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

Halbach F, Rode M, Conti E
RNA 18 124-34 (2012)
Cited: 52 times
EuropePMC logo PMID: 22114319

Abstract

Ski2 is a cytoplasmic RNA helicase that functions together with the exosome in the turnover and quality control of mRNAs. Ski2 is conserved in eukaryotes and is related to the helicase Mtr4, a cofactor of the nuclear exosome involved in the processing and quality control of a variety of structured RNAs. We have determined the 2.4 Å resolution crystal structure of the 113 kDa helicase region of Saccharomyces cerevisiae Ski2. The structure shows that Ski2 has an overall architecture similar to that of Mtr4, with a core DExH region and an extended insertion domain. The insertion is not required for the formation of the Ski2-Ski3-Ski8 complex, but is instead an RNA-binding domain. While this is reminiscent of the Mtr4 insertion, there are specific structural and biochemical differences between the two helicases. The insertion of yeast Mtr4 consists of a β-barrel domain that is flexibly attached to a helical stalk, contains a KOW signature motif, and binds in vitro-transcribed tRNA(i)(Met), but not single-stranded RNA. The β-barrel domain of yeast Ski2 does not contain a KOW motif and is tightly packed against the helical stalk, forming a single structural unit maintained by a zinc-binding site. Biochemically, the Ski2 insertion has broad substrate specificity, binding both single-stranded and double-stranded RNAs. We speculate that the Ski2 and Mtr4 insertion domains have evolved with different properties tailored to the type of transcripts that are the substrates of the cytoplasmic and nuclear exosome.

Reviews - 4a4k mentioned but not cited (1)

  1. Ski2-like RNA helicase structures: common themes and complex assemblies. Johnson SJ, Jackson RN. RNA Biol 10 33-43 (2013)

Articles - 4a4k mentioned but not cited (2)

  1. The crystal structure of S. cerevisiae Ski2, a DExH helicase associated with the cytoplasmic functions of the exosome. Halbach F, Rode M, Conti E. RNA 18 124-134 (2012)
  2. Concerted structural rearrangements enable RNA channeling into the cytoplasmic Ski238-Ski7-exosome assembly. Keidel A, Kögel A, Reichelt P, Kowalinski E, Schäfer IB, Conti E. Mol Cell 83 4093-4105.e7 (2023)


Reviews citing this publication (17)

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Articles citing this publication (32)

  1. The Exosome Is Recruited to RNA Substrates through Specific Adaptor Proteins. Thoms M, Thomson E, Baßler J, Gnädig M, Griesel S, Hurt E. Cell 162 1029-1038 (2015)
  2. The yeast ski complex: crystal structure and RNA channeling to the exosome complex. Halbach F, Reichelt P, Rode M, Conti E. Cell 154 814-826 (2013)
  3. The exosome-binding factors Rrp6 and Rrp47 form a composite surface for recruiting the Mtr4 helicase. Schuch B, Feigenbutz M, Makino DL, Falk S, Basquin C, Mitchell P, Conti E. EMBO J 33 2829-2846 (2014)
  4. Helicase-Dependent RNA Decay Illuminated by a Cryo-EM Structure of a Human Nuclear RNA Exosome-MTR4 Complex. Weick EM, Puno MR, Januszyk K, Zinder JC, DiMattia MA, Lima CD. Cell 173 1663-1677.e21 (2018)
  5. Post-transcriptional regulation of meiotic genes by a nuclear RNA silencing complex. Egan ED, Braun CR, Gygi SP, Moazed D. RNA 20 867-881 (2014)
  6. The cryo-EM structure of a ribosome-Ski2-Ski3-Ski8 helicase complex. Schmidt C, Kowalinski E, Shanmuganathan V, Defenouillère Q, Braunger K, Heuer A, Pech M, Namane A, Berninghausen O, Fromont-Racine M, Jacquier A, Conti E, Becker T, Beckmann R. Science 354 1431-1433 (2016)
  7. The RNA helicases AtMTR4 and HEN2 target specific subsets of nuclear transcripts for degradation by the nuclear exosome in Arabidopsis thaliana. Lange H, Zuber H, Sement FM, Chicher J, Kuhn L, Hammann P, Brunaud V, Bérard C, Bouteiller N, Balzergue S, Aubourg S, Martin-Magniette ML, Vaucheret H, Gagliardi D. PLoS Genet 10 e1004564 (2014)
  8. RNA unwinding by the Trf4/Air2/Mtr4 polyadenylation (TRAMP) complex. Jia H, Wang X, Anderson JT, Jankowsky E. Proc Natl Acad Sci U S A 109 7292-7297 (2012)
  9. Structural analysis of the yeast Dhh1-Pat1 complex reveals how Dhh1 engages Pat1, Edc3 and RNA in mutually exclusive interactions. Sharif H, Ozgur S, Sharma K, Basquin C, Urlaub H, Conti E. Nucleic Acids Res 41 8377-8390 (2013)
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  12. Structure of the DEAH/RHA ATPase Prp43p bound to RNA implicates a pair of hairpins and motif Va in translocation along RNA. He Y, Staley JP, Andersen GR, Nielsen KH. RNA 23 1110-1124 (2017)
  13. NRDE2 negatively regulates exosome functions by inhibiting MTR4 recruitment and exosome interaction. Wang J, Chen J, Wu G, Zhang H, Du X, Chen S, Zhang L, Wang K, Fan J, Gao S, Wu X, Zhang S, Kuai B, Zhao P, Chi B, Wang L, Li G, Wong CCL, Zhou Y, Li J, Yun C, Cheng H. Genes Dev 33 536-549 (2019)
  14. Structural insights into the interaction of the nuclear exosome helicase Mtr4 with the preribosomal protein Nop53. Falk S, Tants JN, Basquin J, Thoms M, Hurt E, Sattler M, Conti E. RNA 23 1780-1787 (2017)
  15. The Mtr4 ratchet helix and arch domain both function to promote RNA unwinding. Taylor LL, Jackson RN, Rexhepaj M, King AK, Lott LK, van Hoof A, Johnson SJ. Nucleic Acids Res 42 13861-13872 (2014)
  16. Structure of the frequency-interacting RNA helicase: a protein interaction hub for the circadian clock. Conrad KS, Hurley JM, Widom J, Ringelberg CS, Loros JJ, Dunlap JC, Crane BR. EMBO J 35 1707-1719 (2016)
  17. Genetic interactions suggest multiple distinct roles of the arch and core helicase domains of Mtr4 in Rrp6 and exosome function. Klauer AA, van Hoof A. Nucleic Acids Res 41 533-541 (2013)
  18. Kinesin Motor Enzymology: Chemistry, Structure, and Physics of Nanoscale Molecular Machines. Cochran JC. Biophys Rev 7 269-299 (2015)
  19. Multiplex quantitative SILAC for analysis of archaeal proteomes: a case study of oxidative stress responses. McMillan LJ, Hwang S, Farah RE, Koh J, Chen S, Maupin-Furlow JA. Environ Microbiol 20 385-401 (2018)
  20. Structural analysis of mtEXO mitochondrial RNA degradosome reveals tight coupling of nuclease and helicase components. Razew M, Warkocki Z, Taube M, Kolondra A, Czarnocki-Cieciura M, Nowak E, Labedzka-Dmoch K, Kawinska A, Piatkowski J, Golik P, Kozak M, Dziembowski A, Nowotny M. Nat Commun 9 97 (2018)
  21. The human SKI complex regulates channeling of ribosome-bound RNA to the exosome via an intrinsic gatekeeping mechanism. Kögel A, Keidel A, Bonneau F, Schäfer IB, Conti E. Mol Cell 82 756-769.e8 (2022)
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  26. Long-range allostery mediates cooperative adenine nucleotide binding by the Ski2-like RNA helicase Brr2. Absmeier E, Vester K, Ghane T, Burakovskiy D, Milon P, Imhof P, Rodnina MV, Santos KF, Wahl MC. J Biol Chem 297 100829 (2021)
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