Mss116p: A DEAD-box protein facilitates RNA folding

RNA Biology

Volumn 10, Issue 1, 2013, Pages 71-82

  Sachsenmaier, Nora ^a   Waldsich, Christina ^a  

^a UNIVERSITY OF VIENNA   (Austria)

Author keywords

DEAD box proteins; Intron; Ribozyme; RNA folding; RNA helicase; RNA protein interactions

Indexed keywords

ADENOSINE TRIPHOSPHATE; DEAD BOX PROTEIN; MSS116P PROTEIN; UNCLASSIFIED DRUG;

CARBOXY TERMINAL SEQUENCE; DNA DENATURATION; ENZYME STRUCTURE; EXON; GENETIC VARIABILITY; HUMAN; HYDROLYSIS; INTRON; MITOCHONDRION; MOLECULAR MECHANICS; PROTEIN FUNCTION; REVIEW; RNA BINDING; RNA FOLDING; RNA SPLICING;

EID: 84875196720     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.22492     Document Type: Review

References (144)

1. Chan RT, Robart AR, Rajashankar KR, Pyle AM, Toor N. Crystal structure of a group II intron in the pre-catalytic state. Nat Struct Mol Biol 2012; 19:555-7; PMID:22484319; http://dx.doi.org/10.1038/nsmb.2270.
2. Costa M, Michel F. Frequent use of the same tertiary motif by self-folding RNAs. EMBO J 1995; 14:1276-85; PMID:7720718.
3. Costa M, Déme E, Jacquier A, Michel F. Multiple tertiary interactions involving domain II of group II self-splicing introns. J Mol Biol 1997; 267:520-36; PMID:9126835; http://dx.doi.org/10.1006/jmbi.1996.0882. (Pubitemid 27170679)
4. Boudvillain M, Pyle AM. Defining functional groups, core structural features and inter-domain tertiary contacts essential for group II intron self-splicing: a NAIM analysis. EMBO J 1998; 17:7091-104; PMID:9843513; http://dx.doi.org/10.1093/emboj/17.23.7091. (Pubitemid 28550302)
5. Boudvillain M, Delencastre A, Pyle AM. A new RNA tertiary interaction that links active-site domains of a group II intron and anchors them at the site of catalysis. Nature 2000; 406:315-8; PMID:10917534; http://dx.doi.org/10.1038/ 35018589. (Pubitemid 30604410)
6. Fedorova O, Pyle AM. Linking the group II intron catalytic domains: tertiary contacts and structural features of domain 3. EMBO J 2005; 24:3906-16; PMID:16252007; http://dx.doi.org/10.1038/sj.emboj.7600852. (Pubitemid 41637997)
7. Harris-Kerr CL, Zhang M, Peebles CL. The phyloge-netically predicted base-pairing interaction between α and α' is required for group II splicing in vitro. Proc Natl Acad Sci USA 1993; 90:10658-62; PMID:7504276; http://dx.doi.org/10.1073/pnas.90.22.10658. (Pubitemid 23347101)
8. Michel F, Ferat J-L. Structure and activities of group II introns. Annu Rev Biochem 1995; 64:435-61; PMID:7574489; http://dx.doi.org/10.1146/annurev. bi.64.070195.002251.
9. Toor N, Keating KS, Fedorova O, Rajashankar K, Wang J, Pyle AM. Tertiary architecture of the Oceanobacillus iheyensis group II intron. RNA 2010; 16:57-69; PMID:19952115; http://dx.doi. org/10.1261/rna.1844010.
10. Toor N, Keating KS, Pyle AM. Structural insights into RNA splicing. Curr Opin Struct Biol 2009; 19:260-6; PMID:19443210; http://dx.doi.org/10.1016/j. sbi.2009.04.002.
11. Toor N, Keating KS, Taylor SD, Pyle AM. Crystal structure of a self-spliced group II intron. Science 2008; 320:77-82; PMID:18388288; http://dx.doi. org/10.1126/science.1153803. (Pubitemid 351490756)
12. Toor N, Rajashankar K, Keating KS, Pyle AM. Structural basis for exon recognition by a group II intron. Nat Struct Mol Biol 2008; 15:1221-2; PMID:18953333; http://dx.doi.org/10.1038/nsmb.1509.
13. Baird NJ, Fang X W, Srividya N, Pan T, Sosnick TR. Folding of a universal ribozyme: the ribonu-clease P RNA. Q Rev Biophys 2007; 40:113-61; PMID:17931443; http://dx.doi.org/10.1017/S0033583507004623. (Pubitemid 350260890)
14. Pyle AM, Fedorova O, Waldsich C. Folding of group II introns: a model system for large, multi-domain RNAs? Trends Biochem Sci 2007; 32:138-45; PMID:17289393; http://dx.doi.org/10.1016/j. tibs.2007.01.005. (Pubitemid 46367692)
15. 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)
16. Shcherbakova I, Mitra S, Laederach A, Brenowitz M. Energy barriers, pathways, and dynamics during folding of large, multidomain RNAs. Curr Opin Chem Biol 2008; 12:655-66; PMID:18926923; http://dx.doi.org/10.1016/j.cbpa.2008.09. 017.
17. Sosnick TR, Pan T. RNA folding: models and perspectives. Curr Opin Struct Biol 2003; 13:309-16; PMID:12831881; http://dx.doi.org/10.1016/S0959-440X(03) 00066-6. (Pubitemid 36782456)
18. 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)
19. 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)
20. Woodson SA. Recent insights on RNA folding mechanisms from catalytic RNA. Cell Mol Life Sci 2000; 57:796-808; PMID:10892344; http://dx.doi. org/10.1007/s000180050042. (Pubitemid 30392036)
21. Woodson SA. Structure and assembly of group I introns. Curr Opin Struct Biol 2005; 15:324-30; PMID:15922592; http://dx.doi.org/10.1016/j. sbi.2005.05.007. (Pubitemid 40826452)
22. Woodson SA. Compact intermediates in RNA folding. Annu Rev Biophys 2010; 39:61-77; PMID:20192764; http://dx.doi.org/10.1146/annurev. biophys.093008. 131334.
23. Lambowitz AM, Caprara MG, Zimmerly S, Perlman PS. Group I and group II ribozymes as RNPs: Clues to the past and guides to the future. In: Gestland R F, Atkins J F, eds. The RNA world. Cold Spring Harbor: Cold Spring Harbor Laboratory Press, 1999:451-485.
24. Lambowitz AM, Zimmerly S. Mobile group II introns. Annu Rev Genet 2004; 38:1-35; PMID:15568970; http://dx.doi.org/10.1146/annurev. genet.38.072902. 091600. (Pubitemid 40013722)
25. Lehmann K, Schmidt U. Group II introns: structure and catalytic versatility of large natural ribozymes. Crit Rev Biochem Mol Biol 2003; 38:249-303; PMID:12870716; http://dx.doi. org/10.1080/713609236. (Pubitemid 36793893)
26. Pyle AM, Lambowitz AM. Group II introns: ribozymes that splice RNA and invade DNA. In: Gesteland R F, Cech TR, Atkins JF, eds. The RNA World. Cold Spring Harbor, New York: Cold Spring Harbor Laborartory Press, 2006:469-534.
27. Solem A, Zingler N, Pyle AM. J. L-P-T. Group II introns and their protein collaborators. In: Walter NG, Woodson SA, Batey RT, eds. Non-protein coding RNAs. Berlin Heidelberg: Springer-Verlag, 2009:167-182.
28. Weeks KM. Protein-facilitated RNA folding. Curr Opin Struct Biol 1997; 7:336-42; PMID:9204274; http://dx.doi.org/10.1016/S0959-440X(97)80048-6. (Pubitemid 27281401)
29. Zemora G, Waldsich C. RNA folding in living cells. RNA Biol 2010; 7:634-41; PMID:21045541; http://dx.doi.org/10.4161/rna.7.6.13554.
30. 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)
31. Séraphin B, Boulet A, Simon M, Faye G. Construction of a yeast strain devoid of mitochondrial introns and its use to screen nuclear genes involved in mitochondrial splicing. Proc Natl Acad Sci USA 1987; 84:6810-4; PMID:3309947; http://dx.doi.org/10.1073/pnas.84.19.6810.
32. Séraphin B, Simon M, Boulet A, Faye G. Mitochondrial splicing requires a protein from a novel helicase family. Nature 1989; 337:84-7; PMID:2535893; http://dx.doi.org/10.1038/337084a0.
33. Herschlag D. RNA chaperones and the RNA folding problem. J Biol Chem 1995; 270:20871-4; PMID:7545662.
34. Adilakshmi T, Bellur DL, Woodson SA. Concurrent nucleation of 16S folding and induced fit in 30S ribosome assembly. Nature 2008; 455:1268-72; PMID:18784650; http://dx.doi.org/10.1038/nature07298.
35. Bassi GS, de Oliveira DM, White M F, Weeks KM. Recruitment of intron-encoded and co-opted proteins in splicing of the bI3 group I intron RNA. Proc Natl Acad Sci USA 2002; 99:128-33; PMID:11773622; http://dx.doi.org/10. 1073/pnas.012579299. (Pubitemid 34060328)
36. Caprara MG, Lehnert V, Lambowitz AM, Westhof E. A tyrosyl-tRNA synthetase recognizes a conserved tRNA-like structural motif in the group I intron catalytic core. Cell 1996; 87:1135-45; PMID:8978617; http://dx.doi.org/10.1016/ S0092-8674(00)81807-3. (Pubitemid 26427996)
37. Dai L, Chai D, Gu SQ, Gabel J, Noskov SY, Blocker FJ, et al. A three-dimensional model of a group II intron RNA and its interaction with the intron-encoded reverse transcriptase. Mol Cell 2008; 30:472-85; PMID:18424209; http://dx.doi.org/10.1016/j. molcel.2008.04.001.
38. Matsuura M, Saldanha R, Ma H, Wank H, Yang J, Mohr G, et al. A bacterial group II intron encoding reverse transcriptase, maturase, and DNA endonuclease activities: biochemical demonstration of maturase activity and insertion of new genetic information within the intron. Genes Dev 1997; 11:2910-24; PMID:9353259; http://dx.doi.org/10.1101/gad.11.21.2910. (Pubitemid 27481690)
39. Paukstelis PJ, Chen JH, Chase E, Lambowitz AM, Golden BL. Structure of a tyrosyl-tRNA synthetase splicing factor bound to a group I intron RNA. Nature 2008; 451:94-7; PMID:18172503; http://dx.doi. org/10.1038/nature06413.
40. Paukstelis PJ, Coon R, Madabusi L, Nowakowski J, Monzingo A, Robertus J, et al. A tyrosyl-tRNA syn-thetase adapted to function in group I intron splicing by acquiring a new RNA binding surface. Mol Cell 2005; 17:417-28; PMID:15694342; http://dx.doi. org/10.1016/j.molcel.2004.12.026. (Pubitemid 40193312)
41. Talkington MW, Siuzdak G, Williamson JR. An assembly landscape for the 30S ribosomal subunit. Nature 2005; 438:628-32; PMID:16319883; http://dx.doi. org/10.1038/nature04261. (Pubitemid 41740567)
42. Waldsich C, Grossberger R, Schroeder R. RNA chap-erone StpA loosens interactions of the tertiary structure in the td group I intron in vivo. Genes Dev 2002; 16:2300-12; PMID:12208852; http://dx.doi. org/10.1101/gad.231302. (Pubitemid 35013092)
43. Waldsich C, Masquida B, Westhof E, Schroeder R. Monitoring intermediate folding states of the td group I intron in vivo. EMBO J 2002; 21:5281-91; PMID:12356744; http://dx.doi.org/10.1093/emboj/cdf504.
44. Webb AE, Weeks KM. A collapsed state functions to self-chaperone RNA folding into a native ribonucleo-protein complex. Nat Struct Biol 2001; 8:135-40; PMID:11175902; http://dx.doi.org/10.1038/84124. (Pubitemid 32116065)
45. Weeks KM, Cech TR. Assembly of a ribonucleopro-tein catalyst by tertiary structure capture. Science 1996; 271:345-8; PMID:8553068; http://dx.doi. org/10.1126/science.271.5247.345.
46. Pan C, Russell R. Roles of DEAD-box proteins in RNA and RNP Folding. RNA Biol 2010; 7:667-76; PMID:21045543; http://dx.doi.org/10.4161/rna.7.6.13571.
47. Bhaskaran H, Russell R. Kinetic redistribution of native and misfolded RNAs by a DEAD-box chap-erone. Nature 2007; 449:1014-8; PMID:17960235; http://dx.doi.org/10.1038/nature06235. (Pubitemid 350014602)
48. Bifano AL, Caprara MGA. A DExH/D-box protein coordinates the two steps of splicing in a group I intron. J Mol Biol 2008; 383:667-82; PMID:18789947; http://dx.doi.org/10.1016/j.jmb.2008.08.070.
49. Bifano AL, Turk EM, Caprara MG. Structure-guided mutational analysis of a yeast DEAD-box protein involved in mitochondrial RNA splicing. J Mol Biol 2010; 398:429-43; PMID:20307546; http://dx.doi. org/10.1016/j.jmb.2010.03.025.
50. Del Campo M, Mohr S, Jiang Y, Jia H, Jankowsky E, Lambowitz AM. Unwinding by local strand separation is critical for the function of DEAD-box proteins as RNA chaperones. J Mol Biol 2009; 389:674-93; PMID:19393667; http://dx.doi.org/10.1016/j. jmb.2009.04.043.
51. Del Campo M, Tijerina P, Bhaskaran H, Mohr S, Yang Q, Jankowsky E, et al. Do DEAD-box proteins promote group II intron splicing without unwinding RNA? Mol Cell 2007; 28:159-66; PMID:17936712; http://dx.doi.org/10.1016/j.molcel. 2007.07.028. (Pubitemid 47531967)
52. Fedorova O, Pyle AM. The brace for a growing scaffold: mss116 protein promotes RNA folding by stabilizing an early assembly intermediate. J Mol Biol 2012; 422:347-65; PMID:22705286; http://dx.doi. org/10.1016/j.jmb.2012.05.037.
53. Fedorova O, Solem A, Pyle AM. Protein-facilitated folding of group II intron ribozymes. J Mol Biol 2010; 397:799-813; PMID:20138894; http://dx.doi. org/10.1016/j.jmb.2010.02.001.
54. 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)
55. 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.
56. Liebeg A, Mayer O, Waldsich C. DEAD-box protein facilitated RNA folding in vivo. RNA Biol 2010; 7:803-11; PMID:21045551; http://dx.doi.org/10.4161/rna. 7.6.13484.
57. Mohr S, Matsuura M, Perlman PS, Lambowitz AM. A DEAD-box protein alone promotes group II intron splicing and reverse splicing by acting as an RNA chaperone. Proc Natl Acad Sci USA 2006; 103:3569-74; PMID:16505350; http://dx.doi.org/10.1073/pnas.0600332103. (Pubitemid 43376596)
58. Potratz J P, Del Campo M, Wolf RZ, Lambowitz AM, Russell R. ATP-dependent roles of the DEAD-box protein Mss116p in group II intron splicing in vitro and in vivo. J Mol Biol 2011; 411:661-79; PMID:21679717; http://dx.doi.org/10.1016/ j.jmb.2011.05.047.
59. Sinan S, Yuan X, Russell R. The Azoarcus group I intron ribozyme misfolds and is accelerated for refolding by ATP-dependent RNA chaperone proteins. J Biol Chem 2011; 286:37304-12; PMID:21878649; http://dx.doi.org/10.1074/jbc.M111. 287706.
60. Solem A, Zingler N, Pyle AM. A DEAD protein that activates intron self-splicing without unwinding RNA. Mol Cell 2006; 24:611-7; PMID:17188036; http://dx.doi.org/10.1016/j.molcel.2006.10.032. (Pubitemid 350284227)
61. Tijerina P, Bhaskaran H, 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 2006; 103:16698-703; PMID:17075070; http://dx.doi. org/10.1073/pnas.0603127103. (Pubitemid 44737316)
62. Zingler N, Solem A, Pyle AM. Dual roles for the Mss116 cofactor during splicing of the ai5γ group II intron. Nucleic Acids Res 2010; 38:6602-9; PMID:20554854; http://dx.doi.org/10.1093/nar/gkq530.
63. Cordin O, Banroques J, Tanner NK, Linder P. The DEAD-box protein family of RNA helicases. Gene 2006; 367:17-37; PMID:16337753; http://dx.doi. org/10.1016/j.gene.2005.10.019. (Pubitemid 43286737)
64. Fairman-Williams ME, Guenther U P, Jankowsky E. SF1 and SF2 helicases: family matters. Curr Opin Struct Biol 2010; 20:313-24; PMID:20456941; http://dx.doi.org/10.1016/j.sbi.2010.03.011.
65. Hilbert M, Karow AR, Klostermeier D. The mechanism of ATP-dependent RNA unwinding by DEAD box proteins. Biol Chem 2009; 390:1237-50; PMID:19747077; http://dx.doi.org/10.1515/BC.2009.135.
66. Jankowsky E. RNA helicases at work: binding and rearranging. Trends Biochem Sci 2011; 36:19-29; PMID:20813532; http://dx.doi.org/10.1016/j. tibs.2010.07.008.
67. 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)
68. 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.
69. 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.
70. Yang Q, Jankowsky E. ATP-and ADP-dependent modulation of RNA unwinding and strand annealing activities by the DEAD-box protein DED1. Biochemistry 2005; 44:13591-601; PMID:16216083; http://dx.doi.org/10.1021/bi0508946. (Pubitemid 41443687)
71. 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.
72. Del Campo M, Lambowitz AM. Structure of the Yeast DEAD box protein Mss116p reveals two wedges that crimp RNA. Mol Cell 2009; 35:598-609; PMID:19748356; http://dx.doi.org/10.1016/j.mol-cel.2009.07.032.
73. Andersen CB, Ballut L, Johansen JS, Chamieh H, Nielsen KH, Oliveira CL, et al. Structure of the exon junction core complex with a trapped DEAD-box ATPase bound to RNA. Science 2006; 313:1968-72; PMID:16931718; http://dx.doi.org/10.1126/sci-ence.1131981. (Pubitemid 44498005)
74. Bono F, Ebert J, Lorentzen E, Conti E. The crystal structure of the exon junction complex reveals how it maintains a stable grip on mRNA. Cell 2006; 126:713-25; PMID:16923391; http://dx.doi.org/10.1016/j. cell.2006.08.006. (Pubitemid 44233638)
75. Fan JS, Cheng Z, Zhang J, Noble C, Zhou Z, Song H, et al. Solution and crystal structures of mRNA exporter Dbp5p and its interaction with nucleotides. J Mol Biol 2009; 388:1-10; PMID:19281819; http://dx.doi. org/10.1016/j.jmb.2009. 03.004.
76. Sengoku T, Nureki O, Nakamura A, Kobayashi S, Yokoyama S. Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 2006; 125:287-300; PMID:16630817; http://dx.doi. org/10.1016/j.cell.2006.01.054.
77. 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)
78. Collins R, Karlberg T, Lehtiö L, Schütz P, van den Berg S, Dahlgren LG, et al. The DEXD/H-box RNA helicase DDX19 is regulated by an alpha-helical switch. J Biol Chem 2009; 284:10296-300; PMID:19244245; http://dx.doi.org/10.1074/jbc.C900018200.
79. von Moeller H, Basquin C, Conti E. The mRNA export protein DBP5 binds RNA and the cytoplasmic nucleo-porin NUP214 in a mutually exclusive manner. Nat Struct Mol Biol 2009; 16:247-54; PMID:19219046; http://dx.doi.org/10.1038/nsmb. 1561.
80. Mohr G, Del Campo M, Turner KG, Gilman B, Wolf RZ, Lambowitz AM. High-throughput genetic identification of functionally important regions of the yeast DEAD-box protein Mss116p. J Mol Biol 2011; 413:952-72; PMID:21945532; http://dx.doi. org/10.1016/j.jmb.2011.09.015.
81. Mohr G, Del Campo M, Mohr S, Yang Q, Jia H, Jankowsky E, et al. Function of the C-terminal domain of the DEAD-box protein Mss116p analyzed in vivo and in vitro. J Mol Biol 2008; 375:1344-64; PMID:18096186; http://dx.doi.org/10.1016/ j. jmb.2007.11.041.
82. Banroques J, Doère M, Dreyfus M, Linder P, Tanner NK. 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 2010; 396:949-66; PMID:20026132; http://dx.doi.org/10.1016/j.jmb.2009.12. 025.
83. 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.
84. Linder P. Dead-box proteins: a family affair-active and passive players in RNP-remodeling. Nucleic Acids Res 2006; 34:4168-80; PMID:16936318; http://dx.doi. org/10.1093/nar/gkl468. (Pubitemid 44542196)
85. Karow AR, Klostermeier D. A structural model for the DEAD box helicase YxiN in solution: localization of the RNA binding domain. J Mol Biol 2010; 402:629-37; PMID:20691700; http://dx.doi.org/10.1016/j. jmb.2010.07.049.
86. Schütz P, Bumann M, Oberholzer AE, Bieniossek C, Trachsel H, Altmann M, et al. Crystal structure of the yeast eIF4A-eIF4G complex: an RNA-helicase controlled by protein-protein interactions. Proc Natl Acad Sci USA 2008; 105:9564-9; PMID:18606994; http://dx.doi.org/10.1073/pnas.0800418105. (Pubitemid 352031341)
87. Klostermeier D, Rudolph MG. A novel dimeriza-tion motif in the C-terminal domain of the Thermus thermophilus DEAD box helicase Hera confers substantial flexibility. Nucleic Acids Res 2009; 37:421-30; PMID:19050012; http://dx.doi.org/10.1093/nar/gkn947.
88. Rudolph MG, Klostermeier D. The Thermus ther-mophilus DEAD box helicase Hera contains a modified RNA recognition motif domain loosely connected to the helicase core. RNA 2009; 15:1993-2001; PMID:19710183; http://dx.doi.org/10.1261/ rna.1820009.
89. Yang Q, Del Campo M, Lambowitz AM, Jankowsky E. DEAD-box proteins unwind duplexes by local strand separation. Mol Cell 2007; 28:253-63; PMID:17964264; http://dx.doi.org/10.1016/j.mol-cel.2007.08.016. (Pubitemid 47610740)
90. Bizebard T, Ferlenghi I, Iost I, Dreyfus M. Studies on three E. coli DEAD-box helicases point to an unwinding mechanism different from that of model DNA helicas-es. Biochemistry 2004; 43:7857-66; PMID:15196029; http://dx.doi.org/10.1021/bi049852s. (Pubitemid 38787694)
91. 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.
92. 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)
93. Rogers GW Jr., Lima WF, Merrick WC. Further characterization of the helicase activity of eIF4A. Substrate specificity. J Biol Chem 2001; 276:12598-608; PMID:11278350; http://dx.doi.org/10.1074/jbc. M007560200.
94. 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.
95. Chen Y, Potratz J P, Tijerina P, Del Campo M, Lambowitz AM, Russell R. DEAD-box proteins can completely separate an RNA duplex using a single ATP. Proc Natl Acad Sci USA 2008; 105:20203-8; PMID:19088196; http://dx.doi.org/10.1073/ pnas.0811075106.
96. 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.
97. 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.
98. 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.
99. 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.
100. Henn A, Cao W, Hackney DD, De La Cruz EM. The ATPase cycle mechanism of the DEAD-box rRNA helicase, DbpA. J Mol Biol 2008; 377:193-205; PMID:18237742; http://dx.doi.org/10.1016/j. jmb.2007.12.046.
101. 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.
102. 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.
103. Fairman ME, Maroney PA, Wang W, Bowers HA, Gollnick P, Nilsen T W, et al. Protein displacement by DExH/D "RNA helicases" without duplex unwinding. Science 2004; 304:730-4; PMID:15118161; http://dx.doi.org/10.1126/ science.1095596. (Pubitemid 38560878)
104. Jankowsky E, Bowers H. Remodeling of ribonucleo-protein complexes with DExH/D RNA helicases. Nucleic Acids Res 2006; 34:4181-8; PMID:16935886; http://dx.doi.org/10.1093/nar/gkl410. (Pubitemid 44542197)
105. 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)
106. Valdez BC. Structural domains involved in the RNA folding activity of RNA helicase II/Gu protein. Eur J Biochem 2000; 267:6395-402; PMID:11029582; http://dx.doi.org/10.1046/j.1432-1327.2000.01727.x.
107. Polach KJ, Uhlenbeck OC. Cooperative binding of ATP and RNA substrates to the DEAD/H protein DbpA. Biochemistry 2002; 41:3693-702; PMID:11888286; http://dx.doi.org/10.1021/bi012062n. (Pubitemid 34224682)
108. Kos M, Tollervey D. The putative RNA helicase Dbp4p is required for release of the U14 snoRNA from preribosomes in Saccharomyces cerevisiae. Mol Cell 2005; 20:53-64; PMID:16209945; http://dx.doi. org/10.1016/j.molcel.2005.08. 022. (Pubitemid 41396562)
109. Rocak S, Emery B, Tanner NK, Linder P. Characterization of the ATPase and unwinding activities of the yeast DEAD-box protein Has1p and the analysis of the roles of the conserved motifs. Nucleic Acids Res 2005; 33:999-1009; PMID:15718299; http://dx.doi.org/10.1093/nar/gki244. (Pubitemid 41430520)
110. Mallam AL, Jarmoskaite I, Tijerina P, Del Campo M, Seifert S, Guo L, et al. Solution structures of DEAD-box RNA chaperones reveal conformational changes and nucleic acid tethering by a basic tail. Proc Natl Acad Sci USA 2011; 108:12254-9; PMID:21746911; http://dx.doi.org/10.1073/pnas.1109566108.
111. Fedorova O, Waldsich C, Pyle AM. Group II intron folding under near-physiological conditions: collapsing to the near-native state. J Mol Biol 2007; 366:1099-114; PMID:17196976; http://dx.doi.org/10.1016/j. jmb.2006.12.003. (Pubitemid 46186386)
112. Su LJ, Waldsich C, Pyle AM. An obligate intermediate along the slow folding pathway of a group II intron ribozyme. Nucleic Acids Res 2005; 33:6674-87; PMID:16314300; http://dx.doi.org/10.1093/nar/gki973. (Pubitemid 41830475)
113. 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)
114. Waldsich C, Pyle AM. A kinetic intermediate that regulates proper folding of a group II intron RNA. J Mol Biol 2008; 375:572-80; PMID:18022197; http://dx.doi.org/10.1016/j.jmb.2007.10.052. (Pubitemid 350192484)
115. Liebeg A, Waldsich C. Probing RNA structure within living cells. Methods Enzymol 2009; 468:219-38; PMID:20946772; http://dx.doi.org/10.1016/S0076- 6879(09)68011-3.
116. Cao Y, Woodson SA. Destabilizing effect of an rRNA stem-loop on an attenuator hairpin in the 5' exon of the Tetrahymena pre-rRNA. RNA 1998; 4:901-14; PMID:9701282; http://dx.doi.org/10.1017/S1355838298980621. (Pubitemid 28359761)
117. Cao Y, Woodson SA. Refolding of rRNA exons enhances dissociation of the Tetrahymena intron. RNA 2000; 6:1248-56; PMID:10999602; http://dx.doi. org/10.1017/S1355838200000893.
118. Fang XW, Thiyagarajan P, Sosnick TR, Pan T. The rate-limiting step in the folding of a large ribozyme without kinetic traps. Proc Natl Acad Sci USA 2002; 99:8518-23; PMID:12084911; http://dx.doi. org/10.1073/pnas.142288399. (Pubitemid 34693594)
119. 2+-dependent folding of a large ribozyme without kinetic traps. Nat Struct Biol 1999; 6:1091-5; PMID:10581546; http://dx.doi. org/10.1038/70016.
120. Rajkowitsch L, Chen D, Stampfl S, Semrad K, Waldsich C, Mayer O, et al. RNA chaperones, RNA annealers and RNA helicases. RNA Biol 2007; 4:118-30; PMID:18347437; http://dx.doi.org/10.4161/rna.4.3.5445. (Pubitemid 351237913)
121. Nikolcheva T, Woodson SA. Facilitation of group I splicing in vivo: misfolding of the Tetrahymena IVS and the role of ribosomal RNA exons. J Mol Biol 1999; 292:557-67; PMID:10497021; http://dx.doi. org/10.1006/jmbi.1999.3083. (Pubitemid 29457318)
122. Pan T, Sosnick TR. Intermediates and kinetic traps in the folding of a large ribozyme revealed by circular dichroism and UV absorbance spectroscopies and catalytic activity. Nat Struct Biol 1997; 4:931-8; PMID:9360610; http://dx.doi.org/10.1038/nsb1197-931. (Pubitemid 27479445)
123. Pan J, Woodson SA. Folding intermediates of a self-splicing RNA: mispairing of the catalytic core. J Mol Biol 1998; 280:597-609; PMID:9677291; http://dx.doi.org/10.1006/jmbi.1998.1901. (Pubitemid 28336368)
124. Rangan P, Masquida B, Westhof E, Woodson SA. Architecture and folding mechanism of the Azoarcus group I pre-tRNA. J Mol Biol 2004; 339:41-51; PMID:15123419; http://dx.doi.org/10.1016/j. jmb.2004.03.059. (Pubitemid 38569688)
125. Semrad K, Schroeder R. A ribosomal function is necessary for efficient splicing of the T4 phage thymidylate synthase intron in vivo. Genes Dev 1998; 12:1327-37; PMID:9573049; http://dx.doi.org/10.1101/gad.12.9.1327. (Pubitemid 28213408)
126. Bassi GS, Weeks KM. Kinetic and thermodynamic framework for assembly of the six-component bI3 group I intron ribonucleoprotein catalyst. Biochemistry 2003; 42:9980-8; PMID:12924947; http://dx.doi. org/10.1021/bi0346906. (Pubitemid 37012874)
127. Herbert CJ, Labouesse M, Dujardin G, Slonimski P P. The NAM2 proteins from S. cerevisiae and S. douglasii are mitochondrial leucyl-tRNA synthetases, and are involved in mRNA splicing. EMBO J 1988; 7:473-83; PMID:3284745.
128. Kaspar BJ, Bifano AL, Caprara MG. A shared RNA-binding site in the Pet54 protein is required for translational activation and group I intron splicing in yeast mitochondria. Nucleic Acids Res 2008; 36:2958-68; PMID:18388132; http://dx.doi.org/10.1093/nar/gkn045. (Pubitemid 351737188)
129. McGraw P, Tzagoloff A. Assembly of the mitochon-drial membrane system. Characterization of a yeast nuclear gene involved in the processing of the cyto-chrome b pre-mRNA. J Biol Chem 1983; 258:9459-68; PMID:6348045.
130. Rho SB, Martinis SA. The bI4 group I intron binds directly to both its protein splicing partners, a tRNA synthetase and maturase, to facilitate RNA splicing activity. RNA 2000; 6:1882-94; PMID:11142386; http://dx.doi.org/10. 1017/S1355838200001254. (Pubitemid 32001957)
131. Weeks KM, Cech TR. Protein facilitation of group I intron splicing by assembly of the catalytic core and the 5' splice site domain. Cell 1995; 82:221-30; PMID:7628013; http://dx.doi.org/10.1016/0092-8674(95)90309-7.
132. Gampel A, Cech TR. Binding of the CBP2 protein to a yeast mitochondrial group I intron requires the catalytic core of the RNA. Genes Dev 1991; 5:1870-80; PMID:1916266; http://dx.doi.org/10.1101/gad.5.10.1870. (Pubitemid 21905881)
133. Gampel A, Nishikimi M, Tzagoloff A. CBP2 protein promotes in vitro excision of a yeast mitochon-drial group I intron. Mol Cell Biol 1989; 9:5424-33; PMID:2685564. (Pubitemid 20004358)
134. Gampel A, Tzagoloff A. In vitro splicing of the terminal intervening sequence of Saccharomyces cerevisiae cyto-chrome b pre-mRNA. Mol Cell Biol 1987; 7:2545-51; PMID:3302680.
135. Weeks KM, Cech TR. Efficient protein-facilitated splicing of the yeast mitochondrial bI5 intron. Biochemistry 1995; 34:7728-38; PMID:7540041; http://dx.doi.org/10.1021/bi00023a020.
136. Garcia I, Weeks KM. Structural basis for the self-chaperoning function of an RNA collapsed state. Biochemistry 2004; 43:15179-86; PMID:15568809; http://dx.doi.org/10.1021/bi048626f. (Pubitemid 39602178)
137. Watts T, Khalimonchuk O, Wolf RZ, Turk EM, Mohr G, Winge DR. Mne1 is a novel component of the mitochondrial splicing apparatus responsible for processing of a COX1 group I intron in yeast. J Biol Chem 2011; 286:10137-46; PMID:21257754; http://dx.doi. org/10.1074/jbc.M110.205625.
138. Turk EM, Caprara MG. Splicing of yeast aI5be-ta group I intron requires SUV3 to recycle MRS1 via mitochondrial degradosome-promoted decay of excised intron ribonucleoprotein (RNP). J Biol Chem 2010; 285:8585-94; PMID:20064926; http://dx.doi. org/10.1074/jbc.M109.090761.
139. Grohman JK, Del Campo M, Bhaskaran H, Tijerina P, Lambowitz AM, Russell R. Probing the mechanisms of DEAD-box proteins as general RNA chaperones: the C-terminal domain of CYT-19 mediates general recognition of RNA. Biochemistry 2007; 46:3013-22; PMID:17311413; http://dx.doi.org/10.1021/bi0619472. (Pubitemid 46449125)
140. Hilliker A, Gao Z, Jankowsky E, Parker R. The DEAD-box protein Ded1 modulates translation by the formation and resolution of an eIF4F-mRNA complex. Mol Cell 2011; 43:962-72; PMID:21925384; http://dx.doi.org/10.1016/j.molcel. 2011.08.008.
141. Mohr S, Stryker JM, Lambowitz AM. A DEAD-box protein functions as an ATP-dependent RNA chaper-one in group I intron splicing. Cell 2002; 109:769-79; PMID:12086675; http://dx.doi.org/10.1016/S0092-8674(02)00771-7. (Pubitemid 34722271)
142. Mohr G, Zhang A, Gianelos JA, Belfort M, Lambowitz AM. The neurospora CYT-18 protein suppresses defects in the phage T4 td intron by stabilizing the catalytically active structure of the intron core. Cell 1992; 69:483-94; PMID:1533818; http://dx.doi. org/10.1016/0092-8674(92)90449-M.
143. Woodson SA. Taming free energy landscapes with RNA chaperones. RNA Biol 2010; 7:677-86; PMID:21045544; http://dx.doi.org/10.4161/rna.7.6.13615.
144. Michel F, Costa M, Westhof E. The ribozyme core of group II introns: a structure in want of partners. Trends Biochem Sci 2009; 34:189-99; PMID:19299141; http://dx.doi.org/10.1016/j.tibs.2008.12.007.