The crystal structure of S. cerevisiae Ski2, a DExH helicase associated with the cytoplasmic functions of the exosome

RNA

Volumn 18, Issue 1, 2012, Pages 124-134

  Halbach, Felix ^a   Rode, Michaela ^a   Conti, Elena ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Exosome; Helicase; RNA degradation; Structure

Indexed keywords

DOUBLE STRANDED RNA; RNA HELICASE; SINGLE STRANDED RNA; SKI2 PROTEIN; TRANSFER RNA; UNCLASSIFIED DRUG; ZINC BINDING PROTEIN;

ARTICLE; CELL FUNCTION; CRYSTAL STRUCTURE; CYTOPLASM; ENZYME SPECIFICITY; EXOSOME; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN STRUCTURE; RNA BINDING; RNA TRANSCRIPTION; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; CYTOPLASM; DEAD-BOX RNA HELICASES; EXOSOMES; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84055217962     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.029553.111     Document Type: Article

References (55)

1. Adams PD, Afonine PV, Bunkó czi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
2. Allmang C, Kufel J, Chanfreau G, Mitchell P, Petfalski E, Tollervey D. 1999. Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J 18: 5399-5410. (Pubitemid 29465589)
3. Anderson JS, Parker RP. 1998. 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 17: 1497-1506. (Pubitemid 28105528)
4. Araki Y, Takahashi S, Kobayashi T, Kajiho H, Hoshino S, Katada T. 2001. Ski7p G protein interacts with the exosome and the Ski complex for 3′-to-5′ mRNA decay in yeast. EMBO J 20: 4684-4693. (Pubitemid 32848622)
5. Bonneau F, Basquin J, Ebert J, Lorentzen E, Conti E. 2009. The yeast exosome functions as a macromolecular cage to channel RNA substrates for degradation. Cell 139: 547-559.
6. Bousquet-Antonelli C, Presutti C, Tollervey D. 2000. Identification of a regulated pathway for nuclear pre-mRNA turnover. Cell 102: 765-775.
7. Brown JT, Bai X, Johnson AW. 2000. The yeast antiviral proteins Ski2p, Ski3p, and Ski8p exist as a complex in vivo. RNA 6: 449-457. (Pubitemid 30161288)
8. Büttner K, Wenig K, Hopfner KP. 2005. Structural framework for the mechanism of archaeal exosomes in RNA processing. Mol Cell 20: 461-471. (Pubitemid 41572302)
9. Büttner K, Nehring S, Hopfner KP. 2007. Structural basis for DNA duplex separation by a superfamily-2 helicase. Nat Struct Mol Biol 14: 647-652. (Pubitemid 47037060)
10. Chen VB, Arendall WB III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12-21.
11. Cowtan K. 2006. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 62: 1002-1011. (Pubitemid 44337374)
12. Cristodero M, Bottcher B, Diepholz M, Scheffzek K, Clayton C. 2008. The Leishmania tarentolae exosome: purification and structural analysis by electron microscopy. Mol Biochem Parasitol 159: 24-29.
13. de la Cruz J, Kressler D, Tollervey D, Linder P. 1998. Dob1p (Mtr4p) is a putative ATP-dependent RNA helicase required for the 3′ end formation of 5.8S rRNA in Saccharomyces cerevisiae. EMBO J 17: 1128-1140. (Pubitemid 28077666)
14. Dziembowski A, Lorentzen E, Conti E, Séraphin B. 2007. A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat Struct Mol Biol 14: 15-22. (Pubitemid 46067418)
15. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501.
16. Evans P. 2006. Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62: 72-82.
17. Gatfield D, Izaurralde E. 2004. Nonsense-mediated messenger RNA decay is initiated by endonucleolytic cleavage in Drosophila. Nature 429: 575-578. (Pubitemid 38737663)
18. He Y, Andersen GR, Nielsen KH. 2010. Structural basis for the function of DEAH helicases. EMBO Rep 11: 180-186.
19. Hilleren P, McCarthy T, Rosbash M, Parker R, Jensen TH. 2001. Quality control of mRNA 3′-end processing is linked to the nuclear exosome. Nature 413: 538-542. (Pubitemid 32938754)
20. Houalla R, Devaux F, Fatica A, Kufel J, Barrass D, Torchet C, Tollervey D. 2006. Microarray detection of novel nuclear RNA substrates for the exosome. Yeast 23: 439-454. (Pubitemid 43797108)
21. Houseley J, Tollervey D. 2009. The many pathways of RNA degradation. Cell 136: 763-776.
22. Jackson RN, Klauer AA, Hintze BJ, Robinson H, van Hoof A, Johnson SJ. 2010. The crystal structure of Mtr4 reveals a novel arch domain required for rRNA processing. EMBO J 29: 2205-2216.
23. Johnson AW, Kolodner RD. 1995. 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 15: 2719-2727.
24. Kabsch W. 2010. XDS. Acta Crystallogr D Biol Crystallogr 66: 125-132.
25. Kadaba S, Krueger A, Trice T, Krecic AM, Hinnebusch AG, Anderson J. 2004. Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes Dev 18: 1227-1240. (Pubitemid 38720591)
26. Kyrpides NC, Woese CR, Ouzounis CA. 1996. KOW: a novel motif linking a bacterial transcription factor with ribosomal proteins. Trends Biochem Sci 21: 425-426. (Pubitemid 26393730)
27. LaCava J, Houseley J, Saveanu C, Petfalski E, Thompson E, Jacquier A, Tollervey D. 2005. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121: 713-724. (Pubitemid 40797594)
28. Lebreton A, Seraphin B. 2008. Exosome-mediated quality control: substrate recruitment and molecular activity. Biochim Biophys Acta 1779: 558-565.
29. Lebreton A, Tomecki R, Dziembowski A, Seraphin B. 2008. Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature 456: 993-996.
30. Lejeune F, Li X, Maquat LE. 2003. Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol Cell 12: 675-687. (Pubitemid 37222488)
31. Liu Q, Greimann JC, Lima CD. 2006. Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127: 1223-1237. (Pubitemid 44894519)
32. Lorentzen E, Walter P, Fribourg S, Evguenieva-Hackenberg E, Klug G, Conti E. 2005. The archaeal exosome core is a hexameric ring structure with three catalytic subunits. Nat Struct Mol Biol 12: 575-581. (Pubitemid 40980806)
33. Lorentzen E, Dziembowski A, Lindner D, Seraphin B, Conti E. 2007. RNA channelling by the archaeal exosome. EMBO Rep 8: 470-476. (Pubitemid 46696517)
34. Lorentzen E, Basquin J, Conti E. 2008a. Structural organization of the RNA-degrading exosome. Curr Opin Struct Biol 18: 709-713.
35. Lorentzen E, Basquin J, Tomecki R, Dziembowski A, Conti E. 2008b. Structure of the active subunit of the yeast exosome core, Rrp44: diverse modes of substrate recruitment in the RNase II nuclease family. Mol Cell 29: 717-728. (Pubitemid 351400929)
36. Lykke-Andersen S, Brodersen DE, Jensen TH. 2009. Origins and activities of the eukaryotic exosome. J Cell Sci 122: 1487-1494.
37. Mitchell P, Tollervey D. 2003. An NMD pathway in yeast involving accelerated deadenylation and exosome-mediated 3′→5′ degradation. Mol Cell 11: 1405-1413. (Pubitemid 36645158)
38. Mitchell P, Petfalski E, Shevchenko A, Mann M, Tollervey D. 1997. The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′→5′ exoribonucleases. Cell 91: 457-466. (Pubitemid 27508235)
39. Orban TI, Izaurralde E. 2005. Decay of mRNAs targeted by RISC requires XRN1, the Ski complex, and the exosome. RNA 11: 459-469. (Pubitemid 40397179)
40. Pyle AM. 2008. Translocation and unwinding mechanisms of RNA and DNA helicases. Annu Rev Biophys 37: 317-336.
41. 2 double-stranded RNA by L-A-HN and confer cold sensitivity in the presence of M and L-A-HN. Mol Cell Biol 4: 761-770.
42. Schaeffer D, Tsanova B, Barbas A, Reis FP, Dastidar EG, Sanchez-Rotunno M, Arraiano CM, van Hoof A. 2009. The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat Struct Mol Biol 16: 56-62.
43. Schneider C, Leung E, Brown J, Tollervey D. 2009. The N-terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Res 37: 1127-1140.
44. Selmer M, Dunham CM, Murphy FV IV, Weixlbaumer A, Petry S, Kelley AC, Weir JR, Ramakrishnan V. 2006. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313: 1935-1942. (Pubitemid 44497996)
45. Takahashi S, Araki Y, Sakuno T, Katada T. 2003. Interaction between Ski7p and Upf1p is required for nonsense-mediated 3′-to-5′ mRNA decay in yeast. EMBO J 22: 3951-3959. (Pubitemid 36975721)
46. Toh-E A, Wickner RB. 1979. A mutant killer plasmid whose replication depends on a chromosomal "superkiller" mutation. Genetics 91: 673-682. (Pubitemid 9208630)
47. van Hoof A, Lennertz P, Parker R. 2000a. Yeast exosome mutants accumulate 3′-extended polyadenylated forms of U4 small nuclear RNA and small nucleolar RNAs. Mol Cell Biol 20: 441-452. (Pubitemid 30023085)
48. van Hoof A, Staples RR, Baker RE, Parker R. 2000b. Function of the Ski4p (Csl4p) and Ski7p proteins in 3′-to-5′ degradation of mRNA. Mol Cell Biol 20: 8230-8243.
49. van Hoof A, Frischmeyer PA, Dietz HC, Parker R. 2002. Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science 295: 2262-2264. (Pubitemid 34258839)
50. Vanacova S, Wolf J, Martin G, Blank D, Dettwiler S, Friedlein A, Langen H, Keith G, Keller W. 2005. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol 3: e189. doi: 10.1371/journal.pbio.0030189.
51. Walbott H, Mouffok S, Capeyrou R, Lebaron S, Humbert O, van Tilbeurgh H, Henry Y, Leulliot N. 2010. Prp43p contains a processive helicase structural architecture with a specific regulatory domain. EMBO J 29: 2194-2204.
52. Wang L, Lewis MS, Johnson AW. 2005. Domain interactions within the Ski2/3/8 complex and between the Ski complex and Ski7p. RNA 11: 1291-1302. (Pubitemid 41132400)
53. Weir JR, Bonneau F, Hentschel J, Conti E. 2010. Structural analysis reveals the characteristic features of Mtr4, a DExH helicase involved in nuclear RNA processing and surveillance. Proc Natl Acad Sci 107: 12139-12144.
54. Wyers F, Rougemaille M, Badis G, Rousselle JC, Dufour ME, Boulay J, Regnault B, Devaux F, Namane A, Seraphin B, et al. 2005. Cryptic Pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121: 725-737. (Pubitemid 40797595)
55. Zhang W, Dunkle JA, Cate JH. 2009. Structures of the ribosome in intermediate states of ratcheting. Science 325: 1014-1017.