Helicase-mediated changes in RNA structure at the single-molecule level

RNA Biology

Volumn 10, Issue 1, 2013, Pages 133-148

  König, Sebastian L B ^a   Liyanage, Pramodha S ^b   Sigel, Roland K O ^a   Rueda, David ^b,c  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b WAYNE STATE UNIVERSITY   (United States)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

AFM; DEAD box; FRET; Optical tweezers; PIFE; RNA folding; RNA helicase; Single molecule spectroscopy

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DED1 PROTEIN; DOUBLE STRANDED RNA; HCV NS3 PROTEIN; INITIATION FACTOR 4A; MSS116 PROTEIN; NPH II PROTEIN; PROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; RNA HELICASE; UNCLASSIFIED DRUG; VIRUS RNA; YXIN PROTEIN;

5' UNTRANSLATED REGION; ATOMIC FORCE MICROSCOPY; CYTOSOL; FLUORESCENCE ANALYSIS; GENETIC PARAMETERS; HUMAN; INTRON; MOLECULAR INTERACTION; PROTEIN INDUCED FLUORESCENCE ENHANCEMENT; PROTEIN SECONDARY STRUCTURE; REVIEW; RNA DEGRADATION; RNA EXPORT; RNA REMODELING; RNA STRUCTURE; RNA TRANSPORT; RNA UNWINDING; SINGLE MOLECULE FORSTER RESONANCE ENERGY TRANSFER; THERMODYNAMICS;

EID: 84875154599     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.23507     Document Type: Review

References (178)

1. Crick FHC. Central dogma of molecular biology. Nature 1970; 227:561-3; PMID:4913914; http://dx.doi.org/10.1038/227561a0.
2. Garneau NL, Wilusz J, Wilusz CJ. The highways and byways of mRNA decay. Nat Rev Mol Cell Biol 2007; 8:113-26; PMID:17245413; http://dx.doi. org/10.1038/nrm2104. (Pubitemid 46432531)
3. Ibba M, Söll D. Aminoacyl-tRNA synthesis. Annu Rev Biochem 2000; 69:617-50; PMID:10966471; http://dx.doi.org/10.1146/annurev.biochem.69.1.617.
4. Phizicky EM, Hopper AK. tRNA biology charges to the front. Genes Dev 2010; 24:1832-60; PMID:20810645; http://dx.doi.org/10.1101/gad.1956510.
5. Proudfoot NJ, Furger A, Dye MJ. Integrating mRNA processing with transcription. Cell 2002; 108:501-12; PMID:11909521; http://dx.doi.org/10.1016/ S0092-8674(02)00617-7. (Pubitemid 34260875)
6. Yusupov MM, Yusupova GZ, Baucom Å, Lieberman K, Earnest TN, Cate JHD, et al. Crystal structure of the ribosome at 5.5 A resolution. Science 2001; 292:883-96; PMID:11283358; http://dx.doi.org/10.1126/sci-ence.1060089. (Pubitemid 32422479)
7. Bachellerie J-P, Cavaillé J, Hüttenhofer A. The expanding snoRNA world. Biochimie 2002; 84:775-90; PMID:12457565; http://dx.doi.org/10. 1016/S0300-9084(02)01402-5. (Pubitemid 35363462)
8. Faustino NA, Cooper TA. Pre-mRNA splicing and human disease. Genes Dev 2003; 17:419-37; PMID:12600935; http://dx.doi.org/10.1101/gad.1048803. (Pubitemid 36258756)
9. Guo Z, Karunatilaka KS, Rueda D. Single-molecule analysis of protein-free U2-U6 snRNAs. Nat Struct Mol Biol 2009; 16:1154-9; PMID:19881500; http://dx.doi.org/10.1038/nsmb.1672.
10. Hoskins AA, Moore MJ. The spliceosome: a flexible, reversible macromolecular machine. Trends Biochem Sci 2012; 37:179-88; PMID:22480731; http://dx.doi. org/10.1016/j.tibs.2012.02.009.
11. van der Feltz C, Anthony K, Brilot A, Pomeranz Krummel DA. Architecture of the spliceosome' Biochemistry 2012; 51:3321-33; PMID:22471593; http://dx.doi.org/10.1021/bi201215r.
12. Williams GT, Farzaneh F. Are snoRNAs and snoRNA host genes new players in cancer? Nat Rev Cancer 2012; 12:84-8; PMID:22257949.
13. Feng J, Funk WD, Wang S-S, Weinrich SL, Avilion AA, Chiu C-P, et al. The RNA component of human telom-erase. Science 1995; 269:1236-41; PMID:7544491; http://dx.doi.org/10.1126/science.7544491.
14. Bartel D P. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136:215-33; PMID:19167326; http://dx.doi.org/10.1016/j. cell.2009.01.002.
15. Brantl S. Regulatory mechanisms employed by cis-encoded antisense RNAs. Curr Opin Microbiol 2007; 10:102-9; PMID:17387036; http://dx.doi. org/10.1016/j.mib.2007.03.012. (Pubitemid 46590052)
16. Ferré-D'Amaré AR, Winkler WC. The roles of metal ions in regulation by riboswitches. Met Ions Life Sci 2011; 9:141-73; PMID:22010271; http://dx.doi. org/10.1039/9781849732512-00141.
17. Hamilton AJ, Baulcombe DC. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 1999; 286:950-2; PMID:10542148; http://dx.doi.org/10.1126/science.286.5441.950.
18. Montange RK, Batey RT. Riboswitches: emerging themes in RNA structure and function. Annu Rev Biophys 2008; 37:117-33; PMID:18573075; http://dx.doi.org/ 10.1146/annurev.bio-phys.37.032807.130000.
19. Krupovic M, Cvirkaite-Krupovic V. Virophages or satellite viruses? Nat Rev Microbiol 2011; 9:762-3; PMID:22016897; http://dx.doi.org/10.1038/nrmi- cro2676.
20. Simon-Loriere E, Holmes EC. Why do RNA viruses recombine? Nat Rev Microbiol 2011; 9:617-26; PMID:21725337; http://dx.doi.org/10.1038/nrmi-cro2614.
21. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, et al. A unified classification system for eukaryotic transposable elements. Nat Rev Genet 2007; 8:973-82; PMID:17984973; http://dx.doi. org/10.1038/nrg2165. (Pubitemid 350129169)
22. König SLB, Evans AC, Huppert JL. Seven essential questions on G-quadruplexes. BioMol Concepts 2010; 1:197-213; http://dx.doi.org/10.1515/bmc. 2010.011.
23. Batey RT, Rambo R P, Doudna JA. Tertiary motifs in RNA structure and folding. Angew Chem Int Ed Engl 1999; 38:2326-43; PMID:10458781; http://dx.doi.org/10.1002/(SICI)1521-3773(19990816)38:163.0.CO;2-3. (Pubitemid 29399554)
24. Sigel H, Sigel RKO. Metal ion interactions with nucleic acids and their constituents. In: Reedijk J, Poepelmeier K, eds. Comprehensive Inorganic Chemistry. Oxford, United Kingdom: Elsevier Ltd., 2012:in press.
25. Butcher SE, Pyle AM. The molecular interactions that stabilize RNA tertiary structure: RNA motifs, patterns, and networks. Acc Chem Res 2011; 44:1302-11; PMID:21899297; http://dx.doi.org/10.1021/ar200098t.
26. Huppert JL, Bugaut A, Kumari S, Balasubramanian S. G-quadruplexes: the beginning and end of UTRs. Nucleic Acids Res 2008; 36:6260-8; PMID:18832370; http://dx.doi.org/10.1093/nar/gkn511.
27. Pyle AM. Metal ions in the structure and function of RNA. J Biol Inorg Chem 2002; 7:679-90; PMID:12203005; http://dx.doi.org/10.1007/s00775-002-0387-6. (Pubitemid 36056354)
28. Treiber DK, Williamson JR. Exposing the kinetic traps in RNA folding. Curr Opin Struct Biol 1999; 9:339-45; PMID:10361090; http://dx.doi.org/10.1016/ S0959-440X(99)80045-1. (Pubitemid 29454501)
29. Treiber DK, Williamson JR. Beyond kinetic traps in RNA folding. Curr Opin Struct Biol 2001; 11:309-14; PMID:11406379; http://dx.doi.org/10.1016/S0959- 440X(00)00206-2. (Pubitemid 32568270)
30. Williamson JR. Cooperativity in macromo-lecular assembly. Nat Chem Biol 2008; 4:458-65; PMID:18641626; http://dx.doi.org/10.1038/nchem-bio.102.
31. Woodson SA. Metal ions and RNA folding: a highly charged topic with a dynamic future. Curr Opin Chem Biol 2005; 9:104-9; PMID:15811793; http://dx.doi. org/10.1016/j.cbpa.2005.02.004. (Pubitemid 40462481)
32. Zhao R, Rueda D. Memory effects in RNA folding dynamics revealed by single-molecule fluorescence. In: Russell R, ed. Biophysics of RNA folding. New York, NY: Springer, 2012.
33. Herschlag D. RNA chaperones and the RNA folding problem. J Biol Chem 1995; 270:20871-4; PMID:7545662.
34. Pyle AM. Translocation and unwinding mechanisms of RNA and DNA helicases. Annu Rev Biophys 2008; 37:317-36; PMID:18573084; http://dx.doi. org/10.1146/annurev.biophys.37.032807.125908.
35. Gingras A-C, Raught B, Sonenberg N. Regulation of translation initiation by FRAP/mTOR. Genes Dev 2001; 15:807-26; PMID:11297505; http://dx.doi. org/10.1101/gad.887201. (Pubitemid 32295062)
36. Parsyan A, Shahbazian D, Martineau Y, Petroulakis E, Alain T, Larsson O, et al. The helicase protein DHX29 promotes translation initiation, cell proliferation, and tumorigenesis. Proc Natl Acad Sci USA 2009; 106:22217-22; PMID:20018725; http://dx.doi. org/10.1073/pnas.0909773106.
37. Fromont-Racine M, Senger B, Saveanu C, Fasiolo F. Ribosome assembly in eukaryotes. Gene 2003; 313:17-42; PMID:12957375; http://dx.doi.org/10.1016/ S0378-1119(03)00629-2. (Pubitemid 37338237)
38. Mayer C, Grummt I. Ribosome biogenesis and cell growth: mTOR coordinates transcription by all three classes of nuclear RNA polymerases. Oncogene 2006; 25:6384-91; PMID:17041624; http://dx.doi. org/10.1038/sj.onc.1209883. (Pubitemid 44582283)
39. Kar A, Fushimi K, Zhou X, Ray P, Shi C, Chen X, et al. RNA helicase p68 (DDX5) regulates tau exon 10 splicing by modulating a stem-loop structure at the 5¢ splice site. Mol Cell Biol 2011; 31:1812-21; PMID:21343338; http://dx.doi.org/10.1128/MCB.01149-10.
40. Liu Z-R. p68 RNA helicase is an essential human splicing factor that acts at the U1 snRNA-5?splice site duplex. Mol Cell Biol 2002; 22:5443-50; PMID:12101238; http://dx.doi.org/10.1128/MCB.22.15.5443-5450.2002. (Pubitemid 34755755)
41. Linder P, Jankowsky E. From unwinding to clamping-the DEAD box RNA helicase family. Nat Rev Mol Cell Biol 2011; 12:505-16; PMID:21779027; http://dx.doi.org/10.1038/nrm3154.
42. Newman MA, Hammond SM. Emerging paradigms of regulated microRNA processing. Genes Dev 2010; 24:1086-92; PMID:20516194; http://dx.doi. org/10.1101/gad.1919710.
43. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 2009; 11:228-34; PMID:19255566; http://dx.doi.org/10.1038/ncb0309-228.
44. Gong Z, Dong C-H, Lee H, Zhu J, Xiong L, Gong D, et al. A DEAD box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell 2005; 17:256-67; PMID:15598798; http://dx.doi.org/10.1105/tpc.104.027557. (Pubitemid 41673001)
45. Lai M-C, Lee YH, Tarn W-Y. The DEAD-box RNA helicase DDX3 associates with export messenger ribo-nucleoproteins as well as tip-associated protein and participates in translational control. Mol Biol Cell 2008; 19:3847-58; PMID:18596238; http://dx.doi. org/10.1091/mbc.E07-12-1264.
46. Ranji A, Boris-Lawrie K. RNA helicases: emerging roles in viral replication and the host innate response. RNA Biol 2010; 7:775-87; PMID:21173576; http://dx.doi. org/10.4161/rna.7.6.14249.
47. Lattmann S, Stadler MB, Vaughn J P, Akman SA, Nagamine Y. The DEAH-box RNA helicase RHAU binds an intramolecular RNA G-quadruplex in TERC and associates with telomerase holoenzyme. Nucleic Acids Res 2011; 39:9390-404; PMID:21846770; http://dx.doi.org/10.1093/nar/gkr630.
48. Henn A, Bradley MJ, De La Cruz EM. ATP utilization and RNA conformational rearrangement by DEAD-box proteins. Annu Rev Biophys 2012; 41:247-67; PMID:22404686; http://dx.doi.org/10.1146/annurev-biophys-050511-102243.
49. Cao W, Coman MM, Ding S, Henn A, Middleton ER, Bradley MJ, et al. Mechanism of Mss116 ATPase reveals functional diversity of DEAD-Box proteins. J Mol Biol 2011; 409:399-414; PMID:21501623; http://dx.doi.org/10.1016/j.jmb.2011. 04.004.
50. Henn A, Cao W, Licciardello N, Heitkamp SE, Hackney DD, De La Cruz EM. Pathway of ATP utilization and duplex rRNA unwinding by the DEAD-box helicase, DbpA. Proc Natl Acad Sci USA 2010; 107:4046-50; PMID:20160110; http://dx.doi. org/10.1073/pnas.0913081107.
51. Singleton MR, Dillingham MS, Wigley DB. Structure and mechanism of helicases and nucleic acid translocases. Annu Rev Biochem 2007; 76:23-50; PMID:17506634; http://dx.doi.org/10.1146/annurev. biochem.76.052305.115300.
52. Jankowsky E, Fairman ME. RNA helicases-one fold for many functions. Curr Opin Struct Biol 2007; 17:316-24; PMID:17574830; http://dx.doi.org/10.1016/j. sbi.2007.05.007. (Pubitemid 47021361)
53. Pyle AM. RNA helicases and remodeling proteins. Curr Opin Chem Biol 2011; 15:636-42; PMID:21862383; http://dx.doi.org/10.1016/j.cbpa.2011.07.019.
54. Andreou AZ, Klostermeier D. Conformational changes of DEAD-box helicases monitored by single molecule fluorescence resonance energy transfer. Methods Enzymol 2012; 511:75-109; PMID:22713316.
55. Tai C-L, Chi W-K, Chen D-S, Hwang L-H. The helicase activity associated with hepatitis C virus non-structural protein 3 (NS3). J Virol 1996; 70:8477-84; PMID:8970970. (Pubitemid 26378425)
56. Enukashvily N, Donev R, Sheer D, Podgornaya O. Satellite DNA binding and cellular localisation of RNA helicase P68. J Cell Sci 2005; 118:611-22; PMID:15657085; http://dx.doi.org/10.1242/jcs.01605. (Pubitemid 40310127)
57. Eggleston AK, Rahim NA, Kowalczykowski SC. A helicase assay based on the displacement of fluorescent, nucleic acid-binding ligands. Nucleic Acids Res 1996; 24:1179-86; PMID:8614617; http://dx.doi. org/10.1093/nar/24.7.1179. (Pubitemid 26102664)
58. Tseng-Rogenski SS, Chang T-H. RNA unwinding assay for DExD/H-box RNA helicases. Methods Mol Biol 2004; 257:93-102; PMID:14769999.
59. Yodh JG, Schlierf M, Ha T. Insight into helicase mechanism and function revealed through single-molecule approaches. Q Rev Biophys 2010; 43:185-217; PMID:20682090; http://dx.doi.org/10.1017/S0033583510000107.
60. Gordon M P, Ha T, Selvin PR. Single-molecule high-resolution imaging with photobleaching. Proc Natl Acad Sci USA 2004; 101:6462-5; PMID:15096603; http://dx.doi.org/10.1073/pnas.0401638101. (Pubitemid 38585996)
61. Blanco M, Walter NG. Analysis of complex single-molecule FRET time trajectories. Methods Enzymol 2010; 472:153-78; PMID:20580964; http://dx.doi. org/10.1016/S0076-6879(10)72011-5.
62. Diao J, Su Z, Lu X, Yoon T-Y, Shin Y-K, Ha T. Single-vesicle fusion assay reveals Munc18-1 binding to the SNARE core is sufficient for stimulating membrane fusion. ACS Chem Neurosci 2010; 1:168-74; PMID:20300453; http://dx.doi.org/10.1021/cn900034p.
63. Rasnik I, McKinney SA, Ha T. Surfaces and orientations: much to FRET about? Acc Chem Res 2005; 38:542-8; PMID:16028888; http://dx.doi. org/10.1021/ar040138c. (Pubitemid 41128406)
64. Walter NG, Huang C-Y, Manzo AJ, Sobhy MA. Do-it-yourself guide: how to use the modern single-molecule toolkit. Nat Methods 2008; 5:475-89; PMID:18511916; http://dx.doi.org/10.1038/nmeth.1215. (Pubitemid 351761755)
65. Uphoff S, Holden SJ, Le Reste L, Periz J, van de Linde S, Heilemann M, et al. Monitoring multiple distances within a single molecule using switchable FRET. Nat Methods 2010; 7:831-6; PMID:20818380; http://dx.doi.org/10.1038/nmeth. 1502.
66. Chung HS, Gopich IV, McHale K, Cellmer T, Louis JM, Eaton WA. Extracting rate coefficients from single-molecule photon trajectories and FRET efficiency histograms for a fast-folding protein. J Phys Chem A 2011; 115:3642-56; PMID:20509636; http://dx.doi. org/10.1021/jp1009669.
67. Rueda D, Walter NG. Single molecule fluorescence control for nanotechnology. J Nanosci Nanotechnol 2005; 5:1990-2000; PMID:16430133; http://dx.doi. org/10.1166/jnn.2005.505. (Pubitemid 44874822)
68. Karunatilaka KS, Rueda D. Single-molecule fluorescence studies of RNA: a decade's progress. Chem Phys Lett 2009; 476:1-10; PMID:20161154; http://dx.doi. org/10.1016/j.cplett.2009.06.001.
69. Neuman KC, Nagy A. Single-molecule force spec-troscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat Methods 2008; 5:491-505; PMID:18511917; http://dx.doi.org/10.1038/nmeth.1218. (Pubitemid 351761756)
70. Roy R, Hohng S, Ha T. A practical guide to single-molecule FRET. Nat Methods 2008; 5:507-16; PMID:18511918; http://dx.doi.org/10.1038/nmeth.1208. (Pubitemid 351761757)
71. Zhao R, Rueda D. RNA folding dynamics by single-molecule fluorescence resonance energy transfer. Methods 2009; 49:112-7; PMID:19409995; http://dx.doi.org/10.1016/j.ymeth.2009.04.017.
72. Cardo L, Karunatilaka KS, Rueda D, Sigel RKO. Single molecule FRET characterization of large ribozyme folding. In: Sigel A, Sigel H, Sigel RKO, eds. Ribozymes: methods and protocols. Totowa, NJ: Humana Press Inc., 2012:227-51.
73. Andreou AZ, Klostermeier D. The DEAD-box helicase eIF4A: Paradigm or the odd one out? RNA Biol 2012; 10: In press; PMID:22995829.
74. Hopfner K-P, Michaelis J. Mechanisms of nucleic acid translocases: lessons from structural biology and single-molecule biophysics. Curr Opin Struct Biol 2007; 17:87-95; PMID:17157498; http://dx.doi. org/10.1016/j.sbi.2006.11. 003. (Pubitemid 46240807)
75. Rasnik I, Myong S, Ha T. Unraveling helicase mechanisms one molecule at a time. Nucleic Acids Res 2006; 34:4225-31; PMID:16935883; http://dx.doi. org/10.1093/nar/gkl452. (Pubitemid 44542202)
76. Steimer L, Klostermeier D. RNA helicases in infection and disease. RNA Biol 2012; 9:751-71; PMID:22699555; http://dx.doi.org/10.4161/rna.20090.
77. Tinoco I, Chen G, Qu X. RNA Worlds: From Life's Origins to Diversity in Gene Regulation. In: Atkins J F, Gesteland R F, Cech TR, eds. Cold Spring Harbor Perspectives in Biology. Cold Spring Harbor: Cold Spring Harbor Laboratory Press, 2011.
78. Greenleaf WJ, Woodside M T, Block SM. High-resolution, single-molecule measurements of biomo-lecular motion. Annu Rev Biophys Biomol Struct 2007; 36:171-90; PMID:17328679; http://dx.doi. org/10.1146/annurev.biophys.36.101106. 101451. (Pubitemid 46998115)
79. Henn A, Medalia O, Shi S-P, Steinberg M, Franceschi F, Sagi I. Visualization of unwinding activity of duplex RNA by DbpA, a DEAD box helicase, at single-molecule resolution by atomic force microscopy. Proc Natl Acad Sci USA 2001; 98:5007-12; PMID:11296244; http://dx.doi.org/10.1073/pnas.071372498. (Pubitemid 32397073)
80. Marsden S, Nardelli M, Linder P, McCarthy JEG. Unwinding single RNA molecules using helicases involved in eukaryotic translation initiation. J Mol Biol 2006; 361:327-35; PMID:16828800; http://dx.doi. org/10.1016/j.jmb.2006.06. 016. (Pubitemid 44092780)
81. Dohoney KM, Gelles J. X-sequence recognition and DNA translocation by single RecBCD helicase/nucle-ase molecules. Nature 2000; 409:370-4; http://dx.doi. org/10.1038/35053124. (Pubitemid 32151245)
82. Fan H-F, Li H-W. Studying RecBCD helicase translo-cation along Chi-DNA using tethered particle motion with a stretching force. Biophys J 2009; 96:1875-83; PMID:19254546; http://dx.doi.org/10.1016/j. bpj.2008.11.048.
83. Dessinges M-N, Lionnet T, Xi XG, Bensimon D, Croquette V. Single-molecule assay reveals strand switching and enhanced processivity of UvrD. Proc Natl Acad Sci USA 2004; 101:6439-44; PMID:15079074; http://dx.doi.org/10.1073/pnas. 0306713101. (Pubitemid 38585992)
84. Sun B, Wei K-J, Zhang B, Zhang X-H, Dou S-X, Li M, et al. Impediment of E. coli UvrD by DNA-destabilizing force reveals a strained-inchworm mechanism of DNA unwinding. EMBO J 2008; 27:3279-87; PMID:19008855; http://dx.doi.org/10. 1038/emboj.2008.240.
85. Binnig G, Quate C F, Gerber C. Atomic force microscope. Phys Rev Lett 1986; 56:930-3; PMID:10033323; http://dx.doi.org/10.1103/PhysRevLett.56.930.
86. Cohen SR, Bitler A. Use of AFM in bio-related systems. Curr Opin Colloid Interface Sci 2008; 13:316-25; http://dx.doi.org/10.1016/j.cocis.2008.02.002.
87. Heus HA, Puchner EM, van Vugt-Jonker AJ, Zimmermann JL, Gaub HE. Atomic force microscope-based single-molecule force spectroscopy of RNA unfolding. Anal Biochem 2011; 414:1-6; PMID:21402049; http://dx.doi.org/10.1016/j. ab.2011.03.012.
88. Santos NC, Castanho MARB. An overview of the biophysical applications of atomic force microscopy. Biophys Chem 2004; 107:133-49; PMID:14962595; http://dx.doi.org/10.1016/j.bpc.2003.09.001. (Pubitemid 38220955)
89. Vilfan ID, Kamping W, van den Hout M, Candelli A, Hage S, Dekker NH. An RNA toolbox for single-molecule force spectroscopy studies. Nucleic Acids Res 2007; 35:6625-39; PMID:17905817; http://dx.doi. org/10.1093/nar/gkm585. (Pubitemid 350111627)
90. Katan AJ, Dekker C. High-speed AFM reveals the dynamics of single biomolecules at the nanometer scale. Cell 2011; 147:979-82; PMID:22118456; http://dx.doi.org/10.1016/j.cell.2011.11.017.
91. Neaves KJ, Huppert JL, Henderson RM, Edwardson JM. Direct visualization of G-quadruplexes in DNA using atomic force microscopy. Nucleic Acids Res 2009; 37:6269-75; PMID:19696072; http://dx.doi. org/10.1093/nar/gkp679.
92. Picco LM, Bozec L, Ulcinas A, Engledew DJ, Antognozzi M, Horton MA, et al. Breakingthe speed limit with atomic force microscopy. Nanotechnology 2007; 18:044030; http://dx.doi.org/10.1088/0957-4484/18/4/044030.
93. Ashkin A, Dziedzic JM, Bjorkholm JE, Chu S. Observation of a single-beam gradient force optical trap for dielectric particles. Opt Lett 1986; 11:288-90; PMID:19730608; http://dx.doi.org/10.1364/OL.11.000288. (Pubitemid 16117701)
94. Dholakia K, Reece P, Gu M. Optical micromanipula-tion. Chem Soc Rev 2008; 37:42-55; PMID:18197332; http://dx.doi.org/10.1039/b512471a.
95. Abbondanzieri EA, Greenleaf WJ, Shaevitz JW, Landick R, Block SM. Direct observation of base-pair stepping by RNA polymerase. Nature 2005; 438:460-5; PMID:16284617; http://dx.doi.org/10.1038/nature04268. (Pubitemid 41742012)
96. Herbert KM, La Porta A, Wong BJ, Mooney RA, Neuman KC, Landick R, et al. Sequence-resolved detection of pausing by single RNA polymerase molecules. Cell 2006; 125:1083-94; PMID:16777599; http://dx.doi.org/10.1016/j.cell.2006.04.032. (Pubitemid 43866198)
97. Rohrbach A. Switching and measuring a force of 25 femtoNewtons with an optical trap. Opt Express 2005; 13:9695-701; PMID:19503175; http://dx.doi. org/10.1364/OPEX.13.009695. (Pubitemid 41692738)
98. Shaevitz JW, Abbondanzieri EA, Landick R, Block SM. Backtracking by single RNA polymerase molecules observed at near-base-pair resolution. Nature 2003; 426:684-7; PMID:14634670; http://dx.doi. org/10.1038/nature02191. (Pubitemid 38009379)
99. Hodges C, Bintu L, Lubkowska L, Kashlev M, Bustamante C. Nucleosomal fluctuations govern the transcription dynamics of RNA polymerase II. Science 2009; 325:626-8; PMID:19644123; http://dx.doi. org/10.1126/science.1172926.
100. Wang MD, Yin H, Landick R, Gelles J, Block SM. Stretching DNA with optical tweezers. Biophys J 1997; 72:1335-46; PMID:9138579; http://dx.doi. org/10.1016/S0006-3495(97)78780-0. (Pubitemid 27113656)
101. Finer JT, Simmons RM, Spudich JA. Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 1994; 368:113-9; PMID:8139653; http://dx.doi.org/10.1038/368113a0. (Pubitemid 24101520)
102. Svoboda K, Schmidt CF, Schnapp BJ, Block SM. Direct observation of kinesin stepping by optical trapping interferometry. Nature 1993; 365:721-7; PMID:8413650; http://dx.doi.org/10.1038/365721a0. (Pubitemid 23339876)
103. Hendricks AG, Holzbaur ELF, Goldman YE. Force measurements on cargoes in living cells reveal collective dynamics of microtubule motors. Proc Natl Acad Sci USA 2012; 109:18447-52; PMID:23091040; http://dx.doi.org/10.1073/pnas. 1215462109.
104. Block SM. Making light work with optical tweezers. Nature 1992; 360:493-5; PMID:1448176; http://dx.doi.org/10.1038/360493a0.
105. Kozak M. Influences of mRNA secondary structure on initiation by eukaryotic ribosomes. Proc Natl Acad Sci USA 1986; 83:2850-4; PMID:3458245; http://dx.doi. org/10.1073/pnas.83.9.2850. (Pubitemid 16041760)
106. Kozak M. Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene 2005; 361:13-37; PMID:16213112; http://dx.doi.org/10.1016/j. gene.2005.06.037. (Pubitemid 41506931)
107. Vega Laso MR, Zhu D, Sagliocco F, Brown AJP, Tuite M F, McCarthy JEG. Inhibition of translational initiation in the yeast Saccharomyces cerevisiae as a function of the stability and position of hairpin structures in the mRNA leader. J Biol Chem 1993; 268:6453-62; PMID:8454618. (Pubitemid 23099343)
108. Kumari S, Bugaut A, Huppert JL, Balasubramanian S. An RNA G-quadruplex in the 5? UTR of the NRAS proto-oncogene modulates translation. Nat Chem Biol 2007; 3:218-21; PMID:17322877; http://dx.doi. org/10.1038/nchembio864. (Pubitemid 46440536)
109. Rogers GW Jr., Richter NJ, Merrick WC. Biochemical and kinetic characterization of the RNA helicase activity of eukaryotic initiation factor 4A. J Biol Chem 1999; 274:12236-44; PMID:10212190; http://dx.doi. org/10.1074/jbc.274.18.12236.
110. Iost I, Dreyfus M, Linder P. Ded1p, a DEAD-box protein required for translation initiation in Saccharomyces cerevisiae, is an RNA helicase. J Biol Chem 1999; 274:17677-83; PMID:10364207; http://dx.doi.org/10.1074/jbc.274.25. 17677.
111. Hilbert M, Kebbel F, Gubaev A, Klostermeier D. eIF4G stimulates the activity of the DEAD box protein eIF4A by a conformational guidance mechanism. Nucleic Acids Res 2011; 39:2260-70; PMID:21062831; http://dx.doi.org/10.1093/ nar/gkq1127.
112. Dumont S, Cheng W, Serebrov V, Beran RK, Tinoco I Jr., Pyle AM, et al. RNA translocation and unwinding mechanism of HCV NS3 helicase and its coordination by ATP. Nature 2006; 439:105-8; PMID:16397502; http://dx.doi.org/ 10.1038/nature04331. (Pubitemid 43053637)
113. Dimitrova M, Imbert I, Kieny M P, Schuster C. Protein-protein interactions between hepatitis C virus nonstructural proteins. J Virol 2003; 77:5401-14; PMID:12692242; http://dx.doi.org/10.1128/JVI.77.9.5401-5414.2003. (Pubitemid 36460954)
114. Pang PS, Jankowsky E, Planet PJ, Pyle AM. The hepatitis C viral NS3 protein is a processive DNA helicase with cofactor enhanced RNA unwinding. EMBO J 2002; 21:1168-76; PMID:11867545; http://dx.doi. org/10.1093/emboj/21.5.1168. (Pubitemid 34206190)
115. Cheng W, Dumont S, Tinoco I Jr., Bustamante C. NS3 helicase actively separates RNA strands and senses sequence barriers ahead of the opening fork. Proc Natl Acad Sci USA 2007; 104:13954-9; PMID:17709749; http://dx.doi.org/10. 1073/pnas.0702315104. (Pubitemid 350003319)
116. Bustamante C, Marko J F, Siggia ED, Smith S. Entropic elasticity of lambda-phage DNA. Science 1994; 265:1599-600; PMID:8079175; http://dx.doi. org/10.1126/science.8079175.
117. Serebrov V, Pyle AM. Periodic cycles of RNA unwinding and pausing by hepatitis C virus NS3 helicase. Nature 2004; 430:476-80; PMID:15269774; http://dx.doi.org/10.1038/nature02704. (Pubitemid 38987912)
118. Myong S, Bruno MM, Pyle AM, Ha T. Spring-loaded mechanism of DNA unwinding by hepatitis C virus NS3 helicase. Science 2007; 317:513-6; PMID:17656723; http://dx.doi.org/10.1126/sci-ence.1144130. (Pubitemid 47196115)
119. Cheng W, Arunajadai SG, Moffitt JR, Tinoco IJ Jr., Bustamante C. Single-base pair unwinding and asynchronous RNA release by the hepatitis C virus NS3 helicase. Science 2011; 333:1746-9; PMID:21940894; http://dx.doi.org/10. 1126/science.1206023.
120. Appleby TC, Anderson R, Fedorova O, Pyle AM, Wang R, Liu X, et al. Visualizing ATP-dependent RNA trans-location by the NS3 helicase from HCV. J Mol Biol 2011; 405:1139-53; PMID:21145896; http://dx.doi. org/10.1016/j.jmb.2010. 11.034.
121. Fairman-Williams ME, Jankowsky E. Unwinding initiation by the viral RNA helicase NPH-II. J Mol Biol 2012; 415:819-32; PMID:22155080; http://dx.doi. org/10.1016/j.jmb.2011.11.045.
122. Kalinin S, Peulen T, Sindbert S, Rothwell PJ, Berger S, Restle T, et al. A toolkit and benchmark study for FRET-restrained high-precision structural modeling. Nat Methods 2012; 9:1218-25; PMID:23142871; http://dx.doi.org/10.1038/ nmeth.2222.
123. Orte A, Clarke R, Klenerman D. Single-molecule two-colour coincidence detection to probe biomo-lecular associations. Biochem Soc Trans 2010; 38:914-8; PMID:20658976; http://dx.doi.org/10.1042/BST0380914.
124. Karunatilaka KS, Solem A, Pyle AM, Rueda D. Single-molecule analysis of Mss116-mediated group II intron folding. Nature 2010; 467:935-9; PMID:20944626; http://dx.doi.org/10.1038/nature09422.
125. Yang Q, Jankowsky E. The DEAD-box protein Ded1 unwinds RNA duplexes by a mode distinct from translocating helicases. Nat Struct Mol Biol 2006; 13:981-6; PMID:17072313; http://dx.doi.org/10.1038/nsmb1165. (Pubitemid 44684849)
126. Aregger R, Klostermeier D. The DEAD box heli-case YxiN maintains a closed conformation during ATP hydrolysis. Biochemistry 2009; 48:10679-81; PMID:19839642; http://dx.doi.org/10.1021/bi901278p.
127. Karow AR, Klostermeier D. A conformational change in the helicase core is necessary but not sufficient for RNA unwinding by the DEAD box helicase YxiN. Nucleic Acids Res 2009; 37:4464-71; PMID:19474341; http://dx.doi.org/10.1093/ nar/gkp397.
128. Linden MH, Hartmann RK, Klostermeier D. The putative RNase P motif in the DEAD box helicase Hera is dispensable for efficient interaction with RNA and helicase activity. Nucleic Acids Res 2008; 36:5800-11; PMID:18782831; http://dx.doi.org/10.1093/nar/gkn581.
129. Theissen B, Karow AR, Köhler J, Gubaev A, Klostermeier D. Cooperative binding of ATP and RNA induces a closed conformation in a DEAD box RNA helicase. Proc Natl Acad Sci USA 2008; 105:548-53; PMID:18184816; http://dx.doi.org/10.1073/pnas.0705488105. (Pubitemid 351171745)
130. Holden SJ, Uphoff S, Hohlbein J, Yadin D, Le Reste L, Britton OJ, et al. Defining the limits of single-molecule FRET resolution in TIRF microscopy. Biophys J 2010; 99:3102-11; PMID:21044609; http://dx.doi. org/10.1016/j.bpj. 2010.09.005.
131. Ha T, Tinnefeld P. Photophysics of fluorescent probes for single-molecule biophysics and super-resolution imaging. Annu Rev Phys Chem 2012; 63:595-617; PMID:22404588; http://dx.doi.org/10.1146/annurev-physchem-032210-103340.
132. Rasnik I, McKinney SA, Ha T. Nonblinking and long-lasting single-molecule fluorescence imaging. Nat Methods 2006; 3:891-3; PMID:17013382; http://dx.doi.org/10.1038/nmeth934. (Pubitemid 44614723)
133. Cordes T, Vogelsang J, Tinnefeld P. On the mechanism of Trolox as antiblinking and antibleaching reagent. J Am Chem Soc 2009; 131:5018-9; PMID:19301868; http://dx.doi.org/10.1021/ja809117z.
134. Vogelsang J, Kasper R, Steinhauer C, Person B, Heilemann M, Sauer M, et al. A reducing and oxidizing system minimizes photobleaching and blinking of fluorescent dyes. Angew Chem Int Ed Engl 2008; 47:5465-9; PMID:18601270; http://dx.doi. org/10.1002/anie.200801518.
135. Myong S, Cui S, Cornish PV, Kirchhofer A, Gack MU, Jung JU, et al. Cytosolic viral sensor RIG-I is a 5?-tri-phosphate-dependent translocase on double-stranded RNA. Science 2009; 323:1070-4; PMID:19119185; http://dx.doi.org/10.1126/science.1168352.
136. Hwang H, Kim H, Myong S. Protein induced fluorescence enhancement as a single molecule assay with short distance sensitivity. Proc Natl Acad Sci USA 2011; 108:7414-8; PMID:21502529; http://dx.doi. org/10.1073/pnas.1017672108.
137. Huang Z, Ji D, Xia A, Koberling F, Patting M, Erdmann R. Direct observation of delayed fluorescence from a remarkable back-isomerization in Cy5. J Am Chem Soc 2005; 127:8064-6; PMID:15926831; http://dx.doi.org/10.1021/ ja050050+. (Pubitemid 40799661)
138. Markiewicz R P, Vrtis KB, Rueda D, Romano LJ. Single-molecule microscopy reveals new insights into nucleotide selection by DNA polymerase I. Nucleic Acids Res 2012; 40:7975-84; PMID:22669904; http://dx.doi.org/10.1093/nar/gks523.
139. Deniz AA, Dahan M, Grunwell JR, Ha T, Faulhaber AE, Chemla DS, et al. Single-pair fluorescence resonance energy transfer on freely diffusing molecules: observation of Förster distance dependence and sub-populations. Proc Natl Acad Sci USA 1999; 96:3670-5; PMID:10097095; http://dx.doi.org/10. 1073/pnas.96.7.3670. (Pubitemid 29168968)
140. Yang Q, Fairman ME, Jankowsky E. DEAD-box-protein-assisted RNA structure conversion towards and against thermodynamic equilibrium values. J Mol Biol 2007; 368:1087-100; PMID:17391697; http://dx.doi. org/10.1016/j.jmb.2007.02.071. (Pubitemid 46574663)
141. Staley J P, Guthrie C. Mechanical devices of the spli-ceosome: motors, clocks, springs, and things. Cell 1998; 92:315-26; PMID:9476892; http://dx.doi. org/10.1016/S0092-8674(00)80925-3. (Pubitemid 28093010)
142. Schroeder R, Barta A, Semrad K. Strategies for RNA folding and assembly. Nat Rev Mol Cell Biol 2004; 5:908-19; PMID:15520810; http://dx.doi. org/10.1038/nrm1497. (Pubitemid 39486542)
143. Kapanidis AN, Lee NK, Laurence TA, Doose S, Margeat E, Weiss S. Fluorescence-aided molecule sorting: analysis of structure and interactions by alternating-laser excitation of single molecules. Proc Natl Acad Sci USA 2004; 101:8936-41; PMID:15175430; http://dx.doi.org/10.1073/pnas.0401690101. (Pubitemid 38781589)
144. Kapanidis AN, Laurence TA, Lee NK, Margeat E, Kong X, Weiss S. Alternating-laser excitation of single molecules. Acc Chem Res 2005; 38:523-33; PMID:16028886; http://dx.doi.org/10.1021/ar0401348. (Pubitemid 41128404)
145. Kim DW, Gwack Y, Han JH, Choe J. C-terminal domain of the hepatitis C virus NS3 protein contains an RNA helicase activity. Biochem Biophys Res Commun 1995; 215:160-6; PMID:7575585; http://dx.doi.org/10.1006/bbrc.1995.2447.
146. Gross CH, Shuman S. Vaccinia virions lacking the RNA helicase nucleoside triphosphate phosphohydro-lase II are defective in early transcription. J Virol 1996; 70:8549-57; PMID:8970979. (Pubitemid 26378434)
147. Jankowsky E, Gross CH, Shuman S, Pyle AM. The DExH protein NPH-II is a processive and directional motor for unwinding RNA. Nature 2000; 403:447-51; PMID:10667799; http://dx.doi. org/10.1038/35000239. (Pubitemid 30073096)
148. Shuman S. Vaccinia virus RNA helicase. Directionality and substrate specificity. J Biol Chem 1993; 268:11798-802; PMID:8505308. (Pubitemid 23168133)
149. Wong I, Lohman TM. A two-site mechanism for ATP hydrolysis by the asymmetric Rep dimer P2S as revealed by site-specific inhibition with ADP-A1F4. Biochemistry 1997; 36:3115-25; PMID:9115987; http://dx.doi.org/10.1021/ bi9621977. (Pubitemid 27142382)
150. Levin MK, Gurjar MM, Patel SS. ATP binding modulates the nucleic acid affinity of hepatitis C virus helicase. J Biol Chem 2003; 278:23311-6; PMID:12660239; http://dx.doi.org/10.1074/jbc. M301283200. (Pubitemid 36830145)
151. Chen B, Doucleff M, Wemmer DE, De Carlo S, Huang HH, Nogales E, et al. ATP ground-and transition states of bacterial enhancer binding AAA+ ATPases support complex formation with their target protein, sigma54. Structure 2007; 15:429-40; PMID:17437715; http://dx.doi.org/10.1016/j.str.2007.02.007. (Pubitemid 46551727)
152. Liu F, Putnam A, Jankowsky E. ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding. Proc Natl Acad Sci USA 2008; 105:20209-14; PMID:19088201; http://dx.doi. org/10.1073/pnas.0811115106.
153. Gu M, Rice CM. Three conformational snapshots of the hepatitis C virus NS3 helicase reveal a ratchet translocation mechanism. Proc Natl Acad Sci USA 2010; 107:521-8; PMID:20080715; http://dx.doi. org/10.1073/pnas.0913380107.
154. Chakrabarti S, Jayachandran U, Bonneau F, Fiorini F, Basquin C, Domcke S, et al. Molecular mechanisms for the RNA-dependent ATPase activity of Upf1 and its regulation by Upf2. Mol Cell 2011; 41:693-703; PMID:21419344; http://dx.doi.org/10.1016/j.mol-cel.2011.02.010.
155. Kawaoka J, Jankowsky E, Pyle AM. Backbone tracking by the SF2 helicase NPH-II. Nat Struct Mol Biol 2004; 11:526-30; PMID:15146171; http://dx.doi. org/10.1038/nsmb771. (Pubitemid 38691919)
156. Kawaoka J, Pyle AM. Choosing between DNA and RNA: the polymer specificity of RNA helicase NPH-II. Nucleic Acids Res 2005; 33:644-9; PMID:15681616; http://dx.doi.org/10.1093/nar/gki208. (Pubitemid 40360994)
157. Huang HR, Rowe CE, Mohr S, Jiang Y, Lambowitz AM, Perlman PS. 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 2005; 102:163-8; PMID:15618406; http://dx.doi.org/10.1073/pnas.0407896101. (Pubitemid 40094446)
158. Waldsich C, Pyle AM. A folding control element for tertiary collapse of a group II intron ribozyme. Nat Struct Mol Biol 2007; 14:37-44; PMID:17143279; http://dx.doi.org/10.1038/nsmb1181. (Pubitemid 46067421)
159. Halls C, Mohr S, Del Campo M, Yang Q, Jankowsky E, Lambowitz AM. 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 2007; 365:835-55; PMID:17081564; http://dx.doi. org/10.1016/j.jmb.2006.09.083. (Pubitemid 46001664)
160. Ha T, Rasnik I, Cheng W, Babcock H P, Gauss GH, Lohman TM, et al. Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase. Nature 2002; 419:638-41; PMID:12374984; http://dx.doi. org/10.1038/nature01083.
161. Lamichhane R, Solem A, Black W, Rueda D. Single-molecule FRET of protein-nucleic acid and protein-protein complexes: surface passivation and immobilization. Methods 2010; 52:192-200; PMID:20554047; http://dx.doi.org/10. 1016/j.ymeth.2010.06.010.
162. Steiner M, Karunatilaka KS, Sigel RKO, Rueda D. Single-molecule studies of group II intron ribo-zymes. Proc Natl Acad Sci USA 2008; 105:13853-8; PMID:18772388; http://dx.doi.org/10.1073/pnas.0804034105.
163. Steiner M, Rueda D, Sigel RKO. Ca2+ induces the formation of two distinct subpopulations of group II intron molecules. Angew Chem Int Ed Engl 2009; 48:9739-42; PMID:19924747; http://dx.doi. org/10.1002/anie.200903809.
164. Swisher J F, Su LJ, Brenowitz M, Anderson VE, Pyle AM. Productive folding to the native state by a group II intron ribozyme. J Mol Biol 2002; 315:297-310; PMID:11786013; http://dx.doi.org/10.1006/jmbi.2001.5233. (Pubitemid 34729341)
165. Binder M, Eberle F, Seitz S, Mücke N, Hüber CM, Kiani N, et al. Molecular mechanism of signal perception and integration by the innate immune sensor retinoic acid-inducible gene-I (RIG-I). J Biol Chem 2011; 286:27278-87; PMID:21659521; http://dx.doi. org/10.1074/jbc.M111.256974.
166. Hornung V, Ellegast J, Kim S, Brzózka K, Jung A, Kato H, et al. 5?-Triphosphate RNA is the ligand for RIG-I. Science 2006; 314:994-7; PMID:17038590; http://dx.doi.org/10.1126/science.1132505.
167. Gack MU, Shin YC, Joo CH, Urano T, Liang C, Sun L, et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 2007; 446:916-20; PMID:17392790; http://dx.doi. org/10.1038/nature05732. (Pubitemid 46633167)
168. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 2004; 5:730-7; PMID:15208624; http://dx.doi. org/10.1038/ni1087. (Pubitemid 39023305)
169. Saito T, Hirai R, Loo YM, Owen D, Johnson CL, Sinha SC, et al. Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc Natl Acad Sci USA 2007; 104:582-7; PMID:17190814; http://dx.doi.org/10.1073/pnas.0606699104. (Pubitemid 46123068)
170. Ellis RJ, Minton A P. Cell biology: join the crowd. Nature 2003; 425:27-8; PMID:12955122; http://dx.doi.org/10.1038/425027a.
171. Lee S, Lee J, Hohng S. Single-molecule three-color FRET with both negligible spectral overlap and long observation time. PLoS One 2010; 5:e12270; PMID:20808851; http://dx.doi.org/10.1371/journal. pone.0012270.
172. Sakatshii SK, Shubeita GT, Dietler G. On the possibility of observation of single quadrupoles by fluorescence resonance energy transfer scanning near-field optical microscopy. Opt Commun 2000; 188:41-5; http://dx.doi.org/10. 1016/S0030-4018(00)01154-8. (Pubitemid 32196124)
173. Selvin PR. Lanthanide-based resonance energy transfer. J Sel Top Quant Electron 1996; 2:1077-87; http://dx.doi.org/10.1109/2944.577339. (Pubitemid 126543850)
174. Gack MU, Kirchhofer A, Shin YC, Inn K-S, Liang C, Cui S, et al. Roles of RIG-I N-terminal tandem CARD and splice variant in TRIM25-mediated antiviral signal transduction. Proc Natl Acad Sci USA 2008; 105:16743-8; PMID:18948594; http://dx.doi. org/10.1073/pnas.0804947105.
175. Campos LA, Liu J, Wang X, Ramanathan R, English DS, Muñoz V. A photoprotection strategy for microsecond-resolution single-molecule fluorescence spectros-copy. Nat Methods 2011; 8:143-6; PMID:21217750; http://dx.doi.org/10. 1038/nmeth.1553.
176. Tanner NK, Linder P. DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol Cell 2001; 8:251-62; PMID:11545728; http://dx.doi.org/10.1016/S1097-2765(01)00329-X. (Pubitemid 32831543)
177. Kossen K, Uhlenbeck OC. Cloning and biochemical characterization of Bacillus subtilis YxiN, a DEAD protein specifically activated by 23S rRNA: delineation of a novel sub-family of bacterial DEAD proteins. Nucleic Acids Res 1999; 27:3811-20; PMID:10481020; http://dx.doi.org/10.1093/nar/27.19.3811. (Pubitemid 29454429)
178. Kossen K, Karginov F V, Uhlenbeck OC. The carboxy-terminal domain of the DExDH protein YxiN is sufficient to confer specificity for 23S rRNA. J Mol Biol 2002; 324:625-36; PMID:12460566; http://dx.doi. org/10.1016/S0022-2836(02)01140- 3. (Pubitemid 36044102)