RNA helicases - one fold for many functions

Current Opinion in Structural Biology

Volumn 17, Issue 3, 2007, Pages 316-324

  Jankowsky, Eckhard ^a   Fairman, Margaret E ^a  

^a Alzheimer Research Laboratory   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEAD BOX PROTEIN; RNA HELICASE;

CRYSTAL STRUCTURE; NUCLEIC ACID STRUCTURE, METABOLISM AND FUNCTION; PRIORITY JOURNAL; PROTEIN FOLDING; REVIEW; RNA BINDING; RNA METABOLISM; RNA STRUCTURE;

ANIMALS; HUMANS; PROTEIN STRUCTURE, TERTIARY; RNA; RNA HELICASES;

EID: 34347385000     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2007.05.007     Document Type: Review

References (83)

1. Cordin O., Banroques J., Tanner N.K., and Linder P. The DEAD-box protein family of RNA helicases. Gene 367 (2006) 17-37
2. Gorbalenya A.E., and Koonin E.V. Helicases: amino acid comparisons and structure-function relationships. Curr Opin Struct Biol 3 (1993) 419-429
3. Tanner N.K., and Linder P. DExD/H box RNA helicases. From generic motors to specific dissociation functions. Mol Cell 8 (2001) 251-261
4. Linder P. Dead-box proteins: a family affair-active and passive players in RNP-remodeling. Nucleic Acids Res 34 (2006) 4168-4180
5. Jankowsky E., Fairman M.E., and Yang Q. RNA helicases: versatile ATP-driven nanomotors. J Nanosci Nanotechnol 12 (2005) 1983-1989
6. Anantharaman V., Koonin E.V., and Aravind L. Comparative genomics and evolution of proteins involved in RNA metabolism. Nucleic Acids Res 30 (2002) 1427-1464
7. Staley J.P., and Guthrie C. Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 92 (1998) 315-326
8. Kadare G., and Haenni A.L. Virus-encoded RNA helicases. J Virol 71 (1997) 2583-2590
9. Caruthers J.M., and McKay D.B. Helicase structure and mechanism. Curr Opin Struct Biol 12 (2002) 123-133
10. Korolev S., Hsieh J., Gauss G.H., Lohman T.M., and Waksman G. Major domain swiveling revealed by the crystal structures of complexes of E. coli Rep helicase bound to single-stranded DNA and ADP. Cell 90 (1997) 635-647
11. Kim J.L., Morgenstern K.A., Griffith J.P., Dwyer M.D., Thomson J.A., Murcko M.A., Lin C., and Caron P.R. Hepatitis C virus NS3 RNA helicase domain with a bound oligonucleotide: the crystal structure provides insights into the mode of unwinding. Structure 6 (1998) 89-100
12. Velankar S.S., Soultanas P., Dillingham M.S., Subramanya H.S., and Wigley D.B. Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell 97 (1999) 75-84
13. 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. The first crystal structure of a DEAD-box protein with bound RNA reveals a conformation of the nucleic acid that markedly differs from that seen in other helicase complex structures.
14. ••].
15. ••] report crystal structures of the EJC core and show how the DEAD-box protein eIF4AIII is trapped by other factors in a conformation that tightly binds RNA without continuously hydrolyzing ATP.
16. Lee J.Y., and Yang W. UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke. Cell 127 (2006) 1349-1360
17. 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
18. 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
19. Iost I., Dreyfus M., and Linder P. Ded1p, a DEAD-box protein required for translation initiation in Saccharomyces cerevisiae, is an RNA helicase. J Biol Chem 274 (1999) 17677-17683
20. Talavera M.A., and De La Cruz E.M. Equilibrium and kinetic analysis of nucleotide binding to the DEAD-box RNA helicase DbpA. Biochemistry 44 (2005) 959-970
21. Tanaka N., and Schwer B. Mutations in PRP43 that uncouple RNA-dependent NTPase activity and pre-mRNA splicing function. Biochemistry 45 (2006) 6110-6121
22. Tanaka N., and Schwer B. Characterization of the NTPase, RNA-binding, and RNA helicase activities of the DEAH-box splicing factor Prp22. Biochemistry 44 (2005) 9795-9803
23. Shuman S. Vaccinia virus RNA helicase: an essential enzyme related to the DE-H family of RNA-dependent NTPases. Proc Natl Acad Sci USA 89 (1992) 10935-10939
24. Lam A.M., Keeney D., Eckert P.Q., and Frick D.N. Hepatitis C virus NS3 ATPases/helicases from different genotypes exhibit variations in enzymatic properties. J Virol 77 (2003) 3950-3961
25. Cheng Z., Muhlrad D., Lim M.K., Parker R., and Song H. Structural and functional insights into the human Upf1 helicase core. EMBO J 26 (2007) 253-264. The first structure of an SF1 RNA helicase shows high similarity to SF2 proteins, but with additional domains, one of which is implicated in RNA binding.
26. Weng Y., Czaplinski K., and Peltz S.W. ATP is a cofactor of the Upf1 protein that modulates its translation termination and RNA binding activities. RNA 4 (1998) 205-214
27. Jankowsky E., Gross C.H., Shuman S., and Pyle A.M. Active disruption of an RNA-protein interaction by a DExH/D RNA helicase. Science 291 (2001) 121-125
28. Fairman M.E., Maroney P.A., Wang W., Bowers H., Gollnick P., Nilsen T.W., and Jankowsky E. Protein displacement by DExH/D RNA helicases without duplex unwinding. Science 304 (2004) 730-734
29. Mackintosh S.G., and Raney K.D. DNA unwinding and protein displacement by superfamily 1 and superfamily 2 helicases. Nucleic Acids Res 34 (2006) 4154-4159
30. Jankowsky E., Gross C.H., Shuman S., and Pyle A.M. The DExH protein NPH-II is a processive and directional motor for unwinding RNA. Nature 403 (2000) 447-451
31. Kawaoka J., Jankowsky E., and Pyle A.M. Backbone tracking by the SF2 helicase NPH-II. Nat Struct Mol Biol 11 (2004) 526-530
32. Serebrov V., and Pyle A.M. Periodic cycles of RNA unwinding and pausing by hepatitis C virus NS3 helicase. Nature 430 (2004) 476-480
33. Kawaoka J., and Pyle A.M. Choosing between DNA and RNA: the polymer specificity of RNA helicase NPH-II. Nucleic Acids Res 33 (2005) 644-649
34. Dumont S., Cheng W., Serebrov V., Beran R.K., Tinoco I.J., Pyle A.M., and Bustamante C. RNA translocation and unwinding mechanism of HCV NS3 helicase and its coordination by ATP. Nature 439 (2006) 105-108. The movement of the DExH RNA helicase HCV NS3 on RNA is analyzed at the single-molecule level. It is shown that larger steps consist of smaller substeps triggered by ATP binding.
35. Beran R.K., Bruno M.M., Bowers H.A., Jankowsky E., and Pyle A.M. Robust translocation along a molecular monorail: the NS3 helicase from hepatitis C virus traverses unusually large disruptions in its track. J Mol Biol 358 (2006) 974-982
36. 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
37. 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. Analysis of the unwinding mode of a DEAD-box protein reveals that the enzyme uses single-stranded RNA not as the starting point for translocation but for loading of the helicase onto the duplex, from which strand separation is directly initiated. This type of helicase activity explains observations with numerous other DEAD-box proteins and may be the prevalent means of duplex unwinding in cellular RNA metabolism.
38. Diges C.M., and Uhlenbeck O.C. Escherichia coli DbpA is an RNA helicase that requires hairpin 92 of 23S rRNA. EMBO J 20 (2001) 5503-5512
39. Bizebard T., Ferlenghi I., Iost I., and Dreyfus M. Studies on three E. coli DEAD-box helicases point to an unwinding mechanism different from that of model DNA helicases. Biochemistry 43 (2004) 7857-7866
40. Rogers G.W., Richter N.J., and Merrick W.C. Biochemical and kinetic characterization of the RNA helicase activity of eukaryotic initiation factor 4A. J Biol Chem 274 (1999) 12236-12244
41. Yang Q., and Jankowsky E. ATP- and ADP-dependent modulation of RNA unwinding and strand annealing activities by the DEAD-box protein DED1. Biochemistry 44 (2005) 13591-13601
42. Bowers H.A., Maroney P.A., Fairman M.E., Kastner B., Luhrmann R., Nilsen T.W., and Jankowsky E. Discriminatory RNP remodeling by the DEAD-box protein DED1. RNA 12 (2006) 903-912
43. 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
44. Durr H., Flaus A., Owen-Hughes T., and Hopfner K.P. Snf2 family ATPases and DExx box helicases: differences and unifying concepts from high-resolution crystal structures. Nucleic Acids Res 34 (2006) 4160-4167
45. Kos M., and Tollervey D. The putative RNA helicase Dbp4p is required for release of the U14 snoRNA from preribosomes in Saccharomyces cerevisiae. Mol Cell 20 (2005) 53-64
46. Raghunathan P.L., and Guthrie C. RNA unwinding in U4/U6 snRNPs requires ATP hydrolysis and the DEIH-box splicing factor Brr2. Curr Biol 8 (1998) 847-855
47. Rossler O.G., Straka A., and Stahl H. Rearrangement of structured RNA via branch migration structures catalysed by the highly related DEAD-box proteins p68 and p72. Nucleic Acids Res 29 (2001) 2088-2096
48. Chamot D., Colvin K.R., Kujat-Choy S.L., and Owttrim G.W. RNA structural rearrangement via unwinding and annealing by the cyanobacterial RNA helicase, CrhR. J Biol Chem 280 (2005) 2036-2044
49. Uhlmann-Schiffler H., Jalal C., and Stahl H. Ddx42p-a human DEAD box protein with RNA chaperone activities. Nucleic Acids Res 34 (2006) 10-22
50. Halls C., Mohr S., Del Campo M., Yang Q., Jankowsky E., and Lambowitz A.M. Involvement of DEAD-box proteins in group I and group 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
51. 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
52. 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
53. Chen J.Y., Stands L., Staley J.P., Jackups R.R., Latus L.J., and Chang T.H. Specific alterations of U1-C protein or U1 small nuclear RNA can eliminate the requirement of Prp28p, an essential DEAD box splicing factor. Mol Cell 7 (2001) 227-232
54. Kistler A.L., and Guthrie C. Deletion of MUD2, the yeast homolog of U2AF65, can bypass the requirement for sub2, an essential spliceosomal ATPase. Genes Dev 15 (2001) 42-49
55. Perriman R., Barta I., Voeltz G.K., Abelson J., and Ares M.J. ATP requirement for Prp5p function is determined by Cus2p and the structure of U2 small nuclear RNA. Proc Natl Acad Sci USA 100 (2003) 13857-13862
56. Lund M.K., and Guthrie C. The DEAD-box protein Dbp5p is required to dissociate Mex67p from exported mRNPs at the nuclear rim. Mol Cell 20 (2005) 645-651
57. Jankowsky E., and Bowers H. Remodeling of ribonucleoprotein complexes with DExH/D RNA helicases. Nucleic Acids Res 34 (2006) 4181-4188
58. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., Taira K., Akira S., and Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5 (2004) 730-737
59. Yoneyama M., Kikuchi M., Matsumoto K., Imaizumi T., Miyagishi M., Taira K., Foy E., Loo Y.M., Gale M.J., Akira S., et al. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J Immunol 175 (2005) 2851-2858
60. Kato H., Takeuchi O., Sato S., Yoneyama M., Yamamoto M., Matsui K., Uematsu S., Jung A., Kawai T., Ishii K.J., et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441 (2006) 101-105
61. Marques J.T., Devosse T., Wang D., Zamanian-Daryoush M., Serbinowski P., Hartmann R., Fujita T., Behlke M.A., and Williams B.R. A structural basis for discriminating between self and nonself double-stranded RNAs in mammalian cells. Nat Biotechnol 24 (2006) 559-565
62. Pichlmair A., Schulz O., Tan C.P., Naslund T.I., Liljestrom P., Weber F., Reis E., and Sousa C. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′ phosphates. Science 314 (2006) 997-1001
63. Hornung V., Ellegast J., Kim S., Brzozka K., Jung A., Kato H., Poeck H., Akira S., Conzelmann K.K., Schlee M., et al. 5′-triphosphate RNA is the ligand for RIG-I. Science 314 (2006) 994-997
64. Yang L., Lin C., and Liu Z.R. P68 RNA helicase mediates PDGF-induced epithelial mesenchymal transition by displacing Axin from beta-catenin. Cell 127 (2006) 139-155
65. Fuller-Pace F.V. DExD/H box RNA helicases: multifunctional proteins with important roles in transcriptional regulation. Nucleic Acids Res 34 (2006) 4206-4215
66. Walstrom K.M., Schmidt D., Bean C.J., and Kelly W.G. RNA helicase A is important for germline transcriptional control, proliferation, and meiosis in C. elegans. Mech Dev 122 (2005) 707-720
67. Rogers Jr. G.W., Richter N.J., Lima W.F., and Merrick W.C. Modulation of the helicase activity of eIF4A by eIF4B, eIF4H, and eIF4F. J Biol Chem 276 (2001) 30914-30922
68. Oberer M., Marintchev A., and Wagner G. Structural basis for the enhancement of eIF4A helicase activity by eIF4G. Genes Dev 19 (2005) 2212-2223
69. •].
70. •] demonstrate that specific activation of a DEAD-box helicase can be accomplished by another protein and a small molecule cofactor.
71. Granneman S., Lin C., Champion E.A., Nandineni M.R., Zorca C., and Baserga S.J. The nucleolar protein Esf2 interacts directly with the DExD/H box RNA helicase, Dbp8, to stimulate ATP hydrolysis. Nucleic Acids Res 34 (2006) 3189-3199
72. Shibuya T., Tange T.O., Sonenberg N., and Moore M.J. eIF4AIII binds spliced mRNA in the exon junction complex and is essential for nonsense-mediated decay. Nat Struct Mol Biol 11 (2004) 346-351
73. Shibuya T., Tange T.O., Stroupe M.E., and Moore M.J. Mutational analysis of human eIF4AIII identifies regions necessary for exon junction complex formation and nonsense-mediated mRNA decay. RNA 12 (2006) 360-374
74. Ballut L., Marchadier B., Baguet A., Tomasetto C., Seraphin B., and Le Hir H. The exon junction core complex is locked onto RNA by inhibition of eIF4AIII ATPase activity. Nat Struct Mol Biol 12 (2005) 861-869. This study shows that cofactors of RNA helicases not only stimulate but also strongly inhibit the biochemical activities of these enzymes, and that strong inhibition may be equally critical to the biological function of some RNA helicases.
75. Cho H.S., Ha N.C., Kang L.W., Chung K.M., Back S.H., Jang S.K., and Oh B.H. Crystal structure of RNA helicase from genotype 1b hepatitis C virus. A feasible mechanism of unwinding duplex RNA. J Biol Chem 273 (1998) 15045-15052
76. Cheng Z., Coller J., Parker R., and Song H. Crystal structure and functional analysis of DEAD-box protein Dhh1p. RNA 11 (2005) 1258-1270
77. Caruthers J.M., Johnson E.R., and McKay D.B. Crystal structure of yeast initiation factor 4A, a DEAD-box RNA helicase. Proc Natl Acad Sci USA 97 (2000) 13080-13085
78. Story R.M., Li H., and Abelson J.N. Crystal structure of a DEAD box protein from the hyperthermophile Methanococcus jannaschii. Proc Natl Acad Sci USA 98 (2001) 1465-1470
79. Shi H., Cordin O., Minder C.M., Linder P., and Xu R.M. Crystal structure of the human ATP-dependent splicing and export factor UAP56. Proc Natl Acad Sci USA 101 (2004) 17628-17633
80. Xu T., Sampath A., Chao A., Wen D., Nanao M., Chene P., Vasudevan S.G., and Lescar J. Structure of the Dengue virus helicase/nucleoside triphosphatase catalytic domain at a resolution of 2.4 Å. J Virol 79 (2005) 10278-10288
81. Yao N., Hesson T., Cable M., Hong Z., Kwong A.D., Le H.V., and Weber P.C. Structure of the hepatitis C virus RNA helicase domain. Nat Struct Biol 4 (1997) 463-467
82. Mackintosh S.G., Lu J.Z., Jordan J.B., Harrison M.K., Sikora B., Sharma S.D., Cameron C.E., Raney K.D., and Sakon J. Structural and biological identification of residues on the surface of NS3 helicase required for optimal replication of the hepatitis C virus. J Biol Chem 281 (2006) 3528-3535
83. Wu J., Bera A.K., Kuhn R.J., and Smith J.L. Structure of the Flavivirus helicase: implications for catalytic activity, protein interactions, and proteolytic processing. J Virol 79 (2005) 10268-10277