Toward a molecular understanding of RNA remodeling by DEAD-box proteins

RNA Biology

Volumn 10, Issue 1, 2013, Pages 44-55

  Russell, Rick ^a   Jarmoskaite, Inga ^a   Lambowitz, Alan M ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Group I intron; Group II intron; Kinetic trap; Misfolded RNA; RNA chaperone; RNA folding; RNA helicase; RNA unwinding; RNAprotein interaction

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CYT 19 PROTEIN; DEAD BOX PROTEIN; MSS116 PROTEIN; RNA; UNCLASSIFIED DRUG;

CRYSTALLOGRAPHY; INTRON; NONHUMAN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; RNA FOLDING; RNA METABOLISM; RNA SPLICING;

EID: 84875171510     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.22210     Document Type: Review

References (150)

1. 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.
2. 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.
3. 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.
4. Noller H F. RNA structure: reading the ribosome. Science 2005; 309:1508-14; PMID:16141058; http://dx.doi.org/10.1126/science.1111771. (Pubitemid 41266466)
5. Carthew RW, Sontheimer EJ. Origins and Mechanisms of miRNAs and siRNAs. Cell 2009; 136:642-55; PMID:19239886; http://dx.doi.org/10.1016/j. cell.2009.01.035.
6. Wahl MC, Will CL, Lührmann R. The spliceosome: design principles of a dynamic RNP machine. Cell 2009; 136:701-18; PMID:19239890; http://dx.doi. org/10.1016/j.cell.2009.02.009.
7. Collins K. The biogenesis and regulation of telomerase holoenzymes. Nat Rev Mol Cell Biol 2006; 7:484-94; PMID:16829980; http://dx.doi.org/10.1038/ nrm1961. (Pubitemid 44036454)
8. Esakova O, Krasilnikov AS. Of proteins and RNA: the RNase P/MRP family. RNA 2010; 16:1725-47; PMID:20627997; http://dx.doi.org/10.1261/rna.2214510.
9. 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.
10. Jarmoskaite I, Russell R. DEAD-box proteins as RNA helicases and chaperones. Wiley Interdiscip Rev RNA 2011; 2:135-52; PMID:21297876; http://dx.doi. org/10.1002/wrna.50.
11. 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.
12. Herschlag D. RNA chaperones and the RNA folding problem. J Biol Chem 1995; 270:20871-4; PMID:7545662.
13. Schmid SR, Linder P. D-E-A-D protein family of putative RNA helicases. Mol Microbiol 1992; 6:283-91; PMID:1552844; http://dx.doi. org/10.1111/j.1365- 2958.1992.tb01470.x.
14. Lorsch JR, Herschlag D. The DEAD box protein eIF4A. 1. A minimal kinetic and thermodynamic framework reveals coupled binding of RNA and nucleotide. Biochemistry 1998; 37:2180-93; PMID:9485364; http://dx.doi.org/10.1021/ bi972430g. (Pubitemid 28119291)
15. Fairman ME, Maroney PA, Wang W, Bowers HA, Gollnick P, Nilsen TW, 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)
16. 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)
17. Tran EJ, Zhou Y, Corbett AH, Wente SR. The DEAD-box protein Dbp5 controls mRNA export by triggering specific RNA:protein remodeling events. Mol Cell 2007; 28:850-9; PMID:18082609; http://dx.doi. org/10.1016/j.molcel.2007.09.019. (Pubitemid 350217049)
18. Rössler OG, Straka A, Stahl H. Rearrangement of structured RNA via branch migration structures catalysed by the highly related DEAD-box proteins p68 and p72. Nucleic Acids Res 2001; 29:2088-96; PMID:11353078; http://dx.doi.org/10.1093/nar/29.10.2088. (Pubitemid 32472079)
19. 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)
20. Uhlmann-Schiffler H, Jalal C, Stahl H. Ddx42p-a human DEAD box protein with RNA chaper-one activities. Nucleic Acids Res 2006; 34:10-22; PMID:16397294; http://dx.doi.org/10.1093/nar/gkj403. (Pubitemid 43167916)
21. 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)
22. 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.
23. 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)
24. 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)
25. Caruthers JM, Johnson ER, McKay DB. Crystal structure of yeast initiation factor 4A, a DEAD-box RNA helicase. Proc Natl Acad Sci USA 2000; 97:13080-5; PMID:11087862; http://dx.doi.org/10.1073/pnas.97.24.13080.
26. Story RM, Li H, Abelson JN. Crystal structure of a DEAD box protein from the hyperthermophile Methanococcus jannaschii. Proc Natl Acad Sci USA 2001; 98:1465-70; PMID:11171974; http://dx.doi. org/10.1073/pnas.98.4.1465. (Pubitemid 32165522)
27. Shi H, Cordin O, Minder CM, Linder P, Xu RM. Crystal structure of the human ATP-dependent splicing and export factor UAP56. Proc Natl Acad Sci USA 2004; 101:17628-33; PMID:15585580; http://dx.doi. org/10.1073/pnas.0408172101. (Pubitemid 40051937)
28. 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)
29. 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.
30. 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)
31. 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.
32. 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.
33. Nielsen KH, Chamieh H, Andersen CB, Fredslund F, Hamborg K, Le Hir H, et al. Mechanism of ATP turnover inhibition in the EJC. RNA 2009; 15:67-75; PMID:19033377; http://dx.doi.org/10.1261/rna.1283109.
34. 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.
35. 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.
36. Tanner NK, Cordin O, Banroques J, Doère M, Linder P. The Q motif: a newly identified motif in DEAD box helicases may regulate ATP binding and hydrolysis. Mol Cell 2003; 11:127-38; PMID:12535527; http://dx.doi.org/10.1016/ S1097-2765(03)00006-6. (Pubitemid 36126596)
37. Cordin O, Tanner NK, Doère M, Linder P, Banroques J. The newly discovered Q motif of DEAD-box RNA helicases regulates RNA-binding and helicase activity. EMBO J 2004; 23:2478-87; PMID:15201868; http://dx.doi.org/10.1038/sj. emboj.7600272. (Pubitemid 38988220)
38. 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)
39. 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.
40. 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.
41. 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.
42. Fuller-Pace FV, Nicol SM, Reid AD, Lane D P. DbpA: a DEAD box protein specifically activated by 23s rRNA. EMBO J 1993; 12:3619-26; PMID:8253085. (Pubitemid 23256448)
43. Diges CM, Uhlenbeck OC. Escherichia coli DbpA is an RNA helicase that requires hairpin 92 of 23S rRNA. EMBO J 2001; 20:5503-12; PMID:11574482; http://dx.doi.org/10.1093/emboj/20.19.5503. (Pubitemid 32959470)
44. Hardin JW, Hu YX, McKay DB. Structure of the RNA binding domain of a DEAD-box helicase bound to its ribosomal RNA target reveals a novel mode of recognition by an RNA recognition motif. J Mol Biol 2010; 402:412-27; PMID:20673833; http://dx.doi. org/10.1016/j.jmb.2010.07.040.
45. 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.
46. Chimnaronk S, Suzuki T, Manita T, Ikeuchi Y, Yao M, Suzuki T, et al. RNA helicase module in an acetyltrans-ferase that modifies a specific tRNA anticodon. EMBO J 2009; 28:1362-73; PMID:19322199; http://dx.doi. org/10.1038/emboj.2009.69.
47. Lau PW, Guiley KZ, De N, Potter CS, Carragher B, MacRae IJ. The molecular architecture of human Dicer. Nat Struct Mol Biol 2012; 19:436-40; PMID:22426548; http://dx.doi.org/10.1038/nsmb.2268.
48. 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.
49. 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)
50. 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)
51. 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.
52. Banroques J, Cordin O, Doère M, Linder P, Tanner NK. A conserved phenylalanine of motif IV in superfamily 2 helicases is required for cooperative, ATP-dependent binding of RNA substrates in DEAD-box proteins. Mol Cell Biol 2008; 28:3359-71; PMID:18332124; http://dx.doi.org/10.1128/MCB.01555- 07. (Pubitemid 351657099)
53. 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)
54. 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.
55. 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.
56. 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.
57. 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.
58. 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.
59. 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.
60. Tarn WY, Chang TH. The current understanding of Ded1p/DDX3 homologs from yeast to human. RNA Biol 2009; 6:17-20; PMID:19106629; http://dx.doi. org/10.4161/rna.6.1.7440.
61. Karow AR, Theissen B, Klostermeier D. Authentic interdomain communication in an RNA heli-case reconstituted by expressed protein ligation of two helicase domains. FEBS J 2007; 274:463-73; PMID:17229151; http://dx.doi.org/10.1111/j. 1742-4658.2006.05593.x. (Pubitemid 46046655)
62. Rogers GW Jr., Richter NJ, Lima WF, Merrick WC. Modulation of the helicase activity of eIF4A by eIF4B, eIF4H, and eIF4F. J Biol Chem 2001; 276:30914-22; PMID:11418588; http://dx.doi.org/10.1074/jbc. M100157200.
63. Marintchev A, Edmonds KA, Marintcheva B, Hendrickson E, Oberer M, Suzuki C, et al. Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation. Cell 2009; 136:447-60; PMID:19203580; http://dx.doi.org/10.1016/j. cell.2009.01.014.
64. 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.
65. Özes AR, Feoktistova K, Avanzino BC, Fraser CS. Duplex unwinding and ATPase activities of the DEAD-box helicase eIF4A are coupled by eIF4G and eIF4B. J Mol Biol 2011; 412:674-87; PMID:21840318; http://dx.doi.org/10.1016/j. jmb.2011.08.004.
66. Rajagopal V, Park EH, Hinnebusch AG, Lorsch JR. Specific domains in yeast translation initiation factor eIF4G strongly bias RNA unwinding activity of the eIF4F complex toward duplexes with 5'-overhangs. J Biol Chem 2012; 287:20301-12; PMID:22467875; http://dx.doi.org/10.1074/jbc.M112.347278.
67. 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)
68. 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.
69. Bono F, Gehring NH. Assembly, disassembly and recycling: the dynamics of exon junction complexes. RNA Biol 2011; 8:24-9; PMID:21289489; http://dx.doi. org/10.4161/rna.8.1.13618.
70. Gehring NH, Lamprinaki S, Kulozik AE, Hentze MW. Disassembly of exon junction complexes by PYM. Cell 2009; 137:536-48; PMID:19410547; http://dx.doi. org/10.1016/j.cell.2009.02.042.
71. Lund MK, Guthrie C. The DEAD-box protein Dbp5p is required to dissociate Mex67p from exported mRNPs at the nuclear rim. Mol Cell 2005; 20:645-51; PMID:16307927; http://dx.doi.org/10.1016/j.mol-cel.2005.10.005. (Pubitemid 41668648)
72. Ledoux S, Guthrie C. Regulation of the Dbp5 ATPase cycle in mRNP remodeling at the nuclear pore: a lively new paradigm for DEAD-box proteins. Genes Dev 2011; 25:1109-14; PMID:21632821; http://dx.doi. org/10.1101/gad. 2062611.
73. Valkov E, Dean JC, Jani D, Kuhlmann SI, Stewart M. Structural basis for the assembly and disassembly of mRNA nuclear export complexes. Biochim Biophys Acta 2012; 1819:578-92; PMID:22406340; http://dx.doi.org/10.1016/j.bbagrm.2012. 02.017.
74. Noble KN, Tran EJ, Alcázar-Román AR, Hodge CA, Cole CN, Wente SR. The Dbp5 cycle at the nuclear pore complex during mRNA export II: nucleotide cycling and mRNP remodeling by Dbp5 are controlled by Nup159 and Gle1. Genes Dev 2011; 25:1065-77; PMID:21576266; http://dx.doi.org/10.1101/gad. 2040611.
75. Montpetit B, Thomsen ND, Helmke KJ, Seeliger MA, Berger JM, Weis K. A conserved mechanism of DEAD-box ATPase activation by nucleoporins and InsP6 in mRNA export. Nature 2011; 472:238-42; PMID:21441902; http://dx.doi.org/10.1038/ nature09862.
76. 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)
77. 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.
78. Huang Y, Liu ZR. The ATPase, RNA unwinding, and RNA binding activities of recombinant p68 RNA helicase. J Biol Chem 2002; 277:12810-5; PMID:11823473; http://dx.doi.org/10.1074/jbc. M200182200. (Pubitemid 34952644)
79. 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)
80. 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.
81. Wang Q, Arnold JJ, Uchida A, Raney KD, Cameron CE. Phosphate release contributes to the rate-limiting step for unwinding by an RNA helicase. Nucleic Acids Res 2010; 38:1312-24; PMID:19969541; http://dx.doi.org/10.1093/nar/ gkp1118.
82. Mallam AL, Del Campo M, Gilman B, Sidote DJ, Lambowitz AM. Structural basis for RNA-duplex recognition and unwinding by the DEAD-box helicase Mss116p. Nature 2012; 490:121-125; doi: 10.1038/nature11402 2012.
83. 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)
84. Kossen K, Karginov FV, 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)
85. Wang S, Hu Y, Overgaard MT, Karginov FV, Uhlenbeck OC, McKay DB. The domain of the Bacillus subtilis DEAD-box helicase YxiN that is responsible for specific binding of 23S rRNA has an RNA recognition motif fold. RNA 2006; 12:959-67; PMID:16611943; http://dx.doi.org/10.1261/rna.5906. (Pubitemid 43788114)
86. Wang S, Overgaard MT, Hu Y, McKay DB. The Bacillus subtilis RNA helicase YxiN is distended in solution. Biophys J 2008; 94:L01-03; PMID:17951299; http://dx.doi.org/10.1529/biophysj.107.120709.
87. 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)
88. Stevens SW. (2010). The biology of DEAH/RHA proteins and their mechanism of action. In RNA helicases (Jankowsky, E., ed.), Vol. RSC Biomolecular Sciences No. 19, pp. 99-120. Royal Society of Chemistry.
89. Strunk BS, Karbstein K. Powering through ribosome assembly. RNA 2009; 15:2083-104; PMID:19850913; http://dx.doi.org/10.1261/rna.1792109.
90. Shajani Z, Sykes M T, Williamson JR. Assembly of bacterial ribosomes. Annu Rev Biochem 2011; 80:501-26; PMID:21529161; http://dx.doi.org/10.1146/ annurev-biochem-062608-160432.
91. Russell R. RNA misfolding and the action of chaper-ones. Front Biosci 2008; 13:1-20; PMID:17981525; http://dx.doi.org/10.2741/2557.
92. Cech TR. Self-splicing of group I introns. Annu Rev Biochem 1990; 59:543-68; PMID:2197983; http://dx.doi.org/10.1146/annurev.bi.59.070190.002551.
93. Michel F, Westhof E. Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J Mol Biol 1990; 216:585-610; PMID:2258934; http://dx.doi. org/10.1016/0022-2836(90)90386- Z. (Pubitemid 120037393)
94. Cate JH, Gooding AR, Podell E, Zhou K, Golden BL, Kundrot CE, et al. Crystal structure of a group I ribozyme domain: principles of RNA packing. Science 1996; 273:1678-85; PMID:8781224; http://dx.doi. org/10.1126/science.273. 5282.1678. (Pubitemid 26317777)
95. Golden BL, Gooding AR, Podell ER, Cech TR. A preorganized active site in the crystal structure of the Tetrahymena ribozyme. Science 1998; 282:259-64; PMID:9841391; http://dx.doi.org/10.1126/sci-ence.282.5387.259. (Pubitemid 28487190)
96. Adams PL, Stahley MR, Kosek AB, Wang J, Strobel SA. Crystal structure of a self-splicing group I intron with both exons. Nature 2004; 430:45-50; PMID:15175762; http://dx.doi.org/10.1038/nature02642. (Pubitemid 38915218)
97. Lambowitz AM, Perlman PS. Involvement of amino-acyl-tRNA synthetases and other proteins in group I and group II intron splicing. Trends Biochem Sci 1990; 15:440-4; PMID:2278103; http://dx.doi. org/10.1016/0968-0004(90)90283-H.
98. 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.
99. Bifano AL, Caprara MG. 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.
100. Lindahl T, Adams A, Fresco JR. Renaturation of transfer ribonucleic acids through site binding of magnesium. Proc Natl Acad Sci USA 1966; 55:941-8; PMID:5327073; http://dx.doi.org/10.1073/pnas.55.4.941.
101. Aubert M, Scott J F, Reynier M, Monier R. Rearrangement of the conformation of Escherichia coli 5S RNA. Proc Natl Acad Sci USA 1968; 61:292-9; PMID:4880610; http://dx.doi.org/10.1073/pnas.61.1.292.
102. Walstrum SA, Uhlenbeck OC. The self-splicing RNA of Tetrahymena is trapped in a less active conformation by gel purification. Biochemistry 1990; 29:10573-6; PMID:2271667; http://dx.doi.org/10.1021/bi00498a022.
103. Woodson SA, Cech TR. Alternative secondary structures in the 5' exon affect both forward and reverse self-splicing of the Tetrahymena intervening sequence RNA. Biochemistry 1991; 30:2042-50; PMID:1998665; http://dx.doi.org/10. 1021/bi00222a006.
104. 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)
105. Russell R, Herschlag D. New pathways in folding of the Tetrahymena group I RNA enzyme. J Mol Biol 1999; 291:1155-67; PMID:10518951; http://dx.doi. org/10.1006/jmbi.1999.3026. (Pubitemid 29423778)
106. Zhang L, Bao P, Leibowitz MJ, Zhang Y. Slow formation of a pseudoknot structure is rate limiting in the productive co-transcriptional folding of the self-splicing Candida intron. RNA 2009; 15:1986-92; PMID:19710184; http://dx.doi.org/10.1261/rna.1638609.
107. Duncan CD, Weeks KM. SHAPE analysis of long-range interactions reveals extensive and thermodynamically preferred misfolding in a fragile group I intron RNA. Biochemistry 2008; 47:8504-13; PMID:18642882; http://dx.doi.org/10.1021/ bi800207b.
108. 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)
109. Chadalavada DM, Senchak SE, Bevilacqua PC. The folding pathway of the genomic hepatitis delta virus ribozyme is dominated by slow folding of the pseudoknots. J Mol Biol 2002; 317:559-75; PMID:11955009; http://dx.doi.org/10. 1006/jmbi.2002.5434. (Pubitemid 34722169)
110. 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)
111. Rangan P, Masquida B, Westhof E, Woodson SA. Assembly of core helices and rapid tertiary folding of a small bacterial group I ribozyme. Proc Natl Acad Sci USA 2003; 100:1574-9; PMID:12574513; http://dx.doi.org/10.1073/pnas. 0337743100. (Pubitemid 36254489)
112. Roh JH, Guo L, Kilburn JD, Briber RM, Irving T, Woodson SA. Multistage collapse of a bacterial ribozyme observed by time-resolved small-angle X-ray scattering. J Am Chem Soc 2010; 132:10148-54; PMID:20597502; http://dx.doi.org/10.1021/ja103867p.
113. 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.
114. Kruger K, Grabowski PJ, Zaug AJ, Sands J, Gottschling DE, Cech TR. Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell 1982; 31:147-57; PMID:6297745; http://dx.doi.org/10.1016/0092-8674(82)90414-7. (Pubitemid 13215202)
115. Woodson SA, Emerick VL. An alternative helix in the 26S rRNA promotes excision and integration of the Tetrahymena intervening sequence. Mol Cell Biol 1993; 13:1137-45; PMID:8380892. (Pubitemid 23040280)
116. Emerick VL, Woodson SA. Fingerprinting the folding of a group I precursor RNA. Proc Natl Acad Sci USA 1994; 91:9675-9; PMID:7937871; http://dx.doi. org/10.1073/pnas.91.21.9675. (Pubitemid 24311870)
117. Zaug AJ, Grosshans CA, Cech TR. Sequence-specific endoribonuclease activity of the Tetrahymena ribozyme: enhanced cleavage of certain oligonucleotide substrates that form mismatched ribozyme-substrate complexes. Biochemistry 1988; 27:8924-31; PMID:3069131; http://dx.doi.org/10.1021/ bi00425a008.
118. Wan Y, Mitchell D 3rd, Russell R. Catalytic activity as a probe of native RNA folding. Methods Enzymol 2009; 468:195-218; PMID:20946771; http://dx.doi. org/10.1016/S0076-6879(09)68010-1.
119. Potratz J P, Russell R. RNA catalysis as a probe for chaperone activity of DEAD-box helicases. Methods Enzymol 2012; 511:111-30; PMID:22713317.
120. Zarrinkar P P, Williamson JR. Kinetic intermediates in RNA folding. Science 1994; 265:918-24; PMID:8052848; http://dx.doi.org/10.1126/sci-ence. 8052848. (Pubitemid 24281488)
121. Sclavi B, Sullivan M, Chance MR, Brenowitz M, Woodson SA. RNA folding at millisecond intervals by synchrotron hydroxyl radical footprinting. Science 1998; 279:1940-3; PMID:9506944; http://dx.doi. org/10.1126/science.279.5358. 1940. (Pubitemid 28168649)
122. Russell R, Herschlag D. Probing the folding landscape of the Tetrahymena ribozyme: commitment to form the native conformation is late in the folding pathway. J Mol Biol 2001; 308:839-51; PMID:11352576; http://dx.doi.org/10.1006/ jmbi.2001.4751. (Pubitemid 32574363)
123. Russell R, Zhuang X, Babcock H P, Millett IS, Doniach S, Chu S, et al. Exploring the folding landscape of a structured RNA. Proc Natl Acad Sci USA 2002; 99:155-60; PMID:11756689; http://dx.doi. org/10.1073/pnas.221593598. (Pubitemid 34060333)
124. Laederach A, Shcherbakova I, Jonikas MA, Altman RB, Brenowitz M. Distinct contribution of electrostatics, initial conformational ensemble, and macromolecular stability in RNA folding. Proc Natl Acad Sci USA 2007; 104:7045-50; PMID:17438287; http://dx.doi. org/10.1073/pnas.0608765104. (Pubitemid 47186006)
125. 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.
126. Russell R, Das R, Suh H, Travers KJ, Laederach A, Engelhardt MA, et al. The paradoxical behavior of a highly structured misfolded intermediate in RNA folding. J Mol Biol 2006; 363:531-44; PMID:16963081; http://dx.doi.org/10.1016/ j.jmb.2006.08.024. (Pubitemid 44436255)
127. 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)
128. 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)
129. Lambowitz AM, Zimmerly S. Group II introns: mobile ribozymes that invade DNA. Cold Spring Harb Perspect Biol 2011; 3:a003616; PMID:20463000; http://dx.doi.org/10.1101/cshperspect.a003616.
130. Pyle AM. The tertiary structure of group II introns: implications for biological function and evolution. Crit Rev Biochem Mol Biol 2010; 45:215-32; PMID:20446804; http://dx.doi. org/10.3109/10409231003796523.
131. Keating KS, Toor N, Perlman PS, Pyle AM. A structural analysis of the group II intron active site and implications for the spliceosome. RNA 2010; 16:1-9; PMID:19948765; http://dx.doi.org/10.1261/rna.1791310.
132. 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.
133. 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.
134. Köhler D, Schmidt-Gattung S, Binder S. The DEAD-box protein PMH2 is required for efficient group II intron splicing in mitochondria of Arabidopsis thaliana. Plant Mol Biol 2010; 72:459-67; PMID:19960362; http://dx.doi.org/10. 1007/s11103-009-9584-9.
135. Asakura Y, Galarneau E, Watkins K P, Barkan A, van Wijk KJ. Chloroplast RH3 DEAD box RNA helicases in maize and arabidopsis function in splicing of specific group II introns and affect chloroplast ribosome biogenesis. Plant Physiol 2012; 159:961-74; PMID:22576849; http://dx.doi.org/10.1104/pp.112. 197525.
136. 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)
137. 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)
138. 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.
139. 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.
140. Nolte A, Chanfreau G, Jacquier A. Influence of substrate structure on in vitro ribozyme activity of a group II intron. RNA 1998; 4:694-708; PMID:9622128; http://dx.doi.org/10.1017/S1355838298980165. (Pubitemid 28252751)
141. 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)
142. Su LJ, Brenowitz M, Pyle AM. An alternative route for the folding of large RNAs: apparent two-state folding by a group II intron ribozyme. J Mol Biol 2003; 334:639-52; PMID:14636593; http://dx.doi. org/10.1016/j.jmb.2003.09.071. (Pubitemid 37433882)
143. 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.
144. 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.
145. 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)
146. 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)
147. 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.
148. Markov DA, Savkina M, Anikin M, Del Campo M, Ecker K, Lambowitz AM, et al. Identification of proteins associated with the yeast mitochondrial RNA polymerase by tandem affinity purification. Yeast 2009; 26:423-40; PMID:19536766; http://dx.doi. org/10.1002/yea.1672.
149. Cloutier SC, Ma WK, Nguyen LT, Tran EJ. The DEAD-box RNA helicase Dbp2 connects RNA quality control with repression of aberrant transcription. J Biol Chem 2012; 287:26155-66; PMID:22679025; http://dx.doi.org/10.1074/jbc.M112. 383075.
150. Lehnert V, Jaeger L, Michel F, Westhof E. 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 1996; 3:993-1009; PMID:9000010; http://dx.doi. org/10.1016/S1074-5521(96)90166-0. (Pubitemid 27058823)