DEAD-Box Helicase Proteins Disrupt RNA Tertiary Structure Through Helix Capture

PLoS Biology

Volumn 12, Issue 10, 2014, Pages

  Pan, Cynthia ^a   Potratz, Jeffrey P ^a,b   Cannon, Brian ^a,c   Simpson, Zachary B ^a   Ziehr, Jessica L ^a   Tijerina, Pilar ^a   Russell, Rick ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b ST EDWARD'S UNIVERSITY   (United States)

^c LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DEAD BOX PROTEIN; DEAD BOX PROTEIN CYT 19; DEAD BOX PROTEIN DED1; RIBOZYME; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; COMPLEX FORMATION; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HELIX CAPTURE; HELIX UNWINDING; INTRON; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; NUCLEIC ACID STRUCTURE, METABOLISM AND FUNCTION; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTEIN UNFOLDING; RIBOSOME; RNA FOLDING; RNA REMODELING; RNA STABILITY; RNA STRUCTURE; RNA TERTIARY STRUCTURE; SINGLE MOLECULE FORSTER RESONANCE ENERGY TRANSFER; SPLICEOSOME; STRUCTURE ACTIVITY RELATION; TETRAHYMENA THERMOPHILA; METABOLISM; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

DEAD-BOX RNA HELICASES; FLUORESCENCE RESONANCE ENERGY TRANSFER; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RNA, CATALYTIC; TETRAHYMENA THERMOPHILA;

EID: 84920467703     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001981     Document Type: Article

References (62)

1. Will CL, Lührmann R, (2011) Spliceosome structure and function. Cold Spring Harb Perspect Biol 3 doi:10.1101/cshperspect.a003707
2. Breaker RR, (2012) Riboswitches and the RNA world. Cold Spring Harb Perspect Biol 4 doi:10.1101/cshperspect.a003566
3. Noller HF, (2005) RNA structure: reading the ribosome. Science 309: 1508–1514 doi:10.1126/science.1111771
4. Chen J, Tsai A, O'Leary SE, Petrov A, Puglisi JD, (2012) Unraveling the dynamics of ribosome translocation. Curr Opin Struct Biol 22: 804–814 doi:10.1016/j.sbi.2012.09.004
5. Egan ED, Collins K, (2012) Biogenesis of telomerase ribonucleoproteins. RNA 18: 1747–1759 doi:10.1261/rna.034629.112
6. Herschlag D, (1995) RNA chaperones and the RNA folding problem. J Biol Chem 270: 20871–20874.
7. Rajkowitsch L, Chen D, Stampfl S, Semrad K, Waldsich C, et al. (2007) RNA chaperones, RNA annealers and RNA helicases. RNA Biol 4: 118–130.
8. Russell R, (2008) RNA misfolding and the action of chaperones. Front Biosci 13: 1–20.
9. Henn A, Bradley MJ, De La Cruz EM, (2012) ATP utilization and RNA conformational rearrangement by DEAD-box proteins. Annu Rev Biophys 41: 247–267 doi:10.1146/annurev-biophys-050511-102243
10. Linder P, Jankowsky E, (2011) From unwinding to clamping - the DEAD box RNA helicase family. Nat Rev Mol Cell Biol 12: 505–516 doi:10.1038/nrm3154
11. Jankowsky E, (2011) RNA helicases at work: binding and rearranging. Trends Biochem Sci 36: 19–29 doi:10.1016/j.tibs.2010.07.008
12. Russell R, Jarmoskaite I, Lambowitz AM, (2013) Toward a molecular understanding of RNA remodeling by DEAD-box proteins. RNA Biol 10: 44–55 doi:10.4161/rna.22210
13. Fairman ME, Maroney PA, Wang W, Bowers HA, Gollnick P, et al. (2004) Protein displacement by DExH/D “RNA helicases” without duplex unwinding. Science 304: 730–734 doi:10.1126/science.1095596
14. Yang Q, Jankowsky E, (2005) ATP- and ADP-dependent modulation of RNA unwinding and strand annealing activities by the DEAD-box protein DED1. Biochemistry 44: 13591–13601 doi:10.1021/bi0508946
15. Karunatilaka KS, Solem A, Pyle AM, Rueda D, (2010) Single-molecule analysis of Mss116-mediated group II intron folding. Nature 467: 935–939 doi:10.1038/nature09422
16. Rogers GW, Komar AA, Merrick WC, (2002) eIF4A: the godfather of the DEAD box helicases. Prog Nucleic Acid Res Mol Biol 72: 307–331.
17. Tijerina P, Bhaskaran H, 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 U S A 103: 16698–16703 doi:10.1073/pnas.0603127103
18. Russell R, Das R, Suh H, Travers KJ, Laederach A, et al. (2006) The paradoxical behavior of a highly structured misfolded intermediate in RNA folding. J Mol Biol 363: 531–544 doi:10.1016/j.jmb.2006.08.024
19. Sinan S, Yuan X, Russell R, (2011) The Azoarcus group I intron ribozyme misfolds and is accelerated for refolding by ATP-dependent RNA chaperone proteins. J Biol Chem 286: 37304–37312 doi:10.1074/jbc.M111.287706
20. Treiber DK, Rook MS, Zarrinkar PP, Williamson JR, (1998) Kinetic intermediates trapped by native interactions in RNA folding. Science 279: 1943–1946.
21. Shcherbakova I, Mitra S, Laederach A, Brenowitz M, (2008) Energy barriers, pathways, and dynamics during folding of large, multidomain RNAs. Curr Opin Chem Biol 12: 655–666 doi:10.1016/j.cbpa.2008.09.017
22. Jarmoskaite I, Russell R, (2011) DEAD-box proteins as RNA helicases and chaperones. Wiley Interdiscip Rev RNA 2: 135–152 doi:10.1002/wrna.50
23. Mohr S, Stryker JM, Lambowitz AM, (2002) A DEAD-box protein functions as an ATP-dependent RNA chaperone in group I intron splicing. Cell 109: 769–779.
24. Bhaskaran H, Russell R, (2007) Kinetic redistribution of native and misfolded RNAs by a DEAD-box chaperone. Nature 449: 1014–1018 doi:10.1038/nature06235
25. Bartley LE, Zhuang X, Das R, Chu S, Herschlag D, (2003) Exploration of the transition state for tertiary structure formation between an RNA helix and a large structured RNA. J Mol Biol 328: 1011–1026.
26. Narlikar GJ, Herschlag D, (1996) Isolation of a local tertiary folding transition in the context of a globally folded RNA. Nat Struct Biol 3: 701–710.
27. Narlikar GJ, Khosla M, Usman N, Herschlag D, (1997) Quantitating tertiary binding energies of 2′ OH groups on the P1 duplex of the Tetrahymena ribozyme: intrinsic binding energy in an RNA enzyme. Biochemistry 36: 2465–2477 doi:10.1021/bi9610820
28. Solomatin SV, Greenfeld M, Chu S, Herschlag D, (2010) Multiple native states reveal persistent ruggedness of an RNA folding landscape. Nature 463: 681–684 doi:10.1038/nature08717
29. Zhuang X, Bartley LE, Babcock HP, Russell R, Ha T, et al. (2000) A single-molecule study of RNA catalysis and folding. Science 288: 2048–2051.
30. Strobel SA, Cech TR, (1993) Tertiary interactions with the internal guide sequence mediate docking of the P1 helix into the catalytic core of the Tetrahymena ribozyme. Biochemistry 32: 13593–13604.
31. Theissen B, Karow AR, Köhler J, Gubaev A, Klostermeier D, (2008) Cooperative binding of ATP and RNA induces a closed conformation in a DEAD box RNA helicase. Proc Natl Acad Sci U S A 105: 548–553 doi:10.1073/pnas.0705488105
32. Del Campo M, Lambowitz AM, (2009) Structure of the Yeast DEAD box protein Mss116p reveals two wedges that crimp RNA. Mol Cell 35: 598–609 doi:10.1016/j.molcel.2009.07.032
33. Sengoku T, Nureki O, Nakamura A, Kobayashi S, Yokoyama S, (2006) Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 125: 287–300 doi:10.1016/j.cell.2006.01.054
34. Mallam AL, Del Campo M, Gilman B, Sidote DJ, Lambowitz AM, (2012) Structural basis for RNA-duplex recognition and unwinding by the DEAD-box helicase Mss116p. Nature 490: 121–125 doi:10.1038/nature11402
35. Grohman JK, Del Campo M, Bhaskaran H, Tijerina P, Lambowitz AM, et al. (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 doi:10.1021/bi0619472
36. Mallam AL, Jarmoskaite I, Tijerina P, Del Campo M, Seifert S, et al. (2011) Solution structures of DEAD-box RNA chaperones reveal conformational changes and nucleic acid tethering by a basic tail. Proc Natl Acad Sci U S A 108: 12254–12259 doi:10.1073/pnas.1109566108
37. Tarn W-Y, Chang T-H, (2009) The current understanding of Ded1p/DDX3 homologs from yeast to human. RNA Biol 6: 17–20.
38. Linder P, (2003) Yeast RNA helicases of the DEAD-box family involved in translation initiation. Biol Cell 95: 157–167.
39. Putnam AA, Jankowsky E, (2013) DEAD-box helicases as integrators of RNA, nucleotide and protein binding. Biochim Biophys Acta 1829: 884–893 doi:10.1016/j.bbagrm.2013.02.002
40. Yang Q, Del Campo M, Lambowitz AM, Jankowsky E, (2007) DEAD-box proteins unwind duplexes by local strand separation. Mol Cell 28: 253–263 doi:10.1016/j.molcel.2007.08.016
41. Yang Q, Jankowsky E, (2006) The DEAD-box protein Ded1 unwinds RNA duplexes by a mode distinct from translocating helicases. Nat Struct Mol Biol 13: 981–986 doi:10.1038/nsmb1165
42. Betterton MD, Jülicher F, (2005) Opening of nucleic-acid double strands by helicases: active versus passive opening. Phys Rev E Stat Nonlin Soft Matter Phys 71: 011904.
43. Manosas M, Xi XG, Bensimon D, Croquette V, (2010) Active and passive mechanisms of helicases. Nucleic Acids Res 38: 5518–5526 doi:10.1093/nar/gkq273
44. Sattin BD, Zhao W, Travers K, Chu S, Herschlag D, (2008) Direct measurement of tertiary contact cooperativity in RNA folding. J Am Chem Soc 130: 6085–6087 doi:10.1021/ja800919q
45. Engelhardt MA, Doherty EA, Knitt DS, Doudna JA, Herschlag D, (2000) The P5abc peripheral element facilitates preorganization of the Tetrahymena group I ribozyme for catalysis. Biochemistry 39: 2639–2651.
46. Shi X, Bisaria N, Benz-Moy TL, Bonilla S, Pavlichin DS, et al. (2014) Roles of long-range tertiary interactions in limiting dynamics of the Tetrahymena group I ribozyme. J Am Chem Soc 136: 6643–6648 doi:10.1021/ja413033d
47. Jarmoskaite I, Bhaskaran H, Seifert S, 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(29): E2928–E2936 doi:10.1073/pnas.1404307111
48. Rouskin S, Zubradt M, Washietl S, Kellis M, Weissman JS, (2014) Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo. Nature 505: 701–705 doi:10.1038/nature12894
49. Jamieson DJ, Rahe B, Pringle J, Beggs JD, (1991) A suppressor of a yeast splicing mutation (prp8-1) encodes a putative ATP-dependent RNA helicase. Nature 349: 715–717 doi:10.1038/349715a0
50. Chuang RY, Weaver PL, Liu Z, Chang TH, (1997) Requirement of the DEAD-Box protein Ded1p for messenger RNA translation. Science 275: 1468–1471.
51. De la Cruz J, Iost I, Kressler D, Linder P, (1997) The p20 and Ded1 proteins have antagonistic roles in eIF4E-dependent translation in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 94: 5201–5206.
52. Iost I, Dreyfus M, Linder P, (1999) Ded1p, a DEAD-box protein required for translation initiation in Saccharomyces cerevisiae, is an RNA helicase. J Biol Chem 274: 17677–17683.
53. Beckham C, Hilliker A, Cziko A-M, Noueiry A, Ramaswami M, et al. (2008) The DEAD-box RNA helicase Ded1p affects and accumulates in Saccharomyces cerevisiae P-bodies. Mol Biol Cell 19: 984–993 doi:10.1091/mbc.E07-09-0954
54. Hilliker A, Gao Z, Jankowsky E, Parker R, (2011) The DEAD-box protein Ded1 modulates translation by the formation and resolution of an eIF4F-mRNA complex. Mol Cell 43: 962–972 doi:10.1016/j.molcel.2011.08.008
55. Berthelot K, Muldoon M, Rajkowitsch L, Hughes J, McCarthy JEG, (2004) Dynamics and processivity of 40S ribosome scanning on mRNA in yeast. Mol Microbiol 51: 987–1001.
56. Raponi M, Arndt GM, (2002) Dominant genetic screen for cofactors that enhance antisense RNA-mediated gene silencing in fission yeast. Nucleic Acids Res 30: 2546–2554.
57. Ulvila J, Hultmark D, Rämet M, (2010) RNA silencing in the antiviral innate immune defence—role of DEAD-box RNA helicases. Scand J Immunol 71: 146–158 doi:10.1111/j.1365-3083.2009.02362.x
58. Del Campo M, Mohr S, Jiang Y, Jia H, Jankowsky E, et al. (2009) Unwinding by local strand separation is critical for the function of DEAD-box proteins as RNA chaperones. J Mol Biol 389: 674–693 doi:10.1016/j.jmb.2009.04.043
59. Shajani Z, Sykes MT, Williamson JR, (2011) Assembly of bacterial ribosomes. Annu Rev Biochem 80: 501–526 doi:10.1146/annurev-biochem-062608-160432
60. Cordin O, Hahn D, Beggs JD, (2012) Structure, function and regulation of spliceosomal RNA helicases. Curr Opin Cell Biol 24: 431–438 doi:10.1016/j.ceb.2012.03.004
61. Koodathingal P, Staley JP, (2013) Splicing fidelity: DEAD/H-box ATPases as molecular clocks. RNA Biol 10: 1073–1079 doi:10.4161/rna.25245
62. Lehnert V, Jaeger L, Michel F, Westhof E, (1996) New loop-loop tertiary interactions in self-splicing introns of subgroup IC and ID: a complete 3D model of the Tetrahymena thermophila ribozyme. Chem Biol 3: 993–1009.