Russell, R. (2014). DEAD-box protein CYT-19 is activated by exposed helices in a group I intron RNA. Proc. Natl. Acad. Sci. USA 111, E2928-E2936.
28. 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.
29. Karow, A.R. and Klostermeier, D. (2009). A conformational change in the helicase core is necessary but not sufficient for RNA unwinding by the DEAD box helicase YxiN. Nucleic Acids Res. 37, 4464-4471.
30. Karow, A.R. and Klostermeier, D. (2010). A structural model for the DEAD box helicase YxiN in solution: localization of the RNAbinding domain. J. Mol. Biol. 402, 629-637.
31. Klostermeier, D. (2013). Rearranging RNA structures at 75°C? towards the molecular mechanism and physiological function of the Thermus thermophilus DEAD-box helicase hera. Biopolymers 99, 1137-1146.
32. 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.
33. Kossen, K., Karginov, F.V., and Uhlenbeck, O.C. (2002). The carboxyterminal domain of the DExDH protein YxiN is sufficient to confer specificity for 23S rRNA. J. Mol. Biol. 324, 625-636.
34. 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.
35. Linder, P. and Jankowsky, E. (2011). From unwinding to clamping - the DEAD box RNA helicase family. Nat. Rev. Mol. Cell Biol. 12, 505-516.
36. Linder, P., Lasko, P.F., Ashburner, M., Leroy, P., Nielsen, P.J., Nishi, K., Schnier, J., and Slonimski, P.P. (1989). Birth of the D-E-A-D box. [erratum appears in Nature (1989) 20;340:246]. Nature 337, 121-122.
37. Liu, F., Putnam, A., and Jankowsky, E. (2008). ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding. Proc. Natl. Acad. Sci. USA 51, 20209-20214.
38. Mallam, A.L., Jarmoskaite, I., Tijerina, P., Del Campo, M., Seifert, S., Guo, L., Russell, R., and Lambowitz, A.M. (2011). Solution structures of DEAD-box RNA chaperones reveal conformational changes and nucleic acid tethering by a basic tail. Proc. Natl. Acad. Sci. USA 108, 12254-12259.
39. Mallam, A.L., Del Campo, M., Gilman, B., Sidote, D.J., and Lambowitz, A.M. (2012). Structural basis for RNA-duplex recognition and unwinding by the DEAD-box helicase Mss116p. Nature 490, 121-125.
40. Mathys, H., Basquin, J., Ozgur, S., Czarnocki-Cieciura, M., Bonneau, F., Aartse, A., Dziembowski, A., Nowotny, M., Conti, E., and Filipowicz, W. (2014). Structural and biochemical insights to the role of the CCR4-NOT complex and DDX6 ATPase in micro-RNA repression. Mol. Cell 54, 751-765.
41. Mohlmann, S., Mathew, R., Neumann, P., Schmitt, A., Luhrmann, R., and Ficner, R. (2014). Structural and functional analysis of the human spliceosomal DEAD-box helicase Prp28. Acta Crystallogr. D Biol. Crystallogr. 70, 1622-1630.
42. Mohr, G., Del Campo, M., Mohr, S., Yang, Q., Jia, H., Jankowsky, E., and Lambowitz, A.M. (2008). Function of the C-terminal domain of the DEAD-box protein Mss116p analyzed in vivo and in vitro. J. Mol. Biol. 375, 1344-1364.
43. Mohr, G., Del Campo, M., Turner, K.G., Gilman, B., Wolf, R.Z., and Lambowitz, A.M. (2011). High-throughput genetic identification of functionally important regions of the yeast DEAD-box protein Mss116p. J. Mol. Biol. 413, 952-972.
44. Montpetit, B., Thomsen, N.D., Helmke, K.J., Seeliger, M.A., Berger, J.M., and Weis, K. (2011). A conserved mechanism of DEAD-box ATPase activation by nucleoporins and InsP6 in mRNA export. Nature 472, 238-242.
45. 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.
46. Nielsen, K.H., Chamieh, H., Andersen, C.B., Fredslund, F., Hamborg, K., Le Hir, H., and Andersen, G.R. (2008). Mechanism of ATP turnover inhibition in the EJC. RNA 15, 67-75.
47. Oubridge, C., Ito, N., Evans, P.R., Teo, C.H., and Nagai, K. (1994). Crystal structure at 1.92 Å resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature 372, 432-438.
48. Pan, C., Potratz, J.P., Cannon, B., Simpson, Z.B., Ziehr, J.L., Tijerina, P., and Russell, R. (2014). DEAD-box helicase proteins disrupt RNA tertiary structure through helix capture. PLoS Biol 12, e1001981.
49. Pause, A. and Sonenberg, N. (1992). Mutational analysis of a DEAD box RNA helicase: the mammalian translation initiation factor eIF-4A. EMBO J. 11, 2643-2654.
50. Putnam, A.A. and Jankowsky, E. (2013). DEAD-box helicases as integrators of RNA, nucleotide and protein binding. Biochim. Biophys. Acta 1829, 884-893.
51. Raz, E. (2000). The function and regulation of vasa-like genes in germ-cell development. Genome Biol. 1, reviews1017.1-reviews1017.6.
52. Richter, N.J., Rogers, G.W., Jr., Hensold, J.O., and Merrick, W.C. (1999). Further biochemical and kinetic characterization of human eukaryotic initiation factor 4H. J. Biol. Chem. 274, 35415-35424.
53. Rogers, G.W. Jr., 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.
54. Rogers, G.W., Jr., Lima, W.F., and Merrick, W.C. (2001). Further characterization of the helicase activity of eIF4A. Substrate specificity. J. Biol. Chem. 276, 12598-12608.
55. Rogers, G.W., Jr., Komar, A.A., and Merrick, W.C. (2002). eIF4A: the godfather of the DEAD box helicases. Prog. Nucleic Acid Res. Mol. Biol. 72, 307-331.
56. 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 15, 1993-2001.
57. 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.
58. Samatanga, B. and Klostermeier, D. (2014). DEAD-box RNA helicase domains exhibit a continuum between complete functional independence and high thermodynamic coupling in nucleotide and RNA duplex recognition. Nucleic Acids Res. 42, 10644-10654.
59. Schutz, P., Bumann, M., Oberholzer, A.E., Bieniossek, C., Trachsel, H., Altmann, M., and Baumann, U. (2008). Crystal structure of the yeast eIF4A-eIF4G complex: an RNA-helicase controlled by protein-protein interactions. Proc. Natl. Acad. Sci. USA 105, 9564-9569.
60. Schutz, P., Karlberg, T., van den Berg, S., Collins, R., Lehtio, L., Hogbom, M., Holmberg-Schiavone, L., Tempel, W., Park, H.W., Hammarstrom, M., et al. (2010). Comparative structural analysis of human DEAD-box RNA helicases. PLoS One 5, e12791.
61. 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.
62. Sharpe Elles, L.M., Sykes, M.T., Williamson, J.R., and Uhlenbeck, O.C. (2009). A dominant negative mutant of the E. coli RNA helicase DbpA blocks assembly of the 50S ribosomal subunit. Nucleic Acids Res. 37, 6503-6514.
63. Steimer, L. and Klostermeier, D. (2012). RNA helicases in infection and disease. RNA Biol. 9, 751-771.
64. Steimer, L., Wurm, J.P., Linden, M.H., Rudolph, M.G., Wohnert, J., and Klostermeier, D. (2013). Recognition of two distinct elements in the RNA substrate by the RNA binding domain of the T. thermophilus DEAD box helicase Hera. Nucleic Acids Res. 41, 6259-6272.
65. Story, R.M., Li, H., and Abelson, J.N. (2001). Crystal structure of a DEAD box protein from the hyperthermophile Methanococcus jannaschii. Proc. Natl. Acad. Sci. USA 98, 1465-1470.
66. Strohmeier, J., Hertel, I., Diederichsen, U., Rudolph, M.G., and Klostermeier, D. (2011). Changing nucleotide specificity of the DEAD-box helicase Hera abrogates communication between the Q-motif and the P-loop. Biol. Chem. 392, 357-369.
67. Talavera, M.A. and De La Cruz, E.M. (2005). Equilibrium and kinetic analysis of nucleotide binding to the DEAD-box RNA helicase DbpA. Biochemistry 44, 959-970.
68. 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.
69. Tanner, N.K., Cordin, O., Banroques, J., Doere, M., and Linder, P. (2003). The Q motif: a newly identified motif in DEAD box helicases may regulate ATP binding and hydrolysis. Mol. Cell 11, 127-138.
70. Theissen, B., Karow, A.R., Kohler, J., Gubaev, A., and Klostermeier, D. (2008). Cooperative binding of ATP and RNA induces a closed conformation in a DEAD box RNA helicase. Proc. Natl. Acad. Sci. USA 105, 548-553.
71. 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.
72. 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.
73. Wang, S., Hu, Y., Overgaard, M.T., Karginov, F.V., Uhlenbeck, O.C., and McKay, D.B. (2006). The domain of the Bacillus subtilis DEAD-box helicase YxiN that is responsible for specific binding of 23S rRNA has an RNA recognition motif fold. RNA 12, 959-967.
74. Wang, S., Overgaard, M.T., Hu, Y., and McKay, D.B. (2007). The Bacillus subtilis RNA Helicase YxiN is Distended in Solution. Biophys. J. 94, L01-L03.
75. Yang, Q., Del Campo, M., Lambowitz, A.M., and Jankowsky, E. (2007). DEAD-box proteins unwind duplexes by local strand separation. Mol. Cell 28, 253-263.