Ski2-like RNA helicase structures: Common themes and complex assemblies

RNA Biology

Volumn 10, Issue 1, 2013, Pages 33-43

  Johnson, Sean J ^a   Jackson, Ryan N ^a  

^a UTAH STATE UNIVERSITY   (United States)

Author keywords

Brr2; Mtr4; RNA helicase; RNA processing; Ski2; Structure

Indexed keywords

MTR4 PROTEIN; RNA HELICASE; SKI2 PROTEIN; UNCLASSIFIED DRUG; WINGED HELIX TRANSCRIPTION FACTOR;

ENZYME STRUCTURE; EXOSOME; NONHUMAN; PROTEIN RNA BINDING; REVIEW; RNA DEGRADATION; RNA PROCESSING;

EID: 84875128302     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.22101     Document Type: Review

References (120)

1. Caprara MG. Chapter 6 Ski2-Like Proteins: Biology and Mechanism. RNA Helicases: The Royal Society of Chemistry, 2010:149-67.
2. 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.
3. Gorbalenya AE, Koonin EV. Helicases: amino acid sequence comparisons and structure-function relationships. Curr Opin Struct Biol 1993; 3:419-29; http://dx.doi.org/10.1016/S0959-440X(05)80116-2. (Pubitemid 23207576)
4. Jankowsky E, Fairman-Williams ME. Chapter 1 An Introduction to RNA Helicases: Superfamilies, Families, and Major Themes. RNA Helicases: The Royal Society of Chemistry, 2010:1-31.
5. 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.
6. Widner WR, Wickner RB. Evidence that the SKI antiviral system of Saccharomyces cerevisiae acts by blocking expression of viral mRNA. Mol Cell Biol 1993; 13:4331-41; PMID:8321235. (Pubitemid 23187662)
7. Johnson AW, Kolodner RD. Synthetic lethality of sep1 (xrn1) ski2 and sep1 (xrn1) ski3 mutants of Saccharomyces cerevisiae is independent of killer virus and suggests a general role for these genes in translation control. Mol Cell Biol 1995; 15:2719-27; PMID:7739552.
8. Anderson JS, Parker R P. The 3' to 5' degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 3' to 5' exonucleases of the exosome complex. EMBO J 1998; 17:1497-506; PMID:9482746; http://dx.doi. org/10.1093/emboj/17.5.1497. (Pubitemid 28105528)
9. Toh-E A, Guerry P, Wickner RB. Chromosomal super-killer mutants of Saccharomyces cerevisiae. J Bacteriol 1978; 136:1002-7; PMID:363683. (Pubitemid 9075230)
10. Bleichert F, Baserga SJ. The long unwinding road of RNA helicases. Mol Cell 2007; 27:339-52; PMID:17679086; http://dx.doi.org/10.1016/j.molcel.2007.07. 014. (Pubitemid 47126943)
11. Jedrzejczak R, Wang J, Dauter M, Szczesny RJ, Stepien P P, Dauter Z. Human Suv3 protein reveals unique features among SF2 helicases. Acta Crystallogr D Biol Crystallogr 2011; 67:988-96; PMID:22101826; http://dx.doi.org/10.1107/ S0907444911040248.
12. Cordin O, Hahn D, Beggs JD. Structure, function and regulation of spliceosomal RNA helicases. Curr Opin Cell Biol 2012; 24:431-8; PMID:22464735; http://dx.doi.org/10.1016/j.ceb.2012.03.004.
13. 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.
14. Lebreton A, Séraphin B. Exosome-mediated quality control: substrate recruitment and molecular activity. Biochim Biophys Acta 2008; 1779:558-65; PMID:18313413; http://dx.doi.org/10.1016/j. bbagrm.2008.02.003.
15. de la Cruz J, Kressler D, Linder P. Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. Trends Biochem Sci 1999; 24:192-8; PMID:10322435; http://dx.doi.org/10.1016/S0968-0004(99)01376-6. (Pubitemid 29348454)
16. Houseley J, Tollervey D. The many pathways of RNA degradation. Cell 2009; 136:763-76; PMID:19239894; http://dx.doi.org/10.1016/j.cell.2009.01.019.
17. Norbury CJ. Regional specialization: the NEXT big thing in nuclear RNA turnover. Mol Cell 2011; 43:502-4; PMID:21855790; http://dx.doi.org/10.1016/j. mol-cel.2011.08.001.
18. Schaeffer D, Clark A, Klauer AA, Tsanova B, van Hoof A. Functions of the cytoplasmic exosome. Adv Exp Med Biol 2010; 702:79-90; PMID:21618876; http://dx.doi. org/10.1007/978-1-4419-7841-7-7.
19. Anderson JT, Wang X. Nuclear RNA surveillance: no sign of substrates tailing off. Crit Rev Biochem Mol Biol 2009; 44:16-24; PMID:19280429; http://dx.doi. org/10.1080/10409230802640218.
20. Butler JS. The yin and yang of the exosome. Trends Cell Biol 2002; 12:90-6; PMID:11849973; http://dx.doi. org/10.1016/S0962-8924(01)02225-5. (Pubitemid 34146525)
21. Hahn D, Beggs JD. Brr2p RNA helicase with a split personality: insights into structure and function. Biochem Soc Trans 2010; 38:1105-9; PMID:20659012; http://dx.doi.org/10.1042/BST0381105.
22. Newman AJ, Nagai K. Structural studies of the spliceo-some: blind men and an elephant. Curr Opin Struct Biol 2010; 20:82-9; PMID:20089394; http://dx.doi. org/10.1016/j.sbi.2009.12.003.
23. Jackson RN, Klauer AA, Hintze BJ, Robinson H, van Hoof A, Johnson SJ. The crystal structure of Mtr4 reveals a novel arch domain required for rRNA processing. EMBO J 2010; 29:2205-16; PMID:20512111; http://dx.doi.org/10.1038/ emboj.2010.107.
24. Weir JR, Bonneau F, Hentschel J, Conti E. Structural analysis reveals the characteristic features of Mtr4, a DExH helicase involved in nuclear RNA processing and surveillance. Proc Natl Acad Sci USA 2010; 107:12139-44; PMID:20566885; http://dx.doi.org/10.1073/pnas.1004953107.
25. Halbach F, Rode M, Conti E. The crystal structure of S. cerevisiae Ski2, a DExH helicase associated with the cytoplasmic functions of the exosome. RNA 2012; 18:124-34; PMID:22114319; http://dx.doi. org/10.1261/rna.029553.111.
26. Pena V, Jovin SM, Fabrizio P, Orlowski J, Bujnicki JM, Lührmann R, et al. Common design principles in the spliceosomal RNA helicase Brr2 and in the Hel308 DNA helicase. Mol Cell 2009; 35:454-66; PMID:19716790; http://dx.doi.org/10.1016/j.molcel.2009.08.006.
27. Zhang L, Xu T, Maeder C, Bud LO, Shanks J, Nix J, et al. Structural evidence for consecutive Hel308-like modules in the spliceosomal ATPase Brr2. Nat Struct Mol Biol 2009; 16:731-9; PMID:19525970; http://dx.doi. org/10.1038/nsmb.1625.
28. Büttner K, Nehring S, Hopfner K P. Structural basis for DNA duplex separation by a superfamily-2 helicase. Nat Struct Mol Biol 2007; 14:647-52; PMID:17558417; http://dx.doi.org/10.1038/nsmb1246. (Pubitemid 47037060)
29. Oyama T, Oka H, Mayanagi K, Shirai T, Matoba K, Fujikane R, et al. Atomic structures and functional implications of the archaeal RecQ-like helicase Hjm. BMC Struct Biol 2009; 9:2; PMID:19159486; http://dx.doi.org/10.1186/1472-6807-9- 2.
30. Richards JD, Johnson KA, Liu H, McRobbie AM, McMahon S, Oke M, et al. Structure of the DNA repair helicase hel308 reveals DNA binding and auto-inhibitory domains. J Biol Chem 2008; 283:5118-26; PMID:18056710; http://dx.doi.org/10.1074/jbc. M707548200.
31. Zhang X, Nakashima T, Kakuta Y, Yao M, Tanaka I, Kimura M. Crystal structure of an archaeal Ski2p-like protein from Pyrococcus horikoshii OT3. Protein Sci 2008; 17:136-45; PMID:18042682; http://dx.doi. org/10.1110/ps. 073107008.
32. 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.
33. 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.
34. Krissinel E, Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 2004; 60:2256-68; PMID:15572779; http://dx.doi. org/10.1107/S0907444904026460. (Pubitemid 41742778)
35. He Y, Andersen GR, Nielsen KH. Structural basis for the function of DEAH helicases. EMBO Rep 2010; 11:180-6; PMID:20168331; http://dx.doi.org/10.1038/ embor.2010.11.
36. Walbott H, Mouffok S, Capeyrou R, Lebaron S, Humbert O, van Tilbeurgh H, et al. Prp43p contains a processive helicase structural architecture with a specific regulatory domain. EMBO J 2010; 29:2194-204; PMID:20512115; http://dx.doi.org/10.1038/emboj.2010.102.
37. Kudlinzki D, Schmitt A, Christian H, Ficner R. Structural analysis of the C-terminal domain of the spliceosomal helicase Prp22. Biol Chem 2012; In press; http://dx.doi.org/10.1515/hsz-2012-0158.
38. Woodman IL, Bolt EL. Winged helix domains with unknown function in Hel308 and related helicases. Biochem Soc Trans 2011; 39:140-4; PMID:21265761; http://dx.doi.org/10.1042/BST0390140.
39. 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)
40. Bernstein J, Toth EA. Yeast nuclear RNA processing. World J Biol Chem 2012; 3:7-26; PMID:22312453.
41. Holub P, Lalakova J, Cerna H, Pasulka J, Sarazova M, Hrazdilova K, et al. Air2p is critical for the assembly and RNA-binding of the TRAMP complex and the KOW domain of Mtr4p is crucial for exosome activation. Nucleic Acids Res 2012; 40:5679-93; PMID:22402490; http://dx.doi.org/10.1093/nar/gks223.
42. Liang S, Hitomi M, Hu YH, Liu Y, Tartakoff AM. A DEAD-box-family protein is required for nucleocyto-plasmic transport of yeast mRNA. Mol Cell Biol 1996; 16:5139-46; PMID:8756671. (Pubitemid 26272167)
43. Small EC, Leggett SR, Winans AA, Staley J P. The EF-G-like GTPase Snu114p regulates spliceosome dynamics mediated by Brr2p, a DExD/H box ATPase. Mol Cell 2006; 23:389-99; PMID:16885028; http://dx.doi. org/10.1016/j.molcel.2006.05. 043. (Pubitemid 44128846)
44. Guy C P, Bolt EL. Archaeal Hel308 helicase targets replication forks in vivo and in vitro and unwinds lagging strands. Nucleic Acids Res 2005; 33:3678-90; PMID:15994460; http://dx.doi.org/10.1093/nar/gki685. (Pubitemid 41430590)
45. Jia H, Wang X, Anderson JT, Jankowsky E. RNA unwinding by the Trf4/Air2/Mtr4 polyadenyl-ation (TRAMP) complex. Proc Natl Acad Sci USA 2012; 109:7292-7; PMID:22532666; http://dx.doi. org/10.1073/pnas.1201085109.
46. Kyrpides NC, Woese CR, Ouzounis CA. KOW: a novel motif linking a bacterial transcription factor with ribosomal proteins. Trends Biochem Sci 1996; 21:425-6; PMID:8987397; http://dx.doi.org/10.1016/S0968-0004(96)30036-4. (Pubitemid 26393730)
47. Steiner T, Kaiser J T, Marinkoviç S, Huber R, Wahl MC. Crystal structures of transcription factor NusG in light of its nucleic acid-and protein-binding activities. EMBO J 2002; 21:4641-53; PMID:12198166; http://dx.doi. org/10.1093/emboj/cdf455. (Pubitemid 34984351)
48. th, Weixlbaumer A, Petry S, Kelley AC, et al. Structure of the 70S ribo-some complexed with mRNA and tRNA. Science 2006; 313:1935-42; PMID:16959973; http://dx.doi. org/10.1126/science. 1131127. (Pubitemid 44497996)
49. Zhang W, Dunkle JA, Cate JH. Structures of the ribosome in intermediate states of ratcheting. Science 2009; 325:1014-7; PMID:19696352; http://dx.doi. org/10.1126/science.1175275.
50. Voorhees RM, Weixlbaumer A, Loakes D, Kelley AC, Ramakrishnan V. Insights into substrate stabilization from snapshots of the peptidyl transferase center of the intact 70S ribosome. Nat Struct Mol Biol 2009; 16:528-33; PMID:19363482; http://dx.doi.org/10.1038/nsmb.1577.
51. Ponting C P. Proteins of the endoplasmic-reticulum-associated degradation pathway: domain detection and function prediction. Biochem J 2000; 351:527-35; PMID:11023840; http://dx.doi.org/10.1042/0264-6021:3510527.
52. Bloom L, Calabro V. FN3: a new protein scaffold reaches the clinic. Drug Discov Today 2009; 14:949-55; PMID:19576999; http://dx.doi.org/10.1016/j. drudis.2009.06.007.
53. Kim DH, Rossi JJ. The first ATPase domain of the yeast 246-kDa protein is required for in vivo unwinding of the U4/U6 duplex. RNA 1999; 5:959-71; PMID:10411139; http://dx.doi.org/10.1017/S135583829999012X. (Pubitemid 29321075)
54. Liu S, Li P, Dybkov O, Nottrott S, Hartmuth K, Lührmann R, et al. Binding of the human Prp31 Nop domain to a composite RNA-protein platform in U4 snRNP. Science 2007; 316:115-20; PMID:17412961; http://dx.doi.org/10.1126/ science.1137924. (Pubitemid 46559531)
55. van Nues RW, Beggs JD. Functional contacts with a range of splicing proteins suggest a central role for Brr2p in the dynamic control of the order of events in spli-ceosomes of Saccharomyces cerevisiae. Genetics 2001; 157:1451-67; PMID:11290703. (Pubitemid 32298816)
56. Gajiwala KS, Burley SK. Winged helix proteins. Curr Opin Struct Biol 2000; 10:110-6; PMID:10679470; http://dx.doi.org/10.1016/S0959-440X(99)00057-3. (Pubitemid 30099335)
57. Bonneau F, Basquin J, Ebert J, Lorentzen E, Conti E. The yeast exosome functions as a macromolecular cage to channel RNA substrates for degradation. Cell 2009; 139:547-59; PMID:19879841; http://dx.doi. org/10.1016/j.cell.2009.08. 042.
58. Liu Q, Greimann JC, Lima CD. Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 2006; 127:1223-37; PMID:17174896; http://dx.doi. org/10.1016/j.cell.2006.10.037. (Pubitemid 44894519)
59. Lorentzen E, Dziembowski A, Lindner D, Seraphin B, Conti E. RNA channelling by the archaeal exosome. EMBO Rep 2007; 8:470-6; PMID:17380186; http://dx.doi.org/10.1038/sj.embor.7400945. (Pubitemid 46696517)
60. Lorentzen E, Walter P, Fribourg S, Evguenieva-Hackenberg E, Klug G, Conti E. The archaeal exo-some core is a hexameric ring structure with three catalytic subunits. Nat Struct Mol Biol 2005; 12:575-81; PMID:15951817; http://dx.doi.org/10.1038/nsmb952. (Pubitemid 40980806)
61. Navarro MV, Oliveira CC, Zanchin NI, Guimarães BG. Insights into the mechanism of progressive RNA degradation by the archaeal exosome. J Biol Chem 2008; 283:14120-31; PMID:18353775; http://dx.doi. org/10.1074/jbc. M801005200.
62. Wang H W, Wang J, Ding F, Callahan K, Bratkowski MA, Butler JS, et al. Architecture of the yeast Rrp44 exosome complex suggests routes of RNA recruitment for 3' end processing. Proc Natl Acad Sci USA 2007; 104:16844-9; PMID:17942686; http://dx.doi. org/10.1073/pnas.0705526104. (Pubitemid 350210953)
63. Büttner K, Wenig K, Hopfner K P. Structural framework for the mechanism of archaeal exosomes in RNA processing. Mol Cell 2005; 20:461-71; PMID:16285927; http://dx.doi.org/10.1016/j.molcel.2005.10.018. (Pubitemid 41572302)
64. Doma MK, Parker R. RNA quality control in eukary-otes. Cell 2007; 131:660-8; PMID:18022361; http://dx.doi.org/10.1016/j.cell.2007.10.041.
65. Januszyk K, Lima CD. Structural components and architectures of RNA exosomes. Adv Exp Med Biol 2010; 702:9-28; PMID:21618871; http://dx.doi. org/10.1007/978-1-4419-7841-7-2.
66. Lykke-Andersen S, Brodersen DE, Jensen TH. Origins and activities of the eukaryotic exosome. J Cell Sci 2009; 122:1487-94; PMID:19420235; http://dx.doi. org/10.1242/jcs.047399.
67. Lykke-Andersen S, Tomecki R, Jensen TH, Dziembowski A. The eukaryotic RNA exosome: same scaffold but variable catalytic subunits. RNA Biol 2011; 8:61-6; PMID:21289487; http://dx.doi.org/10.4161/rna.8.1.14237.
68. Lebreton A, Tomecki R, Dziembowski A, Séraphin B. Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature 2008; 456:993-6; PMID:19060886; http://dx.doi.org/10.1038/nature07480.
69. Dziembowski A, Lorentzen E, Conti E, Séraphin B. A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat Struct Mol Biol 2007; 14:15-22; PMID:17173052; http://dx.doi.org/10.1038/nsmb1184. (Pubitemid 46067418)
70. Schaeffer D, Tsanova B, Barbas A, Reis F P, Dastidar EG, Sanchez-Rotunno M, et al. The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat Struct Mol Biol 2009; 16:56-62; PMID:19060898; http://dx.doi. org/10.1038/nsmb.1528.
71. Schneider C, Leung E, Brown J, Tollervey D. The N-terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Res 2009; 37:1127-40; PMID:19129231; http://dx.doi.org/10.1093/nar/gkn1020.
72. Januszyk K, Liu Q, Lima CD. Activities of human RRP6 and structure of the human RRP6 catalytic domain. RNA 2011; 17:1566-77; PMID:21705430; http://dx.doi.org/10.1261/rna.2763111.
73. Midtgaard S F, Assenholt J, Jonstrup AT, Van LB, Jensen TH, Brodersen DE. Structure of the nuclear exosome component Rrp6p reveals an interplay between the active site and the HRDC domain. Proc Natl Acad Sci USA 2006; 103:11898-903; PMID:16882719; http://dx.doi.org/10.1073/pnas.0604731103. (Pubitemid 44215783)
74. Phillips S, Butler JS. Contribution of domain structure to the RNA 3' end processing and degradation functions of the nuclear exosome subunit Rrp6p. RNA 2003; 9:1098-107; PMID:12923258; http://dx.doi. org/10.1261/rna.5560903. (Pubitemid 37093619)
75. Doma MK, Parker R. Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 2006; 440:561-4; PMID:16554824; http://dx.doi.org/10.1038/nature04530.
76. Mitchell P, Tollervey D. An NMD pathway in yeast involving accelerated deadenylation and exosome-medi-ated 3'5' degradation. Mol Cell 2003; 11:1405-13; PMID:12769863; http://dx.doi.org/10.1016/S1097-2765(03)00190-4. (Pubitemid 36645158)
77. Allmang C, Kufel J, Chanfreau G, Mitchell P, Petfalski E, Tollervey D. Functions of the exosome in rRNA, snoR-NA and snRNA synthesis. EMBO J 1999; 18:5399-410; PMID:10508172; http://dx.doi.org/10.1093/emboj/18.19.5399. (Pubitemid 29465589)
78. de la Cruz J, Kressler D, Tollervey D, Linder P. Dob1p (Mtr4p) is a putative ATP-dependent RNA helicase required for the 3' end formation of 5.8S rRNA in Saccharomyces cerevisiae. EMBO J 1998; 17:1128-40; PMID:9463390; http://dx.doi.org/10.1093/emboj/17.4.1128. (Pubitemid 28077666)
79. van Hoof A, Lennertz P, Parker R. Yeast exosome mutants accumulate 3'-extended polyadenylated forms of U4 small nuclear RNA and small nucleolar RNAs. Mol Cell Biol 2000; 20:441-52; PMID:10611222; http://dx.doi.org/10.1128/ MCB.20.2.441-452.2000. (Pubitemid 30023085)
80. Lubas M, Christensen MS, Kristiansen MS, Domanski M, Falkenby LG, Lykke-Andersen S, et al. Interaction profiling identifies the human nuclear exosome targeting complex. Mol Cell 2011; 43:624-37; PMID:21855801; http://dx.doi.org/10.1016/j.molcel.2011.06.028.
81. Wolin SL, Sim S, Chen X. Nuclear noncoding RNA surveillance: is the end in sight? Trends Genet 2012; 28:306-13; PMID:22475369; http://dx.doi.org/10. 1016/j. tig.2012.03.005.
82. Houseley J, Tollervey D. Yeast Trf5p is a nuclear poly(A) polymerase. EMBO Rep 2006; 7:205-11; PMID:16374505; http://dx.doi.org/10.1038/sj.embor. 7400612.
83. LaCava J, Houseley J, Saveanu C, Petfalski E, Thompson E, Jacquier A, et al. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 2005; 121:713-24; PMID:15935758; http://dx.doi. org/10.1016/j.cell.2005.04.029. (Pubitemid 40797594)
84. Vanácová S, Wolf J, Martin G, Blank D, Dettwiler S, Friedlein A, et al. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol 2005; 3:e189; PMID:15828860; http://dx.doi.org/10. 1371/journal.pbio.0030189.
85. Wyers F, Rougemaille M, Badis G, Rousselle JC, Dufour ME, Boulay J, et al. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 2005; 121:725-37; PMID:15935759; http://dx.doi.org/10.1016/j. cell.2005.04.030. (Pubitemid 40797595)
86. Brown JT, Bai X, Johnson AW. The yeast antiviral proteins Ski2p, Ski3p, and Ski8p exist as a complex in vivo. RNA 2000; 6:449-57; PMID:10744028; http://dx.doi. org/10.1017/S1355838200991787. (Pubitemid 30161288)
87. Synowsky SA, Heck AJ. The yeast Ski complex is a hetero-tetramer. Protein Sci 2008; 17:119-25; PMID:18042677; http://dx.doi.org/10.1110/ps.073155908.
88. Araki Y, Takahashi S, Kobayashi T, Kajiho H, Hoshino S, Katada T. Ski7p G protein interacts with the exosome and the Ski complex for 3'-to-5' mRNA decay in yeast. EMBO J 2001; 20:4684-93; PMID:11532933; http://dx.doi.org/10.1093/ emboj/20.17.4684. (Pubitemid 32848622)
89. Peng WT, Robinson MD, Mnaimneh S, Krogan NJ, Cagney G, Morris Q, et al. A panoramic view of yeast noncoding RNA processing. Cell 2003; 113:919-33; PMID:12837249; http://dx.doi.org/10.1016/S0092- (Pubitemid 36792034)
90. Chen CY, Gherzi R, Ong SE, Chan EL, Raijmakers R, Pruijn GJ, et al. AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 2001; 107:451-64; PMID:11719186; http://dx.doi. org/10.1016/S0092-8674(01)00578-5. (Pubitemid 33152781)
91. Schilders G, van Dijk E, Pruijn GJ. C1D and hMtr4p associate with the human exosome subunit PM/Scl-100 and are involved in pre-rRNA processing. Nucleic Acids Res 2007; 35:2564-72; PMID:17412707; http://dx.doi. org/10.1093/nar/gkm082. (Pubitemid 47073670)
92. Tomecki R, Kristiansen MS, Lykke-Andersen S, Chlebowski A, Larsen KM, Szczesny RJ, et al. The human core exosome interacts with differentially localized processive RNases: hDIS3 and hDIS3L. EMBO J 2010; 29:2342-57; PMID:20531386; http://dx.doi. org/10.1038/emboj.2010.121.
93. Callahan K P, Butler JS. TRAMP complex enhances RNA degradation by the nuclear exosome component Rrp6. J Biol Chem 2010; 285:3540-7; PMID:19955569; http://dx.doi.org/10.1074/jbc.M109.058396.
94. Bayne EH, White SA, Allshire RC. DegrAAAded into silence. Cell 2007; 129:651-3; PMID:17512398; http://dx.doi.org/10.1016/j.cell.2007.05.004. (Pubitemid 46813113)
95. Jensen TH, Moore C. Reviving the exosome. Cell 2005; 121:660-2; PMID:15935750; http://dx.doi. org/10.1016/j.cell.2005.05.018. (Pubitemid 40797586)
96. Keller C, Woolcock K, Hess D, Bühler M. Proteomic and functional analysis of the noncanoni-cal poly(A) polymerase Cid14. RNA 2010; 16:1124-9; PMID:20403971; http://dx.doi.org/10.1261/rna.2053710.
97. Schmid M, Küchler B, Eckmann CR. Tw o conserved regulatory cytoplasmic poly(A) polymerases, GLD-4 and GLD-2, regulate meiotic progression in C. elegans. Genes Dev 2009; 23:824-36; PMID:19339688; http://dx.doi.org/10. 1101/gad.494009.
98. Etheridge RD, Clemens DM, Gershon PD, Aphasizhev R. Identification and characterization of nuclear non-canonical poly(A) polymerases from Trypanosoma brucei. Mol Biochem Parasitol 2009; 164:66-73; PMID:19070634; http://dx.doi.org/10.1016/j.molbio-para.2008.11.004.
99. Nakamura R, Takeuchi R, Takata K, Shimanouchi K, Abe Y, Kanai Y, et al. TRF4 is involved in polyad-enylation of snRNAs in Drosophila melanogaster. Mol Cell Biol 2008; 28:6620-31; PMID:18765642; http://dx.doi.org/10.1128/MCB.00448- 08.
100. Lange H, Sement FM, Gagliardi D. MTR4, a putative RNA helicase and exosome co-factor, is required for proper rRNA biogenesis and development in Arabidopsis thaliana. Plant J 2011; 68:51-63; PMID:21682783; http://dx.doi.org/10.1111/j.1365-313X.2011.04675.x.
101. Cheng P, He Q, He Q, Wang L, Liu Y. Regulation of the Neurospora circadian clock by an RNA helicase. Genes Dev 2005; 19:234-41; PMID:15625191; http://dx.doi. org/10.1101/gad.1266805. (Pubitemid 40111119)
102. Dez C, Dlakic M, Tollervey D. Roles of the HEAT repeat proteins Utp10 and Utp20 in 40S ribosome maturation. RNA 2007; 13:1516-27; PMID:17652137; http://dx.doi.org/10.1261/rna.609807. (Pubitemid 47347422)
103. Rougemaille M, Gudipati RK, Olesen JR, Thomsen R, Seraphin B, Libri D, et al. Dissecting mechanisms of nuclear mRNA surveillance in THO/sub2 complex mutants. EMBO J 2007; 26:2317-26; PMID:17410208; http://dx.doi.org/10.1038/sj. emboj.7601669. (Pubitemid 46685852)
104. Wery M, Ruidant S, Schillewaert S, Leporé N, Lafontaine DL. The nuclear poly(A) polymerase and Exosome cofactor Trf5 is recruited cotranscriptionally to nucleolar surveillance. RNA 2009; 15:406-19; PMID:19141608; http://dx.doi.org/10.1261/rna.1402709.
105. Inoue K, Mizuno T, Wada K, Hagiwara M. Novel RING finger proteins, Air1p and Air2p, interact with Hmt1p and inhibit the arginine methylation of Npl3p. J Biol Chem 2000; 275:32793-9; PMID:10896665; http://dx.doi.org/10.1074/jbc. M004560200.
106. Castaño IB, Heath-Pagliuso S, Sadoff BU, Fitzhugh DJ, Christman M F. A novel family of TRF (DNA topoi-somerase I-related function) genes required for proper nuclear segregation. Nucleic Acids Res 1996; 24:2404-10; PMID:8710513; http://dx.doi.org/10.1093/nar/24.12.2404. (Pubitemid 26193605)
107. Jia H, Wang X, Liu F, Guenther U P, Srinivasan S, Anderson J T, et al. The RNA helicase Mtr4p modulates polyadenylation in the TRAMP complex. Cell 2011; 145:890-901; PMID:21663793; http://dx.doi. org/10.1016/j.cell.2011.05.010.
108. Wlotzka W, Kudla G, Granneman S, Tollervey D. The nuclear RNA polymerase II surveillance system targets polymerase III transcripts. EMBO J 2011; 30:1790-803; PMID:21460797; http://dx.doi.org/10.1038/emboj.2011.97.
109. Bernstein J, Ballin JD, Patterson DN, Wilson GM, Toth EA. Unique properties of the Mtr4p-poly(A) complex suggest a role in substrate targeting. Biochemistry 2010; 49:10357-70; PMID:21058657; http://dx.doi. org/10.1021/bi101518x.
110. Bernstein J, Patterson DN, Wilson GM, Toth EA. Characterization of the essential activities of Saccharomyces cerevisiae Mtr4p, a 3'-5' helicase partner of the nuclear exosome. J Biol Chem 2008; 283:4930-42; PMID:18096702; http://dx.doi.org/10.1074/jbc. M706677200.
111. Hamill S, Wolin SL, Reinisch KM. Structure and function of the polymerase core of TRAMP, a RNA surveillance complex. Proc Natl Acad Sci USA 2010; 107:15045-50; PMID:20696927; http://dx.doi. org/10.1073/pnas.1003505107.
112. Fasken MB, Leung S W, Banerjee A, Kodani MO, Chavez R, Bowman EA, et al. Air1 zinc knuckles 4 and 5 and a conserved IWRXY motif are critical for the function and integrity of the Trf4/5-Air1/2-Mtr4 poly-adenylation (TRAMP) RNA quality control complex. J Biol Chem 2011; 286:37429-45; PMID:21878619; http://dx.doi.org/10.1074/jbc.M111.271494.
113. Baker CL, Loros JJ, Dunlap JC. The circadian clock of Neurospora crassa. FEMS Microbiol Rev 2012; 36:95-110; PMID:21707668; http://dx.doi.org/10.1111/j. 1574-6976.2011.00288.x.
114. Guo J, Cheng P, Yuan H, Liu Y. The exosome regulates circadian gene expression in a posttranscrip-tional negative feedback loop. Cell 2009; 138:1236-46; PMID:19747717; http://dx.doi.org/10.1016/j. cell.2009.06.043.
115. Shi M, Collett M, Loros JJ, Dunlap JC. FRQ-interacting RNA helicase mediates negative and positive feedback in the Neurospora circadian clock. Genetics 2010; 184:351-61; PMID:19948888; http://dx.doi. org/10.1534/genetics. 109.111393.
116. Cheng Z, Liu Y, Wang C, Parker R, Song H. Crystal structure of Ski8p, a WD-repeat protein with dual roles in mRNA metabolism and meiotic recombination. Protein Sci 2004; 13:2673-84; PMID:15340168; http://dx.doi.org/10.1110/ps. 04856504. (Pubitemid 39274635)
117. Madrona AY, Wilson DK. The structure of Ski8p, a protein regulating mRNA degradation: Implications for WD protein structure. Protein Sci 2004; 13:1557-65; PMID:15152089; http://dx.doi.org/10.1110/ps.04704704. (Pubitemid 38669243)
118. Wang L, Lewis MS, Johnson AW. Domain interactions within the Ski2/3/8 complex and between the Ski complex and Ski7p. RNA 2005; 11:1291-302; PMID:16043509; http://dx.doi.org/10.1261/rna.2060405. (Pubitemid 41132400)
119. Miyashita M, Oshiumi H, Matsumoto M, Seya T. DDX60, a DEXD/H box helicase, is a novel antiviral factor promoting RIG-I-like receptor-mediated signaling. Mol Cell Biol 2011; 31:3802-19; PMID:21791617; http://dx.doi.org/10. 1128/MCB.01368-10.
120. The PyMOL Molecular Graphics System, Schrödinger, LLC.